Abstract
Key message
Autophagy receptor OsNBR1 modulates salt stress tolerance by affecting ROS accumulation in rice.
Abstract
The NBR1 (next to BRCA1 gene 1), as important selective receptors, whose functions have been reported in animals and plants. Although the function of NBR1 responses to abiotic stress has mostly been investigated in Arabidopsis thaliana, the role of NBR1 under salt stress conditions remains unclear in rice (Oryza sativa). In this study, by screening the previously generated activation-tagged line, we identified a mutant, activation tagging 10 (AC10), which exhibited salt stress-sensitive phenotypes. TAIL-PCR (thermal asymmetric interlaced PCR) showed that the AC10 line carried a loss-of-function mutation in the OsNBR1 gene. OsNBR1 was found to be a positive regulator of salt stress tolerance and was localized in aggregates. A loss-of-function mutation in OsNBR1 increased salt stress sensitivity, whereas overexpression of OsNBR1 enhanced salt stress resistance. The osnbr1 mutants showed higher ROS (reactive oxygen species) production, whereas the OsNBR1 overexpression (OsNBR1OE) lines showed lower ROS production, than Kitaake plants under normal and salt stress conditions. Furthermore, RNA-seq analysis revealed that expression of OsRBOH9 (respiratory burst oxidase homologue) was increased in osnbr1 mutants, resulting in increased ROS accumulation in osnbr1 mutants. Together our results established that OsNBR1 responds to salt stress by influencing accumulation of ROS rather than by regulating transport of Na+ and K+ in rice.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
The Sequence Read Archive (SRA) database at the National Center for Biotechnology Information (NCBI) has received the RNA-seq data generated in this investigation and has been assigned the accession number PRJNA1022517. This published article and its supplemental information files contain all of the data created or analyzed during this study.
References
Bassham DC (2007) Plant autophagy more than a starvation response. Curr Opin Plant Biol 10(6):587–593. https://doi.org/10.1016/j.pbi.2007.06.006
Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2(1):2–11. https://doi.org/10.4161/auto.2092
Cai Y, Jia T, Lam SK, Ding Y, Gao C, San MWY, Pimpl P, Jiang L (2011) Multiple cytosolic and transmembrane determinants are required for the trafficking of SCAMP1 via an ER-Golgi-TGN-PM pathway. Plant J 65(6):882–896. https://doi.org/10.1111/j.1365-313X.2010.04469.x
Carroll B, Otten EG, Manni D, Stefanatos R, Menzies FM, Smith GR, Jurk D, Kenneth N, Wilkinson S, Passos JF, Attems J, Veal EA, Teyssou E, Seilhean D, Millecamps S, Eskelinen EL, Bronowska AK, Rubinsztein DC, Sanz A, Korolchuk VI (2018) Oxidation of SQSTM1/p62 mediates the link between redox state and protein homeostasis. Nat Commun 9(1):256. https://doi.org/10.1038/s41467-017-02746-z
Cui Y, Zhao Q, Gao C, Ding Y, Zeng Y, Ueda T, Nakano A, Jiang L (2014) Activation of the Rab7 GTPase by the MON1-CCZ1 complex is essential for PVC-to-Vacuole trafficking and plant growth in Arabidopsis. Plant Cell 26(5):2080–2097. https://doi.org/10.1105/tpc.114.123141
Floyd BE, Morriss SC, Macintosh GC, Bassham DC (2012) What to eat: evidence for selective autophagy in plants. J Integr Plant Biol 54(11):907–920. https://doi.org/10.1111/j.1744-7909.2012.01178.x
Forte M, Bianchi F, Cotugno M, Marchitti S, Stanzione R, Maglione V, Sciarretta S, Valenti V, Carnevale R, Versaci F, Frati G, Volpe M, Rubattu S (2021) An interplay between UCP2 and ROS protects cells from high-salt-induced injury through autophagy stimulation. Cell Death Dis 12(10):919. https://doi.org/10.1038/s41419-021-04188-4
