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Plant abiotic stress response and nutrient use efficiency

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Abstract

Abiotic stresses and soil nutrient limitations are major environmental conditions that reduce plant growth, productivity and quality. Plants have evolved mechanisms to perceive these environmental challenges, transmit the stress signals within cells as well as between cells and tissues, and make appropriate adjustments in their growth and development in order to survive and reproduce. In recent years, significant progress has been made on many fronts of the stress signaling research, particularly in understanding the downstream signaling events that culminate at the activation of stress- and nutrient limitation-responsive genes, cellular ion homeostasis, and growth adjustment. However, the revelation of the early events of stress signaling, particularly the identification of primary stress sensors, still lags behind. In this review, we summarize recent work on the genetic and molecular mechanisms of plant abiotic stress and nutrient limitation sensing and signaling and discuss new directions for future studies.

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References

  • Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., and Genschik, P. (2008). The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20, 2117–2129.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwal, M., Hao, Y., Kapoor, A., Dong, C.H., Fujii, H., Zheng, X., and Zhu, J.K. (2006). A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281, 37636–37645..

    Article  CAS  PubMed  Google Scholar 

  • Ali, A., Kim, J.K., Jan, M., Khan, H.A., Khan, I.U., Shen, M., Park, J., Lim, C.J., Hussain, S., Baek, D., et al. (2019a). Rheostatic control of ABA signaling through HOS15-mediated OST1 degradation. Mol Plant 12, 1447–1462.

    Article  CAS  PubMed  Google Scholar 

  • Ali, A., Maggio, A., Bressan, R.A., and Yun, D.J. (2019b). Role and Functional Differences of HKT1-Type Transporters in Plants under Salt Stress. Int J Med Sci 20, 1059.

    CAS  Google Scholar 

  • Amzal, B., Julin, B., Vahter, M., Wolk, A., Johanson, G., and Akesson, A. (2009). Population toxicokinetic modeling of cadmium for health risk assessment. Environ Health Perspectives 117, 1293–1301.

    Article  CAS  Google Scholar 

  • Andrés, Z., Pérez-Hormaeche, J., Leidi, E.O., Schlücking, K., Steinhorst, L., McLachlan, D.H., Schumacher, K., Hetherington, A.M., Kudla, J., Cubero, B., et al. (2014). Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake. Proc Natl Acad Sci USA 111, E1806–E1814.

    PubMed  PubMed Central  Google Scholar 

  • Apse, M.P., Aharon, G.S., Snedden, W.A., and Blumwald, E. (1999). Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285, 1256–1258.

    Article  CAS  PubMed  Google Scholar 

  • Bac-Molenaar, J.A., Fradin, E.F., Becker, F.F.M., Rienstra, J.A., van der Schoot, J., Vreugdenhil, D., and Keurentjes, J.J.B. (2015). Genomewide association mapping of fertility reduction upon heat stress reveals developmental stage-specific QTLs in Arabidopsis thaliana. Plant Cell 27, 1857–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balzergue, C., Dartevelle, T., Godon, C., Laugier, E., Meisrimler, C., Teulon, J.M., Creff, A., Bissler, M., Brouchoud, C., Hagège, A., et al. (2017). Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun 8, 15300.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baniwal, S.K., Chan, K.Y., Scharf, K.D., and Nover, L. (2007). Role of heat stress transcription factor HsfA5 as specific repressor of HsfA4. J Biol Chem 282, 3605–3613.

    Article  CAS  PubMed  Google Scholar 

  • Banti, V., Mafessoni, F., Loreti, E., Alpi, A., and Perata, P. (2010). The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152, 1471–1483.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barnabás, B., Jäger, K., and Fehér, A. (2008). The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31, 11–38.

    PubMed  Google Scholar 

  • Barragán, V., Leidi, E.O., Andrés, Z., Rubio, L., De Luca, A., Fernández, J. A., Cubero, B., and Pardo, J.M. (2012). Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24, 1127–1142.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bassil, E., Ohto, M., Esumi, T., Tajima, H., Zhu, Z., Cagnac, O., Belmonte, M., Peleg, Z., Yamaguchi, T., and Blumwald, E. (2011a). The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23, 224–239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bassil, E., Tajima, H., Liang, Y.C., Ohto, M.A., Ushijima, K., Nakano, R., Esumi, T., Coku, A., Belmonte, M., and Blumwald, E. (2011b). The Arabidopsis Na+/H+ antiporters NHX1 and NHX2 control vacuolar pH and K+ homeostasis to regulate growth, flower development, and reproduction. Plant Cell 23, 3482–3497.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baxter, A., Mittler, R., and Suzuki, N. (2014). ROS as key players in plant stress signalling. J Exp Bot 65, 1229–1240.

    Article  CAS  PubMed  Google Scholar 

  • Baxter, I. (2015). Should we treat the ionome as a combination of individual elements, or should we be deriving novel combined traits? J Exp Bot 66, 2127–2131.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Belda-Palazon, B., Rodriguez, L., Fernandez, M.A., Castillo, M.C., Anderson, E.M., Gao, C., Gonzalez-Guzman, M., Peirats-Llobet, M., Zhao, Q., De Winne, N., et al. (2016). FYVE1/FREE1 interacts with the PYL4 ABA receptor and mediates its delivery to the vacuolar degradation pathway. Plant Cell 28, 2291–2311.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berthomieu, P., Conejero, G., Nublat, A., Brackenbury, W.J., Lambert, C., Savio, C., Uozumi, N., Oiki, S., Yamada, K., Cellier, F., et al. (2003). Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22, 2004–2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhaskara, G.B., Wen, T.N., Nguyen, T.T., and Verslues, P.E. (2017). Protein phosphatase 2Cs and microtubule-associated stress protein 1 control microtubule stability, plant growth, and drought response. Plant Cell 29, 169–191.

    Article  CAS  PubMed  Google Scholar 

  • Bloom, A.J., and Lancaster, K.M. (2018). Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nat Plants 4, 414–422.

    Article  CAS  PubMed  Google Scholar 

  • Blumwald, E., and Poole, R.J. (1985). Na+/H+ antiport in isolated tonoplast vesicles from storage tissue of Beta vulgaris. Plant Physiol 78, 163–167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boeynaems, S., Alberti, S., Fawzi, N.L., Mittag, T., Polymenidou, M., Rousseau, F., Schymkowitz, J., Shorter, J., Wolozin, B., Van Den Bosch, L., et al. (2018). Protein phase separation: a new phase in cell biology. Trends Cell Biol 28, 420–435.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bothe, H. (2011). Plants in heavy metal soils. In Detoxification of Heavy Metals (Springer), pp. 35–57.

  • Brandt, B., Brodsky, D.E., Xue, S., Negi, J., Iba, K., Kangasjärvi, J., Ghassemian, M., Stephan, A.B., Hu, H., and Schroeder, J.I. (2012). Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109, 10593–10598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bueso, E., Rodriguez, L., Lorenzo-Orts, L., Gonzalez-Guzman, M., Sayas, E., Muñoz-Bertomeu, J., Ibañez, C., Serrano, R., and Rodriguez, P.L. (2014). The single-subunit RING-type E3 ubiquitin ligase RSL1 targets PYL4 and PYR1 ABA receptors in plasma membrane to modulate abscisic acid signaling. Plant J 80, 1057–1071.

    Article  CAS  PubMed  Google Scholar 

  • Burla, B., Pfrunder, S., Nagy, R., Francisco, R.M., Lee, Y., and Martinoia, E. (2013). Vacuolar transport of abscisic acid glucosyl ester is mediated by ATP-binding cassette and proton-antiport mechanisms in Arabidopsis. Plant Physiol 163, 1446–1458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Busch, F.A., Sage, R.F., and Farquhar, G.D. (2018). Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat Plants 4, 46–54.

    Article  CAS  PubMed  Google Scholar 

  • Busoms, S., Paajanen, P., Marburger, S., Bray, S., Huang, X.Y., Poschenrieder, C., Yant, L., and Salt, D.E. (2018). Fluctuating selection on migrant adaptive sodium transporter alleles in coastal Arabidopsis thaliana. Proc Natl Acad Sci USA 115, E12443–E12452.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bustos, R., Castrillo, G., Linhares, F., Puga, M.I., Rubio, V., Pérez-Pérez, J., Solano, R., Leyva, A., and Paz-Ares, J. (2010). A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6, e1001102.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Byrt, C.S., Platten, J.D., Spielmeyer, W., James, R.A., Lagudah, E.S., Dennis, E.S., Tester, M., and Munns, R. (2007). HKT1;5-like cation transporters linked to Na+ exclusion loci in wheat, Nax2 and Kna1. Plant Physiol 143, 1918–1928.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Byrt, C.S., Zhao, M., Kourghi, M., Bose, J., Henderson, S.W., Qiu, J., Gilliham, M., Schultz, C., Schwarz, M., Ramesh, S.A., et al. (2017). Non-selective cation channel activity of aquaporin AtPIP2;1 regulated by Ca2+ and pH. Plant Cell Environ 40, 802–815.

    Article  CAS  PubMed  Google Scholar 

  • Cai, C., Lanman, N.A., Withers, K.A., DeLeon, A.M., Wu, Q., Gribskov, M., Salt, D.E., and Banks, J.A. (2019). Three genes define a bacteriallike arsenic tolerance mechanism in the arsenic hyperaccumulating fern Pteris vittata. Curr Biol 29, 1625–1633.e3.

    Article  CAS  PubMed  Google Scholar 

  • Campbell, M.T., Bandillo, N., Al Shiblawi, F.R.A., Sharma, S., Liu, K., Du, Q., Schmitz, A.J., Zhang, C., Véry, A.A., Lorenz, A.J., et al. (2017). Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content. PLoS Genet 13, e1006823.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cao, Y., Feng, H., Sun, D., Xu, G., Rathinasabapathi, B., Chen, Y., and Ma, L.Q. (2019). Heterologous Expression of Pteris vittata Phosphate Transporter PvPht1;3 Enhances Arsenic Translocation to and Accumulation in Tobacco Shoots. Environ Sci Technol 53, 10636–10644.

    Article  CAS  PubMed  Google Scholar 

  • Castillo, M.C., Lozano-Juste, J., González-Guzmán, M., Rodriguez, L., Rodriguez, P.L., and León, J. (2015). Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8, ra89.

    Article  PubMed  CAS  Google Scholar 

  • Castrillo, G., Teixeira, P.J.P.L., Paredes, S.H., Law, T.F., de Lorenzo, L., Feltcher, M.E., Finkel, O.M., Breakfield, N.W., Mieczkowski, P., Jones, C.D., et al. (2017). Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cavrak, V.V., Lettner, N., Jamge, S., Kosarewicz, A., Bayer, L.M., and Mittelsten Scheid, O. (2014). How a retrotransposon exploits the plant’s heat stress response for its activation. PLoS Genet 10, e1004115.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chan, Z., Wang, Y., Cao, M., Gong, Y., Mu, Z., Wang, H., Hu, Y., Deng, X., He, X.J., and Zhu, J.K. (2016). RDM4 modulates cold stress resistance in Arabidopsis partially through the CBF-mediated pathway. New Phytol 209, 1527–1539.

    Article  CAS  PubMed  Google Scholar 

  • Chao, D.Y., Chen, Y., Chen, J., Shi, S., Chen, Z., Wang, C., Danku, J.M., Zhao, F.J., and Salt, D.E. (2014). Genome-wide association mapping identifies a new arsenate reductase enzyme critical for limiting arsenic accumulation in plants. PLoS Biol 12, e1002009.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chao, D.Y., Silva, A., Baxter, I., Huang, Y.S., Nordborg, M., Danku, J., Lahner, B., Yakubova, E., and Salt, D.E. (2012). Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Genet 8, e1002923.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, C., Chen, H., Lin, Y.S., Shen, J.B., Shan, J.X., Qi, P., Shi, M., Zhu, M.Z., Huang, X.H., Feng, Q., et al. (2014). A two-locus interaction causes interspecific hybrid weakness in rice. Nat Commun 5, 3357.

    Article  PubMed  CAS  Google Scholar 

  • Chen, D.H., Liu, H.P., and Li, C.L. (2019a). Calcium-dependent protein kinase CPK9 negatively functions in stomatal abscisic acid signaling by regulating ion channel activity in Arabidopsis. Plant Mol Biol 99, 113–122.

    Article  CAS  PubMed  Google Scholar 

  • Chen, H.H., Qu, L., Xu, Z.H., Zhu, J.K., and Xue, H.W. (2018). EL1-like casein kinases suppress ABA signaling and responses by phosphorylating and destabilizing the ABA receptors PYR/PYLs in Arabidopsis. Mol Plant 11, 706–719.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J., Yu, F., Liu, Y., Du, C., Li, X., Zhu, S., Wang, X., Lan, W., Rodriguez, P.L., Liu, X., et al. (2016). FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proc Natl Acad Sci USA 113, E5519–E5527.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, Y., Hua, C.Y., Chen, J.X., Rathinasabapathi, B., Cao, Y., and Ma, L. Q. (2019b). Expressing arsenite antiporter PvACR3;1 in rice (Oryza sativa L.) decreases inorganic arsenic content in rice grains. Environ Sci Technol 53, 10062–10069.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y., Sun, S.K., Tang, Z., Liu, G., Moore, K.L., Maathuis, F.J.M., Miller, A.J., McGrath, S.P., and Zhao, F.J. (2017a). The Nodulin 26-like intrinsic membrane protein OsNIP3;2 is involved in arsenite uptake by lateral roots in rice. J Exp Bot 68, 3007–3016.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Z.C., Yamaji, N., Horie, T., Che, J., Li, J., An, G., and Ma, J.F. (2017b). A magnesium transporter OsMGT1 plays a critical role in salt tolerance in rice. Plant Physiol 174, 1837–1849.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, C., Wang, Z., Ren, Z., Zhi, L., Yao, B., Su, C., Liu, L., and Li, X. (2017). SCFAtPP2-B11 modulates ABA signaling by facilitating SnRK2.3 degradation in Arabidopsis thaliana. PLoS Genet 13, e1006947.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B.H., Hong, X., Agarwal, M., and Zhu, J.K. (2003). ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17, 1043–1054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christmann, A., Hoffmann, T., Teplova, I., Grill, E., and Müller, A. (2005). Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis. Plant Physiol 137, 209–219.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clemens, S., Aarts, M.G.M., Thomine, S., and Verbruggen, N. (2013). Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18, 92–99.

