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Journal of Integrative Agriculture  2016, Vol. 15 Issue (11): 2469-2480    DOI: 10.1016/S2095-3119(15)61306-5
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Identification and expression analysis of group III WRKY transcription factors in cotton
DOU Ling-ling1, 2, GUO Ya-ning1, 2, Ondati Evans2, PANG Chao-you2, WEI Heng-ling2, SONG Mei-zhen2, FAN Shu-li2, YU Shu-xun1, 2
1 College of Agronomy, Northwest A & F University, Yangling 712100, P.R.China
2 State Key Laboratory of Cotton Biology/Institute of Cotton Research, Chinese Academy of Agricultural Siences, Anyang 455000, P.R.China
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Abstract      The WRKY proteins constitute a large family of transcription factors in plants containing highly conserved WRKYGQK sequences and zinc-finger-like motifs. To comprehensively study WRKY III genes in cotton, we analyzed the genome sequences of Gossypium hirsutum, G. raimondii and G. arboreum. According to the three genome sequences, 18 group III GhWRKY genes were identified in G. hirsutum, 12 both in G. raimondii and G. arboreum. Phylogenetic and motif analysis showed that proteins with high similarities could be clustered together and had the same motif components. The ratios of non-synonymous (Ka) to synonymous (Ks) of the GhWRKY to GrWRKY or GaWRKY were lower than 1, which indicated that group III WRKY genes in Gossypium species are under purifying selection. Expression analysis revealed that group III GhWRKY genes expressed during fiber development and leaf senescence, and most of them could be induced by salicylic acid (SA), jasmonic acid (JA), ethylene, abscisic acid (ABA), mannitol, and NaCl both in roots and cotyledons. Our study gives a briefly introduction on cotton group III WRKY genes and implicates their potential function in cotton fiber development, leaf senescence and abiotic stresses.
Keywords:  Gossypium        WRKY        phylogenetic analysis        expression analysis        development        abiotic stress  
Received: 13 October 2015   Accepted:
Fund: 

We appreciate the National High-Tech R&D Program of China (2013AA102601) for the financial support provided to this project.

Corresponding Authors:  YU Shu-xun, Tel/Fax: +86-372-2525363, E-mail: ysx195311@163.com   
About author:  DOU Ling-ling, E-mail: xjyldll@126.com;

Cite this article: 

DOU Ling-ling, GUO Ya-ning, Ondati Evans, PANG Chao-you, WEI Heng-ling, SONG Mei-zhen, FAN Shu-li, YU Shu-xun. 2016. Identification and expression analysis of group III WRKY transcription factors in cotton. Journal of Integrative Agriculture, 15(11): 2469-2480.

Bao Y, Hu G J, Flagel L E, Salmon A, Bezanilla M, Paterson A H, Wang Z N, Wendel J F. 2011. Parallel up-regulation of the profilin gene family following independent domestication of diploid and allopolyploid cotton (Gossypium). Proceedings of the National Academy of Sciences of the United States of America, 108, 21152–21157.

Besseau S, Li J, Palva E T. 2012. WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. Journal of Experimental Botany, 63, 2667–2679.

Cai C P, Niu E L, Du H, Zhao L, Feng Y, Guo W Z. 2014. Genome-wide analysis of the WRKY transcription factor gene family in Gossypium raimondii and the expression of orthologs in cultivivated tetraploid cotton. The Crop Journal, 2, 87–101.

Dai X, Wang Y, Zhang W H. 2015. OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. Journal of Experimental Botany, 67, 947-960.

Ding M Q, Chen J D, Jiang Y R, Lin L F, Cao Y F, Wang M H, Zhang Y T, Rong J K, Ye W W. 2015. Genome-wide investigation and transcriptome analysis of the WRKY gene family in Gossypium. Molecular Genetics Genomics, 290, 151–171.

Dong C J, Li L, Shang Q M, Liu X Y, Zhang Z G. 2014. Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings. Planta, 240, 687–700.

Dou L L, Zhang X H, Pang C Y, Song M Z, Wei H L, Fan S L, Yu S X. 2014. Genome-wide analysis of the WRKY gene family in cotton. Molecular Genetics and Genomics, 289, 1103–1121.

Duan Q Q, Jiang W, Ding M, Lin Y, Huang D F. 2014. Light affects the chloroplast ultrastructure and post-storage photosynthetic performance of watermelon (Citrullus lanatus) plug seedlings. PLOS ONE, 9, e111165.

Eulgem T, Rushton P J, Robatzek S, Somssich I E. 2000. The WRKY superfamily of plant transcription factors. Trends in Plant Science, 5, 199–206.

