Abstract
Key message
Here, we reviewed major transcription factors of maize that confer drought stress tolerance, and their target genes and involved signaling pathway. Transcription factors in maize can be promising candidates for improving comprehensive resistance of multiple environmental stimuli.
Abstract
Adverse environmental stress is the main influencing factor affecting plant growth and reproduction, which poses tremendous threats to sustainable agriculture development and crops productivity worldwide. Among various abiotic stress factors, drought is the most vital adversity with the characteristics of frequent occurrences, long duration, and globality. Maize (Zea mays L.) is a major source of food supply for human being and livestock and recently for biofuel. Maize is the crop that is highly susceptible to drought stress. Drought stress tolerance in plants is quite complex, and it is not ideal to improve crop drought tolerance through a single resistant gene. Transcription factors participate in the regulation of plant growth and development, morphogenesis, and various environmental stress responses via regulating the expression level of their target stress-responsive genes independently or cross talk with other transcription factors, thereby the comprehensive resistance of multiple stresses in crops is improved. This review aims to summarize the major drought-tolerant transcription factors in maize and their regulatory network. With the continuous identification of maize transcription factors, more will be demonstrated to confer drought tolerance either in maize or other crops. It is expected that the transcription factors will greatly enrich the functional gene resources and will be a benefit to drought-tolerant maize cultivars breeding.
Similar content being viewed by others
References
Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78
Arase F, Nishitani H, Egusa M, Nishimoto N, Sakurai S, Sakamoto N, Kaminaka H (2012) IAA8 involved in lateral root formation interacts with the TIR1 auxin receptor and ARF transcription factors in Arabidopsis. PLoS ONE 7:e43414
Bartoli CG, Casalongué CA, Simontacchi M, Marquez-Garcia B, Foyer CH (2013) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88
Bruno L, Pacenza M, Forgione I, Lamerton LR, Greco M, Chiappetta A, Bitonti MB (2017) In Arabidopsis thaliana cadmium impact on the growth of primary root by altering SCR expression and auxin-cytokinin cross-talk. Front Plant Sci 8:1323
Cai R, Zhao Y, Wang Y, Lin Y, Peng X, Li Q, Chang Y, Jiang H, Xiang Y, Cheng B (2014) Overexpression of a maize WRKY58 gene enhances drought and salt tolerance in transgenic rice. Plant Cell Tissue Organ Cult 119(3):565–577
Cai R, Dai W, Zhang C, Wang Y, Wu M, Zhao Y, Ma Q, Xiang Y, Cheng B (2017) The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta 246(6):1215–1231
Chang W, Yin D (2009) Overexpression of maize ZmDBP3 enhances tolerance to drought and cold stress in transgenic Arabidopsis plants. Biologia 64(6):1108–1114
Cushman JC, Bohnert HJ (2000) Genomic approaches to plant stress tolerance. Curr Opin Plant Biol 3(2):117–124
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Ann Rev Plant Biol 61:651–679
Daryanto S, Wang L, Jacinthe PA (2016) Global synthesis of drought effects on maize and wheat production. PLoS ONE 11(5):e0156362
Datta K, Baisakh N, Ganguly M, Krishnan S, Yamaguchi Shinozaki K, Datta SK (2012) Overexpression of Arabidopsis and rice stress genes’ inducible transcription factor confers drought and salinity tolerance to rice. Plant Biotechnol J 10(5):579–586
Edmeades GO (2013) Progress in achieving and delivering drought tolerance in maize-an update. ISAAA, Ithaca, NY
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206
Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612
Hu HH, Dai MQ, Yao JL, Xiao BZ, Li XH, Zhang QF, Xiong LZ (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 35:12987–12992
Jia Z, Lian Y, Zhu Y, He J, Cao Z, Wang G (2009) Cloning and characterization of a putative transcription factor induced by abiotic stress in Zea mays. Afr J Biotechnol 8(24):6764–6771
Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, PareekA S-P (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029