    Article  CAS  PubMed  Google Scholar 

  • Cohen-Peer, R., Schuster, S., Meiri, D., Breiman, A., and Avni, A. (2010). Sumoylation of Arabidopsis heat shock factor A2 (HsfA2) modifies its activity during acquired thermotholerance. Plant Mol Biol 74, 33–45.

    Article  CAS  PubMed  Google Scholar 

  • Collins, L.J., Schonfeld, B., and Chen, X.S. (2011). The epigenetics of noncoding RNA. In Handbook of Epigenetics: The New Molecular and Medical Genetics (Academic Press), pp. 49–61.

  • Compant, S., Samad, A., Faist, H., and Sessitsch, A. (2019). A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. J Adv Res 19, 29–37.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corratgé-Faillie, C., Ronzier, E., Sanchez, F., Prado, K., Kim, J.H., Lanciano, S., Leonhardt, N., Lacombe, B., and Xiong, T.C. (2017). The Arabidopsis guard cell outward potassium channel GORK is regulated by CPK33. FEBS Lett 591, 1982–1992.

    Article  PubMed  CAS  Google Scholar 

  • Crisp, P.A., Ganguly, D., Eichten, S.R., Borevitz, J.O., and Pogson, B.J. (2016). Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv 2, e1501340.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cui, P., and Xiong, L. (2015). Environmental stress and pre-mRNA splicing. Mol Plant 8, 1302–1303.

    Article  CAS  PubMed  Google Scholar 

  • Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R. (2010). Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61, 651–679.

    Article  CAS  PubMed  Google Scholar 

  • Dall’Osto, L., Cazzaniga, S., North, H., Marion-Poll, A., and Bassi, R. (2007). The Arabidopsis aba4-1 mutant reveals a specific function for neoxanthin in protection against photooxidative stress. Plant Cell 19, 1048–1064.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Davletova, S., Rizhsky, L., Liang, H., Shengqiang, Z., Oliver, D.J., Coutu, J., Shulaev, V., Schlauch, K., and Mittler, R. (2005). Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17, 268–281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Angeli, A., Zhang, J., Meyer, S., and Martinoia, E. (2013). AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nat Commun 4, 1804.

    Article  PubMed  CAS  Google Scholar 

  • Demidchik, V., Shabala, S., Isayenkov, S., Cuin, T.A., and Pottosin, I. (2018). Calcium transport across plant membranes: mechanisms and functions. New Phytol 220, 49–69.

    Article  CAS  PubMed  Google Scholar 

  • Demir, F., Horntrich, C., Blachutzik, J.O., Scherzer, S., Reinders, Y., Kierszniowska, S., Schulze, W.X., Harms, G.S., Hedrich, R., Geiger, D., et al. (2013). Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc Natl Acad Sci USA 110, 8296–8301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz, M., Sanchez-Barrena, M.J., Gonzalez-Rubio, J.M., Rodriguez, L., Fernandez, D., Antoni, R., Yunta, C., Belda-Palazon, B., Gonzalez-Guzman, M., Peirats-Llobet, M., et al. (2016). Calcium-dependent oligomerization of CAR proteins at cell membrane modulates ABA signaling. Proc Natl Acad Sci USA 113, E396–E405.

    Article  CAS  PubMed  Google Scholar 

  • Ding, Y., Jia, Y., Shi, Y., Zhang, X., Song, C., Gong, Z., and Yang, S. (2018). OST 1-mediated BTF 3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J 37.

  • Ding, Y., Li, H., Zhang, X., Xie, Q., Gong, Z., and Yang, S. (2015). OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32, 278–289.

    Article  CAS  PubMed  Google Scholar 

  • Ding, Y., Lv, J., Shi, Y., Gao, J., Hua, J., Song, C., Gong, Z., and Yang, S. (2019). EGR 2 phosphatase regulates OST 1 kinase activity and freezing tolerance in Arabidopsis. EMBO J 38, e99819.

    Article  PubMed  CAS  Google Scholar 

  • Dobermann, A., and Fairhurst, T. (2000). Rice: Nutrient Disorders and Nutrient Management (Potash & Phosphate Institute (PPI), Potash & Phosphate Institute of Canada (PPIC) and International Rice Research Institute (IRRI)).

  • Doherty, C.J., Van Buskirk, H.A., Myers, S.J., and Thomashow, M.F. (2009). Roles for Arabidopsis CAMTA transcription factors in coldregulated gene expression and freezing tolerance. Plant Cell 21, 972–984.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, C.H., Agarwal, M., Zhang, Y., Xie, Q., and Zhu, J.K. (2006). The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103, 8281–8286.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, H., Bai, L., Zhang, Y., Zhang, G., Mao, Y., Min, L., Xiang, F., Qian, D., Zhu, X., and Song, C.P. (2018). Modulation of guard cell turgor and drought tolerance by a peroxisomal acetate–malate shunt. Mol Plant 11, 1278–1291.

    Article  CAS  PubMed  Google Scholar 

  • Dong, J., Ma, G., Sui, L., Wei, M., Satheesh, V., Zhang, R., Ge, S., Li, J., Zhang, T.E., Wittwer, C., et al. (2019). Inositol pyrophosphate InsP8 acts as an intracellular phosphate signal in Arabidopsis. Mol Plant 12, 1463–1473.

    Article  CAS  PubMed  Google Scholar 

  • Dong, M.A., Farré, E.M., and Thomashow, M.F. (2011). Circadian clockassociated 1 and late elongated hypocotyl regulate expression of the Crepeat binding factor (CBF) pathway in Arabidopsis. Proc Natl Acad Sci USA 108, 7241–7246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duszyn, M., Świeżawska, B., Szmidt-Jaworska, A., and Jaworski, K. (2019). Cyclic nucleotide gated channels (CNGCs) in plant signalling—Current knowledge and perspectives. J Plant Physiol 241, 153035.

    Article  CAS  PubMed  Google Scholar 

  • Eisenach, C., Baetz, U., Huck, N.V., Zhang, J., De Angeli, A., Beckers, G.J. M., and Martinoia, E. (2017). ABA-induced stomatal closure involves ALMT4, a phosphorylation-dependent vacuolar anion channel of Arabidopsis. Plant Cell 29, 2552–2569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenhut, M., Roell, M.S., and Weber, A.P.M. (2019). Mechanistic understanding of photorespiration paves the way to a new green revolution. New Phytol 223, 1762–1769.

    Article  PubMed  Google Scholar 

  • El Mahi, H., Pérez-Hormaeche, J., De Luca, A., Villalta, I., Espartero, J., Gámez-Arjona, F., Fernández, J.L., Bundó, M., Mendoza, I., Mieulet, D., et al. (2019). A critical role of sodium flux via the plasma membrane Na+/H+ exchanger SOS1 in the salt tolerance of rice. Plant Physiol 180, 1046–1065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eleftheriou, E.P., Adamakis, I.D.S., Panteris, E., and Fatsiou, M. (2015). Chromium-induced ultrastructural changes and oxidative stress in roots of Arabidopsis thaliana. Int J Med Sci 16, 15852–15871.

    CAS  Google Scholar 

  • Eremina, M., Unterholzner, S.J., Rathnayake, A.I., Castellanos, M., Khan, M., Kugler, K.G., May, S.T., Mayer, K.F.X., Rozhon, W., and Poppenberger, B. (2016). Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. Proc Natl Acad Sci USA 113, E5982–E5991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Essah, P.A., Davenport, R., and Tester, M. (2003). Sodium influx and accumulation in Arabidopsis. Plant Physiol 133, 307–318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fabiañska, I., Gerlach, N., Almario, J., and Bucher, M. (2019). Plantmediated effects of soil phosphorus on the root-associated fungal microbiota in Arabidopsis thaliana. New Phytol 221, 2123–2137.

    Article  PubMed  CAS  Google Scholar 

  • Falcone, D.L., Ogas, J.P., and Somerville, C.R. (2004). Regulation of membrane fatty acid composition by temperature in mutants of Arabidopsis with alterations in membrane lipid composition. BMC Plant Biol 4, 17.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fan, S.K., Fang, X.Z., Guan, M.Y., Ye, Y.Q., Lin, X.Y., Du, S.T., and Jin, C. W. (2014). Exogenous abscisic acid application decreases cadmium accumulation in Arabidopsis plants, which is associated with the inhibition of IRT1-mediated cadmium uptake. Front Plant Sci 5, 721.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fang, X., Zhao, G., Zhang, S., Li, Y., Gu, H., Li, Y., Zhao, Q., and Qi, Y. (2019). Chloroplast-to-nucleus signaling regulates microRNA biogenesis in Arabidopsis. Dev Cell 48, 371–382.e4.

    Article  CAS  PubMed  Google Scholar 

  • Fang, Y., Liao, K., Du, H., Xu, Y., Song, H., Li, X., and Xiong, L. (2015). A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66, 6803–6817.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farooq, M.A., Ali, S., Hameed, A., Bharwana, S.A., Rizwan, M., Ishaque, W., Farid, M., Mahmood, K., and Iqbal, Z. (2016). Cadmium stress in cotton seedlings: Physiological, photosynthesis and oxidative damages alleviated by glycinebetaine. South African J Bot 104, 61–68.

    Article  CAS  Google Scholar 

  • Feng, C.Z., Chen, Y., Wang, C., Kong, Y.H., Wu, W.H., and Chen, Y.F. (2014). Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80, 654–668.

    Article  CAS  PubMed  Google Scholar 

  • Feng, J., Chen, L., and Zuo, J. (2019). Protein S-nitrosylation in plants: Current progresses and challenges. J Integr Plant Biol 61, 1206–1223.

    Article  PubMed  Google Scholar 

  • Feng, W., Kita, D., Peaucelle, A., Cartwright, H.N., Doan, V., Duan, Q., Liu, M.C., Maman, J., Steinhorst, L., Schmitz-Thom, I., et al. (2018). The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28, 666–675.e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein, R.R. (1994). Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5, 765–771.

    Article  Google Scholar 

  • Finkelstein, R.R., Gampala, S.S.L., and Rock, C.D. (2002). Abscisic acid signaling in seeds and seedlings. Plant Cell 14, S15–S45.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein, R.R., and Lynch, T.J. (2000). The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12, 599–609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finkelstein, R.R., Li Wang, M., Lynch, T.J., Rao, S., and Goodman, H.M. (1998). The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. Plant Cell 10, 1043–1054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fliegel, L. (2019). Structural and functional changes in the Na+/H+ exchanger isoform 1, induced by Erk1/2 phosphorylation. Int J Med Sci 20, 2378.

    CAS  Google Scholar 

  • Franklin, K.A., and Whitelam, G.C. (2007). Light-quality regulation of freezing tolerance in Arabidopsis thaliana. Nat Genet 39, 1410–1413.

    Article  CAS  PubMed  Google Scholar 

  • Fujii, H., Chinnusamy, V., Rodrigues, A., Rubio, S., Antoni, R., Park, S.Y., Cutler, S.R., Sheen, J., Rodriguez, P.L., and Zhu, J.K. (2009). In vitro reconstitution of an abscisic acid signalling pathway. Nature 462, 660–664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii, H., Verslues, P.E., and Zhu, J.K. (2007). Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. Plant Cell 19, 485–494.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii, H., and Zhu, J.K. (2009). Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106, 8380–8385.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii, Y., Tanaka, H., Konno, N., Ogasawara, Y., Hamashima, N., Tamura, S., Hasegawa, S., Hayasaki, Y., Okajima, K., and Kodama, Y. (2017). Phototropin perceives temperature based on the lifetime of its photoactivated state. Proc Natl Acad Sci USA 114, 9206–9211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita, Y., Fujita, M., Satoh, R., Maruyama, K., Parvez, M.M., Seki, M., Hiratsu, K., Ohme-Takagi, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17, 3470–3488.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita, Y., Nakashima, K., Yoshida, T., Katagiri, T., Kidokoro, S., Kanamori, N., Umezawa, T., Fujita, M., Maruyama, K., Ishiyama, K., et al. (2009). Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol 50, 2123–2132.

    Article  CAS  PubMed  Google Scholar 

  • Gao, F., Han, X., Wu, J., Zheng, S., Shang, Z., Sun, D., Zhou, R., and Li, B. (2012). A heat-activated calcium-permeable channel—Arabidopsis cyclic nucleotide-gated ion channel 6—is involved in heat shock responses. Plant J 70, 1056–1069.

    Article  CAS  PubMed  Google Scholar 

  • Gao, H., Brandizzi, F., Benning, C., and Larkin, R.M. (2008). A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana. Proc Natl Acad Sci USA 105, 16398–16403.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, X.Q., Li, C.G., Wei, P.C., Zhang, X.Y., Chen, J., and Wang, X.C. (2005). The dynamic changes of tonoplasts in guard cells are important for stomatal movement in Vicia faba. Plant Physiol 139, 1207–1216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaxiola, R.A., Rao, R., Sherman, A., Grisafi, P., Alper, S.L., and Fink, G.R. (1999). The Arabidopsis thaliana proton transporters, AtNhx1 and Avp1, can function in cation detoxification in yeast. Proc Natl Acad Sci USA 96, 1480–1485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ge, K., Liu, X., Li, X., Hu, B., and Li, L. (2017). Isolation of an ABA transporter-like 1 gene from Arachis hypogaea that affects ABA import and reduces ABA sensitivity in Arabidopsis. Front Plant Sci 8, 1150.

    Article  PubMed  PubMed Central  Google Scholar 

  • Geiger, D., Maierhofer, T., Al-Rasheid, K.A.S., Scherzer, S., Mumm, P., Liese, A., Ache, P., Wellmann, C., Marten, I., Grill, E., et al. (2011). Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4, ra32.

    Article  PubMed  CAS  Google Scholar 

  • Geiger, D., Scherzer, S., Mumm, P., Marten, I., Ache, P., Matschi, S., Liese, A., Wellmann, C., Al-Rasheid, K.A.S., Grill, E., et al. (2010). Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107, 8023–8028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geiger, D., Scherzer, S., Mumm, P., Stange, A., Marten, I., Bauer, H., Ache, P., Matschi, S., Liese, A., Al-Rasheid, K.A.S., et al. (2009). Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair. Proc Natl Acad Sci USA 106, 21425–21430.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmour, S.J., Sebolt, A.M., Salazar, M.P., Everard, J.D., and Thomashow, M.F. (2000). Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124, 1854–1865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmour, S.J., Zarka, D.G., Stockinger, E.J., Salazar, M.P., Houghton, J.M., and Thomashow, M.F. (1998). Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16, 433–442.

