EcbZIP60, a basic leucine zipper transcription factor from Eleusine coracana L. improves abiotic stress tolerance in tobacco by activating unfolded protein response pathway

Alvim FC, Carolino SMB, Cascardo JCM, Nunes CC, Martinez CA, Otoni WC, Fontes EPB (2001) Enhanced accumulation of BiP in transgenic plants confers tolerance to water. Plant Physiol 126:1042–1054 Bengert P, Dandekar T (2003) A software tool-box for analysis of regulatory RNA elements. Nucl Acids Res 3:3441–3445 Chen L, Hellmann H (2013) Plant E3 ligases: flexible enzymes in a sessile world. Mol Plant 6:1388–1404 Chen H, Chen W, Zhou J, He H, Chen L, Chen H (2012) Basic leucine zipper transcription factor OsbZIP16 positively regulates drought resistance in rice. Plant Sci 193:8–17 Christensen A, Svensson K, Persson S, Jung J, Michalak M, Widell S, Sommarin M (2008) Functional characterization of Arabidopsis calreticulin1a: a key alleviator of endoplasmic reticulum stress. Plant Cell Physiol 49:912–924 Datta K, Schmidt A, Marcus A (1989) Characterization of two soybean repetitive proline-rich proteins and a cognate cDNA from geminated axes. Plant Cell 1:945–952 Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH (2011) Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci USA 108:7247–7252 Fisher RA (1960) The design of experiments. Hafner Publishing Company, Inc., New York, pp 1–248 Fu X-Z, Khan EU, Hu S-S, Fan Q-J, Liu J-H (2011) Overexpression of the betaine aldehyde dehydrogenase gene from Atriplex hortensis enhances salt tolerance in the transgenic trifoliate orange (Poncirus trifoliata L. Raf.). Environ Exp Bot 74:106–113 Fujita M, Mizukado S, Fujita Y, Ichikawa T, Nakazawa M, Seki M, Matsui M, Yamaguchi-Shinozaki K, Shinozaki K (2007) Identification of stress-tolerance-related transcription-factor genes via mini-scale full length cDNA over-eXpressor (FOX) gene hunting system. Biochem Biophys Res Commun 364:250–257 Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915 Gay C, Collins J, Gebicki JM (1999) Hydroperoxide assay with the ferric-xylenol orange complex. Anal Biochem 273:149–155 Gelebart P, Opas M, Michalak M (2005) Calreticulin, a Ca2+-binding chaperone of the endoplasmic reticulum. Int J Biochem Cell Biol 37:260–266 Govind G, Harshavardhan VT, Patricia JK, Dhanalakshmi R, Senthil- Kumar M, Sreenivasulu N, Udayakumar M (2009) Identification and functional validation of a unique set of drought induced genes preferentially expressed in response to gradual water stress in peanut. Mol Genet Genomics 281:591–605 Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414 Guo P, Baum M, Grando S, Ceccarelli S, Guihua Bai G, Li R et al (2009) Differentially expressed genes between drought-tolerant and drought-sensitive barley genotypes in response to drought stress during the reproductive stage. J Exp Bot 60:3531–3544 Hayashi S, Wakasa Y, Takahashi H, Kawakatsu T, Takaiwa F (2012) Signal transduction by IRE1-mediated splicing of bZIP50 and other stress sensors in the ER stress response of rice. Plant J 69:946–956 Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334 Hossain MA, Lee Y, Cho J-I, Ahn C-H, Lee S-K, Jeon J-S et al (2010) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signalling in rice. Plant Mol Biol 72:557–566 Howell SH (2013) Endoplasmic reticulum stress responses in plants. Ann Rev Plant Biol 64:477–499 Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285 Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20:3107–3121 Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111 Jin XF, Jiong AS, Peng RH, Liu JG, Gao F, Chen JM, Yao QH (2010) OsAREB1, an ABRE binding protein responding to ABA and glucose, has multiple functions in Arabidopsis. BMC Rep 43:34–39 Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14:343–357 Leborgne-Castel N, Jelitto-Van Dooren EPWM, Crofts AJ, Denecke J (1999) Overexpression of BiP in tobacco alleviates endoplasmic reticulum stress. Plant Cell 11:459–470 Lee SC, Choi HW, Hwang IS, Choi DS, Hwang BK (2006) Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses. Planta 224:1209–1225 Lenka SK, Katiyar A, Chinnusamy V, Bansal KC (2011) Comparative analysis of drought-responsive transcriptome in Indica rice genotypes with contrasting drought tolerance. Plant Biotechnol J 9:315–327 Li B, Wei A, Song C, Li N, Zhang J (2008) Heterologous expression of the TsVP gene improves the drought resistance of maize. Plant Biotechnol J 6:146–159 Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240 Liu JX, Srivastava R, Che P, Howell SH (2007a) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119 Liu JX, Srivastava R, Che P, Howell SH (2007b) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909 Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787 Lu D-P, Christopher DA (2008) Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol Genet Genomics 280:199–210 Lu G, Gao