Garratt R, Oliva G, Caracelli I, LeiteLeite AA (1993) Studies of the zein-like alpha-prolamins based on an analysis of amino acid sequences: implications for their evolution and three-dimensional structure. Proteins 15(1):88–99. https://doi.org/10.1002/prot.340150111
Guo J, Wang H, Guan W, Guo Q, Wang J, Yang J, Peng Y, Shan J, Gao M, Shi S, Shangguan X, Liu B, Jing S, Zhang J, Xu C, Huang J, Rao W, Zheng X, Wu D, Zhou C, Du B, Chen R, Zhu L, Zhu Y, Walling LL, Zhang Q, He G (2023) A tripartite rheostat controls self-regulated host plant resistance to insects. Nature 618(7966):799–807. https://doi.org/10.1038/s41586-023-06197-z
Han S, Yu B, Wang Y, Liu Y (2011) Role of plant autophagy in stress response. Protein Cell 2(10):784–791. https://doi.org/10.1007/s13238-011-1104-4
Hossain MS, Dietz KJ (2016) Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Front Plant Sci 10(7):548. https://doi.org/10.3389/fpls.2016.00548
Ichimura Y, Kominami E, Tanaka K, Komatsu M (2008) Selective turnover of p62/A170/SQSTM1 by autophagy. Autophagy 4(8):1063–1066. https://doi.org/10.4161/auto.6826
Ismail AM, Horie T (2017) Genomics, physiology, and molecular breeding approaches for improving salt tolerance. Annu Rev Plant Biol 68:405–434. https://doi.org/10.1146/annurev-arplant-042916-040936
Ji C, Zhou J, Guo R, Lin Y, Kung CH, Hu S, Ng WY, Zhuang X, Jiang L (2020) AtNBR1 is a selective autophagic receptor for AtExo70E2 in Arabidopsis. Plant Physiol 184(2):777–791. https://doi.org/10.1104/pp.20.00470
Johansen T, Lamark T (2011) Selective autophagy mediated by autophagic adapter proteins. Autophagy 7(3):279–296. https://doi.org/10.4161/auto.7.3.14487
Jung H, Lee HN, Marshall RS, Lomax AW, Yoon MJ, Kim J, Kim JH, Vierstra RD, Chung T (2020) Arabidopsis cargo receptor NBR1 mediates selective autophagy of defective proteins. J Exp Bot 71(1):73–89. https://doi.org/10.1093/jxb/erz404
Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22(11):2623–2633. https://doi.org/10.1093/emboj/cdg277
Li GB, He JX, Wu JL, Wang H, Zhang X, Liu J, Hu XH, Zhu Y, Shen S, Bai YF, Yao ZL, Liu XX, Zhao JH, Li DQ, Li Y, Huang F, Huang YY, Zhao ZX, Zhang JW, Zhou SX, Ji YP, Pu M, Qin P, Li S, Chen X, Wang J, He M, Li W, Wu XJ, Xu ZJ, Wang WM, Fan J (2022) Overproduction of OsRACK1A, an effector-targeted scaffold protein promoting OsRBOHB-mediated ROS production, confers rice floral resistance to false smut disease without yield penalty. Mol Plant 15(11):1790–1806. https://doi.org/10.1016/j.molp.2022.10.009
Lin Z, Wang YL, Cheng LS, Zhou LL, Xu QT, Liu DC, Deng XY, Mei FZ, Zhou ZQ (2021) Mutual regulation of ROS accumulation and cell autophagy in wheat roots under hypoxia stress. Plant Physiol Biochem 158:91–102. https://doi.org/10.1016/j.plaphy
Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5(7):954–963. https://doi.org/10.4161/auto.5.7.9290
Liu WJ, Ye L, Huang WF, Guo LJ, Xu ZG, Wu HL, Yang C, Liu HF (2016) p62 links the autophagy pathway and the ubiqutin-proteasome system upon ubiquitinated protein degradation. Cell Mol Biol Lett 21:29. https://doi.org/10.1186/s11658-016-0031-z
Liu Y, Chen X, Xue S, Quan T, Cui D, Han L, Cong W, Li M, Yun DJ, Liu B, Xu ZY (2021) SET DOMAIN GROUP 721 protein functions in saline-alkaline stress tolerance in the model rice variety Kitaake. Plant Biotechnol J 19(12):2576–2588. https://doi.org/10.1111/pbi.13683
Liu Y, Li M, Yu J, Ma A, Wang J, Yun DJ, Xu ZY (2023) Plasma membrane-localized Hsp40/DNAJ chaperone protein facilitates OsSUVH7-OsBAG4-OsMYB106 transcriptional complex formation for OsHKT1;5 activation. J Integr Plant Biol 65(1):265–279. https://doi.org/10.1111/jipb.13403