    Article  CAS  PubMed  Google Scholar 

  • Giraudat, J., Hauge, B.M., Valon, C., Smalle, J., Parcy, F., and Goodman, H.M. (1992). Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4, 1251.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gong, M., van der Luit, A.H., Knight, M.R., and Trewavas, A.J. (1998). Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol 116, 429–437.

    Article  CAS  PubMed Central  Google Scholar 

  • Gong, Z., Dong, C.H., Lee, H., Zhu, J., Xiong, L., Gong, D., Stevenson, B., and Zhu, J.K. (2005). A DEAD box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17, 256–267.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González-Guzmán, M., Apostolova, N., Bellés, J.M., Barrero, J.M., Piqueras, P., Ponce, M.R., Micol, J.L., Serrano, R., and Rodríguez, P. L. (2002). The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde. Plant Cell 14, 1833–1846.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Grabov, A., and Blatt, M.R. (1998). Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells. Proc Natl Acad Sci USA 95, 4778–4783.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grondin, A., Rodrigues, O., Verdoucq, L., Merlot, S., Leonhardt, N., and Maurel, C. (2015). Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27, 1945–1954.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan, Q., Lu, X., Zeng, H., Zhang, Y., and Zhu, J. (2013a). Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74, 840–851.

    Article  CAS  PubMed  Google Scholar 

  • Guan, Q., Wu, J., Zhang, Y., Jiang, C., Liu, R., Chai, C., and Zhu, J. (2013b). A DEAD box RNA helicase is critical for pre-mRNA splicing, cold-responsive gene regulation, and cold tolerance in Arabidopsis. Plant Cell 25, 342–356.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guan, Q., Yue, X., Zeng, H., and Zhu, J. (2014). The protein phosphatase RCF2 and its interacting partner NAC019 are critical for heat stress-esponsive gene regulation and thermotolerance in Arabidopsis. Plant Cell 26, 438–453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, B., Liu, C., Li, H., Yi, K., Ding, N., Li, N., Lin, Y., and Fu, Q. (2016). Endogenous salicylic acid is required for promoting cadmium tolerance of Arabidopsis by modulating glutathione metabolisms. J Hazard Mater 316, 77–86.

    Article  CAS  PubMed  Google Scholar 

  • Guo, X., Liu, D., and Chong, K. (2018). Cold signaling in plants: Insights into mechanisms and regulation. J Integr Plant Biol 60, 745–756.

    Article  PubMed  Google Scholar 

  • Guo, Y., Halfter, U., Ishitani, M., and Zhu, J.K. (2001). Molecular characterization of functional domains in the protein kinase SOS2 that is required for plant salt tolerance. Plant Cell 13, 1383–1400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez-Alanís, D., Yong-Villalobos, L., Jiménez-Sandoval, P., Alatorre-Cobos, F., Oropeza-Aburto, A., Mora-Macías, J., Sánchez-Rodríguez, F., Cruz-Ramírez, A., and Herrera-Estrella, L. (2017). Phosphate starvation-dependent iron mobilization induces CLE14 expression to trigger root meristem differentiation through CLV2/PEPR2 sgnaling. Dev Cell 41, 555–570.e3.

    Article  PubMed  CAS  Google Scholar 

  • Hahn, A., Bublak, D., Schleiff, E., and Scharf, K.D. (2011). Crosstalk between Hsp90 and Hsp70 chaperones and heat stress transcription factors in tomato. Plant Cell 23, 741–755.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamamoto, S., Horie, T., Hauser, F., Deinlein, U., Schroeder, J.I., and Uozumi, N. (2015). HKT transporters mediate salt stress resistance in plants: from structure and function to the field. Curr Opin Biotech 32, 113–120.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, D.W.A., Hills, A., and Blatt, M.R. (2001). Extracellular Ba2+ and voltage interact to gate Ca2+ channels at the plasma membrane of stomatal guard cells. FEBS Lett 491, 99–103.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, D.W.A., Hills, A., Kohler, B., and Blatt, M.R. (2000). Ca2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proc Natl Acad Sci USA 97, 4967–4972.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamilton, E.S., Schlegel, A.M., and Haswell, E.S. (2015). United in diversity: mechanosensitive ion channels in plants. Annu Rev Plant Biol 66, 113–137.

    Article  CAS  PubMed  Google Scholar 

  • Han, J.P., Köster, P., Drerup, M.M., Scholz, M., Li, S., Edel, K.H., Hashimoto, K., Kuchitsu, K., Hippler, M., and Kudla, J. (2019). Finetuning of RBOHF activity is achieved by differential phosphorylation and Ca2+ binding. New Phytol 221, 1935–1949.

    Article  CAS  PubMed  Google Scholar 

  • Hanikenne, M., Talke, I.N., Haydon, M.J., Lanz, C., Nolte, A., Motte, P., Kroymann, J., Weigel, D., and Krämer, U. (2008). Evolution of metal hyperaccumulation required cis-regulatory changes and triplication of HMA4. Nature 453, 391–395.

    Article  CAS  PubMed  Google Scholar 

  • Haruta, M., Sabat, G., Stecker, K., Minkoff, B.B., and Sussman, M.R. (2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408–411.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashi, S., Kuramata, M., Abe, T., Takagi, H., Ozawa, K., and Ishikawa, S. (2017). Phytochelatin synthase OsPCS1 plays a crucial role in reducing arsenic levels in rice grains. Plant J 91, 840–848.

    Article  CAS  PubMed  Google Scholar 

  • Hewezi, T., Piya, S., Qi, M., Balasubramaniam, M., Rice, J.H., and Baum, T.J. (2016). Arabidopsis miR827 mediates post-transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. Plant J 88, 179–192.

    Article  CAS  PubMed  Google Scholar 

  • Ho, C.H., Lin, S.H., Hu, H.C., and Tsay, Y.F. (2009). CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194.

    Article  CAS  PubMed  Google Scholar 

  • Hong, J.H., Savina, M., Du, J., Devendran, A., Kannivadi Ramakanth, K., Tian, X., Sim, W.S., Mironova, V.V., and Xu, J. (2017). A sacrifice-for-survival mechanism protects root stem cell niche from chilling stress. Cell 170, 102–113.e14.

    Article  CAS  PubMed  Google Scholar 

  • Horie, T., Costa, A., Kim, T.H., Han, M.J., Horie, R., Leung, H.Y., Miyao, A., Hirochika, H., An, G., and Schroeder, J.I. (2007). Rice OsHKT2;1 transporter mediates large Na+ influx component into K+-starved roots for growth. EMBO J 26, 3003–3014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou, C., Tian, W., Kleist, T., He, K., Garcia, V., Bai, F., Hao, Y., Luan, S., and Li, L. (2014). DUF221 proteins are a family of osmosensitive calcium-permeable cation channels conserved across eukaryotes. Cell Res 24, 632–635.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, B., and Chu, C. (2020). Nitrogen-phosphorus interplay: old story with molecular tale. New Phytol 225, 1455–1460.

    Article  CAS  PubMed  Google Scholar 

  • Hu, B., Jiang, Z., Wang, W., Qiu, Y., Zhang, Z., Liu, Y., Li, A., Gao, X., Liu, L., Qian, Y., et al. (2019). Nitrate-NRT1.1B-SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat Plants 5, 401–413.

    Article  CAS  PubMed  Google Scholar 

  • Hu, H., Dai, M., Yao, J., Xiao, B., Li, X., Zhang, Q., and Xiong, L. (2006). Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103, 12987–12992.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, Y., Jiang, L., Wang, F., and Yu, D. (2013). Jasmonate regulates the inducer of CBF expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25, 2907–2924.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua, D., Wang, C., He, J., Liao, H., Duan, Y., Zhu, Z., Guo, Y., Chen, Z., and Gong, Z. (2012). A Plasma Membrane Receptor Kinase, GHR1, Mediates Abscisic Acid- and Hydrogen Peroxide-Regulated Stomatal Movement in Arabidopsis. Plant Cell 24, 2546–2561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, A.C., Jiang, T., Liu, Y.X., Bai, Y.C., Reed, J., Qu, B., Goossens, A., Nützmann, H.W., Bai, Y., and Osbourn, A. (2019). A specialized metabolic network selectively modulates Arabidopsis root microbiota. Science 364, eaau6389.

    Article  CAS  PubMed  Google Scholar 

  • Huang, S., Spielmeyer, W., Lagudah, E.S., James, R.A., Platten, J.D., Dennis, E.S., and Munns, R. (2006). A sodium transporter (HKT7) is a candidate for Nax1, a gene for salt tolerance in durum wheat. Plant Physiol 142, 1718–1727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hussain, D., Haydon, M.J., Wang, Y., Wong, E., Sherson, S.M., Young, J., Camakaris, J., Harper, J.F., and Cobbett, C.S. (2004). P-type ATPase heavy metal transporters with roles in essential zinc homeostasis in Arabidopsis. Plant Cell 16, 1327–1339.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda, M., Mitsuda, N., and Ohme-Takagi, M. (2011). Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol 157, 1243–1254.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imes, D., Mumm, P., Böhm, J., Al-Rasheid, K.A.S., Marten, I., Geiger, D., and Hedrich, R. (2013). Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. Plant J 74, 372–382.

    Article  CAS  PubMed  Google Scholar 

  • Irigoyen, M.L., Iniesto, E., Rodriguez, L., Puga, M.I., Yanagawa, Y., Pick, E., Strickland, E., Paz-Ares, J., Wei, N., De Jaeger, G., et al. (2014). Targeted degradation of abscisic acid receptors is mediated by the ubiquitin ligase substrate adaptor DDA1 in Arabidopsis. Plant Cell 26, 712–728.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isayenkov, S.V., and Maathuis, F.J.M. (2019). Plant salinity stress: many unanswered questions remain. Front Plant Sci 10, 80.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ishikawa, S., Ishimaru, Y., Igura, M., Kuramata, M., Abe, T., Senoura, T., Hase, Y., Arao, T., Nishizawa, N.K., and Nakanishi, H. (2012). Ionbeam irradiation, gene identification, and marker-assisted breeding in the development of low-cadmium rice. Proc Natl Acad Sci USA 109, 19166–19171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isner, J.C., Begum, A., Nuehse, T., Hetherington, A.M., and Maathuis, F.J.M. (2018). KIN7 kinase regulates the vacuolar TPK1 K+ channel during stomatal closure. Curr Biol 28, 466–472.e4.

    Article  CAS  PubMed  Google Scholar 

  • Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2001). Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27, 325–333.

    Article  CAS  PubMed  Google Scholar 

  • Jablonska, E., Socha, K., Reszka, E., Wieczorek, E., Skokowski, J., Kalinowski, L., Fendler, W., Seroczynska, B., Wozniak, M., Borawska, M.H., et al. (2017). Cadmium, arsenic, selenium and iron—Implications for tumor progression in breast cancer. Environ Toxicol Pharmacol 53, 151–157.

    Article  CAS  PubMed  Google Scholar 

  • Jafari, A., Kamarehie, B., Ghaderpoori, M., Khoshnamvand, N., and Birjandi, M. (2018). The concentration data of heavy metals in Iranian grown and imported rice and human health hazard assessment. Data Brief 16, 453–459.

    Article  PubMed  Google Scholar 

  • Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., and Thomashow, M.F. (1998). Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280, 104–106.

    Article  CAS  PubMed  Google Scholar 

  • James, R.A., Davenport, R.J., and Munns, R. (2006). Physiological characterization of two genes for Na+ exclusion in durum wheat, Nax1 and Nax2. Plant Physiol 142, 1537–1547.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jammes, F., Song, C., Shin, D., Munemasa, S., Takeda, K., Gu, D., Cho, D., Lee, S., Giordo, R., Sritubtim, S., et al. (2009). MAP kinases MPK9 and MPK12 are preferentially expressed in guard cells and positively regulate ROS-mediated ABA signaling. Proc Natl Acad Sci USA 106, 20520–20525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia, Y., Ding, Y., Shi, Y., Zhang, X., Gong, Z., and Yang, S. (2016). The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis. New Phytol 212, 345–353.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, B., Shi, Y., Zhang, X., Xin, X., Qi, L., Guo, H., Li, J., and Yang, S. (2017). PIF3 is a negative regulator of the CBF pathway and freezing tolerance in Arabidopsis. Proc Natl Acad Sci USA 114, E6695–E6702.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, Z., Zhou, X., Tao, M., Yuan, F., Liu, L., Wu, F., Wu, X., Xiang, Y., Niu, Y., Liu, F., et al. (2019). Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572, 341–346.

    Article  CAS  PubMed  Google Scholar 

  • Jojoa-Cruz, S., Saotome, K., Murthy, S.E., Tsui, C.C.A., Sansom, M.S., Patapoutian, A., and Ward, A.B. (2018). Cryo-EM structure of the mechanically activated ion channel OSCA1.2. eLife 7, e41845.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jung, J.H., Domijan, M., Klose, C., Biswas, S., Ezer, D., Gao, M., Khattak, A.K., Box, M.S., Charoensawan, V., Cortijo, S., et al. (2016). Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889.

    Article  CAS  PubMed  Google Scholar 

  • Kamiya, T., Tanaka, M., Mitani, N., Ma, J.F., Maeshima, M., and Fujiwara, T. (2009). NIP1;1, an aquaporin homolog, determines the arsenite sensitivity of Arabidopsis thaliana. J Biol Chem 284, 2114–2120.

    Article  CAS  PubMed  Google Scholar 

  • Kang, J., Hwang, J.U., Lee, M., Kim, Y.Y., Assmann, S.M., Martinoia, E., and Lee, Y. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci USA 107, 2355–2360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karmous, I., Trevisan, R., El Ferjani, E., Chaoui, A., and Sheehan, D. (2017). Redox biology response in germinating Phaseolus vulgaris seeds exposed to copper: Evidence for differential redox buffering in seedlings and cotyledon. PLoS ONE 12, e0184396.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Katiyar-Agarwal, S., Zhu, J., Kim, K., Agarwal, M., Fu, X., Huang, A., and Zhu, J.K. (2006). The plasma membrane Na+/H+ antiporter SOS1 interacts with RCD1 and functions in oxidative stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 103, 18816–18821.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan, G.A., Vogiatzaki, E., Glauser, G., and Poirier, Y. (2016). Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory. Plant Physiol 171, 632–644.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiba, T., Inaba, J., Kudo, T., Ueda, N., Konishi, M., Mitsuda, N., Takiguchi, Y., Kondou, Y., Yoshizumi, T., Ohme-Takagi, M., et al. (2018). Repression of nitrogen starvation responses by members of the Arabidopsis GARP-type transcription factor NIGT1/HRS1 subfamily. Plant Cell 30, 925–945.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidokoro, S., Maruyama, K., Nakashima, K., Imura, Y., Narusaka, Y., Shinwari, Z.K., Osakabe, Y., Fujita, Y., Mizoi, J., Shinozaki, K., et al. (2009). The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol 151, 2046–2057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kidokoro, S., Yoneda, K., Takasaki, H., Takahashi, F., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2017). Different cold-signaling pathways function in the responses to rapid and gradual decreases in temperature. Plant Cell 29, 760–774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, H.J., Hyun, Y., Park, J.Y., Park, M.J., Park, M.K., Kim, M.D., Kim, H. J., Lee, M.H., Moon, J., Lee, I., et al. (2004a). A genetic link between cold responses and flowering time through FVE in Arabidopsis thaliana. Nat Genet 36, 167–171.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J.M., Sasaki, T., Ueda, M., Sako, K., and Seki, M. (2015). Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6, 114.