Fan X Q, Guo Q, Xu P, Gong Y Y, Shu H M, Yang Y, Ni W C, Zhang X G, Shen X L. 2015. Transcriptome-wide identification of salt-responsive members of the WRKY gene family in Gossypium aridum. PLOS ONE, 10, e0126148

Guo R Y, Yu F F, Gao Z, An H L, Cao X C, Guo X Q. 2011. GhWRKY3, a novel cotton (Gossypium hirsutum L.) WRKY gene, is involved in diverse stress responses. Molecular Biology Reports, 38, 49–58.

He H S, Dong Q, Shao Y H, Jiang H Y, Zhu S W, Cheng B J, Xiang Y. 2012. Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Reports, 31, 1199–1217.

Hendrix B, Stewart J M. 2005. Estimation of the nuclear DNA content of Gossypium species. Annal of Botany, 95, 789–797.

Herve M R, Delourme R, Gravot A, Marnet N, Berardocco S, Cortesero A M. 2014. Manipulating feeding stimulation to protect crops against insect pests? Journal of Chemical Ecology, 40, 1220–1231.

Higashi K, Ishiga Y, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y. 2008. Modulation of defense signal transduction by flagellin-induced WRKY41 transcription factor in Arabidopsis thaliana. Molecular Genetics and Genomics, 279, 303–312.

Hovav R, Udall J A, Chaudhary B, Hovav E, Flagel L, Hu G, Wendel J F. 2008. The evolution of spinnable cotton fiber entailed prolonged development and a novel metabolism. PLoS Genetics, 4, e25.

Hu G J, Koh J, Yoo M J, Grupp K, Chen S X, Wendel J F. 2013. Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytologist, 200, 570–582.

Hu Y R, Dong Q Y, Yu D Q. 2012. Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Science, 185, 288–297.

Kalde M, Barth M, Somssich I E, Lippok B. 2003. Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Molecular Plant-Microbe Interactions, 16, 295–305.

Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J, Marra M A. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.

Li F, Fan G, Lu C, Xiao G, Zou C, Kohel R J, Ma Z, Shang H, Ma X, Wu J, Liang X, Huang G, Percy R G, Liu K, Yang W, Chen W, Du X, Shi C, Yuan Y, Ye W, et al. 2015. Genome sequence of cultivated upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nature Biotechnology, 33, 524–530.

Li F G, Fan G Y, Wang K B, Sun F M, Yuan Y L, Song G L, Li Q, Ma Z Y, Lu C R, Zou C S, Chen W B, Liang X M, Shang H H, Liu W Q, Shi C C, Xiao G H, Gou C Y, Ye W W, Xu X, Zhang X Y, et al. 2014. Genome sequence of the cultivated cotton Gossypium arboreum. Nature Genetics, 46, 567–572.

Li J, Besseau S, Toronen P, Sipari N, Kollist H, Holm L, Palva E T. 2013. Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytologist, 200, 455–472.

Li J, Brader G, Palva E T. 2004. The WRKY70 transcription factor: A node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. The Plant Cell, 16, 319–331.

Librado P, Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(–??C) method. Methods, 25, 402–408.

Ma J, Zhang D, Shao Y, Liu P, Jiang L, Li C. 2014. Genome-wide analysis of the WRKY transcription factors in Aegilops tauschii. Cytogenetics and Genome Research, 144, 243–253.

Ma W X, Noble W S, Bailey T L. 2014. Motif-based analysis of large nucleotide data sets using MEME-ChIP. Nature Protocols, 9, 1428–1450.

Martha M V, Alisa H, Eric A S, Nicole J D, Shawn C, James S, Vitor F M, Jay S, Maritza R, Hans T A, Leon H A, Peter E A T. 2014. Effects of elevated CO2 on maize defence against mycotoxigenic Fusarium verticillioides. Plant, Cell and Environment, 37, 2691–2706.

Miura K, Tada Y. 2014. Regulation of water, salinity, and cold stress responses by salicylic acid. Frontiers in Plant Science, 5, 4.

Moreno J E, Ballare C L. 2014. Phytochrome regulation of plant immunity in Vegetation Canopies. Journal of Chemical Ecology, 40, 848–857.

Muthamilarasan M, Bonthala V S, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M. 2015. Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Frontiers in Plant Science, 6, 910.

Paterson A H, Wendel J F, Gundlach H, Guo H, Jenkins J, Jin D C, Llewellyn D, Showmaker K C, Shu S Q, Udall J, Yoo M J, Byers R, Chen W, Doron-Faigenboim A, Duke M V, Gong L, Grimwood J, Grover C, Grupp K, Hu G J, et al. 2012. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature, 492, 423–427.