C, Zheng X, Han B (2009) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Planta 229:605–615 Lv SL, Zhang K, Gao Q, Lian L, Song Y, Zhang J (2008) Overexpression of an H+-PPase gene from Thellungiella halophila in cotton enhances salt tolerance and improves growth and photosynthetic performance. Plant Cell Physiol 49:1150–1164 Marraccini P, Vinecky F, Alves GSC, Ramos HJO, Elbelt S, Vieira NG et al (2012) Differentially expressed genes and proteins upon drought acclimation in tolerant and sensitive genotypes of Coffea canephora. J Exp Bot 63:4191–4212 Mukherjee K, Choudhury AR, Gupta B, Gupta S, Sengupta DN (2006) An ABRE-binding factor, OSBZ8, is highly expressed in salt tolerant cultivars than in salt sensitive cultivars of indica rice. BMC Plant Biol 6:18 Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350 Olszewski N, Sun TP, Gubler F (2002) Gibberellin signalling: biosynthesis, catabolism and response pathway. Plant Cell 14:61–80 Patterson M, Sneyd J, Friel DD (2007) Depolarization-induced Calcium responses in sympathetic neurons: relative contributions from Ca2+ entry, extrusion, ER/mitochondrial Ca2+ uptake and release, and Ca2+ buffering. J Gen Physiol 129:29–56 Powell LE, Tautvydas KJ (1967) Chromatography of gibberellins on silica gel partition columns. Nature 213:292–309 Raheleh R, Ramazanali K-N, Ali G, Abdolreza B, Farzaneh N, Masoud R (2012) Use of biochemical indices and antioxidant enzymes as a screening technique for drought tolerance in Chickpea genotypes (Cicer arietinum L.). Afr J Agric Res 39:5372–5380 Ramegowda V, Senthil-Kumar M, Nataraja KN, Reddy MK, Mysore KS, Udayakumar M (2012) Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS One 7:e40397 Recchia GH, Caldas DGG, Beraldo ALA, da Silva MJ, Tsai SM (2013) Transcriptional analysis of drought-induced genes in the roots of a tolerant genotype of the common bean (Phaseolus vulgaris L.). Int J Mol Sci 14:7155–7179 Sanan-Mishra N, Pham XH, Sopory SK, Tuteja N (2005) Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. Proc Natl Acad Sci USA 102:509–514 Schutze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13:247–255 Shameer K, Ambika S, Varghese SM, Karaba N, Udayakumar M, Sowdhamini R (2009) STIFDB—arabidopsis stress responsive TF database. Int J Plant Genomics 5:1–8 Shaterian J, Georges F, Hussain A, Waterer D, Jong HD, Tanino KK (2005) Root to shoot communication and abscisic acid in calreticulin (CR) gene expression and salt-stress tolerance in grafted diploid potato clones. Environ Exp Bot 53:323–332 Shimizu H, Sato K, Berberich T, Miyazaki A, Ozaki R, Imai R, Kusano T (2005) LIP19, a basic region leucine zipper protein, is a Fos-like molecular switch in the cold signaling of rice plants. Plant Cell Physiol 46:1623–1634 Sun L, Yang Z-T, Song Z-T, Wang M-J, Sun L, Lu S-J, Liu J-X (2013) The plant-specific transcription factor gene NAC103 is induced by bZIP60 through a new cis-regulatory element to modulate the unfolded protein response in Arabidopsis. Plant J 76:274–286 Takahashi H, Kawakatsu T, Wakasa Y, Hayashi S, Takaiwa F (2012) A Rice transmembrane bzip transcription factor, OsbZIP39, regulates the endoplasmic reticulum stress response. Plant Cell Physiol 53:144–153 Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768 Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi- Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637 Upreti KK, Reddy YTN, Shivu Prasad SR, Bindu GV, Jayaram HL, Rajan Shailendra (2013) Hormonal changes in response to paclobutrazol induced early flowering in mango cv. Totapuri. Sci Hort 150:414–418 Valente MA, Faria JA, Soares-Ramos JR, Reis PA, Pinheiro GL, Piovesan ND et al (2009) The ER luminal binding protein (BiP) mediates an increase in drought tolerance in soybean and delays drought-induced leaf senescence in soybean and tobacco. J Exp Bot 60:533–546 Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949–956 Wakasa Y, Yasuda H, Oono Y, Kawakatsu T, Hirose S, Takahashi H et al (2011) Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. Plant J 65:675–689 Wang Y, Gao C, Liang Y, Wang C, Yang C, Liu G (2010) A novel bZIP gene from Tamarix hispida mediates physiological responses to salt stress in tobacco plants. J Plant Physiol 167:222–230 Wang P, Li Z, Wei J, Zhao Z, Sun D, Cui S (2012) A Na+/Ca2+ exchanger-like protein (AtNCL) involved in salt stress in Arabidopsis. J Biol Chem 287:44062–44070 Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952 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 Yang Y-G, Lv W-T, Li M-J, Wang B, Sun D-M, Deng X (2013) Maize membrane-bound transcription factor Zmbzip17 is a key regulator in the cross-talk of ER quality control and ABA signaling. Plant Cell Physiol 54:2020–2033 Zhu JK (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53:247–273 Zou M, Guan Y, Ren H, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66:675–683