Kakumanu A, Ambavaram MM, Klumas C, Krishnan A, Batlang U, Myers E, Grene R, Pereira A (2012) Effects of drought on gene expression in maize reproductive and leaf meristem tissue revealed by RNA-Seq. Plant Physiol 160:846–867
Kim YS, Kim SG, Park JE, Park HY, Lim MH, Chua NH, Park CM (2006) A membrane-bound NAC transcription factor regulates cell division in Arabidopsis. Plant Cell 18(11):3132–3144
Kim YS, Sakuraba Y, Han SH, Yoo SC, Paek NC (2013) Mutation of the Arabidopsis NAC016 transcription factor delays leaf senescence. Plant Cell Physiol 54:1660–1672
Kimotho RN, Baillo EH, Zhang Z (2019) Transcription factors involved in abiotic stress responses in Maize and their roles in enhanced productivity in the post genomics era. Peer J 7:e7211
Kizis D, Pagès M (2002) Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J 30(6):679–689
Krichevsky A, Zaltsman A, Kozlovsky SV, Tian GW, Citovsky V (2009) Regulation of root elongation by histone acetylation in Arabidopsis. J Mol Biol 385:45–50
Lata C, Yadav A, Prasad M (2011) Role of plant transcription factors in abiotic stress tolerance. Abiotic stress response in plants, vol 10. INTECH Open Access Publishers, London, pp 269–296
Lee SJ, Kang JY, Park HJ, Kim MD, Bae MS, Choi HI, Kim SY (2010) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity. Plant Physiol 153(2):716–727
Li H, Gao Y, Xu H, Dai Y, Deng D, Chen J (2013) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. Plant Growth Regul 70(3):207–216
Lim J, Jung JW, Lim CE, Lee MH, Kim BJ, Kim M, Bruce WB, Benfey PN (2005) Conservation and diversification of SCARECROW in maize. Plant Mol Biol 59(4):619–630
Liu HT, Li B, Shang ZL, Li XZ, Mu RL, Sun DY, Zhou RG (2003) Calmodulin is involved in heat shock signal transduction in wheat. Plant Physiol 132(3):1186–1195
Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K, Qin F (2013a) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet 9(9):e1003790
Liu X, Zhai S, Zhao Y, Sun B, Liu C, Yang A, Zhang J (2013b) Overexpression of the phosphatidylinositol synthase gene (ZmPIS) conferring drought stress tolerance by altering membrane lipid composition and increasing ABA synthesis in maize. Plant Cell Environ 36(5):1037–1055
Llorca CM, Potschin M, Zentgraf U (2014) bZIPs and WRKYs: two large transcription factor families executing two different functional strategies. Front Plant Sci 5:169
Lu M, Ying S, Zhang DF, Shi YS, Song YC, Wang TY, Li Y (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31(9):1701–1711
Luan M, Xu M, Lu Y, Zhang L, Fan Y, Wang L (2015) Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. Gene 555(2):178–185
Ma H, Liu C, Li Z, Ran Q, Xie G, Wang B, Fang S, Chu J, Zhang J (2018) ZmbZIP4 contributes to stress resistance in maize by regulating ABA synthesis and root development. Plant Physiol 178(2):753–770
Mantovani R (1999) The molecular biology of the CCAAT-binding factor NF-Y. Gene 239(1):15–27
Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran LS, Qin F (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6:8326
Mao H, Yu L, Han R, Li Z, Liu H (2016) ZmNAC55, a maize stress-responsive NAC transcription factor, confers drought resistance in transgenic Arabidopsis. Plant Physiol Biochem 105:55–66
Mitsuda N, Seki M, Shinozaki K, Ohme-Takagi M (2005) The NAC transcription factors NST1 and NST2 of Arabidopsis regulate secondary wall thickenings and are required for anther dehiscence. Plant Cell 17:2993–3006
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103
Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170
Nelson D, Donald E, Adams TR, Creelman RA, Wu J, Warner DC, Hinchey BS, Kumimoto RW, Maszle DR, Canales RD, Krolikowski KA, Dotson SB, Gutterson N, Ratcliffe OJ, Heard JE (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(42):16450–16455
Nemali KS, Bonin C, Dohleman FG, Stephens M, Reeves WR, Nelson DE, Castiglioni P, Whitsel JE, Sammons B, Silday RA, Anstrom D, Sharp RE, Patharkar OR, Clay D, Coffin M, Nemeth MA, Leibman ME, Luethy M, Lawson M (2014) Physiological responses related to increased grain yield under drought in the first biotechnology-derived drought-tolerant maize. Plant Cell Environ 38(9):1866–1880
Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2945
Nuccio ML, Wu J, Mowers R, Zhou HP, Meghji M, Primavesi LF, Paul MJ, Chen X, Gao Y, Haque E, Basu SS, Lagrimini LM (2015) Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nat Biotechnol 33:862–869
Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465:30–44
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10:79–87
Opitz N, Paschold A, Marcon C, Malik WA, Lanz C, Piepho HP, Hochholdinger F (2014) Transcriptomic complexity in young maize primary roots in response to low water potentials. BMC Genom 15:741
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150(4):1648–1655
Paul S, Gayen D, Datta SK, Datta K (2015) Dissecting root proteome of transgenic rice cultivars unravels metabolic alterations and accumulation of novel stress responsive proteins under drought stress. Plant Sci 234:133–143
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381
Qin F, Kakimoto M, Sakuma Y, Maruyama K, Osakabe Y, Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50(1):54–69
Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52(9):1569–1582
Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Crelman R, Pilgrim M, Broun P, Zhang JZ, Ghandehari D, Sherman BK, Yu GL (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110
Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 290(3):998–1009
Sakuma Y, Maryyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103(49):18822–18827
Saleh A, Lumbreras V, Lopez C, Dominguez-Puigjaner E, Kizis D, Pagès M (2006) Maize DBF1-interactor protein 1 containing an R3H domain is a potential regulator of DBF1 activity in stress responses. Plant J 46(5):747–757
Seeve CM, Cho IJ, Hearne LB, Srivastava GP, Joshi T, Smith DO, Sharp RE, Oliver MJ (2017) Water-deficit-induced changes in transcription factor expression in maize seedlings. Plant Cell Environ 40:686–701
Shao H, Wang H, Tang X (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902
Sharoni AM, Nuruzzaman M, Satoh K, Shimizu T, Kondoh H, Sasaya T, Choi IR, Omura T, Kikuchi S (2011) Gene structures, classification and expression models of the AP2/EREBP transcription factor family in rice. Plant Cell Physiol 52:344–360
Shavrukov Y, Baho M, Lopato S, Langridge P (2016) The TaDREB3 transgene transferred by conventional crossings to different genetic backgrounds of bread wheat improves drought tolerance. Plant Biotechnol J 14(1):313–322
Shi J, Habben JE, Archibald RL, Drummond BJ, Chamberlin MA, Williams RW, Lafitte HR, Weers BP (2015) Overexpression of ARGOS genes modifies plant sensitivity to ethylene, leading to improved drought tolerance in both Arabidopsis and Maize. Plant Physiol 169(1):266–282
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227
Shiriga K, Sharma R, Kumar K, Yadav SK, Hossain F, Thirunavukkarasu N (2014) Genome-wide identification and expression pattern of drought responsive members of the NAC family in maize. Meta Gene 2:407–417
Singh D, Laxmi A (2015) Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front Plant Sci 6:895
Singh B, Bohra A, Mishra S, Joshi R, Pandey S (2015) Embracing new-generation ‘omics’ tools to improve drought tolerance in cereal and food legume crops. Biol Plant 59:413–428
Smith DL, Fedoroff NV (1995) LRP1, a gene expressed in lateral and adventitious root primordia of Arabidopsis. Plant Cell 7:735–745
Song X, Li Y, Hou X (2013) Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genom 14:573
Su H, Cao Y, Ku L, Yao W, Cao Y, Ren Z, Dou D, Wang H, Ren Z, Liu H, Tian L, Zheng Y, Chen C, Chen Y (2018) Dual functions of ZmNF-YA3 in photoperiod-dependent flowering and abiotic stress responses in maize. J Exp Bot 69(21):5177–5189
Townley HE, Knight MR (2002) Calmodulin as a potential negative regulator of Arabidopsis COR gene expression. Plant Physiol 128(4):1169–1172
Tran LS, Nakashima K, Sakuma Y, Simpson SD, Fujita Y, Maruyama K, Fujita M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16(9):2481–2498
Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:1–7
Vilela B, Moreno-Cortés A, Rabissi A, Leung J, Pagès M, Lumbreras V (2013) The maize OST1 kinase homolog phosphorylates and regulates the maize SNAC1-type transcription factor. PLoS ONE 8(2):e58105
