Abstract
Background
WRKY proteins play a vital role in the regulation of several imperative plant metabolic processes and pathways, especially under biotic and abiotic stresses. Although WRKY genes have been characterized in various major crop plants, their identification and characterization in pulse legumes is still in its infancy. Chickpea (Cicer arietinum L.) is the most important pulse legume grown in arid and semi-arid tropics.
Objective
In silico identification and characterization of WRKY transcription factor-encoding genes in chickpea genome.
Methods
For this purpose, a systematic genome-wide analysis was carried out to identify the non-redundant WRKY transcription factors in the chickpea genome.
Results
We have computationally identified 70 WRKY-encoding non-redundant genes which were randomly distributed on all the chickpea chromosomes except chromosome 8. The evolutionary phylogenetic analysis classified the WRKY proteins into three major groups (I, II and III) and seven sub-groups (IN, IC, IIa, IIb, IIc, IId and IIe). The gene structure analysis revealed the presence of 2–7 introns among the family members. Along with the presence of absolutely conserved signatory WRKY domain, 19 different domains were also found to be conserved in a group-specific manner. Insights of gene duplication analysis revealed the predominant role of segmental duplications for the expansion of WRKY genes in chickpea. Purifying selection seems to be operated during the evolution and expansion of paralogous WRKY genes. The transcriptome data-based in silico expression analysis revealed the differential expression of CarWRKY genes in root and shoot tissues under salt, drought, and cold stress conditions. Moreover, some of these genes showed identical expression pattern under these stresses, revealing the possibility of involvement of these genes in conserved abiotic stress–response pathways.
Conclusion
This genome-wide computational analysis will serve as a base to accelerate the functional characterization of WRKY TFs especially under biotic and abiotic stresses.
Similar content being viewed by others
References
Acharjee S, Sarmah BK (2013) Biotechnologically generating ‘super chickpea’ for food and nutritional security. Plant Sci 207:108–116
Ali L, Madrid E, Varshney R, Azam S, Millan T, Rubio J, Gil J (2014) Mapping and identification of a Cicer arietinum NSP2 gene involved in nodulation pathway. Theor Appl Genet 127:481–488
Ali MA et al (2018) Transcription factors WRKY11 and WRKY17 are involved in abiotic stress responses in Arabidopsis. J Plant Physiol 226:12–21
Bailey TL et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208
Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446
Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691
Brand LH, Fischer NM, Harter K, Kohlbacher O, Wanke D (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41:9764–9778
Cai X et al (2013) Genome-wide analysis of plant-specific Dof transcription factor family in tomato. J Integr Plant Biol 55:552–566
Cai C, Niu E, Du H, Zhao L, Feng Y, Guo W (2014) Genome-wide analysis of the WRKY transcription factor gene family in Gossypium raimondii and the expression of orthologs in cultivated tetraploid cotton. Crop J 2:87–101
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Chen L, Yang Y, Liu C, Zheng Y, Xu M, Wu N, Sheng J, Shen L (2015) Characterization of WRKY transcription factors in Solanum lycopersicum reveals collinearity and their expression patterns under cold treatment. Biochem Biophys Res Commun 464:962–968
da Silva EG, Ito TM, de Souza SGH (2017) ‘In silico’genome-wide identification and phylogenetic analysis of the WRKY transcription factor family in sweet orange (‘Citrus sinensis’). Aust J Crop Sci 11:716
de Almeida DSM et al (2017) Genome-wide identification and characterization of cacao WRKY transcription factors and analysis of their expression in response to witches’ broom disease. PLoS ONE 12:e0187346
Ding M, Chen J, Jiang Y, Lin L, Cao Y, Wang M, Zhang Y, Rong J, Ye W (2015) Genome-wide investigation and transcriptome analysis of the WRKY gene family in Gossypium. Mol Genet Genom 290:151–171
Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37
