Abstract
Basic leucine zipper transcription factor (bZIP) is involved in signaling transduction for various stress responses. Here we reported a bZIP transcription factor (accession: JX887153) isolated from a salt-resistant lotus root using cDNA-AFLP approach with RT-PCR and RACE-PCR method. Full-length cDNA which consisted of a single open reading frame encoded a putative polypeptide of 488 amino acids. On the basis of 78, 76, and 75 % sequence similarity with the bZIPs from Medicago truncatula (XP_003596814.1), Carica papaya (ABS01351.1) and Arabidopsis thaliana (NP_563810.2), we designed it as LrbZIP. Semi quantitative RT-PCR results, performed on the total RNA extracted from tips of lotus root, showed that LrbZIP expression was increased with 250 mM NaCl treatment for 18 h. Effects of low temperature on the expression of LrbZIP was also studied, and its expression was significantly enhanced with a 4 °C treatment for 12 h. In addition, LrbZIP expression was strongly induced by treatment with exogenous 100 μM ABA. To evaluate its function across the species, tobacco (Nicotiana tabacum L.) was transformed with LrbZIP in a binary vector construct. Transgenic plants exhibited higher resistance as compared with the control according to the results of the root growth, chlorophyll content and electrolyte leakage when exposed to NaCl treatment. In addition, LrCDPK2, LrLEA, and TPP also showed enhanced expression in the transgenic plants. Overall, expression of LrbZIP was probably very important for salt-resistant lotus root to survive through salt stress.
Similar content being viewed by others
References
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669
Maas E, Grieve C (1990) Spike and leaf development in salt-stressed wheat. Crop Sci 30:1309–1313
Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238
Husain S, Munns R, Condon A (2003) Effect of sodium exclusion trait on chlorophyll retention and growth of durum wheat in saline soil. Aus J of Agri Res 54:589–598
Munns R, James R, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043
Hall J, Flowers T (1973) The effect of salt on protein synthesis in the halophyte Suaeda maritima. Planta 110:361–368
Murguia JR, Belles JM, Serrano R (1995) A salt-sensitive 3′(2′),5′-bisphosphate nucleotidase involved in sulfate activation. Science 267:232–234
Salt DE (2004) Update on plant ionomics. Plant Physiol 136:2451–2456
Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527
Lahner B, Gong J, Mahmoudian M, Smith EL, Abid KB, Rogers EE, Guerinot ML, Harper JF, Ward JM, McIntyre L (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat Biotech 21:1215–1221
Santa-Cruz A, Acosta M, Rus A, Bolarin MC (1999) Short-term salt tolerance mechanisms in differentially salt tolerant tomato species. Plant Physiol Biochem 37:65–71
Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199
Wang X, Li Y, Ji W, Bai X, Cai H, Zhu D, Sun XL, Chen LJ, Zhu YM (2011) A novel Glycine soja tonoplast intrinsic protein gene responds to abiotic stress and depresses salt and dehydration tolerance in transgenic Arabidopsis thaliana. J Plant Physiol 168(11):1241–1248. doi:10.1016/j.jplph.2011.01.016
Zhang H, Mao X, Jing R, Chang X, Xie H (2011) Characterization of a common wheat (Triticum aestivum L.) TaSnRK2. 7 gene involved in abiotic stress responses. J Exp Bot 62:975–988
Yokotani N, Higuchi M, Kondou Y, Ichikawa T, Iwabuchi M, Hirochika H, Matsui M, Oda K (2011) A novel chloroplast protein, CEST induces tolerance to multiple environmental stresses and reduces photooxidative damage in transgenic Arabidopsis. J Exp Bot 62:557–569
Kang HG, Kim J, Kim B, Jeong H, Choi SH, Kim EK, Lee HY, Lim PO (2011) Overexpression of FTL1/DDF1, an AP2 transcription factor, enhances tolerance to cold, drought, and heat stresses in Arabidopsis thaliana. Plant Sci 180:634–641
Xu GY, Rocha PSCF, Wang ML, Xu ML, Cui YC, Li LY, Zhu YX, Xia X (2011) A novel rice calmodulin-like gene, OsMSR2, enhances drought and salt tolerance and increases ABA sensitivity in Arabidopsis. Planta 234(1):47–59. doi:10.1007/s00425-011-1386-z