Wang L, Zhao J, Fan Y (2002) Gene cloning and function analysis of ABP9 protein which specifically binds to ABRE2 motif of maize Cat1 gene. Chin Sci Bull 47(22):1871–1875
Wang CT, Yang Q, Yang YM (2011) Characterization of the ZmDBP4 gene encoding a CRT/DRE-binding protein responsive to drought and cold stress in maize. Acta Physiol Plant 33(2):575–583
Wang B, Zheng J, Liu Y, Wang J, Wang G (2012a) Cloning and characterization of the stress induced bZIP gene ZmbZIP60 from maize. Mol Biol Rep 39(5):6319–6327
Wang XP, Liu T, Li CH, Zhao Z (2012b) Gene expression profiles in maize (Zea mays L.) leaves inoculation with southern corn rust (Puccinia polysora Underw.). Acta Physiol Plant 34:997–1006
Wang Z, Cheng K, Wan L, Yan L, Jiang H, Liu S, Lei Y, Liao B (2015) Genome-wide analysis of the basic leucine zipper (bZIP) transcription factor gene family in six legume genomes. BMC Genom 16:1053
Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48(10):1233–1241
Wang C, Lu G, Hao Y, Guo H, Guo Y, Zhao J, Cheng H (2017) ABP9, a maize bZIP transcription factor, enhances tolerance to salt and drought in transgenic cotton. Planta 246(3):453–469
Wang B, Li Z, Ran Q, Li P, Peng Z, Zhang J (2018a) ZmNF-YB16 overexpression improves drought resistance and yield by enhancing photosynthesis and the antioxidant capacity of maize plants. Front Plant Sci 9:709
Wang CT, Ru JN, Liu YW, Li M, Zhao D, Yang JF, Fu JD, Xu ZS (2018b) Maize WRKY transcription factor ZmWRKY106 confers drought and heat tolerance in transgenic plants. Int J Mol Sci 19(10):3046
Wang CT, Ru JN, Liu YW, Yang JF, Li M, Xu ZS, Fu JD (2018c) The Maize WRKY transcription factor ZmWRKY40 confers drought resistance in transgenic Arabidopsis. Int J Mol Sci 19(9):2580
Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19(6):463–476
Xiang Y, Sun X, Gao S, Qin F, Dai M (2017) Deletion of an endoplasmic reticulum stress response element in a ZmPP2C-A gene facilitates drought tolerance of maize seedlings. Mol Plant 10(3):456–469
Xie Q, Frugis G, Colgan D, Chua NH (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036
Xu ZS, Chen M, Li LC, Ma YZ (2011) Functions and application of the AP2/ERF transcription factor family in crop improvement. J Integr Plant Biol 53:570–585
Xu ZY, Kim SY, Kim DH, Dong T, Park Y, Jin JB, Joo SH, Kim SK, Hong JC, Hwang D, Hwang I (2013) The Arabidopsis NAC transcription factor ANAC096 cooperates with bZIP-type transcription factors in dehydration and osmotic stress responses. Plant Cell 25(11):4708–4724
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264
Ying S, Zhang DF, Fu J, Shi YS, Song YC, Wang TY, Li Y (2012) Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta 235(2):253–266
Zhang X, Wollenweber B, Jiang D, Liu F, Zhao J (2008) Water deficits and heat shock effects on photosynthesis of a transgenic Arabidopsis thaliana constitutively expressing ABP9, a bZIP transcription factor. J Exp Bot 59(4):839–848
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(4–5):365–378
Zhang Z, Li X, Zhang C, Zou H, Wu Z (2016) Isolation, structural analysis, and expression characteristics of the maize nuclear factor Y gene families. Biochem Biophys Res Commun 478(2):752–758
Zhang T, Tan D, Zhang L, Zhang X, Han Z (2017) Phylogenetic analysis and drought-responsive expression profiles of the WRKY transcription factor family in maize. Agric Gene 3:99–108
Zhou W, Jia C, Wu X, Hu R, Yu G, Zhang X, Liu J, Pan H (2016) ZmDBF3, a novel transcription factor from maize (Zea mays L.), is involved in multiple abiotic stress tolerance. Plant Mol Biol Rep 34(1):353–364
Acknowledgements
This work was supported by the Young Scientists Fund of the National Natural Science Foundation of China (Grant No. 31801378).
Author information
Authors and Affiliations
Contributions
PL drafted the manuscript. JZ edited and revised the manuscript, all authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Leng, P., Zhao, J. Transcription factors as molecular switches to regulate drought adaptation in maize. Theor Appl Genet 133, 1455–1465 (2020). https://doi.org/10.1007/s00122-019-03494-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-019-03494-y