Rehmeyer C J, Li W X, Kusaba M, Farman M L. 2009. The telomere-linked helicase (TLH) gene family in Magnaporthe oryzae: revised gene structure reveals a novel TLH-specific protein motif. Current Genetics, 55, 253–262.

Shi W N, Liu D D, Hao L L, Wu C A, Guo X Q, Li H. 2014. GhWRKY39, a member of the WRKY transcription factor family in cotton, has a positive role in disease resistance and salt stress tolerance. Plant Cell Tissue and Organ Culture, 118, 17–32.

Shiono K, Yamauchi T, Yamazaki S, Mohanty B, Malik A I, Nagamura Y, Nishizawa N K, Tsutsumi N, Colmer T D, Nakazono M. 2014. Microarray analysis of laser-microdissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa). Journal of Experimental Botany, 65, 4795–4806.

Singh B, Avci U, Inwood S E E, Grimson M J, Landgraf J, Mohnen D, Sorensen I, Wilkerson C G, Willats W G T, Haigler C H. 2009. A specialized outer layer of the primary cell wall joins elongating cotton fibers into tissue-like bundles. Plant Physiology, 150, 684–699.

Song H, Wang P F, Nan Z B, Wang X J. 2014a. The WRKY transcription factor genes In Lotus Japonicus. Internal Journal of Genomics, doi: 10.1155/2014/420128

Song M Z, Fan S L, Pang C Y, Wei H L, Yu S X. 2014b. Genetic analysis of the antioxidant enzymes, methane dicarboxylic aldehyde (MDA) and chlorophyll content in leaves of the short season cotton (Gossypium hirsutum L.). Euphytica, 198, 153–162.

Strader L C, Chen G L, Bartel B. 2010. Ethylene directs auxin to control root cell expansion. The Plant Journal, 64, 874–884.

Sun J, An H, Shi W, Guo X, Li H. 2012. Molecular cloning and characterization of GhWRKY11, a gene implicated in pathogen responses from cotton. South African Journal of Botany, 81, 113–123.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731–2739.

Van Aken O, Zhang B T, Law S, Narsai R, Whelan J. 2013. AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondrial and chloroplast proteins. Plant Physiology, 162, 254–271.

Wang L N, Zhu W, Fang L C, Sun X M, Su L Y, Liang Z C, Wang N, Londo J P, Li S H, Xin H P. 2014. Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biology, 14, 103.

Wang X L, Yan Y, Li Y Z, Chu X Q, Wu C G, Guo X Q. 2014. GhWRKY40, a multiple stress-responsive cotton WRKY gene, plays an important role in the wounding response and enhances susceptibility to Ralstonia solanacearum infection in transgenic Nicotiana benthamiana. PLOS ONE, 9, e93577.

Wang Y Y, Feng L, Zhu Y X, Li Y, Yan H W, Xiang Y. 2015. Comparative genomic analysis of the WRKY III gene family in populus, grape, Arabidopsis and rice. Biology Direct, 10, 48.

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 Research, 19, 153–164.

Yang Z R, Zhang C J, Yang X J, Liu K, Wu Z X, Zhang X Y, Zheng W, Xun Q Q, Liu C L, Lu L L, Yang Z E, Qian Y Y, Xu Z Z, Li C F, Li J, Li F G. 2014. PAG1, a cotton brassinosteroid catabolism gene, modulates fiber elongation. New Phytologist, 203, 437–448.

Yu F F, Huaxia Y F, Lu W J, Wu C G, Cao X C, Guo X Q. 2012. GhWRKY15, a member of the WRKY transcription factor family identified from cotton (Gossypium hirsutum L.), is involved in disease resistance and plant development. BMC Plant Biology, 12, 144.

Zhang Y J, Wang L J. 2005. The WRKY transcription factor superfamily: Its origin in eukaryotes and expansion in plants. Bmc Evolutionary Biology, 5, 1.

Zhu H Y, Han X Y, Lü J H, Zhao L A, Xu X Y, Zhang T Z, Guo W Z. 2011. Structure, expression differentiation and evolution of duplicated fiber developmental genes in Gossypium barbadense and G. hirsutum. BMC Plant Biology, 11, 40.

Zhu Y N, Shi D Q, Ruan M B, Zhang L L, Meng Z H, Liu J, Yang W C. 2013. Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic dtresses in cotton (Gossypium hirsutum L.). PLOS ONE, 8, e80218.
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