Hu HH, You J, Fang YJ, Zhu XY, Qi ZY, Xiong LH (2010) Erratum to: characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Bio 72:567–568
Rodriguez-Uribe L, Connell MAO (2006) A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean (Phaseolus acutifolius) and common bean (P. vulgaris). J Exp Bot 5:1391–1398
Jakoby M, Weisshaar B, Droge-Laser W, Carbajosa JV, Tiedeman J, Kroj T (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111
Zhang X, Wang L, Meng H, Wen H, Fan Y, Zhao J (2011) Maize ABP9 enhances tolerance to multiple stresses in transgenic Arabidopsis by modulating ABA signaling and cellular levels of reactive oxygen species. Plant Mol Biol 75:365–378
Yanez M, Caceres S, Orellana S, Bastıas A, Verdugo I, Ruiz-Lara S, Casaretto JA (2009) An abiotic stress-responsive bZIP transcription factor from wild and cultivated tomatoes regulates stress-related genes. Plant Cell Rep 28:1497–1507
Wang YC, Gao CQ, Liang YN, Wang C, Yang CP, Liu GF (2010) A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress into tobacco plants. J Plant Physiol 167:222–230
Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidospsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high salinity conditions. Pro Natl Acad Sci USA 97:11632–11637
Xue GP, Loveridge CW (2003) HvDRF1 is involved in abscisic acid-mediated gene regulation in barley and produces two forms of AP2 transcriptional activators, interacting preferably with a CT-rich element. Plant J 37:326–339
Zou MJ, Guan YC, Ren HB, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66:675–683
Kim S (2005) The role of ABF family bZIP class transcription factors in stress response. Physiol Plant 126:519–527
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227
Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA-response element-binding factors. Plant J 44:939–949
Du H, Zhao X, You JS, Park JY, Kim SH, Chang KJ (2010) Antioxidant and hepatic protective effects of lotus root hot water extract with taurine supplementation in rats fed a high fat diet. J Biomed Sci 17(Suppl 1):S39. doi:10.1186/1423-0127-17-S1-S39
Sakamoto Y (1977) Lotus. Hosei University Press, Tokyo
Liu J, Zhang M, Wang S (2010) Processing characteristics and flavour of full lotus root powder beverage. J Sci Food Agric 90:2482–2489
Slocum PD, Robinson P (1996) Water gardening, water lilies and lotuses. Timber, Portland, OR
Borgi W, Ghedira K, Chouchane N (2007) Antiinflammatory and analgesic activities of zizyphus lotus root barks. Fitoterapia 78:16–19
Renato BRAZ, Hechenleitner AAW, Cavalcanti OA (2007) Extraction, structural modification and characterization of lotus roots polysaccharides (Nelumbo nucifera Gaertn). Excipient with potential application in modified drug delivery systems. Lat Am J Pharm 26:706–710
Terashima M, Awano K, Honda Y, Yoshino N, Mori T, Fujita H, Ohashi Y, Seguchi O, Kobayashi K, Yamagishi M, Fitzgerald PJ, Yock PG, Maeda K (2011) Arteries within the artery after kawasaki diease-A lotus root appearance by intravascular ultrasound. Circulation 106(7):887. doi:10.1161/01.CIR.0000030708.86783.92
Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M (1995) AFLP: a new technique for DNA fingerprinting. Nuc Acids Res 23:4407–4414
Lang P, Zhang C, Ebel R, Dane F, Dozier W (2005) Identification of cold acclimated genes in leaves of Citrus unshiu by mRNA differential display. Gene 359:111–118
Cheng LB, Huan ST, Sheng YD, Hua XJ, Song SQ, Jing XM (2009) GMCHI, cloned from soybean [Glycine max (L.) Meer.], enhances survival in transgenic Arabidopsis under abiotic stress. Plant Cell Rep 28:145–153
Vuylsteke M, Daele HVD, Vercauteren A, Zabeau M, Kuiper M (2006) Genetic dissection of transcriptional regulation by cDNAAFLP. Plant J 45:439–446
Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231
Hiscox JD, Israelstam GF (1979) A method for extraction of chlorophyll from leaf tissue without maceration. Can J Bot 59:463–469
Umezawa T, Mizumo K, Fujimura T (2002) Discrimination of genes expressed in response to the ionic or osmotic effect of salt stress in soybean with cDNAa-AFLP. Plant Cell Environ 25:1617–1625
