Abstract
RAV1 (Related to ABI3/VP1) has been widely studied in plants such as Arabidopsis, pepper and rice; however, the functions of RAVs in maize have not been described. In this study, a novel gene ZmRAV1 was amplified from a Zea mays inbred line H21. This gene was predicted to encode a transcription factor with 2 distinct DNA-binding domains, AP2 and B3, which are both present in members of the RAV family. Transient expression assays of a 35S::YFP-ZmRAV1 fusion construct in onion epidermal cells revealed that the ZmRAV1 protein is localized in the nucleus. ZmRAV1 expression was upregulated in maize by dehydration, salt, and ABA stress. Overexpression of ZmRAV1 in transgenic Arabidopsis plants enhanced salt and osmotic stress tolerance compared to the wild type, further confirmed by increased survival rate, longer primary roots and physiological characteristics such as lower relative electrolyte leakages. Illumina sequencing revealed that a number of salt responsive genes, primarily involved in reactive oxygen species scavenging, were upregulated in the ZmRAV1 transgenic line compared to the wild-type plants. The detection of the activity of antioxidant enzyme in WT and 35S::ZmRAV1 plants under salt stress shown that, higher maintenance of POD contributes to the salt tolerance of Arabidopsis transgenic lines. These data suggest that ZmRAV1 functions as a transcriptional activator that may be involved in the salt and osmotic resistance signaling pathways in plants.
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Abeles FB, Dunn LJ, Morgens P, Callahan A, Dinterman RE, Schmidt J (1988) Induction of 33-kD and 60-kD peroxidases during ethylene-induced senescence of cucumber cotyledons. Plant Physiol 87:609–615
Akai M, Onai K, Morishita M, Mino H, Shijuku T, Maruyama H, Arai F, Itoh S, Hazama A, Checchetto V, Szabo I, Yukutake Y, Suematsu M, Yasui M, Ishiura M, Uozumi N (2012) Aquaporin AqpZ is involved in cell volume regulation and sensitivity to osmotic stress in Synechocystis sp. strain PCC 6803. J Bacteriol 194:6828–6836
Allen RD, Webb RP, Schake SA (1997) Use of transgenic plants to study antioxidant defenses. Free Radic Biol Med 23:473–479
Amaya I, Botella MA, de la Calle M, Medina MI, Heredia A, Bressan RA, Hasegawa PM, Quesada MA, Valpuesta V (1999) Improved germination under osmotic stress of tobacco plants overexpressing a cell wall peroxidase. FEBS Lett 457:80–84
Amir Hossain M, Lee Y, 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
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995
Cao Z, Jia Z, Liu Y, Wang M, Zhao J, Zheng J, Wang G (2010) Constitutive expression of ZmsHSP in Arabidopsis enhances their cytokinin sensitivity. Mol Biol Rep 37:1089–1097
Dai M, Hu Y, Zhao Y, Liu H, Zhou DX (2007) A WUSCHEL-LIKE HOMEOBOX gene represses a YABBY gene expression required for rice leaf development. Plant Physiol 144:380–390
Diedhiou CJ, Popova OV, Golldack D (2009a) Comparison of saltresponsive gene regulation in rice and in the salt-tolerant Festuca rubra ssp. litoralis. Plant Signal Behav 4:533–535
Diedhiou CJ, Popova OV, Golldack D (2009b) Transcript profiling of the salt-tolerant Festuca rubra ssp. litoralis reveals a regulatory network controlling salt acclimatization. J Plant Physiol 166:697–711
Fernandes AP, Holmgren A (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6:63–74
Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM (1998) The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA 2 domain protein. Plant Cell 10:1043–1054
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690
Ghars MA, Richard L, Lefebvre-De Vos D, Leprince AS, Parre E, Bordenave M, Abdelly C, Savoure A (2012) Phospholipases C and D modulate proline accumulation in Thellungiella halophila/salsuginea differently according to the severity of salt or hyperosmotic stress. Plant Cell Physiol 53:183–192