    PubMed  PubMed Central  Google Scholar 

  • Kim, J.S., Mizoi, J., Kidokoro, S., Maruyama, K., Nakajima, J., Nakashima, K., Mitsuda, N., Takiguchi, Y., Ohme-Takagi, M., Kondou, Y., et al. (2012). Arabidopsis GROWTH-REGULATING FACTOR7 functions as a transcriptional repressor of abscisic acid- and osmotic stress-responsive genes, including DREB2A. Plant Cell 24, 3393–3405.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, S., Kang, J.Y., Cho, D.I., Park, J.H., and Kim, S.Y. (2004b). ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40, 75–87.

  • Kim, T.H., Böhmer, M., Hu, H., Nishimura, N., and Schroeder, J.I. (2010). Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61, 561–591.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, W.Y., Ali, Z., Park, H.J., Park, S.J., Cha, J.Y., Perez-Hormaeche, J., Quintero, F.J., Shin, G., Kim, M.R., Qiang, Z., et al. (2013). Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in Arabidopsis. Nat Commun 4, 1352.

    Article  PubMed  CAS  Google Scholar 

  • Kim, W.Y., Fujiwara, S., Suh, S.S., Kim, J., Kim, Y., Han, L., David, K., Putterill, J., Nam, H.G., and Somers, D.E. (2007). ZEITLUPE is a circadian photoreceptor stabilized by GIGANTEA in blue light. Nature 449, 356–360.

    Article  CAS  PubMed  Google Scholar 

  • Kindgren, P., Ard, R., Ivanov, M., and Marquardt, S. (2018). Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nat Commun 9, 4561.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Knight, H., Trewavas, A.J., and Knight, M.R. (1996). Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation.. Plant Cell 8, 489–503.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, A., Takahashi, A., Kakimoto, Y., Miyazawa, Y., Fujii, N., Higashitani, A., and Takahashi, H. (2007). A gene essential for hydrotropism in roots. Proc Natl Acad Sci USA 104, 4724–4729.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, N.I., Yamaji, N., Yamamoto, H., Okubo, K., Ueno, H., Costa, A., Tanoi, K., Matsumura, H., Fujii-Kashino, M., Horiuchi, T., et al. (2017). OsHKT1;5 mediates Na+ exclusion in the vasculature to protect leaf blades and reproductive tissues from salt toxicity in rice. Plant J 91, 657–670.

    Article  CAS  PubMed  Google Scholar 

  • Kong, L., Cheng, J., Zhu, Y., Ding, Y., Meng, J., Chen, Z., Xie, Q., Guo, Y., Li, J., Yang, S., et al. (2015). Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat Commun 6, 8630.

    Article  CAS  PubMed  Google Scholar 

  • Königshofer, H., Tromballa, H.W., and Löppert, H.G. (2008). Early events in signalling high-temperature stress in tobacco BY2 cells involve alterations in membrane fluidity and enhanced hydrogen peroxide production. Plant Cell Environ 31, 1771–1780.

    Article  PubMed  CAS  Google Scholar 

  • Koornneef, M., Jorna, M.L., Brinkhorst-van der Swan, D.L.C., and Karssen, C.M. (1982). The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh.. Theoret Appl Genet 61, 385–393.

    Article  CAS  Google Scholar 

  • Koornneef, M., Reuling, G., and Karssen, C.M. (1984). The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol Plant 61, 377–383.

    Article  CAS  Google Scholar 

  • Koprivova, A., Schuck, S., Jacoby, R.P., Klinkhammer, I., Welter, B., Leson, L., Martyn, A., Nauen, J., Grabenhorst, N., Mandelkow, J.F., et al. (2019). Root-specific camalexin biosynthesis controls the plant growth-promoting effects of multiple bacterial strains. Proc Natl Acad Sci USA 116, 15735–15744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotak, S., Larkindale, J., Lee, U., von Koskull-Döring, P., Vierling, E., and Scharf, K.D. (2007a). Complexity of the heat stress response in plants. Curr Opin Plant Biol 10, 310–316.

    Article  CAS  PubMed  Google Scholar 

  • Kotak, S., Vierling, E., Bäumlein, H., and von Koskull-Döring, P. (2007b). A novel transcriptional cascade regulating expression of heat stress proteins during seed development of Arabidopsis. Plant Cell 19, 182–195.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kragelund, B.B., Jensen, M.K., and Skriver, K. (2012). Order by disorder in plant signaling. Trends Plant Sci 17, 625–632.

    Article  CAS  PubMed  Google Scholar 

  • Krochko, J.E., Abrams, G.D., Loewen, M.K., Abrams, S.R., and Cutler, A. J. (1998). (+)-Abscisic acid 8′-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol 118, 849–860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M., Kummer, U., Parniske, M., Romeis, T., and Schumacher, K. (2018). Advances and current challenges in calcium signaling. New Phytol 218, 414–431.

    Article  PubMed  Google Scholar 

  • Kumar, D., Kumar, R., Baek, D., Hyun, T.K., Chung, W.S., Yun, D.J., and Kim, J.Y. (2017). Arabidopsis thaliana RECEPTOR DEAD KINASE1 functions as a positive regulator in plant responses to ABA. Mol Plant 10, 223–243.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S.V., and Wigge, P.A. (2010). H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140, 136–147.

    Article  CAS  PubMed  Google Scholar 

  • Kuromori, T., Miyaji, T., Yabuuchi, H., Shimizu, H., Sugimoto, E., Kamiya, A., Moriyama, Y., and Shinozaki, K. (2010). ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107, 2361–2366.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuromori, T., Sugimoto, E., and Shinozaki, K. (2011). Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. Plant J 67, 885–894.

    Article  CAS  PubMed  Google Scholar 

  • Kushiro, T., Okamoto, M., Nakabayashi, K., Yamagishi, K., Kitamura, S., Asami, T., Hirai, N., Koshiba, T., Kamiya, Y., and Nambara, E. (2004). The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′- hydroxylases: key enzymes in ABA catabolism. EMBO J 23, 1647–1656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkindale, J., Hall, J.D., Knight, M.R., and Vierling, E. (2005). Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138, 882–897.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkindale, J., and Huang, B. (2004). Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. J Plant Physiol 161, 405–413.

    Article  CAS  PubMed  Google Scholar 

  • Larsson, S.C., Orsini, N., and Wolk, A. (2015). Urinary cadmium concentration and risk of breast cancer: a systematic review and dose-response meta-analysis. Am J Epidemiol 182, 375–380.

    Article  PubMed  Google Scholar 

  • Lee, B., Kapoor, A., Zhu, J., and Zhu, J.K. (2006a). STABILIZED1, a stress-upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18, 1736–1749.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, C.M., and Thomashow, M.F. (2012). Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci USA 109, 15054–15059.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, K.H., Piao, H.L., Kim, H.Y., Choi, S.M., Jiang, F., Hartung, W., Hwang, I., Kwak, J.M., Lee, I.J., and Hwang, I. (2006b). Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109–1120.

    Article  CAS  PubMed  Google Scholar 

  • Lee, U., Rioflorido, I., Hong, S.W., Larkindale, J., Waters, E.R., and Vierling, E. (2007). The Arabidopsis ClpB/Hsp100 family of proteins: chaperones for stress and chloroplast development. Plant J 49, 115–127.

    Article  CAS  PubMed  Google Scholar 

  • Legris, M., Klose, C., Burgie, E.S., Rojas, C.C.R., Neme, M., Hiltbrunner, A., Wigge, P.A., Schäfer, E., Vierstra, R.D., and Casal, J.J. (2016). Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354, 897–900.

    Article  CAS  PubMed  Google Scholar 

  • Lei, G.J., Sun, L., Sun, Y., Zhu, X.F., Li, G.X., and Zheng, S.J. (2020). Jasmonic acid alleviates cadmium toxicity in Arabidopsis via suppression of cadmium uptake and translocation. J Integr Plant Biol 62, 218–227.

    Article  CAS  PubMed  Google Scholar 

  • Leung, J., Bouvier-Durand, M., Morris, P.C., Guerrier, D., Chefdor, F., and Giraudat, J. (1994). Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264, 1448–1452.

    Article  CAS  PubMed  Google Scholar 

  • Leung, J., Merlot, S., and Giraudat, J. (1997). The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9, 759.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li, B., Gao, Z., Liu, X., Sun, D., and Tang, W. (2019a). Transcriptional Profiling Reveals a Time-of-Day-Specific Role of REVEILLE 4/8 in Regulating the First Wave of Heat Shock–Induced Gene Expression in Arabidopsis. Plant Cell 31, 2353–2369.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, H., Ding, Y., Shi, Y., Zhang, X., Zhang, S., Gong, Z., and Yang, S. (2017a). MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43, 630–642.e4.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Ye, K., Shi, Y., Cheng, J., Zhang, X., and Yang, S. (2017b). BZR1 positively regulates freezing tolerance via CBF-dependent and CBFindependent pathways in Arabidopsis. Mol Plant 10, 545–559.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Li, Y., Zhao, Q., Li, T., Wei, J., Li, B., Shen, W., Yang, C., Zeng, Y., Rodriguez, P.L., et al. (2019b). The plant ESCRT component FREE1 shuttles to the nucleus to attenuate abscisic acid signalling. Nat Plants 5, 512–524.

    Article  CAS  PubMed  Google Scholar 

  • Li, S., Tian, Y., Wu, K., Ye, Y., Yu, J., Zhang, J., Liu, Q., Hu, M., Li, H., Tong, Y., et al. (2018a). Modulating plant growth–metabolism coordination for sustainable agriculture. Nature 560, 595–600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, W., de Ollas, C., and Dodd, I.C. (2018b). Long-distance ABA transport can mediate distal tissue responses by affecting local ABA concentrations. J Integr Plant Biol 60, 16–33.

    Article  CAS  PubMed  Google Scholar 

  • Li, X., Ma, D., Lu, S.X., Hu, X., Huang, R., Liang, T., Xu, T., Tobin, E.M., and Liu, H. (2016). Blue light- and low temperature-regulated COR27 and COR28 play roles in the Arabidopsis circadian clock. Plant Cell 28, 2755–2769.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, X.M., Chao, D.Y., Wu, Y., Huang, X., Chen, K., Cui, L.G., Su, L., Ye, W.W., Chen, H., Chen, H.C., et al. (2015). Natural alleles of a proteasome α2 subunit gene contribute to thermotolerance and adaptation of African rice. Nat Genet 47, 827–833.

    Article  CAS  PubMed  Google Scholar 

  • Li, Y., Gu, M., Zhang, X., Zhang, J., Fan, H., Li, P., Li, Z., and Xu, G. (2014). Engineering a sensitive visual-tracking reporter system for realtime monitoring phosphorus deficiency in tobacco. Plant Biotechnol J 12, 674–684.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z., Li, Z., Gao, X., Chinnusamy, V., Bressan, R., Wang, Z.X., Zhu, J.K., Wu, J.W., and Liu, D. (2012). ROP11 GTPase negatively regulates ABA signaling by protecting ABI1 phosphatase activity from inhibition by the ABA receptor RCAR1/PYL9 in Arabidopsis. J Integr Plant Biol 54, 180–188.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang, X., and Zhou, J.M. (2018). Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol 69, 267–299.

    Article  CAS  PubMed  Google Scholar 

  • Lin, H., Yang, Y., Quan, R., Mendoza, I., Wu, Y., Du, W., Zhao, S., Schumaker, K.S., Pardo, J.M., and Guo, Y. (2009). Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis. Plant Cell 21, 1607–1619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, M., Chai, K., Ko, S., Kuang, L., Lur, H.S., and Charng, Y. (2014). A positive feedback Loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol 164, 2045–2053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin, Z., Li, Y., Zhang, Z., Liu, X., Hsu, C.C., Du, Y., Sang, T., Zhu, C., Wang, Y., Satheesh, V., et al. (2020). A RAF-SnRK2 kinase cascade mediates early osmotic stress signaling in higher plants. Nat Commun 11, 613.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindsay, E.R., and Maathuis, F.J.M. (2016). Arabidopsis thaliana NIP7;1 is involved in tissue arsenic distribution and tolerance in response to arsenate. FEBS Lett 590, 779–786.

    Article  CAS  PubMed  Google Scholar 

  • Liu, C.L., Gao, Z.Y., Shang, L.G., Yang, C.H., Ruan, B.P., Zeng, D.L., Guo, L.B., Zhao, F.J., Huang, C.F., and Qian, Q. (2020). Natural variation in the promoter of OsHMA3 contributes to differential grain cadmium accumulation between Indica and Japonica rice. J Integr Plant Biol 62, 314–329.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Zhang, C., Yang, J., Yu, N., and Wang, E. (2018a). Hormone modulation of legume-rhizobial symbiosis. J Integr Plant Biol 60, 632–648.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H., Zhao, H., Wu, L., Liu, A., Zhao, F.J., and Xu, W. (2017a). Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulator Sedum plumbizincicola. New Phytol 215, 687–698.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H.C., Liao, H.T., and Charng, Y.Y. (2011). The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ 34, 738–751.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H.T., Gao, F., Li, G.L., Han, J.L., Liu, D.L., Sun, D.Y., and Zhou, R.G. (2008). The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55, 760–773.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H.T., Li, G.L., Chang, H., Sun, D.Y., Zhou, R.G., and Li, B. (2007). Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant Cell Environ 30, 156–164.