Luo L, Zhang P, Zhu R, Fu J, Su J, Zheng J, Wang Z, Wang D, Gong Q (2017) Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front Plant Sci 8:1459. https://doi.org/10.3389/fpls.2017.01459
Lyu L, Chen Z, McCarty N (2022) TRIM44 links the UPS to SQSTM1/p62-dependent aggrephagy and removing misfolded proteins. Autophagy 18(4):783–798. https://doi.org/10.1080/15548627.2021.1956105
Ma X, Zhang Q, Zhu Q, Liu W, Chen Y, Qiu R, Wang B, Yang Z, Li H, Lin Y, Xie Y, Shen R, Chen S, Wang Z, Chen Y, Guo J, Chen L, Zhao X, Dong Z, Liu YG (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8(8):1274–1284. https://doi.org/10.1016/j.molp.2015.04.007
Marshall RS, Vierstra RD (2018) Autophagy: the master of bulk and selective recycling. Annu Rev Plant Biol 69:173–208. https://doi.org/10.1146/annurev-arplant-042817-040606
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
Mizushima N, Noda T, Yoshimori T, Tanaka Y, Ishii T, George MD, Klionsky DJ, Ohsumi M, Ohsumi Y (1998) A protein conjugation system essential for autophagy. Nature 395(6700):395–398. https://doi.org/10.1038/26506
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
Nan N, Wang J, Shi Y, Qian Y, Jiang L, Huang S, Liu Y, Wu Y, Liu B, Xu ZY (2020) Rice plastidial NAD-dependent malate dehydrogenase 1 negatively regulates salt stress response by reducing the vitamin B6 content. Plant Biotechnol J 18(1):172–184. https://doi.org/10.1111/pbi.13184
Nguyen HM, Sako K, Matsui A, Suzuki Y, Mostofa MG, Ha CV, Tanaka M, Tran LP, Habu Y, Seki M (2017) Ethanol enhances high-salinity stress tolerance by detoxifying reactive oxygen species in Arabidopsis thaliana and Rice. Front Plant Sci 8:1001. https://doi.org/10.3389/fpls.2017.01001
Rasmussen NL, Kournoutis A, Lamark T, Johansen T (2022) NBR1: the archetypal selective autophagy receptor. J Cell Biol. https://doi.org/10.1083/jcb.202208092
Rubio N, Verrax J, Dewaele M, Verfaillie T, Johansen T, Piette J, Agostinis P (2014) p38(MAPK)-regulated induction of p62 and NBR1 after photodynamic therapy promotes autophagic clearance of ubiquitin aggregates and reduces reactive oxygen species levels by supporting Nrf2-antioxidant signaling. Free Radic Biol Med 67:292–303. https://doi.org/10.1016/j.freeradbiomed
Schmidt R, Mieulet D, Hubberten HM, Obata T, Hoefgen R, Fernie AR, Fisahn J, San Segundo B, Guiderdoni E, Schippers JH, Mueller-Roeber B (2013) Salt-responsive ERF1 regulates reactive oxygen species-dependent signaling during the initial response to salt stress in rice. Plant Cell 25(6):2115–2131. https://doi.org/10.1105/tpc.113.113068
Shaid S, Brandts CH, Serve H, Dikic I (2013) Ubiquitination and selective autophagy. Cell Death Differ 20(1):21–30. https://doi.org/10.1038/cdd.2012.72
Su W, Bao Y, Lu Y, He F, Wang S, Wang D, Yu X, Yin W, Xia X, Liu C (2020) Poplar autophagy receptor NBR1 enhances salt stress tolerance by regulating selective autophagy and antioxidant system. Front Plant Sci 11:568411. https://doi.org/10.3389/fpls.2020.568411
Svenning S, Lamark T, Krause K, Johansen T (2011) Plant NBR1 is a selective autophagy substrate and a functional hybrid of the mammalian autophagic adapters NBR1 and p62/SQSTM1. Autophagy 7(9):993–1010. https://doi.org/10.4161/auto.7.9.16389
Wang Q, Shen T, Ni L, Chen C, Jiang J, Cui Z, Wang S, Xu F, Yan R, Jiang M (2023) Phosphorylation of OsRbohB by the protein kinase OsDMI3 promotes H2O2 production to potentiate ABA responses in rice. Mol Plant 16(5):882–902. https://doi.org/10.1016/j.molp.2023.04.003
Waterson MJ, Chan TP, Pletcher SD (2015) Adaptive physiological response to perceived scarcity as a mechanism of sensory modulation of life span. J Gerontol A Biol Sci Med Sci 70(9):1088–1091. https://doi.org/10.1093/gerona/glv039
