Towards Understanding the Transcriptional Control of Abiotic Stress Tolerance Mechanisms in Food Legumes

  • Rebecca FordEmail author
  • Saleem Khan
  • Nitin Mantri


A multitude of environmental and subsoil conditions cause abiotic constraints to the growth and productivity of legume food species. These stresses often occur simultaneously, leading to compounded effects of low and unreliable yields. Since legumes are a major food source, particularly in regions of major population growth, it is imperative that better tolerant and adapted varieties are developed. For this, transgenic approaches integrated within traditional breeding programs are proposed to offer substantial productivity gains through fast-tracking the development and deployment of well adapted and tolerant varieties to regions of greatest need. For this to occur, knowledge of the major tolerance genes and more importantly their regulators is required. Accordingly, recent functional genomics approaches have begun to shed light on the transcriptional, and hence regulatory and mechanistic controls governing tolerances to several of the major abiotic stresses, such as drought, temperature and salinity within temperate legume food species. Functional validation of these regulatory signals, their action on downstream genes and associated pathways is underway within several large international programs. This chapter will review these advances in knowledge to date within the model and crop grain legume species, to identify and characterize the molecular targets for the future selection and breeding of sustainably tolerant crops. Specifically, this chapter aims to summarize progress towards identifying and understanding the functions of the WRKY transcription factors involved in instigating and regulating abiotic stress tolerance mechanisms and their potential for improving abiotic stress tolerance within temperate legume food species.


Abiotic stress tolerance Hormone-signalling Host defence Legume Pathogenesis-related gene Signalling Transcription factor WRKY 