    Article  CAS  PubMed  Google Scholar 

  • Liu, H.T., Sun, D.Y., and Zhou, R.G. (2010). Ca2+ and AtCaM3 are involved in the expression of heat shock protein gene in Arabidopsis. Plant Cell Environ 28, 1276–1284.

    Article  Google Scholar 

  • Liu, J., Ishitani, M., Halfter, U., Kim, C.S., and Zhu, J.K. (2000). The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97, 3730–3734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, J., and Zhu, J.K. (1998). A calcium sensor homolog required for plant salt tolerance. Science 280, 1943–1945.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J., Zhang, C., Wei, C., Liu, X., Wang, M., Yu, F., Xie, Q., and Tu, J. (2016). The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice. Plant Physiol 170, 429–443.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J., Shi, Y., and Yang, S. (2018b). Insights into the regulation of Crepeat binding factors in plant cold signaling. J Integr Plant Biol 60, 780–795.

    Article  PubMed  Google Scholar 

  • Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998). Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10, 1391–1406.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, X., Wang, J., and Sun, L. (2018c). Structure of the hyperosmolality-gated calcium-permeable channel OSCA1.2. Nat Commun 9, 5060.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu, Y., and Bassham, D.C. (2012). Autophagy: Pathways for self-eating in plant cells. Annu Rev Plant Biol 63, 215–237.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Z., Jia, Y., Ding, Y., Shi, Y., Li, Z., Guo, Y., Gong, Z., and Yang, S. (2017b). Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell 66, 117–128.e5.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Z., Yan, J.P., Li, D.K., Luo, Q., Yan, Q., Liu, Z.B., Ye, L.M., Wang, J. M., Li, X.F., and Yang, Y. (2015). UDP-glucosyltransferase71c5, a major glucosyltransferase, mediates abscisic acid homeostasis in Arabidopsis. Plant Physiol 167, 1659–1670.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo, J.S., Huang, J., Zeng, D.L., Peng, J.S., Zhang, G.B., Ma, H.L., Guan, Y., Yi, H.Y., Fu, Y.L., Han, B., et al. (2018). A defensin-like protein drives cadmium efflux and allocation in rice. Nat Commun 9, 645.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lv, Q., Zhong, Y., Wang, Y., Wang, Z., Zhang, L., Shi, J., Wu, Z., Liu, Y., Mao, C., Yi, K., et al. (2014). SPX4 negatively regulates phosphate signaling and homeostasis through its interaction with PHR2 in rice. Plant Cell 26, 1586–1597.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, J.F., Yamaji, N., Mitani, N., Xu, X.Y., Su, Y.H., McGrath, S.P., and Zhao, F.J. (2008). Transporters of arsenite in rice and their role in arsenic accumulation in rice grain. Proc Natl Acad Sci USA 105, 9931–9935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma, L., Ye, J., Yang, Y., Lin, H., Yue, L., Luo, J., Long, Y., Fu, H., Liu, X., Zhang, Y., et al. (2019). The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev Cell 48, 697–709.e5.

    Article  CAS  PubMed  Google Scholar 

  • Ma, Y., Dai, X., Xu, Y., Luo, W., Zheng, X., Zeng, D., Pan, Y., Lin, X., Liu, H., Zhang, D., et al. (2015). COLD1 confers chilling tolerance in rice. Cell 160, 1209–1221.

    Article  CAS  PubMed  Google Scholar 

  • Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., and Grill, E. (2009). Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064–1068.

    Article  CAS  PubMed  Google Scholar 

  • Maeda, Y., Konishi, M., Kiba, T., Sakuraba, Y., Sawaki, N., Kurai, T., Ueda, Y., Sakakibara, H., and Yanagisawa, S. (2018). A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat Commun 9, 1376.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maierhofer, T., Diekmann, M., Offenborn, J.N., Lind, C., Bauer, H., Hashimoto, K.S., Al-Rasheid, K.A., Luan, S., Kudla, J., Geiger, D., et al. (2014). Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Sci Signal 7, ra86.

    Article  PubMed  CAS  Google Scholar 

  • Maity, K., Heumann, J.M., McGrath, A.P., Kopcho, N.J., Hsu, P.K., Lee, C. W., Mapes, J.H., Garza, D., Krishnan, S., Morgan, G.P., et al. (2019). Cryo-EM structure of OSCA1.2 from Oryza sativa elucidates the mechanical basis of potential membrane hyperosmolality gating. Proc Natl Acad Sci USA 116, 14309–14318.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mao, H., Wang, H., Liu, S., Li, Z., Yang, X., Yan, J., Li, J., Tran, L.S.P., and Qin, F. (2015). A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6, 8326.

    Article  CAS  PubMed  Google Scholar 

  • Marchive, C., Roudier, F., Castaings, L., Bréhaut, V., Blondet, E., Colot, V., Meyer, C., and Krapp, A. (2013). Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat Commun 4, 1713.

    Article  PubMed  CAS  Google Scholar 

  • Martinière, A., Lavagi, I., Nageswaran, G., Rolfe, D.J., Maneta-Peyret, L., Luu, D.T., Botchway, S.W., Webb, S.E.D., Mongrand, S., Maurel, C., et al. (2012). Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci USA 109, 12805–12810.

    Article  PubMed  PubMed Central  Google Scholar 

  • Maruyama, K., Todaka, D., Mizoi, J., Yoshida, T., Kidokoro, S., Matsukura, S., Takasaki, H., Sakurai, T., Yamamoto, Y.Y., Yoshiwara, K., et al. (2012). Identification of cis-acting promoter elements in coldand dehydration-induced transcriptional pathways in Arabidopsis, rice, and soybean. DNA Res 19, 37–49.

    Article  CAS  PubMed  Google Scholar 

  • Maruyama, K., Urano, K., Yoshiwara, K., Morishita, Y., Sakurai, N., Suzuki, H., Kojima, M., Sakakibara, H., Shibata, D., Saito, K., et al. (2014). Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant Physiol 164, 1759–1771.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mäser, P., Eckelman, B., Vaidyanathan, R., Horie, T., Fairbairn, D.J., Kubo, M., Yamagami, M., Yamaguchi, K., Nishimura, M., Uozumi, N., et al. (2002). Altered shoot/root Na+ distribution and bifurcating salt sensitivity in Arabidopsis by genetic disruption of the Na+ transporter AtHKT1. FEBS Lett 531, 157–161.

    Article  PubMed  Google Scholar 

  • McAinsh, M.R., and Pittman, J.K. (2009). Shaping the calcium signature. New Phytol 181, 275–294.

    Article  CAS  PubMed  Google Scholar 

  • McClung, C.R., and Davis, S.J. (2010). Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Curr Biol 20, R1086–R1092.

    Article  CAS  PubMed  Google Scholar 

  • Melcher, K., Ng, L.M., Zhou, X.E., Soon, F.F., Xu, Y., Suino-Powell, K.M., Park, S.Y., Weiner, J.J., Fujii, H., Chinnusamy, V., et al. (2009). A gatelatch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462, 602–608.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer, K., Leube, M.P., and Grill, E. (1994). A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 1452–1455.

    Article  CAS  PubMed  Google Scholar 

  • Meyer, S., Mumm, P., Imes, D., Endler, A., Weder, B., Al-Rasheid, K.A.S., Geiger, D., Marten, I., Martinoia, E., and Hedrich, R. (2010). AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63, 1054–1062.

    Article  CAS  PubMed  Google Scholar 

  • Miller, M.J., Barrett-Wilt, G.A., Hua, Z., and Vierstra, R.D. (2010). Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc Natl Acad Sci USA 107, 16512–16517.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra, S.K., Tripp, J., Winkelhaus, S., Tschiersch, B., Theres, K., Nover, L., and Scharf, K.D. (2002). In the complex family of heat stress transcription factors, HSfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16, 1555–1567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura, K., Jin, J.B., Lee, J., Yoo, C.Y., Stirm, V., Miura, T., Ashworth, E. N., Bressan, R.A., Yun, D.J., and Hasegawa, P.M. (2007). SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19, 1403–1414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura, K., Ohta, M., Nakazawa, M., Ono, M., and Hasegawa, P.M. (2011). ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J 67, 269–279.

    Article  CAS  PubMed  Google Scholar 

  • Miyazono, K.I., Miyakawa, T., Sawano, Y., Kubota, K., Kang, H.J., Asano, A., Miyauchi, Y., Takahashi, M., Zhi, Y., Fujita, Y., et al. (2009). Structural basis of abscisic acid signalling. Nature 462, 609–614.

    Article  CAS  PubMed  Google Scholar 

  • Møller, I.S., Gilliham, M., Jha, D., Mayo, G.M., Roy, S.J., Coates, J.C., Haseloff, J., and Tester, M. (2009). Shoot Na+ exclusion and increased salinity tolerance engineered by cell type-specific alteration of Na+ transport in Arabidopsis. Plant Cell 21, 2163–2178.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mora-Macías, J., Ojeda-Rivera, J.O., Gutiérrez-Alanís, D., Yong-Villalobos, L., Oropeza-Aburto, A., Raya-González, J., Jiménez-Domínguez, G., Chávez-Calvillo, G., Rellán-Álvarez, R., and Herrera-Estrella, L. (2017). Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci USA 114, E3563–E3572.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Mori, I.C., Murata, Y., Yang, Y., Munemasa, S., Wang, Y.F., Andreoli, S., Tiriac, H., Alonso, J.M., Harper, J.F., Ecker, J.R., et al. (2006). CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+-permeable channels and stomatal closure. PLoS Biol 4, e327.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morimoto, K., Mizoi, J., Qin, F., Kim, J.S., Sato, H., Osakabe, Y., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2013). Stabilization of Arabidopsis DREB2A is required but not sufficient for the induction of target genes under conditions of stress. PLoS ONE 8, e80457.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Morton, M.J.L., Awlia, M., Al-Tamimi, N., Saade, S., Pailles, Y., Negrão, S., and Tester, M. (2019). Salt stress under the scalpel – Dissecting the genetics of salt tolerance. Plant J 97, 148–163.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Müller, D.B., Vogel, C., Bai, Y., and Vorholt, J.A. (2016). The plant microbiota: systems-level insights and perspectives. Annu Rev Genet 50, 211–234.

    Article  PubMed  CAS  Google Scholar 

  • Munns, R., James, R.A., Xu, B., Athman, A., Conn, S.J., Jordans, C., Byrt, C.S., Hare, R.A., Tyerman, S.D., Tester, M., et al. (2012). Wheat grain yield on saline soils is improved by an ancestral Na+ transporter gene. Nat Biotechnol 30, 360–364.

    Article  CAS  PubMed  Google Scholar 

  • Murata, Y., Pei, Z.M., Mori, I.C., and Schroeder, J. (2001). Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell 13, 2513–2523.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murthy, S.E., Dubin, A.E., Whitwam, T., Jojoa-Cruz, S., Cahalan, S.M., Mousavi, S.A.R., Ward, A.B., and Patapoutian, A. (2018). OSCA/TMEM63 are an Evolutionarily Conserved Family of Mechanically Activated Ion Channels. eLife 7, e41844.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mustilli, A.C., Merlot, S., Vavasseur, A., Fenzi, F., and Giraudat, J. (2002). Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14, 3089–3099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima, K., Fujita, Y., Kanamori, N., Katagiri, T., Umezawa, T., Kidokoro, S., Maruyama, K., Yoshida, T., Ishiyama, K., Kobayashi, M., et al. (2009). Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50, 1345–1363.

    Article  CAS  PubMed  Google Scholar 

  • Nakashima, K., Tran, L.S.P., Van Nguyen, D., Fujita, M., Maruyama, K., Todaka, D., Ito, Y., Hayashi, N., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51, 617–630.

    Article  CAS  PubMed  Google Scholar 

  • Negi, J., Matsuda, O., Nagasawa, T., Oba, Y., Takahashi, H., Kawai-Yamada, M., Uchimiya, H., Hashimoto, M., and Iba, K. (2008). CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452, 483–486.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, D.E., Repetti, P.P., Adams, T.R., Creelman, R.A., Wu, J., Warner, D.C., Anstrom, D.C., Bensen, R.J., Castiglioni, P.P., Donnarummo, M. G., et al. (2007). Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proc Natl Acad Sci USA 104, 16450–16455.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura, N., Hitomi, K., Arvai, A.S., Rambo, R.P., Hitomi, C., Cutler, S. R., Schroeder, J.I., and Getzoff, E.D. (2009). Structural mechanism of abscisic acid binding and signaling by dimeric PYR1. Science 326, 1373–1379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishizawa-Yokoi, A., Nosaka, R., Hayashi, H., Tainaka, H., Maruta, T., Tamoi, M., Ikeda, M., Ohme-Takagi, M., Yoshimura, K., Yabuta, Y., et al. (2011). HsfA1d and HsfA1e involved in the transcriptional regulation of HsfA2 function as key regulators for the Hsf signaling network in response to environmental stress. Plant Cell Physiol 52, 933–945.

    Article  CAS  PubMed  Google Scholar 

  • Niyogi, K.K., Grossman, A.R., and Björkman, O. (1998). Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10, 1121–1134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nocito, F.F., Lancilli, C., Dendena, B., Lucchini, G., and Sacchi, G.A. (2011). Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant Cell Environ 34, 994–1008.

    Article  CAS  PubMed  Google Scholar 

  • Norén, L., Kindgren, P., Stachula, P., Rühl, M., Eriksson, M.E., Hurry, V., and Strand, Å. (2016). HSP90, ZTL, PRR5 and HY5 integrate circadian and plastid signaling pathways to regulate CBF and COR expression. Plant Physiol 171, 1392–1406.

    PubMed  PubMed Central  Google Scholar 

  • Ohama, N., Sato, H., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2017). Transcriptional regulatory network of plant heat stress response. Trends Plant Sci 22, 53–65.

    Article  CAS  PubMed  Google Scholar 

  • Ohta, M., Guo, Y., Halfter, U., and Zhu, J.K. (2003). A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100, 11771–11776.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okamoto, M., Tanaka, Y., Abrams, S.R., Kamiya, Y., Seki, M., and Nambara, E. (2009). High humidity induces abscisic acid 8′-hydroxylase in stomata and vasculature to regulate local and systemic abscisic acid responses in Arabidopsis. Plant Physiol 149, 825–834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, J., Lim, C.J., Shen, M., Park, H.J., Cha, J.Y., Iniesto, E., Rubio, V., Mengiste, T., Zhu, J.K., Bressan, R.A., et al. (2018). Epigenetic switch from repressive to permissive chromatin in response to cold stress. Proc Natl Acad Sci USA 115, E5400–E5409.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park, S., Lee, C.M., Doherty, C.J., Gilmour, S.J., Kim, Y.S., and Thomashow, M.F. (2015). Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network. Plant J 82, 193–207.