Xing Y, Wei X, Liu Y, Wang MM, Sui Z, Wang X, Zhu W, Wu M, Lu C, Fei YH, Jiang Y, Zhang Y, Wang Y, Guo F, Cao JL, Qi J, Wang W (2021) Autophagy inhibition mediated by MCOLN1/TRPML1 suppresses cancer metastasis via regulating a ROS-driven TP53/p53 pathway. Autophagy 18(8):1932–1954. https://doi.org/10.1080/15548627.2021.2008752
Xu ZY, Lee KH, Dong T, Jeong JC, Jin JB, Kanno Y, Kim DH, Kim SY, Seo M, Bressan RA, Yun DJ, Hwang I (2012) A vacuolar beta-glucosidase homolog that possesses glucose-conjugated abscisic acid hydrolyzing activity plays an important role in osmotic stress responses in Arabidopsis. Plant Cell 24(5):2184–2199. https://doi.org/10.1105/tpc.112.095935
Yoshida S, Fomo DA, Cock JH, Gomez KA (1976) Routine procedures for growing rice plants in culture solution. In: Laboratory manual for physiological studies of rice, pp 61–66
Young PG, Passalacqua MJ, Chappell K, Llinas RJ, Bartel B (2019) A facile forward-genetic screen for Arabidopsis autophagy mutants reveals twenty-one loss-of-function mutations disrupting six ATG genes. Autophagy 15(6):941–959. https://doi.org/10.1080/15548627.2019.1569915
Zhang Y, Su J, Duan S, Ao Y, Wang H (2011) A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods 7(1):30
Zhang T, Guo L, Wang Y, Yang Y (2018) Macroautophagy regulates nuclear NOTCH1 activity through multiple p62 binding sites. IUBMB Life 70(10):985–994. https://doi.org/10.1002/iub.1891
Zhou J, Wang J, Cheng Y, Chi YJ, Fan B, Yu JQ, Chen Z (2013) NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet 9(1):e1003196. https://doi.org/10.1371/journal.pgen
Zhou J, Wang J, Yu JQ, Chen Z (2014a) Role and regulation of autophagy in heat stress responses of tomato plants. Front Plant Sci 5:174. https://doi.org/10.3389/fpls.2014.00174
Zhou J, Zhang Y, Qi J, Chi Y, Fan B, Yu JQ, Chen Z (2014b) E3 ubiquitin ligase CHIP and NBR1-mediated selective autophagy protect additively against proteotoxicity in plant stress responses. PLoS Genet 10(1):e1004116. https://doi.org/10.1371/journal.pgen
Zhu C, Shen S, Zhang S, Huang M, Zhang L, Chen X (2022) Autophagy in bone remodeling: a regulator of oxidative stress. Front Endocrinol (lausanne) 13:898634. https://doi.org/10.3389/fendo.2022.898634
Zientara-Rytter K, Sirko A (2014) Significant role of PB1 and UBA domains in multimerization of Joka2, a selective autophagy cargo receptor from tobacco. Front Plant Sci 5:13. https://doi.org/10.3389/fpls.2014.00013
Zientara-Rytter K, Lukomska J, Moniuszko G, Gwozdecki R, Surowiecki P, Lewandowska M, Liszewska F, Wawrzynska A, Sirko A (2011) Identification and functional analysis of Joka2, a tobacco member of the family of selective autophagy cargo receptors. Autophagy 7(10):1145–1158. https://doi.org/10.4161/auto.7.10.16617
Funding
This work was supported by the National Natural Science Foundation of China (32272027, 32102235) and Natural Science Foundation of Jilin Province (20230101259JC).
Author information
Authors and Affiliations
Contributions
Z-YX devised the project. Z-YX and YL supervised the project. AM performed the most physiological analyses and wrote the manuscript. NN performed the most of biochemical assays and some physiological analyses. YS performed molecular cloning and some cell biological analyses. JW performed RNA-seq and data analysis. PG, JY, WL, GZ, and DZ performed some biochemical assays. D-JY provided helpful suggestions for improving the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Byeong-ha Lee.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ma, A., Nan, N., Shi, Y. et al. Autophagy receptor OsNBR1 modulates salt stress tolerance in rice. Plant Cell Rep 43, 17 (2024). https://doi.org/10.1007/s00299-023-03111-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00299-023-03111-9