Giraudat J, Hauge BM, Valon C, Smalle J, Parcy F, Goodman HM (1992) Isolation of the Arabidopsis ABI3 gene by positional cloning. Plant Cell 4:1251–1261
Guo Y, Huang C, Xie Y, Song F, Zhou X (2010) A tomato glutaredoxin gene SlGRX1 regulates plant responses to oxidative, drought and salt stresses. Planta 232:1499–1509
Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant Cell Physiol 42:462–468
Hsieh TH, Li CW, Su RC, Cheng CP, Sanjaya, Tsai YC, Chan MT (2010) A tomato bZIP transcription factor, SlAREB, is involved in water deficit and salt stress response. Planta 231:1459–1473
Hu W, Yuan Q, Wang Y, Cai R, Deng X, Wang J, Zhou S, Chen M, Chen L, Huang C, Ma Z, Yang G, He G (2012) Overexpression of a wheat aquaporin gene, TaAQP8, enhances salt stress tolerance in transgenic tobacco. Plant Cell Physiol 53:2127–2141
Hu YX, Wang YX, Liu XF, Li JY (2004) Arabidopsis RAV1 is downregulated by brassinosteroid and may act as a negative regulator during plant development. Cell Res 14:8–15
Huang XY, Chao DY, Gao JP, Zhu MZ, Shi M, Lin HX (2009) A previously unknown zinc finger protein, DST, regulates drought and salt tolerance in rice via stomatal aperture control. Genes Dev 23:1805–1817
Je BI, Piao HL, Park SJ, Park SH, Kim CM, Xuan YH, Huang J, Do Choi Y, An G, Wong HL, Fujioka S, Kim MC, Shimamoto K, Han CD (2010) RAV-Like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell 22:1777–1791
Jiang Y, Yang B, Deyholos MK (2009) Functional characterization of the Arabidopsis bHLH92 transcription factor in abiotic stress. Mol Genet Genomics 282:503–516
Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225
Kagaya Y, Ohmiya K, Hattori T (1999) RAV1, a novel DNA-binding protein, binds to bipartite recognition sequence through two distinct DNA-binding domains uniquely found in higher plants. Nucleic Acids Res 27:470–478
Kukavica BM, Veljovicc-Jovanovicc SD, Menckhoff L, Luthje S (2012) Cell wall-bound cationic and anionic class III isoperoxidases of pea root: biochemical characterization and function in root growth. J Exp Bot 63:4631–4645
Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967
Lippold F, Sanchez DH, Musialak M, Schlereth A, Scheible WR, Hincha DK, Udvardi MK (2009) AtMyb41 regulates transcriptional and metabolic responses to osmotic stress in Arabidopsis. Plant Physiol 149:1761–1772
Marrs KA (1996) The functions and regulation of glutathione stransferases in plants. Annu Rev Plant Physiol Plant Mol Biol 47:127–158
McCarty DR, Hattori T, Carson CB, Vasil V, Lazar M, Vasil IK (1991) The Viviparous-1 developmental gene of maize encodes a novel transcriptional activator. Cell 66:895–905
Meyer Y, Buchanan BB, Vignols F, Reichheld JP (2009) Thioredoxins and glutaredoxins: unifying elements in redox biology. Annu Rev Genet 43:335–367
Miller JH (1992) In A short course in bacterial genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor:74
Morin R, Bainbridge M, Fejes A, Hirst M, Krzywinski M, Pugh T, McDonald H, Varhol R, Jones S, Marra M (2008) Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. Biotechniques 45:81–94
Muries B, Carvajal M, Martinez-Ballesta MD (2013) Response of three broccoli cultivars to salt stress, in relation to water status and expression of two leaf aquaporins. Planta
Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432
Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95
Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, 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
Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182
Raffaello T, Kerio S, Asiegbu FO (2012) Role of the HaHOG1 MAP kinase in response of the conifer root and but rot pathogen (Heterobasidion annosum) to osmotic and oxidative stress. PLoS One 7:e31186
Riechmann JL, Heard J, Martin G, Reuber L, Jiang C, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu G (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110
Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646