Hurst HC (1994) Transcription factors 1: bZIP proteins. Protein Profile 1:123–168
Correa LGG, Riano-Pachon DM, Schrago CG, Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS One 3(8):e2944
Amoutzias GD, Veron AS, Weiner J, Robinson-Rechavi M, Bornberg-Bauer E, Oliver SG, Robertson DL (2007) One billion years of bZIP transcription factor evolution: conservation and change in dimerization and DNA-Binding site specificity. Mol Biol Evol 24:827–835
Huang XS, Liu JH, Chen XJ (2010) Overexpression of PtrABF gene, a bzip transcription factor isolated from Poncirus trifoliata, enhances dehydration and drought tolerance in tobacco via scavenging ROS and modulating expression of stress-responsive genes. BMC Plant Bio 10:230–248
Dong XF, Cui N, Wang L, Zhao XC, Qu B, Li TL, Zhang GL (2012) The SnRK protein kinase family and the function of SnRK1 protein kinase. Int J Agric Biol 14:575–579
Cho YH, Hong JW, Kim EC, Yoo SD (2012) Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development. Plant Physiol 158:1955–1964
Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia YL, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genomics 8:175
Sembdner G, Parthie B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Ann Rev Plant Biol 44:569–589
Yang S, Zeevaart J (2006) Expression of ABA 8′-hydroxylases in relation to leaf water relations and seed development in bean. Plant J 47:675–686
Finkelstein R, Gampala S, Rock C (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:15–45
Seki M, Narusaka M, Ishida J, Nanjo T, Fujita M, Oono Y, Kamiya A, Nakajima M, Enju A, Sakurai T (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J 31:279–292
Li C, Junttila O, Heino P, Palva E (2003) Different responses of northern and southern ecotypes of Betula pendula to exogenous ABA application. Tree Physiol 23:481–487
Menkens AE, Schindler U, Cashmore AR (1995) The G-box: a ubiquitous regulatory DNA element in plants bound by the GBF family of bZIPs protein. Trends Biochem Sci 20:506–512
Kim SY (2006) The role of ABF family bZIP class transcription factors in stress response. Physiol Plant 126:519–527
Jaglo K, Kleff S, Amundsen K, Zhang X, Haake V, Zhang J, Deits T, Thomashow M (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Ann Rev Plant Biol 57:781–803
García MNM, Giammaria V, Grandellis C, Téllez-Iñón MT, Ulloa RM, Capiati DA (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235:761–778
Hossain MA, Lee YJ, Cho JI, Ahn CH, Lee SK, Jeon JS, Kang H, Lee CH, An G, Park PB (2010) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol 72:557–566
Kim S, Kang JY, Cho D-I, Park JH, Kim SY (2004) 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
Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA forfull activation. Plant J 61:672–685
Kang J, Choi H, Im M, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357
Abdeen A, Schnell J, Miki B (2010) Transcriptome analysis reveals absence of unintended effects in drought-tolerant transgenic plants overexpressing the transcription factor ABF3. BMC Genomics 211:69–90
Oh SJ, Song SI, Kim YS, Jang HJ, Kim SY, Kim M, Kim YK, Nahm BH, Kim JK (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351
Shi H, Lee B, Wu S, Zhu J (2003) Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nat Biotech 21:81–85
Apse MP, Blumwald E (2002) Engineering salt tolerance in plants. Cur Opin Biotechnol 13:146–150
Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768
Zhang HX, Hodson JN, Williams JP, 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
Xue Z, Zhi D, Xue G, Zhang H, Zhao Y, Xia G (2004) Enhanced salt tolerance of transgenic wheat (Tritivum aestivum L.) expressing a vacuolar Na+/H+ antiporter gene with improved grain yields in saline soils in the field and a reduced level of leaf Na+. Plant Sci 167:849–859
Wu CA, Yang GD, Meng QW, Zheng CC (2004) The cotton GhNHX1 gene encoding a novel putative tonoplast Na(+)/H(+) antiporter plays an important role in salt stress. Plant Cell Physiol 45:600–607