    Article  CAS  PubMed  Google Scholar 

  • Park, S.Y., Fung, P., Nishimura, N., Jensen, D.R., Fujii, H., Zhao, Y., Lumba, S., Santiago, J., Rodrigues, A., Chow, T.F.F., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068–1071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park, Y., Xu, Z.Y., Kim, S.Y., Lee, J., Choi, B., Lee, J., Kim, H., Sim, H.J., and Hwang, I. (2016). Spatial regulation of ABCG25, an ABA exporter, is an important component of the mechanism controlling cellular ABA levels. Plant Cell 28, 2528–2544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pei, Z.M., Murata, Y., Benning, G., Thomine, S., Klüsener, B., Allen, G.J., Grill, E., and Schroeder, J.I. (2000). Calcium channels activated by hydrogen peroxide mediate abscisic acidsignalling in guard cells. Nature 406, 731–734.

    Article  CAS  PubMed  Google Scholar 

  • Peng, S., Huang, J., Sheehy, J.E., Laza, R.C., Visperas, R.M., Zhong, X., Centeno, G.S., Khush, G.S., and Cassman, K.G. (2004). Rice yields decline with higher night temperature from global warming. Proc Natl Acad Sci USA 101, 9971–9975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petersen, E.N., Chung, H.W., Nayebosadri, A., and Hansen, S.B. (2016). Kinetic disruption of lipid rafts is a mechanosensor for phospholipase D. Nat Commun 7, 13873.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Priest, D.M., Ambrose, S.J., Vaistij, F.E., Elias, L., Higgins, G.S., Ross, A. R.S., Abrams, S.R., and Bowles, D.J. (2006). Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana. Plant J 46, 492–502.

    Article  CAS  PubMed  Google Scholar 

  • Puga, M.I., Mateos, I., Charukesi, R., Wang, Z., Franco-Zorrilla, J.M., de Lorenzo, L., Irigoyen, M.L., Masiero, S., Bustos, R., Rodríguez, J., et al. (2014). SPX1 is a phosphate-dependent inhibitor of Phosphate Starvation Response 1 in Arabidopsis. Proc Natl Acad Sci USA 111, 14947–14952.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi, J., Song, C.P., Wang, B., Zhou, J., Kangasjärvi, J., Zhu, J.K., and Gong, Z. (2018). Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack. J Integr Plant Biol 60, 805–826.

    Article  CAS  PubMed  Google Scholar 

  • Qiao, B., Zhang, Q., Liu, D., Wang, H., Yin, J., Wang, R., He, M., Cui, M., Shang, Z., Wang, D., et al. (2015). A calcium-binding protein, rice annexin OsANN1, enhances heat stress tolerance by modulating the production of H2O2. J Exp Bot 66, 5853–5866.

    Article  CAS  PubMed  Google Scholar 

  • Qin, F., Kakimoto, M., Sakuma, Y., Maruyama, K., Osakabe, Y., Tran, L.S. P., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2007). Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50, 54–69.

    Article  CAS  PubMed  Google Scholar 

  • Qin, F., Sakuma, Y., Tran, L.S.P., Maruyama, K., Kidokoro, S., Fujita, Y., Fujita, M., Umezawa, T., Sawano, Y., Miyazono, K.I., et al. (2008). Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20, 1693–1707.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin, T., Tian, Q., Wang, G., and Xiong, L. (2019). LOWER TEMPERATURE 1 enhances ABA responses and plant drought tolerance by modulating the stability and localization of C2-domain ABA-related proteins in Arabidopsis. Mol Plant 12, 1243–1258.

    Article  CAS  PubMed  Google Scholar 

  • Quan, R., Lin, H., Mendoza, I., Zhang, Y., Cao, W., Yang, Y., Shang, M., Chen, S., Pardo, J.M., and Guo, Y. (2007). SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19, 1415–1431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quintero, F.J., Martinez-Atienza, J., Villalta, I., Jiang, X., Kim, W.Y., Ali, Z., Fujii, H., Mendoza, I., Yun, D.J., Zhu, J.K., et al. (2011). Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci USA 108, 2611–2616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quintero, F.J., Ohta, M., Shi, H., Zhu, J.K., and Pardo, J.M. (2002). Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci USA 99, 9061–9066.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavendra, A.S., Gonugunta, V.K., Christmann, A., and Grill, E. (2010). ABA perception and signalling. Trends Plant Sci 15, 395–401.

    Article  CAS  PubMed  Google Scholar 

  • Reguera, M., Bassil, E., Tajima, H., Wimmer, M., Chanoca, A., Otegui, M. S., Paris, N., and Blumwald, E. (2015). pH regulation by NHX-Type antiporters is required for receptor-mediated protein trafficking to the vacuole in Arabidopsis. Plant Cell 27, 1200–1217.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reindl, A., Schöffl, F., Schell, J., Koncz, C., and Bakó, L. (1997). Phosphorylation by a cyclin-dependent kinase modulates DNA binding of the Arabidopsis heat-shock transcription factor HSF1 in vitro. Plant Physiol 115, 93–100.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren, S.C., Song, X.F., Chen, W.Q., Lu, R., Lucas, W.J., and Liu, C.M. (2019). CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex. J Integr Plant Biol 61, 1043–1061.

    CAS  PubMed  Google Scholar 

  • Ren, X., Chen, Z., Liu, Y., Zhang, H., Zhang, M., Liu, Q., Hong, X., Zhu, J. K., and Gong, Z. (2010). ABO3, a WRKY transcription factor, mediates plant responses to abscisic acid and drought tolerance in Arabidopsis. Plant J 63, 417–429.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren, Z.H., Gao, J.P., Li, L.G., Cai, X.L., Huang, W., Chao, D.Y., Zhu, M.Z., Wang, Z.Y., Luan, S., and Lin, H.X. (2005). A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37, 1141–1146.

    Article  CAS  PubMed  Google Scholar 

  • Rizhsky, L., Davletova, S., Liang, H., and Mittler, R. (2004). The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279, 11736–11743.

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez, L., Gonzalez-Guzman, M., Diaz, M., Rodrigues, A., Izquierdo-Garcia, A.C., Peirats-Llobet, M., Fernandez, M.A., Antoni, R., Fernandez, D., Marquez, J.A., et al. (2014). C2-domain abscisic acid-related proteins mediate the interaction of PYR/PYL/RCAR abscisic acid receptors with the plasma membrane and regulate abscisic acid sensitivity in Arabidopsis. Plant Cell 26, 4802–4820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez, P.L., Benning, G., and Grill, E. (1998). ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett 421, 185–190.

    Article  CAS  PubMed  Google Scholar 

  • Rubio, F., Gassmann, W., and Schroeder, J.I. (1995). Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270, 1660–1663.

    Article  CAS  PubMed  Google Scholar 

  • Rubio, V., Linhares, F., Solano, R., Martín, A.C., Iglesias, J., Leyva, A., and Paz-Ares, J. (2001). A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15, 2122–2133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruelland, E., Vaultier, M.N., Zachowski, A., and Hurry, V. (2009). Cold signalling and cold acclimation in plants. Adv Bot Res 49, 35–150.

    Article  CAS  Google Scholar 

  • Ruggiero, B., Koiwa, H., Manabe, Y., Quist, T.M., Inan, G., Saccardo, F., Joly, R.J., Hasegawa, P.M., Bressan, R.A., and Maggio, A. (2004). Uncoupling the effects of abscisic acid on plant growth and water relations. Analysis of sto1/nced3, an abscisic acid-deficient but salt stress-tolerant mutant in Arabidopsis. Plant Physiol 136, 3134–3147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rus, A., Baxter, I., Muthukumar, B., Gustin, J., Lahner, B., Yakubova, E., and Salt, D.E. (2006). Natural variants of AtHKT1 enhance Na+ accumulation in two wild populations of Arabidopsis. PLoS Genet 2, e210.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rus, A., Lee, B., Muñoz-Mayor, A., Sharkhuu, A., Miura, K., Zhu, J.K., Bressan, R.A., and Hasegawa, P.M. (2004). AtHKT1 facilitates Na+ homeostasis and K+ nutrition in planta. Plant Physiol 136, 2500–2511.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rus, A., Yokoi, S., Sharkhuu, A., Reddy, M., Lee, B.H., Matsumoto, T.K., Koiwa, H., Zhu, J.K., Bressan, R.A., and Hasegawa, P.M. (2001). AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98, 14150–14155.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruschhaupt, M., Mergner, J., Mucha, S., Papacek, M., Doch, I., Tischer, S. V., Hemmler, D., Chiasson, D., Edel, K.H., Kudla, J., et al. (2019). Rebuilding core abscisic acid signaling pathways of Arabidopsis in yeast. EMBO J 38, e101859.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rytz, T.C., Miller, M.J., McLoughlin, F., Augustine, R.C., Marshall, R.S., Juan, Y.T., Charng, Y.Y., Scalf, M., Smith, L.M., and Vierstra, R.D. (2018). SUMOylome profiling reveals a diverse array of nuclear targets modified by the SUMO ligase SIZ1 during heat stress. Plant Cell 30, 1077–1099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saito, S., Hamamoto, S., Moriya, K., Matsuura, A., Sato, Y., Muto, J., Noguchi, H., Yamauchi, S., Tozawa, Y., Ueda, M., et al. (2018). Nmyristoylation and S-acylation are common modifications of Ca2+-regulated Arabidopsis kinases and are required for activation of the SLAC1 anion channel. New Phytol 218, 1504–1521.

    Article  CAS  PubMed  Google Scholar 

  • Sakuma, Y., Maruyama, K., Osakabe, Y., Qin, F., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006a). Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18, 1292–1309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma, Y., Maruyama, K., Qin, F., Osakabe, Y., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006b). Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103, 18822–18827.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Bermejo, E., Castrillo, G., del Llano, B., Navarro, C., Zarco-Fernández, S., Martinez-Herrera, D.J., Leo-del Puerto, Y., Muñoz, R., Cámara, C., Paz-Ares, J., et al. (2014). Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat Commun 5, 4617.

    Article  PubMed  CAS  Google Scholar 

  • Santiago, J., Dupeux, F., Round, A., Antoni, R., Park, S.Y., Jamin, M., Cutler, S.R., Rodriguez, P.L., and Márquez, J.A. (2009). The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462, 665–668.

    Article  CAS  PubMed  Google Scholar 

  • Saruhashi, M., Kumar Ghosh, T., Arai, K., Ishizaki, Y., Hagiwara, K., Komatsu, K., Shiwa, Y., Izumikawa, K., Yoshikawa, H., Umezawa, T., et al. (2015). Plant Raf-like kinase integrates abscisic acid and hyperosmotic stress signaling upstream of SNF1-related protein kinase2. Proc Natl Acad Sci USA 112, E6388–E6396.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki, A., Yamaji, N., and Ma, J.F. (2014). Overexpression of OsHMA3 enhances Cd tolerance and expression of Zn transporter genes in rice. J Exp Bot 65, 6013–6021.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki, A., Yamaji, N., Yokosho, K., and Ma, J.F. (2012). Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24, 2155–2167.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki, T., Mori, I.C., Furuichi, T., Munemasa, S., Toyooka, K., Matsuoka, K., Murata, Y., and Yamamoto, Y. (2010). Closing plant stomata requires a homolog of an aluminum-activated malate transporter. Plant Cell Physiol 51, 354–365.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato, A., Sato, Y., Fukao, Y., Fujiwara, M., Umezawa, T., Shinozaki, K., Hibi, T., Taniguchi, M., Miyake, H., Goto, D.B., et al. (2009). Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem J 424, 439–448.

    Article  CAS  PubMed  Google Scholar 

  • Sato, H., Mizoi, J., Tanaka, H., Maruyama, K., Qin, F., Osakabe, Y., Morimoto, K., Ohori, T., Kusakabe, K., Nagata, M., et al. (2014). Arabidopsis DPB3-1, a DREB2A interactor, specifically enhances heat stress-induced gene expression by forming a heat stress-specific transcriptional complex with NF-Y subunits. Plant Cell 26, 4954–4973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato, H., Suzuki, T., Takahashi, F., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2019). NF-YB2 and NF-YB3 have functionally diverged and differentially induce drought and heat stress-specific genes. Plant Physiol 180, 1677–1690.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K., Takahashi, H., Watanabe, A., and Akagi, H. (2012). Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol 53, 213–224.

    Article  CAS  PubMed  Google Scholar 

  • Schachtman, D.P., and Schroeder, J.I. (1994). Structure and transport mechanism of a high-affinity potassium uptake transporter from higher plants. Nature 370, 655–658.

    Article  CAS  PubMed  Google Scholar 

  • Scherzer, S., Maierhofer, T., Al-Rasheid, K.A.S., Geiger, D., and Hedrich, R. (2012). Multiple calcium-dependent kinases modulate ABAactivated guard cell anion channels. Mol Plant 5, 1409–1412.

    Article  CAS  PubMed  Google Scholar 

  • Schroeder, J.I., and Hagiwara, S. (1990). Repetitive increases in cytosolic Ca2+ of guard cells by abscisic acid activation of nonselective Ca2+ permeable channels. Proc Natl Acad Sci USA 87, 9305–9309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A., and McCarty, D.R. (1997). Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276, 1872–1874.

    Article  CAS  PubMed  Google Scholar 

  • Sedaghatmehr, M., Thirumalaikumar, V.P., Kamranfar, I., Marmagne, A., Masclaux-Daubresse, C., and Balazadeh, S. (2019). A regulatory role of autophagy for resetting the memory of heat stress in plants. Plant Cell Environ 42, 1054–1064.

    Article  CAS  PubMed  Google Scholar 

  • Seo, M., Peeters, A.J.M., Koiwai, H., Oritani, T., Marion-Poll, A., Zeevaart, J.A.D., Koornneef, M., Kamiya, Y., and Koshiba, T. (2000). The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc Natl Acad Sci USA 97, 12908–12913.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo, P.J., Park, M.J., Lim, M.H., Kim, S.G., Lee, M., Baldwin, I.T., and Park, C.M. (2012). A self-regulatory circuit of CIRCADIAN CLOCK-ASSOCIATED1 underlies the circadian clock regulation of temperature responses in Arabidopsis. Plant Cell 24, 2427–2442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shabala, S., Wu, H., and Bose, J. (2015). Salt stress sensing and early signalling events in plant roots: Current knowledge and hypothesis. Plant Sci 241, 109–119.