Rouhier N, Gelhaye E, Jacquot JP (2004) Plant glutaredoxins: still mysterious reducing systems. Cell Mol Life Sci 61:1266–1277
Rouhier N, Unno H, Bandyopadhyay S, Masip L, Kim SK, Hirasawa M, Gualberto JM, Lattard V, Kusunoki M, Knaff DB, Georgiou G, Hase T, Johnson MK, Jacquot JP (2007) Functional, structural, and spectroscopic characterization of a glutathioneligated [2Fe-2S] cluster in poplar glutaredoxin C1. Proc Natl Acad Sci USA 104:7379–7384
Roxas VP, Lodhi SA, Garrett DK, Mahan JR, Allen RD (2000) Stress tolerance in transgenic tobacco seedlings that overexpress glutathione S-transferase/glutathione peroxidase. Plant Cell Physiol 41:1229–1234
Roxas VP, Smith RK, Jr., Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathione peroxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991
Shannon LM, Kay E, Lew JY (1966) Peroxidase isozymes from horseradish roots. I. Isolation and physical properties. J Biol Chem 241:2166–2172
Sohn KH, Lee SC, Jung HW, Hong JK, Hwang BK (2006) Expression and functional roles of the pepper pathogen-induced transcription factor RAV1 in bacterial disease resistance, and drought and salt stress tolerance. Plant Mol Biol 61:897–915
Suzuki M, Kao CY, McCarty DR (1997) The conserved B3 domain of VIVIPAROUS1 has a cooperative DNA binding activity. Plant Cell 9:799–807
Swaminathan K, Peterson K, Jack T (2008) The plant B3 superfamily. Trends Plant Sci 13:647–655
Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11:1195–1206
Wilson K, Long D, Swinburne J, Coupland G (1996) A Dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. Plant Cell 8:659–671
Woo HR, Kim JH, Kim J, Lee U, Song IJ, Lee HY, Nam HG, Lim PO (2010) The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. J Exp Bot 61:3947–3957
Wu HJ, Zhang Z, Wang JY, Oh DH, Dassanayake M, Liu B, Huang Q, Sun HX, Xia R, Wu Y, Wang YN, Yang Z, Liu Y, Zhang W, Zhang H, Chu J, Yan C, Fang S, Zhang J, Wang Y, Zhang F, Wang G, Lee SY, Cheeseman JM, Yang B, Li B, Min J, Yang L, Wang J, Chu C, Chen SY, Bohnert HJ, Zhu JK, Wang XJ, Xie Q (2012) Insights into salt tolerance from the genome of Thellungiella salsuginea. Proc Natl Acad Sci USA 109:12219–12224
Xue J, Bao YY, Li BL, Cheng YB, Peng ZY, Liu H, Xu HJ, Zhu ZR, Lou YG, Cheng JA, Zhang CX (2010) Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS One 5:e14233
Yan L, Xu C, Kang Y, Gu T, Wang D, Zhao S, Xia G (2013) The heterologous expression in Arabidopsis thaliana of sorghum transcription factor SbbHLH1 downregulates lignin synthesis. J Exp Bot 64:3021–3032
Yang O, Popova OV, Suthoff U, Luking I, Dietz KJ, Golldack D (2009) The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436:45–55
Yang R, Deng C, Ouyang B, Ye Z (2011) Molecular analysis of two salt-responsive NAC-family genes and their expression analysis in tomato. Mol Biol Rep 38:857–863
Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229:1065–1075
Zhang G, Chen M, Li L, Xu Z, Chen X, Guo J, Ma Y (2009) Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco. J Exp Bot 60:3781–3796
Zhang L, Xi D, Li S, Gao Z, Zhao S, Shi J, Wu C, Guo X (2011) A cotton group C MAP kinase gene, GhMPK2, positively regulates salt and drought tolerance in tobacco. Plant Mol Biol 77:17–31
Zheng J, Fu J, Gou M, Huai J, Liu Y, Jian M, Huang Q, Guo X, Dong Z, Wang H, Wang G (2010) Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Mol Biol 72:407–421
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Zhu Q, Zhang J, Gao X, Tong J, Xiao L, Li W, Zhang H (2010) The Arabidopsis AP2/ERF transcription factor RAP2.6 participates in ABA, salt and osmotic stress responses. Gene 457:1–12
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Min, H., Zheng, J. & Wang, J. Maize ZmRAV1 contributes to salt and osmotic stress tolerance in transgenic arabidopsis. J. Plant Biol. 57, 28–42 (2014). https://doi.org/10.1007/s12374-013-0284-2
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DOI: https://doi.org/10.1007/s12374-013-0284-2