Cheng SH, Willmann MR, Chen HC, Sheen J (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129:469–485
Ludwig AA, Romeis T, Jones JDG (2004) CDPK mediated signalling pathways: specificity and cross talk. J Exp Bot 55:181–188
Sathyanarayanan P, Poovaiah B (2004) Decoding Ca(2+) signals in plants. CRC Crit Rev Plant Sci 23:1–11
Witte CP, Keinath N, Dubiella U, Demoulière R, Seal A, Romeis T (2010) Tobacco calcium-dependent protein kinases are differentially phosphorylated in vivo as part of a kinase cascade that regulates stress response. J Biological Chem 285:9740–9748
Romeis T (2001) Protein kinases in the plant defence response. Curr Opin Plant Biol 4:407–414
Dalal M, Tayal D, Chinnusamy V, Bansal KC (2009) Abiotic stress and ABA-inducible Group 4 LEA from Brassica napus plays a key role in salt and drought tolerance. J Biotechnol 139:137–145
Ginger A, Swire-Clark WR, Marcotte JR (1999) The wheat LEA protein Em functions as an osmoprotective molecule in Saccharomyces cerevisia. Plant Mol Biol 39:117–128
Zhang Y, Li Y, Lai J, Zhang H, Liu Y, Liang L, Xie Q (2012) Ectopic expression of a LEA protein gene TsLEA1 from Thellungiella salsuginea confers salt-tolerance in yeast and Arabidopsis. Mol Biol Rep 39:4627–4633
Imai L, Chang A, Otha EA, Bray TM (1996) A lea-class gene of tomato confers salt and freezing tolerance when expressed in Saccharomyces cerevisiae. Gene 170:243–248
Zhang L, Ohta A, Takagi M, Imai R (2000) Expression of plant group 2 and group 3 lea genes in Saccharomyces cerevisiae revealed functional divergence among LEA proteins. J Biochem 127:611–616
Lai SLN, Grlyani VH, Khurana PJ (2008) Overexpression of HVA1 gene from barley generates tolerance to salinity and water stress in transgenic mulberry (Morus indica). Transgenic Res 17:651–663
Blackman SA, Wettlaufer SH, Obendorf RL, Leopold AC (1991) Maturation proteins associated with desiccation tolerance in soybean. Plant Physiol 96:868–874
Xu D, Duan X, Wang B, Hong B, Ho THD, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 1:249–257
RoyChoudhury A, Roy C, Sengupta DN (2007) Transgenic tobacco plants overexpressing the heterologous lea gene Rab16A from rice during high salt and water deficit display enhanced tolerance to salinity stress. Plant Cell Rep 26:1839–1859
Kondrak M, Marincs F, Antal F, Juhasz Z, Banfalvi Z (2012) Effects of yeast trehalose-6-phosphate synthase 1 on gene expression and carbohydrate contents of potato leaves under drought stress conditions. BMC Plant Biol 12:74
Reina-Bueno M, Argandoña M, Salvador M, Rodríguez-Moya J, Iglesias-Guerra F, Csonka LN, Nieto JJ, Vargas C (2012) Role of trehalose in salinity and temperature tolerance in the model halophilic bacterium Chromohalobacter salexigens. PLoS One 7:e33587
Wingler A (2002) The function of trehalose biosynthesis in plants. Phytochemistry 60:437–440
Miranda JA, Avonce N, Suárez R, Thevelein JM, Van Dijck P, Iturriaga G (2007) A bifunctional TPS-TPP enzyme from yeast confers tolerance to multiple and extreme abiotic-stress conditions in transgenic Arabidopsis. Planta 226:1411–1421
Ge L, Chao D, Shi M et al (2008) Overexpression of the trehalose-6-phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress-responsive genes. Planta 228:191–201
Acknowledgments
Authors thank Xiong Liben for her suggestions and language check. This work was supported by Special Fund for Agro-scientific Research in the Public Interest (200903017-02), China Postdoctoral Science Foundation (2012M511805) and Jiangsu Postdoctoral Science Foundation (1102144C).
Author information
Authors and Affiliations
Corresponding author
Additional information
Libao Cheng and Shuyan Li have contribution equally to this research work.
Rights and permissions
About this article
Cite this article
Cheng, L., Li, S., Hussain, J. et al. Isolation and functional characterization of a salt responsive transcriptional factor, LrbZIP from lotus root (Nelumbo nucifera Gaertn). Mol Biol Rep 40, 4033–4045 (2013). https://doi.org/10.1007/s11033-012-2481-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-012-2481-3