Abstract
WRKY transcription factors are important molecules in regulating plant development and resistance. Recently, the sequenced Arabidopsis lyrata genome allows us to characterize the number and structure of WRKY genes in this species. A total of 71 AlWRKY factors were classified into the previously defined polyphyletic WRKY groups I to III. The exon/intron structure and motif compositions of WRKYs were highly conserved in each group, but tended to be different between groups and species. The WRKY family has a set of genes similar to that in A. thaliana, but in Populus trichocarpa this family has expanded significantly, except for the subgroup III genes. Segmental duplication and gene conversion events have played important roles during the evolution of the WRKY gene family in the three species. Especially, the gene expansion events differentiated in WRKY subgroups during the evolution, and we have detected positive selection in several sites of the group III genes. In addition, this subgroup was the most structurally diversified in the WRKY family. Our study demonstrated that the group III members of WRKY gene families in A. lyrata, A. thaliana, and P. trichocarpa have experienced different selection pressure during the process of evolution and this may have played a vital role in plant adaptation.
This is a preview of subscription content, access via your institution.




References
Qu LJ, Zhu YX (2006) Transcription factor families in Arabidopsis: major progress and outstanding issues for future research. Curr Opin Plant Biol 9:544–549
Xiong Y, Liu T, Tian C et al (2005) Transcription factors in rice: a genome-wide comparative analysis between monocots and eudicots. Plant Mol Biol 59:191–203
Babu MM, Iyer LM, Balaji S et al (2006) The natural history of the WRKY-GCM1 zinc fingers and the relationship between transcription factors and transposons. Nucleic Acids Res 34:6505–6520
Marquez CP, Pritham EJ (2010) Phantom, a new subclass of mutator DNA transposons found in insect viruses and widely distributed in animals. Genetics 185:1507–1517
Rushton PJ, Macdonald H, Huttly AK et al (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of a-Amy2 genes. Plant Mol Biol 29:691–702
Sun C, Palmqvist S, Olsson H et al (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugar responsive elements of the iso1 promoter. Plant Cell 15:2076–2092
Ishiguro SN, 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 beta-amylase from sweet potato. Mol Gen Genet 244:563–571
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1
Liu JJ, Ekramoddoullah AKM (2009) Identification and characterization of the WRKY transcription factor family in Pinus monticola. Genome 52:77–88
Eulgem T, Rushton PJ, Robatzek S et al (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206
Huang S, Gao Y, Liu J et al (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics 287:495–513
He HS, Dong Q, Shao YH et al (2012) Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep 31:1199–1217
Mangelsen E, Kilian J, Berendzen KE et al (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare) WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9:194
Wu KL, Guo ZJ, Wang HH et al (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Res 12:9–26
Dong JX, Chen CH, Chen ZX (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655
Birkenbihl RP, Somssich IE (2011) Transcriptional plant responses critical for resistance towards necrotrophic pathogens. Front Plant Sci 2:76
Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol 15:431–437
Ramamoorthy R, Jiang SY, Kumar N et al (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49:865–879
Song Y, Ai CR, Jing SJ et al (2010) Research progress on function analysis of rice WRKY genes. Rice Sci 17:60–72
Rushton DL, Tripathi P, Rabara RC et al (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11
Chen L, Song Y, Li S et al (2012) The role of WRKY transcription factors in plant abiotic stresses. BBA 1819:120–128
Rushton PJ, Somssich IE, Ringler P et al (2010) WRKY transcription factors. Trends Plant Sci 15:247–258
Wang H, Avci U, Nakashima J et al (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci USA 107:22338–22343
Beilstein MA, Nagalingum NS, Clements MD et al (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. PNAS 107:18724–18728
Ossowski S, Schneeberger K, Lucas-Lledó JI et al (2010) The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327:92–94
Wright SI, Lauga B, Charlesworth D (2002) Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol Biol Evol 19:1407–1420
Yogeeswaran K, Frary A, York TL et al (2005) Comparative genome analyses of Arabidopsis spp.: inferring chromosomal rearrangement events in the evolutionary history of A. thaliana. Genome Res 15:505–515
Koch MA, Kiefer M (2005) Genome evolution among cruciferous plants: a lecture from the comparison of the genetic maps of three diploid species—Capsella rubella, Arabidopsis lyrata subsp. petraea, and A. thaliana. Am J Bot 92:761–767
Hu TT, Pattyn P, Bakker EG et al (2011) The Arabidopsis lyrata genome sequence and the basis of rapid genome size change. Nat Genet 43:476–481
Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604
Wang Q, Wang M, Zhang X et al (2011) WRKY gene family evolution in Arabidopsis thaliana. Genetica 139:973–983
Guo AY, Zhu QH, Chen X et al (2007) GSDS:a gene structure display server. Hereditas (Beijing) 29:1023–1026
Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Thomas MK, Christopher JC, Melissa MP et al (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6:29
Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6:13
Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591
Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936
Yang Z (2000) Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. J Mol Evol 51:423–432
Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479
Yang Z, Wong WSW, Nielsen R (2005) Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22:1107–1118
Cannon SB, Mitra A, Baumgarten A et al (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10
Jiao Y, Wickett NJ, Ayyampalayam S et al (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100
Tang H, Bowers JE, Wang X et al (2008) Synteny and collinearity in plant genomes. Science 320:486–488
Wilkins O, Nahal H, Foong J et al (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993
Hu R, Qi G, Kong Y et al (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145
Ling J, Jiang W, Zhang Y et al (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Plant Biol 12:471
Xie Z, Zhang ZL, Zou X et al (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
Wei KF, Chen J, Chen YF et al (2012) Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Res 19:153–164
Acknowledgments
We thank Prof. Tore Samuelsson from University of Gothenburg for valuable discussion on our manuscript writing. This work was supported by the Yunnan Provincial Government High Level Talent Introduction grant through the Department of Science and Technology.
Author information
Authors and Affiliations
Corresponding author
Additional information
Yu Song and Jie Gao have contributed equally.
Electronic supplementary material
Below is the link to the electronic supplementary material.
11434_2013_57_MOESM2_ESM.xlsx
Supplemental Table 1. Gene conversion events analysis of WRKY genes in Arabidopsis lyrata and Populus trichocarpa (XLSX 59 kb).
About this article
Cite this article
Song, Y., Gao, J. Genome-wide analysis of WRKY gene family in Arabidopsis lyrata and comparison with Arabidopsis thaliana and Populus trichocarpa . Chin. Sci. Bull. 59, 754–765 (2014). https://doi.org/10.1007/s11434-013-0057-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11434-013-0057-9