Abscisic acid


Amplified fragment length polymorphism


APETALA2/Ethylene-responsive factor


Dehydration-responsive element binding


Indole Acetic Acid


Legume anthocyanin production




9-cis-epoxycarotenoid dioxygenase


Polyethylene glycol


Transcription factor


Tobacco mosaic virus


Tryptophan Arginine Lysine


  1. Cabello J, Lodeyro AF, Zurbriggen MD (2014) Novel perspectives for the engineering of abiotic stress tolerance in plants. Curr Opin Biotechnol 26:62–70CrossRefPubMedGoogle Scholar
  2. Caldana C, Scheible WR, Mueller-Roeber B, Ruzicic S (2007) A quantitative RT-PCR platform for high-throughput expression profiling of 2500 rice transcription factors. Plant Methods 3:7CrossRefPubMedCentralPubMedGoogle Scholar
  3. Chavan V, Kamble A (2013) β-Aminobutyric acid primed expression of WRKY and defence genes in Brassica carinata against Alternaria blight. J Phytopathol 20(2):120–128. doi: 10.1111/jph.12132 Google Scholar
  4. Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye XG, Xia LQ, Ma YZ (2007) GmDREB2, a soybean DRE-binding transcription factor, conferred drought and high-salt tolerance in transgenic plants. Biochem Biophys Res Commun 353:299–305CrossRefPubMedGoogle Scholar
  5. Chen M, Xu Z, Xia L, Li L, Cheng X, Dong J, Wang Q, Ma Y (2009) Cold-induced modulation and functional analyses of the DRE-binding transcription factor gene, GmDREB3, in soybean (Glycine max L.). J Exp Bot 60:121–135CrossRefPubMedCentralPubMedGoogle Scholar
  6. Chen N, Yang Q, Su M, Pan L, Chi X, Chen M, He Y, Yang Z, Wang T, Wang M, Yu S (2012a) Cloning of six ERF family transcription factor genes from peanut and analysis of their expression during abiotic stress. Plant Mol Biol Report 30:1415–1425CrossRefGoogle Scholar
  7. Ciolkowski I, Wanke D, Birkenbihl R, Somssich I (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68:81–92CrossRefPubMedCentralPubMedGoogle Scholar
  8. Combier JP, Frugier F, Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088CrossRefPubMedCentralPubMedGoogle Scholar
  9. Czechowski T, Bari RP, Stitt M, Scheible WR, Udvardi MK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38:366–379CrossRefPubMedGoogle Scholar
  10. Dinari A, Niazi A, Afsharifar AR, Ramezani A (2013) Identification of upregulated genes under cold stress in cold-tolerant chickpea using the cDNA-AFLP approach. PLoS One 8(1):e52757. doi: 10.1371/journal.pone.0052757 CrossRefPubMedCentralPubMedGoogle Scholar
  11. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defence signaling. Curr Opin Plant Biol 10:366–371CrossRefPubMedGoogle Scholar
  12. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206CrossRefPubMedGoogle Scholar
  13. Gao S, Chen M, Xu Z, Zhao C, Li L, Xu H, Tang Y, Zhao X, Ma Y (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75:537–553CrossRefPubMedGoogle Scholar
  14. Gruber V, Blanchet S, Diet A, Zahaf O, Boualem A, Kakar K, Alunni B, Udvardi M, Frugier F, Crespi M (2009) Identification of transcription factors involved in root apex responses to salt stress in Medicago truncatula. Mol Genet Genomics 281:55–66CrossRefPubMedCentralPubMedGoogle Scholar
  15. Guo Y, Gan S (2006) AtNAP, a NAC family transcription factor, has an important role in leaf senescence. Plant J 46:601–612CrossRefPubMedGoogle Scholar
  16. Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zou HF, Lei G, Tian AG, Zhang WK, Ma B, Zhang JS, Chen SY (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68(2):302–313CrossRefPubMedGoogle Scholar
  17. Hecht V, Laurie RE, Schoor JKV, Ridge S, Knowles CL, Liew LC, Sussmilch FC, Murfet IC, Macknight RC, Weller JL (2011) The Pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod. Plant Cell 23:147–161CrossRefPubMedCentralPubMedGoogle Scholar
  18. Hu Y, Chen L, Wang H, Zhang L, Wang F, Yu D (2013) Arabidopsis transcription factor WRKY8 functions antagonistically with its interacting partner VQ9 to modulate salinity stress tolerance. Plant J 74(5):730–745CrossRefPubMedGoogle Scholar
  19. Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G, Yadav M, Kant C, Sharma P, Yadav G, Bhatia S, Tyagi AK, Chattopadhyay D (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74(5):715–729CrossRefPubMedGoogle Scholar
  20. Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69(1–2):91–105CrossRefPubMedGoogle Scholar
  21. Jin H, Xu G, Meng Q, Huang F, Yu D (2013) GmNAC5, a NAC transcription factor, is a transient response regulator induced by abiotic stress in soybean. Scientific World Journal 2013:768972CrossRefPubMedCentralPubMedGoogle Scholar
  22. Kakar K, Wandrey M, Czechowski T, Gaertner T, Scheible WR, Stitt M, Torres-Jerez I, Xiao Y, Redman JC, Wu HC et al (2008) A community resource for high-throughput quantitative RT-PCR analysis of transcription factor gene expression in Medicago truncatula. Plant Methods 4:18CrossRefPubMedCentralPubMedGoogle Scholar
  23. Kavar T, Maras M, Kidrič M, Šuštar-Vozlič J, Meglič V (2008) Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol Breed 21:159–172CrossRefGoogle Scholar