Eulgem T (2006) Dissecting the WRKY web of plant defense regulators. PLoS Pathog 2:e126
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Garg R, Bhattacharjee A, Jain M (2015) Genome-scale transcriptomic insights into molecular aspects of abiotic stress responses in chickpea. Plant Mol Biol Rep 33:388–400
Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) Proteomics protocols handbook. Springer, New York, pp 571–607
Giacomelli JI, Weigel D, Chan RL, Manavella PA (2012) Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol 195:766–773
Guo Y, Qiu L-J (2013) Genome-wide analysis of the Dof transcription factor gene family reveals soybean-specific duplicable and functional characteristics. PLoS ONE 8:e76809
Han Y, Ding T, Su B, Jiang H (2016) Genome-wide identification, characterization and expression analysis of the chalcone synthase family in maize. Int J Mol Sci 17:161
Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297
Huang X, Li K, Xu X, Yao Z, Jin C, Zhang S (2015) Genome-wide analysis of WRKY transcription factors in white pear (Pyrus bretschneideri) reveals evolution and patterns under drought stress. BMC Genom 16:1104
Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and β-amylase from sweet potato. Mol Gen Genet MGG 244:563–571
Jain M, Misra G, Patel RK, Priya P, Jhanwar S, Khan AW, Shah N, Singh VK, Garg R, Jeena G (2013) A draft genome sequence of the pulse crop chickpea (Cicer arietinum L.). Plant J 74:715–729
Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69:91–105
Jiang W, Yu D (2009) Arabidopsis WRKY2 transcription factor mediates seed germination and postgermination arrest of development by abscisic acid. BMC Plant Biol 9:96
Jin J, Tian F, Yang D-C, Meng Y-Q, Kong L, Luo J, Gao G (2016) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. https://doi.org/10.1093/nar/gkw982
Jing Z, Liu Z (2018) Genome-wide identification of WRKY transcription factors in kiwifruit (Actinidia spp.) and analysis of WRKY expression in responses to biotic and abiotic stresses. Gene Genom 40:429–446
Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359–1375
Knudsen B, Knudsen T, Flensborg M, Sandmann H, Heltzen M, Andersen A, Dickenson M, Bardram J, Steffensen P, Mønsted S (2011) Clc sequence viewer. A/S Cb, version 6
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874
Li W, Cheng J, Wu Z, Qin C, Tan S, Tang X, Cui J, Zhang L, Hu K (2015) An InDel-based linkage map of hot pepper (Capsicum annuum). Mol Breed 35:32
Li M-Y, Xu Z-S, Tian C, Huang Y, Wang F, Xiong A-S (2016) Genomic identification of WRKY transcription factors in carrot (Daucus carota) and analysis of evolution and homologous groups for plants. Sci Rep 6:23101
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Ling J et al (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genom 12:471
Liu H, Yang W, Liu D, Han Y, Zhang A, Li S (2011) Ectopic expression of a grapevine transcription factor VvWRKY11 contributes to osmotic stress tolerance in Arabidopsis. Mol Biol Rep 38:417–427
Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu ÜH, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genom 9:194
Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, Rieseberg LH, Otto SP (2011) Recently formed polyploid plants diversify at lower rates. Science 333:1257–1257
Mukhtar MS, Deslandes L, Auriac MC, Marco Y, Somssich IE (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum. Plant J 56:935–947
Panchy N, Lehti-Shiu M, Shiu S-H (2016) Evolution of gene duplication in plants. Plant Physiol 171:2294–2316
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655
Qin Y, Tian Y, Liu X (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. Biochem. Biophys Res Commun 464:428–433
Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47
Rinerson CI, Rabara RC, Tripathi P, Shen QJ, Rushton PJ (2015) The evolution of WRKY transcription factors. BMC Plant Biol 15:66
Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sani AS et al (2017) Genetic diversity, population structure, and genetic correlation with climatic variation in chickpea (Cicer arietinum) landraces from Pakistan. Plant Genome 11:170067
Schluttenhofer C, Yuan L (2015) Regulation of specialized metabolism by WRKY transcription factors. Plant Physiol 167:295–306
Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543
Sievers F et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539
Song H, Nan Z (2014) Genome-wide identification and analysis of WRKY transcription factors in Medicago truncatula. Hereditas 36:152–168
Song H, Wang P, Nan Z, Wang X (2014) The WRKY transcription factor genes in lotus japonicus. Int J Genom. https://doi.org/10.1155/2014/420128
Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Thudi M et al (2016) Whole genome re-sequencing reveals genome-wide variations among parental lines of 16 mapping populations in chickpea (Cicer arietinum L.). BMC Plant Biol 16:10
Varshney RK et al (2013) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 31:1120–1134
Verma M, Kumar V, Patel RK, Garg R, Jain M (2015) CTDB: an integrated chickpea transcriptome database for functional and applied genomics. PLoS ONE 10:e0136880
Vom Endt D, Kijne JW, Memelink J (2002) Transcription factors controlling plant secondary metabolism: what regulates the regulators? Phytochemistry 61:107–114
Voorrips R (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78
Wang QQ, Liu F, Chen XS, Ma XJ, Zeng HQ, Yang ZM (2010) Transcriptome profiling of early developing cotton fiber by deep-sequencing reveals significantly differential expression of genes in a fuzzless/lintless mutant. Genomics 96:369–376
Wang Q, Wang M, Zhang X, Hao B, Kaushik S, Pan Y (2011) WRKY gene family evolution in Arabidopsis thaliana. Genetica 139:973
Wang H-L, Yang J, Boykin LM, Zhao Q-Y, Wang Y-J, Liu S-S, Wang X-W (2014a) Developing conversed microsatellite markers and their implications in evolutionary analysis of the Bemisia tabaci complex. Sci Rep 4:6351
Wang L et al (2014b) Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biol 14:103
Wang N, Xia E-H, Gao L-Z (2016) Genome-wide analysis of WRKY family of transcription factors in common bean, Phaseolus vulgaris: chromosomal localization, structure, evolution and expression divergence. Plant Gene 5:22–30
Wei K-F, Chen J, Chen Y-F, Wu L-J, Xie D-X (2012) Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Res 19:153–164
Wei Y et al (2016) Genome-wide identification and expression analysis of the WRKY gene family in cassava. Front Plant Sci 7:25
Wu K-L, Guo Z-J, Wang H-H, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9–26
Xiao Y et al (2017) Genome-wide identification of WRKY genes and their expression profiles under different abiotic stresses in Elaeis guineensis. PLoS ONE 12:e0189224
Xie Z, Zhang Z-L, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137:176–189
Xu X, Breen G, Chen C-K, Huang Y-S, Wu Y-Y, Asherson P (2010) Association study between a polymorphism at the 3′-untranslated region of CLOCK gene and attention deficit hyperactivity disorder. Behav Brain Funct 6:481
Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9:68
Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13:1527–1540
Yu Y, Wang N, Hu R, Xiang F (2016) Genome-wide identification of soybean WRKY transcription factors in response to salt stress. Springer Plus 5:920
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1
Zhang C et al (2017) Genome-wide identification of the potato WRKY transcription factor family. PLoS ONE 12:e0181573
Zhang M et al (2018) Transcriptome-wide identification and screening of WRKY factors involved in the regulation of taxol biosynthesis in Taxus chinensis. Sci Rep 8:5197
Zou Z, Yang L, Wang D, Huang Q, Mo Y, Xie G (2016) Gene structures, evolution and transcriptional profiling of the WRKY gene family in castor bean (Ricinus communis L.). PLoS ONE 11:e0148243
Acknowledgements
The authors acknowledge the Punjab Agricultural Research Board (Government of Punjab), Lahore, Pakistan for funding through Project PARB-938, as well as Centre for Advanced Studies in Agriculture and Food Security (CAS-AFS).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Waqas, M., Azhar, M.T., Rana, I.A. et al. Genome-wide identification and expression analyses of WRKY transcription factor family members from chickpea (Cicer arietinum L.) reveal their role in abiotic stress-responses. Genes Genom 41, 467–481 (2019). https://doi.org/10.1007/s13258-018-00780-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13258-018-00780-9