    Article  CAS  PubMed  Google Scholar 

  • Shang, Y., Yan, L., Liu, Z.Q., Cao, Z., Mei, C., Xin, Q., Wu, F.Q., Wang, X. F., Du, S.Y., Jiang, T., et al. (2010). The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22, 1909–1935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, H., Zhong, X., Zhao, F., Wang, Y., Yan, B., Li, Q., Chen, G., Mao, B., Wang, J., Li, Y., et al. (2015). Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nat Biotechnol 33, 996–1003.

    Article  CAS  PubMed  Google Scholar 

  • Shi, H., Ishitani, M., Kim, C., and Zhu, J.K. (2000). The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97, 6896–6901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, H., Lee, B., Wu, S.J., and Zhu, J.K. (2003). Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotechnol 21, 81–85.

    Article  CAS  PubMed  Google Scholar 

  • Shi, H., Quintero, F.J., Pardo, J.M., and Zhu, J.K. (2002). The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14, 465–477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, S., Wang, T., Chen, Z., Tang, Z., Wu, Z., Salt, D.E., Chao, D.Y., and Zhao, F.J. (2016). OsHAC1;1 and OsHAC1;2 function as arsenate reductases and regulate arsenic accumulation. Plant Physiol 172, 1708–1719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., and Yang, S. (2012). Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 24, 2578–2595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi, Y., Ding, Y., and Yang, S. (2015). Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol 56, 7–15.

    Article  CAS  PubMed  Google Scholar 

  • Shkolnik, D., Nuriel, R., Bonza, M.C., Costa, A., and Fromm, H. (2018). MIZ1 regulates ECA1 to generate a slow, long-distance phloem-transmitted Ca2+ signal essential for root water tracking in Arabidopsis. Proc Natl Acad Sci USA 115, 8031–8036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Siddiqui, K.S., and Cavicchioli, R. (2006). Cold-adapted enzymes. Annu Rev Biochem 75, 403–433.

    Article  CAS  PubMed  Google Scholar 

  • Sierla, M., Hõrak, H., Overmyer, K., Waszczak, C., Yarmolinsky, D., Maierhofer, T., Vainonen, J.P., Salojärvi, J., Denessiouk, K., Laanemets, K., et al. (2018). The receptor-like pseudokinase GHR1 is required for stomatal closure. Plant Cell 30, 2813–2837.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sirichandra, C., Gu, D., Hu, H.C., Davanture, M., Lee, S., Djaoui, M., Valot, B., Zivy, M., Leung, J., Merlot, S., et al. (2009). Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583, 2982–2986.

    Article  CAS  PubMed  Google Scholar 

  • Song, W.Y., Park, J., Mendoza-Cózatl, D.G., Suter-Grotemeyer, M., Shim, D., Hörtensteiner, S., Geisler, M., Weder, B., Rea, P.A., Rentsch, D., et al. (2010). Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc Natl Acad Sci USA 107, 21187–21192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song, W.Y., Yamaki, T., Yamaji, N., Ko, D., Jung, K.H., Fujii-Kashino, M., An, G., Martinoia, E., Lee, Y., and Ma, J.F. (2014). A rice ABC transporter, OsABCC1, reduces arsenic accumulation in the grain. Proc Natl Acad Sci USA 111, 15699–15704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stockinger, E.J., Gilmour, S.J., and Thomashow, M.F. (1997). Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Natl Acad Sci USA 94, 1035–1040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su, H., Cao, Y., Ku, L., Yao, W., Cao, Y., Ren, Z., Dou, D., Wang, H., Ren, Z., Liu, H., et al. (2018). Dual functions of ZmNF-YA3 in photoperiod-dependent flowering and abiotic stress responses in maize. J Exp Bot 69, 5177–5189.

    Article  CAS  PubMed  Google Scholar 

  • Sun, L., Lu, S.J., Zhang, S.S., Zhou, S.F., Sun, L., and Liu, J.X. (2013). The lumen-facing domain is important for the biological function and organelle-to-organelle movement of bZIP28 during ER stress in Arabidopsis. Mol Plant 6, 1605–1615.

    Article  CAS  PubMed  Google Scholar 

  • Sussmilch, F.C., Brodribb, T.J., and McAdam, S.A.M. (2017). What are the evolutionary origins of stomatal responses to abscisic acid in land plants? J Integr Plant Biol 59, 240–260.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki, N., Sejima, H., Tam, R., Schlauch, K., and Mittler, R. (2011). Identification of the MBF1 heat-response regulon of Arabidopsis thaliana. Plant J 66, 844–851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Świeżawska, B., Duszyn, M., Jaworski, K., and Szmidt-Jaworska, A. (2018). Downstream targets of cyclic nucleotides in plants. Front Plant Sci 9, 1428.

    Article  PubMed  PubMed Central  Google Scholar 

  • Takahashi, F., Suzuki, T., Osakabe, Y., Betsuyaku, S., Kondo, Y., Dohmae, N., Fukuda, H., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2018). A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556, 235–238.

    Article  CAS  PubMed  Google Scholar 

  • Takahashi, Y., Zhang, J., Hsu, P.K., Ceciliato, P.H.O., Zhang, L., Dubeaux, G., Munemasa, S., Ge, C., Zhao, Y., Hauser, F., et al. (2020). MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nat Commun 11, 12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takasaki, H., Maruyama, K., Kidokoro, S., Ito, Y., Fujita, Y., Shinozaki, K., Yamaguchi-Shinozaki, K., and Nakashima, K. (2010). The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genomics 284, 173–183.

    Article  CAS  PubMed  Google Scholar 

  • Takehisa, H., and Sato, Y. (2019). Transcriptome monitoring visualizes growth stage-dependent nutrient status dynamics in rice under field conditions. Plant J 97, 1048–1060.

    Article  CAS  PubMed  Google Scholar 

  • Tan, B.C., Schwartz, S.H., Zeevaart, J.A.D., and McCarty, D.R. (1997). Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94, 12235–12240.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang, L., Mao, B., Li, Y., Lv, Q., Zhang, L.P., Chen, C., He, H., Wang, W., Zeng, X., Shao, Y., et al. (2017). Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Sci Rep 7, 14438.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tao, Q., Jupa, R., Liu, Y., Luo, J., Li, J., Kováè, J., Li, B., Li, Q., Wu, K., Liang, Y., et al. (2019). Abscisic acid-mediated modifications of radial apoplastic transport pathway play a key role in cadmium uptake in hyperaccumulator Sedum alfredii. Plant Cell Environ 42, 1425–1440.

    Article  CAS  PubMed  Google Scholar 

  • Taub, D.R., and Wang, X. (2008). Why are nitrogen concentrations in plant tissues lower under elevated CO2? A critical examination of the hypotheses. J Integr Plant Biol 50, 1365–1374.

    Article  CAS  PubMed  Google Scholar 

  • Thomsen, A.R.B., Plouffe, B., Cahill Iii, T.J., Shukla, A.K., Tarrasch, J.T., Dosey, A.M., Kahsai, A.W., Strachan, R.T., Pani, B., Mahoney, J.P., et al. (2016). GPCR-G protein-β-arrestin super-complex mediates sustained G protein signaling. Cell 166, 907–919.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • To, T.K., Nakaminami, K., Kim, J.M., Morosawa, T., Ishida, J., Tanaka, M., Yokoyama, S., Shinozaki, K., and Seki, M. (2011). Arabidopsis HDA6 is required for freezing tolerance. Biochem Biophys Res Commun 406, 414–419.

    Article  CAS  PubMed  Google Scholar 

  • Tran, L.S.P., Nakashima, K., Sakuma, Y., Simpson, S.D., Fujita, Y., Maruyama, K., Fujita, M., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2004). Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a droughtresponsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16, 2481–2498.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vahisalu, T., Kollist, H., Wang, Y.F., Nishimura, N., Chan, W.Y., Valerio, G., Lamminmäki, A., Brosché, M., Moldau, H., Desikan, R., et al. (2008). SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452, 487–491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valdés, A.E., Overnäs, E., Johansson, H., Rada-Iglesias, A., and Engström, P. (2012). The homeodomain-leucine zipper (HD-Zip) class I transcription factors ATHB7 and ATHB12 modulate abscisic acid signalling by regulating protein phosphatase 2C and abscisic acid receptor gene activities. Plant Mol Biol 80, 405–418.

    Article  PubMed  CAS  Google Scholar 

  • Vanderauwera, S., Suzuki, N., Miller, G., van de Cotte, B., Morsa, S., Ravanat, J.L., Hegie, A., Triantaphylidès, C., Shulaev, V., Van Montagu, M.C.E., et al. (2011). Extranuclear protection of chromosomal DNA from oxidative stress. Proc Natl Acad Sci USA 108, 1711–1716.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venkatachalam, K., and Montell, C. (2007). TRP channels. Annu Rev Biochem 76, 387–417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verret, F., Wheeler, G., Taylor, A.R., Farnham, G., and Brownlee, C. (2010). Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling. New Phytol 187, 23–43.

    Article  CAS  PubMed  Google Scholar 

  • Vlachonasios, K.E., Thomashow, M.F., and Triezenberg, S.J. (2003). Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15, 626–638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkov, R.A., Panchuk, I.I., Mullineaux, P.M., and Schöffl, F. (2006). Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Biol 61, 733–746.

    Article  CAS  PubMed  Google Scholar 

  • von Koskull-Döring, P., Scharf, K.D., and Nover, L. (2007). The diversity of plant heat stress transcription factors. Trends Plant Sci 12, 452–457.

    Article  PubMed  CAS  Google Scholar 

  • Wahid, A., Gelani, S., Ashraf, M., and Foolad, M. (2007). Heat tolerance in plants: An overview. Environ Exp Bot 61, 199–223.

    Article  Google Scholar 

  • Wang, C., Na, G.N., Bermejo, E.S., Chen, Y., Banks, J.A., Salt, D.E., and Zhao, F.J. (2018a). Dissecting the components controlling root-to-shoot arsenic translocation in Arabidopsis thaliana. New Phytol 217, 206–218.

    Article  PubMed  CAS  Google Scholar 

  • Wang, H., Tang, J., Liu, J., Hu, J., Liu, J., Chen, Y., Cai, Z., and Wang, X. (2018b). Abscisic acid signaling inhibits brassinosteroid signaling through dampening the dephosphorylation of BIN2 by ABI1 and ABI2. Mol Plant 11, 315–325.

    Article  CAS  PubMed  Google Scholar 

  • Wang, K., He, J., Zhao, Y., Wu, T., Zhou, X., Ding, Y., Kong, L., Wang, X., Wang, Y., Li, J., et al. (2018c). EAR1 negatively regulates ABA signaling by enhancing 2C protein phosphatase activity. Plant Cell 30, 815–834.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, L., Hua, D., He, J., Duan, Y., Chen, Z., Hong, X., and Gong, Z. (2011). Auxin Response Factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet 7, e1002172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, P., Cui, X., Zhao, C., Shi, L., Zhang, G., Sun, F., Cao, X., Yuan, L., Xie, Q., and Xu, X. (2017). COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response. J Integr Plant Biol 59, 78–85.

    Article  CAS  PubMed  Google Scholar 

  • Wang, P., Zhang, W., Mao, C., Xu, G., and Zhao, F.J. (2016). The role of OsPT8 in arsenate uptake and varietal difference in arsenate tolerance in rice. J Exp Bot 67, 6051–6059.

    Article  CAS  PubMed  Google Scholar 

  • Wang, P., Du, Y., Hou, Y.J., Zhao, Y., Hsu, C.C., Yuan, F., Zhu, X., Tao, W. A., Song, C.P., and Zhu, J.K. (2015). Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci USA 112, 613–618.

    Article  CAS  PubMed  Google Scholar 

  • Wang, P., Zhao, Y., Li, Z., Hsu, C.C., Liu, X., Fu, L., Hou, Y.J., Du, Y., Xie, S., Zhang, C., et al. (2018d). Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol Cell 69, 100–112.e6.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Q., Qu, G.P., Kong, X., Yan, Y., Li, J., and Jin, J.B. (2018e). Arabidopsis small ubiquitin-related modifier protease ASP1 positively regulates abscisic acid signaling during early seedling development. J Integr Plant Biol 60, 924–937.

    Article  CAS  PubMed  Google Scholar 

  • Wang, X., Ding, Y., Li, Z., Shi, Y., Wang, J., Hua, J., Gong, Z., Zhou, J.M., and Yang, S. (2019). PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Dev Cell 51, 222–235.e5.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Z., Ruan, W., Shi, J., Zhang, L., Xiang, D., Yang, C., Li, C., Wu, Z., Liu, Y., Yu, Y., et al. (2014). Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. Proc Natl Acad Sci USA 111, 14953–14958.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ward, J.M., Mäser, P., and Schroeder, J.I. (2009). Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71, 59–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weinl, S., and Kudla, J. (2009). The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184, 517–528.

    Article  CAS  PubMed  Google Scholar 

  • Weng, J.K., Ye, M., Li, B., and Noel, J.P. (2016). Co-evolution of hormone metabolism and signaling networks expands plant adaptive plasticity. Cell 166, 881–893.

  • Wild, R., Gerasimaite, R., Jung, J.Y., Truffault, V., Pavlovic, I., Schmidt, A., Saiardi, A., Jessen, H.J., Poirier, Y., Hothorn, M., et al. (2016). Control of eukaryotic phosphate homeostasis by inositol polyphosphate sensor domains. Science 352, 986–990.

    Article  CAS  PubMed  Google Scholar 

  • Wong, C.K.E., and Cobbett, C.S. (2009). HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181, 71–78.