  24. Kujur A, Bajaj D, Saxena MS, Tripathi S, Upadhyaya HL, Gowda CLL, Singh S, Jain M, Tyagi AK, Parida SK (2013) Functionally relevant microsatellite markers from chickpea transcription factor genes for efficient genotyping applications and trait association mapping. DNA Res 20(4):355–374CrossRefPubMedCentralPubMedGoogle Scholar
  25. Lai Z, Vinod KM, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8:68CrossRefPubMedCentralPubMedGoogle Scholar
  26. Li S, Fu Q, Huang W, Yu D (2009) Functional analysis of an Arabidopsis transcription factor WRKY25 in heat stress. Plant Cell Rep 28(4):683–693CrossRefPubMedGoogle Scholar
  27. Li S, Zhou X, Chen L, Huang W, Yu D (2010) Functional characterization of Arabidopsis thaliana WRKY39 in heat stress. Mol Cells 29(5):475–483CrossRefPubMedGoogle Scholar
  28. Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233(6):1237–1252CrossRefPubMedGoogle Scholar
  29. Li J, Dai X, Liu T, Zhao PX (2012) LegumeIP: an integrative database for comparative genomics and transcriptomics of model legumes. Nucleic Acids Res 40(Database issue):D1221–D1229CrossRefPubMedCentralPubMedGoogle Scholar
  30. 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 228:225–240CrossRefPubMedGoogle Scholar
  31. Libault M, Joshi T, Takahashi K, Hurley-Sommer A, Puricelli K, Blake S, Xu D, Nguyen HT, Stacey G (2009) Large-scale analysis of putative soybean regulatory gene expression identifies a Myb gene involved in soybean nodule development. Plant Physiol 151:1207–1220CrossRefPubMedCentralPubMedGoogle Scholar
  32. Liu X, Hong L, Yun X, Yao Y, Hu B, Li L (2011) Improved drought and salt tolerance in transgenic Arabidopsis overexpressing a NAC transcriptional factor from Arachis hypogaea. Biosci Biotechnol Biochem 75:443–450CrossRefPubMedGoogle Scholar
  33. Liu JH, Peng T, Dai W (2013) Critical cis-acting elements and interacting transcription factors: key players associated with abiotic stress responses in plants. Plant Mol Biol Report. Doi:  10.1007/s11105-013-0667-z
  34. Luchi S, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2000) A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol 123:553–562CrossRefGoogle Scholar
  35. Luise HB, Nina MF, Klaus H, Oliver K, Dierk W (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41(21):9764–9778. doi: 10.1093/nar/gkt732 CrossRefGoogle Scholar
  36. Luo X, Bai X, Sun X, Zhu D, Liu B, Ji W, Cai H, Cao L, Wu J, Hu M, Liu X, Tang L, Zhu Y (2013) Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J Exp Bot 64(8):2155–2169CrossRefPubMedGoogle Scholar
  37. Lv S, Jiang P, Chen X, Fan P, Wang X, Li Y (2012) Multiple compartmentalization of sodium conferred salt tolerance in Salicornia europaea. Plant Physiol Biochem 51:47–52CrossRefPubMedGoogle Scholar
  38. Madrid E, Gil J, Rubiales D, Krajinski F, Schlereth A, Millán T (2010) Transcription factor profiling leading to the identification of putative transcription factors involved in the Medicago truncatula-Uromyces striatus interaction. Theor Appl Genet 12:1311–1321CrossRefGoogle Scholar
  39. Mantri N, Ford R, Coram TE, Pang ECK (2007) Transcriptional profiling of chickpea genes differentially regulated in response to high-salinity, cold and drought. BMC Genomics 8:303CrossRefPubMedCentralPubMedGoogle Scholar
  40. Mantri N, Pang ECK, Ford R (2010a) Molecular biology for stress management. In: Yadav SS, McNeil DN, Weeden N, Patil SS (eds) Climate change and management of cool season grain legume crops. Springer, Heidelberg, pp 377–408CrossRefGoogle Scholar
  41. Mantri N, Ford R, Coram TE, Pang ECK (2010b) Evidence of unique and shared responses to major biotic and abiotic stresses in chickpea. Environ Exp Bot 69(3):286–292CrossRefGoogle Scholar
  42. Mantri N, Patade V, Penna S, Ford R, Pang ECK (2012) Abiotic stress responses in plants - present and future. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism to productivity. Springer, New York, pp 1–19CrossRefGoogle Scholar
  43. Mantri N, Basker N, Pang ECK, Ford R, Pardeshi V (2013) The role of miRNAs in legumes with a focus on abiotic stress response. Plant Genome. doi: 10.3835/plantgenome2013.05.0013 Google Scholar
  44. Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2009) In silico analysis of transcription factor repertoire and prediction of stress responsive transcription factors in soybean. DNA Res 16:353–369CrossRefPubMedCentralPubMedGoogle Scholar
  45. Paul S, Kundu A, Pal A (2011) Identification and validation of conserved microRNAs along with their differential expression in roots of Vigna unguiculata grown under salt stress. Plant Cell Tiss Org Cult 105:233–242CrossRefGoogle Scholar
  46. Peel G, Pang Y, Modolo LV, Dixon RA (2009) The LAP1 MYB transcription factor orchestrates anthocyanidin biosynthesis and glycosylation in Medicago. Plant J 59:136–149CrossRefPubMedGoogle Scholar
  47. Peng H, Cheng H, Chen C, Yu X, Yang J, Gao W, Shi Q, Zhang H, Li J, Ma H (2009a) A NAC transcription factor gene of Chickpea (Cicer arietinum), CarNAC3, is involved in drought stress response and various developmental processes. J Plant Physiol 166(17):1934–1945CrossRefPubMedGoogle Scholar
  48. Peng H, Cheng H, Yu X, Shi Q, Zhang H, Li J, Ma H (2009b) Characterization of a chickpea (Cicer arietinum L.) NAC family gene, CarNAC5, which is both developmentally- and stress-regulated. Plant Physiol Biochem 47:1037–1045CrossRefPubMedGoogle Scholar