    Article  CAS  PubMed  Google Scholar 

  • Wu, A., Allu, A.D., Garapati, P., Siddiqui, H., Dortay, H., Zanor, M.I., Asensi-Fabado, M.A., Munné-Bosch, S., Antonio, C., Tohge, T., et al. (2012). JUNGBRUNNEN1, a reactive oxygen species-responsive NAC transcription factor, regulates longevity in Arabidopsis. Plant Cell 24, 482–506.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu, F., Chi, Y., Jiang, Z., Xu, Y., Xie, L., Huang, F., Wan, D., Ni, J., Yuan, F., Wu, X., et al. (2020). Hydrogen peroxide sensor HPCA1 is an LRR receptor kinase in Arabidopsis. Nature 578, 577–581.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Q., Wang, M., Shen, J., Chen, D., Zheng, Y., and Zhang, W. (2019). ZmOST1 mediates abscisic acid regulation of guard cell ion channels and drought stress responses. J Integr Plant Biol 61, 478–491.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Q., Zhang, X., Peirats-Llobet, M., Belda-Palazon, B., Wang, X., Cui, S., Yu, X., Rodriguez, P.L., and An, C. (2016). Ubiquitin ligases RGLG1 and RGLG5 regulate abscisic acid signaling by controlling the turnover of phosphatase PP2CA. Plant Cell 28, 2178–2196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong, L., Ishitani, M., Lee, H., and Zhu, J.K. (2001). The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor sulfurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13, 2063–2083.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu, J., Shi, S., Wang, L., Tang, Z., Lv, T., Zhu, X., Ding, X., Wang, Y., Zhao, F.J., and Wu, Z. (2017). OsHAC4 is critical for arsenate tolerance and regulates arsenic accumulation in rice. New Phytol 215, 1090–1101.

    Article  CAS  PubMed  Google Scholar 

  • Xu, W., Dai, W., Yan, H., Li, S., Shen, H., Chen, Y., Xu, H., Sun, Y., He, Z., and Ma, M. (2015). Arabidopsis NIP3;1 plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Mol Plant 8, 722–733.

    Article  CAS  PubMed  Google Scholar 

  • Xu, Z.Y., Lee, K.H., Dong, T., Jeong, J.C., Jin, J.B., Kanno, Y., Kim, D.H., Kim, S.Y., Seo, M., Bressan, R.A., et al. (2012). A vacuolar β-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24, 2184–2199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yaeno, T., and Iba, K. (2008). BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiol 148, 1032–1041.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamada, K., Fukao, Y., Hayashi, M., Fukazawa, M., Suzuki, I., and Nishimura, M. (2007). Cytosolic HSP90 regulates the heat shock response that is responsible for heat acclimation in Arabidopsis thaliana. J Biol Chem 282, 37794–37804.

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi, T., Aharon, G.S., Sottosanto, J.B., and Blumwald, E. (2005). Vacuolar Na+/H+ antiporter cation selectivity is regulated by calmodulin from within the vacuole in a Ca2+- and pH-dependent manner. Proc Natl Acad Sci USA 102, 16107–16112.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi, T., Apse, M.P., Shi, H., and Blumwald, E. (2003). Topological analysis of a plant vacuolar Na+/H+ antiporter reveals a luminal C terminus that regulates antiporter cation selectivity. Proc Natl Acad Sci USA 100, 12510–12515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan, H., Xu, W., Xie, J., Gao, Y., Wu, L., Sun, L., Feng, L., Chen, X., Zhang, T., Dai, C., et al. (2019). Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nat Commun 10, 2562.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yan, J., Wang, P., Wang, P., Yang, M., Lian, X., Tang, Z., Huang, C.F., Salt, D.E., and Zhao, F.J. (2016). A loss-of-function allele of OsHMA3 associated with high cadmium accumulation in shoots and grain of Japonica rice cultivars. Plant Cell Environ 39, 1941–1954.

    Article  CAS  PubMed  Google Scholar 

  • Yang, T., Chaudhuri, S., Yang, L., Du, L., and Poovaiah, B.W. (2010a). A calcium/calmodulin-regulated member of the receptor-like kinase family confers cold tolerance in plants. J Biol Chem 285, 7119–7126.

    Article  CAS  PubMed  Google Scholar 

  • Yang, T., Shad Ali, G., Yang, L., Du, L., Reddy, A.S.N., and Poovaiah, B. W. (2010b). Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal Behav 5, 991–994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang, Y., and Guo, Y. (2018). Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217, 523–539.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., Wang, C., Xue, Y., Liu, X., Chen, S., Song, C.P., Yang, Y., and Guo, Y. (2019). Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10, 1199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yao, L., Cheng, X., Gu, Z., Huang, W., Li, S., Wang, L., Wang, Y.F., Xu, P., Ma, H., and Ge, X. (2018). The AWPM-19 family protein OsPM1 mediates abscisic acid influx and drought response in rice. Plant Cell 30, 1258–1276.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye, K., Li, H., Ding, Y., Shi, Y., Song, C.P., Gong, Z., and Yang, S. (2019). BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell 31, 2682–2696.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ye, Y., Li, P., Xu, T., Zeng, L., Cheng, D., Yang, M., Luo, J., and Lian, X. (2017). OsPT4 contributes to arsenate uptake and transport in rice. Front Plant Sci 8, 2197.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yin, P., Fan, H., Hao, Q., Yuan, X., Wu, D., Pang, Y., Yan, C., Li, W., Wang, J., and Yan, N. (2009). Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol 16, 1230–1236.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, T., Mogami, J., and Yamaguchi-Shinozaki, K. (2014). ABA-dependent and ABA-independent signaling in response to osmotic stress in plants. Curr Opin Plant Biol 21, 133–139.

    Article  CAS  PubMed  Google Scholar 

  • Yoshida, T., Ohama, N., Nakajima, J., Kidokoro, S., Mizoi, J., Nakashima, K., Maruyama, K., Kim, J.M., Seki, M., Todaka, D., et al. (2011). Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genomics 286, 321–332.

    Article  CAS  PubMed  Google Scholar 

  • Yu, F., Lou, L., Tian, M., Li, Q., Ding, Y., Cao, X., Wu, Y., Belda-Palazon, B., Rodriguez, P.L., Yang, S., et al. (2016). ESCRT-I component VPS23A affects ABA signaling by recognizing ABA receptors for endosomal degradation. Mol Plant 9, 1570–1582.

    Article  CAS  PubMed  Google Scholar 

  • Yu, F., Qian, L., Nibau, C., Duan, Q., Kita, D., Levasseur, K., Li, X., Lu, C., Li, H., Hou, C., et al. (2012). FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci USA 109, 14693–14698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, J., Han, J., Kim, Y.J., Song, M., Yang, Z., He, Y., Fu, R., Luo, Z., Hu, J., Liang, W., et al. (2017). Two rice receptor-like kinases maintain male fertility under changing temperatures. Proc Natl Acad Sci USA 114, 12327–12332.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, Y., and Assmann, S.M. (2018). Inter-relationships between the heterotrimeric Gβ subunit AGB1, the receptor-like kinase FERONIA, and RALF1 in salinity response. Plant Cell Environ 41, 2475–2489.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan, F., Yang, H., Xue, Y., Kong, D., Ye, R., Li, C., Zhang, J., Theprungsirikul, L., Shrift, T., Krichilsky, B., et al. (2014). OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514, 367–371.

    Article  CAS  PubMed  Google Scholar 

  • Zeevaart, J.A.D. (1980). Changes in the levels of abscisic acid and its metabolites in excised leaf blades of Xanthium strumarium during and after water stress. Plant Physiol 66, 672–678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, A., Ren, H.M., Tan, Y.Q., Qi, G.N., Yao, F.Y., Wu, G.L., Yang, L. W., Hussain, J., Sun, S.J., and Wang, Y.F. (2016a). S-type anion channels SLAC1 and SLAH3 function as essential negative regulators of inward K+ channels and stomatal opening in Arabidopsis. Plant Cell 28, 949–965.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, B., Wu, S., Zhang, Y., Xu, T., Guo, F., Tang, H., Li, X., Wang, P., Qian, W., and Xue, Y. (2016b). A high temperature-dependent mitochondrial lipase EXTRA GLUME1 promotes floral phenotypic robustness against temperature fluctuation in rice (Oryza sativa L.). PLoS Genet 12, e1006152.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang, H., Liu, D., Yang, B., Liu, W.Z., Mu, B., Song, H., Chen, B., Li, Y., Ren, D., Deng, H., et al. (2020a). Arabidopsis CPK6 positively regulates ABA signaling and drought tolerance through phosphorylating ABA-responsive element-binding factors. J Exp Bot 71, 188–203.

    Article  PubMed  CAS  Google Scholar 

  • Zhang, H., Zhu, H., Pan, Y., Yu, Y., Luan, S., and Li, L. (2014). A DTX/MATE-type transporter facilitates abscisic acid efflux and modulates ABA sensitivity and drought tolerance in Arabidopsis. Mol Plant 7, 1522–1532.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H.X., and Blumwald, E. (2001). Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19, 765–768.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, H.X., Hodson, J.N., Williams, J.P., and Blumwald, E. (2001). Engineering salt-tolerant Brassica plants: characterization of yield and seed oil quality in transgenic plants with increased vacuolar sodium accumulation. Proc Natl Acad Sci USA 98, 12832–12836.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Liu, Y.X., Zhang, N., Hu, B., Jin, T., Xu, H., Qin, Y., Yan, P., Zhang, X., Guo, X., et al. (2019). NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nat Biotechnol 37, 676–684.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Zhang, N., Liu, Y.X., Zhang, X., Hu, B., Qin, Y., Xu, H., Wang, H., Guo, X., Qian, J., et al. (2018a). Root microbiota shift in rice correlates with resident time in the field and developmental stage. Sci China Life Sci 61, 613–621.

    Article  PubMed  Google Scholar 

  • Zhang, J., Zhou, Z., Bai, J., Tao, X., Wang, L., Zhang, H., and Zhu, J.K. (2020b). Disruption of MIR396e and MIR396f improves rice yield under nitrogen-deficient conditions. Natl Sci Rev 7, 102–112.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J.L., and Shi, H. (2013). Physiological and molecular mechanisms of plant salt tolerance. Photosynth Res 115, 1–22.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, L., Li, X., Li, D., Sun, Y., Li, Y., Luo, Q., Liu, Z., Wang, J., Li, X., Zhang, H., et al. (2018b). CARK1 mediates ABA signaling by phosphorylation of ABA receptors. Cell Discov 4, 30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, M., Wang, D., Kang, Y., Wu, J.X., Yao, F., Pan, C., Yan, Z., Song, C., and Chen, L. (2018c). Structure of the mechanosensitive OSCA channels. Nat Struct Mol Biol 25, 850–858.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S., Zhuang, K., Wang, S., Lv, J., Ma, N., and Meng, Q. (2017a). A novel tomato SUMO E3 ligase, SlSIZ1, confers drought tolerance in transgenic tobacco. J Integr Plant Biol 59, 102–117.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, S.S., Yang, H., Ding, L., Song, Z.T., Ma, H., Chang, F., and Liu, J. X. (2017b). Tissue-specific transcriptomics reveals an important role of the unfolded protein response in maintaining fertility upon heat stress in Arabidopsis. Plant Cell 29, 1007–1023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Z., Li, J., Li, F., Liu, H., Yang, W., Chong, K., and Xu, Y. (2017c). OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell 43, 731–743.e5.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, C., Wang, P., Si, T., Hsu, C.C., Wang, L., Zayed, O., Yu, Z., Zhu, Y., Dong, J., Tao, W.A., et al. (2017). MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43, 618–629.e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, C., Zayed, O., Yu, Z., Jiang, W., Zhu, P., Hsu, C.C., Zhang, L., Tao, W.A., Lozano-Durán, R., and Zhu, J.K. (2018a). Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci USA 115, 13123–13128.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao, C., Zhang, Z., Xie, S., Si, T., Li, Y., and Zhu, J.K. (2016). Mutational evidence for the critical role of CBF genes in cold acclimation in Arabidopsis. Plant Physiol pp.00533.2016.

  • Zhao, Y., Zhang, Z., Gao, J., Wang, P., Hu, T., Wang, Z., Hou, Y.J., Wan, Y., Liu, W., Xie, S., et al. (2018b). Arabidopsis duodecuple mutant of PYL ABA receptors reveals PYL repression of ABA-independent SnRK2 activity. Cell Rep 23, 3340–3351.e5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng, Z., Wang, Z., Wang, X., and Liu, D. (2019). Blue light-triggered chemical reactions underlie phosphate deficiency-induced inhibition of root elongation of Arabidopsis seedlings grown in petri dishes. Mol Plant 12, 1515–1523.

    Article  CAS  PubMed  Google Scholar 

  • Zhong, L., Zhou, W., Wang, H., Ding, S., Lu, Q., Wen, X., Peng, L., Zhang, L., and Lu, C. (2013). Chloroplast small heat shock protein HSP21 Interacts with plastid nucleoid protein pTAC5 and is essential for chloroplast development in Arabidopsis under heat stress. Plant Cell 25, 2925–2943.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, H., Lin, H., Chen, S., Becker, K., Yang, Y., Zhao, J., Kudla, J., Schumaker, K.S., and Guo, Y. (2014a). Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell 26, 1166–1182.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, J., Jiao, F.C., Wu, Z., Li, Y., Wang, X., He, X., Zhong, W., and Wu, P. (2008). OsPHR2 is involved in phosphate-starvation signaling and excessive phosphate accumulation in shoots of plants. Plant Physiol 146, 1673–1686.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, J., Wang, J., Cheng, Y., Chi, Y.J., Fan, B., Yu, J.Q., and Chen, Z. (2013). NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet 9, e1003196.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou, J., Wang, J., Yu, J.Q., and Chen, Z. (2014b). Role and regulation of autophagy in heat stress responses of tomato plants. Front Plant Sci 5, 174.

    PubMed  PubMed Central  Google Scholar 

  • Zhu, J., Jeong, J.C., Zhu, Y., Sokolchik, I., Miyazaki, S., Zhu, J.K., Hasegawa, P.M., Bohnert, H.J., Shi, H., Yun, D.J., et al. (2008). Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105, 4945–4950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, J.K. (2016). Abiotic stress signaling and responses in plants. Cell 167, 313–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, J., Dong, C.H., and Zhu, J.K. (2007a). Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10, 290–295.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, J.K. (2001). Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4, 401–406.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, S.Y., Yu, X.C., Wang, X.J., Zhao, R., Li, Y., Fan, R.C., Shang, Y., Du, S.Y., Wang, X.F., Wu, F.Q., et al. (2007b). Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19, 3019–3036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou, J.J., Wei, F.J., Wang, C., Wu, J.J., Ratnasekera, D., Liu, W.X., and Wu, W.H. (2010). Arabidopsis calcium-dependent protein kinase CPK10 functions in abscisic acid- and Ca2+-mediated stomatal regulation in response to drought stress. Plant Physiol 154, 1232–1243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Gong, Z., Xiong, L., Shi, H. et al. Plant abiotic stress response and nutrient use efficiency. Sci. China Life Sci. 63, 635–674 (2020). https://doi.org/10.1007/s11427-020-1683-x

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