  49. Peng H, Yu X, Cheng H, Shi Q, Zhang H, Li J, Ma H (2010) Cloning and characterization of a novel NAC family gene CarNAC1 from chickpea (Cicer arietinum L.). Mol Biotechnol 44:30–40CrossRefPubMedGoogle Scholar
  50. Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17:369–381CrossRefPubMedGoogle Scholar
  51. Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65(1):35–47CrossRefGoogle Scholar
  52. Ribamar J, Neto CF, Panolfi V, Correa F, Guimaraes M, Benko-Iseppon A-M, Romero C, de Oliviera Silva RL, Abdelnoor RV, Nepomuceno AL, Kido EA (2013) Early transcriptional response of soybean contrasting accessions to root dehydration. PLoS One 8(12):e83466. doi: 10.1371/journal.pone.0083466 CrossRefGoogle Scholar
  53. Rodriguez-Uribe L, O’Connell M (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 57(6):1391–1398CrossRefPubMedGoogle Scholar
  54. Şahin-Çevik M, Moore GA (2013) Identification of a drought-and cold-stress inducible WRKY gene in the cold-hardy Citrus relative Poncirus trifoliata. N Z J Crop Hortic Sci 41(2):57–68CrossRefGoogle Scholar
  55. Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiol 142:113–123CrossRefPubMedCentralPubMedGoogle Scholar
  56. Song H, Zhibiao N (2014) Genome-wide identification and characteristic of WRKY in Medicago truncatula. Yi Chuan 36(2):152–168CrossRefPubMedGoogle Scholar
  57. Timko MP, Rushton PJ, Laudeman TW, Bokowiec MT, Chipumuro E, Cheung F, Town CD, Chen X (2008) Sequencing and analysis of the gene-rich space of cowpea. BMC Genomics 9:103CrossRefPubMedCentralPubMedGoogle Scholar
  58. Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498CrossRefPubMedGoogle Scholar
  59. Varshney RK, Song C, Saxena R, Azam S, Yu S, Sharpe A, Cannon S, Baek J et al (2013) Draft genome sequence of chickpea (Cicer arietinum) provides a resource for trait improvement. Nat Biotechnol 31:240–246CrossRefPubMedGoogle Scholar
  60. Wan X, Li L (2006) Regulation of ABA level and water-stress tolerance of Arabidopsis by ectopic expression of a peanut 9-cis-epoxycarotenoid dioxygenase gene. Biochem Biophys Res Commun 347:1030–1038CrossRefPubMedGoogle Scholar
  61. Wang X, Du B, Liu M, Sun N, Qi X (2013) Arabidopsis transcription factor WRKY33 is involved in drought by directly regulating the expression of CesA8. Am J Plant Sci 4:21–27CrossRefGoogle Scholar
  62. Xie ZM, Zou H-F, Lei G, Wei W, Zhou Q-Y, Niu C-F, Liao Y, Tian A-G, Ma B, Zhang W-K, Zhang J-S, Chen S-Y (2009) Soybean trihelix transcription factors GmGT-2A and GmGT-2B improve plant tolerance to abiotic stresses in transgenic Arabidopsis. PLoS One 4:e6898CrossRefPubMedCentralPubMedGoogle Scholar
  63. Yamasaki K, Kigawa T, Seki M, Shinozaki K, Yokoyama S (2013) DNA-binding domains of plant-specific transcription factors: structure, function, and evolution. Trends Plant Sci 18:267–276CrossRefPubMedGoogle Scholar
  64. Zhang Y, Wang L (2005) The WRKY transcription factor super family: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1CrossRefPubMedCentralPubMedGoogle Scholar
  65. Zhang JY, Broeckling CD, Blancaflor EB, Sledge MK, Sumner LW, Wang ZY (2005) Overexpression of WXP1, a putative Medicago truncatula AP2 domain-containing transcription factor gene, increases cuticular wax accumulation and enhances drought tolerance in transgenic alfalfa (Medicago sativa). Plant J 42:689–707CrossRefPubMedGoogle Scholar
  66. Zhang JY, Broeckling CD, Sumner LW, Wang ZY (2007) Heterologous expression of two Medicago truncatula putative ERF transcription factor genes, WXP1 and WXP2, in Arabidopsis led to increased leaf wax accumulation and improved drought tolerance, but differential response in freezing tolerance. Plant Mol Biol 64:265–278CrossRefPubMedGoogle Scholar
  67. Zhang G, Chen M, Chen X, Xu Z, Guan S, Li L-C, Li A, Guo J, Mao L, Ma Y (2008) Phylogeny, gene structures, and expression patterns of the ERF gene family in soybean (Glycine max L.). J Exp Bot 59:4095–4107CrossRefPubMedCentralPubMedGoogle Scholar
  68. Zhang G, Chen M, Li L-C, Xu Z, Chen X, Guo J, Ma Y (2009a) 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 60:3781–3796CrossRefPubMedCentralPubMedGoogle Scholar
  69. Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY‐type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6(5):486–503CrossRefPubMedGoogle Scholar
  70. Zhu B, Ye C, Lu H, Chen X, Chai G, Chen J, Wang C (2006) Identification and characterization of a novel heat shock transcription factor gene, GmHsfA1, in soybeans (Glycine max). J Plant Res 119:247–256CrossRefPubMedGoogle Scholar
  71. Zou C, Jiang W, Yu D (2010) Male gametophyte-specific WRKY34 transcription factor mediates cold sensitivity of mature pollen in Arabidopsis. J Exp Bot 61(14):3901–3914CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.School of Natural SciencesGriffith UniversityBrisbaneAustralia
  2. 2.Faculty of Veterinary and Agricultural SciencesThe University of MelbourneMelbourneAustralia
  3. 3.School of Applied Sciences, Health Innovation Research InstituteRMIT UniversityMelbourneAustralia

Personalised recommendations