Multiple-strategy analyses of ZmWRKY subgroups and functional exploration of ZmWRKY genes in pathogen responses.

The WRKY transcription factor family plays crucial roles in biotic responses, such as fungi, bacteria, viruses and nematode infections and insect attacks. In this article, multiple-strategy analyses of the three subgroups were performed in order to gain structural and evolutionary proofs of the overall WRKY family and unravel the functions possessed by each group or subgroup. Thus we analyzed the similarity of WRKY factors between maize and Arabidopsis based on homology modelling. The gene structure and motif analyses of Group II demonstrated that specific motifs existing in the given subgroups may contribute to the functional diversification of WRKY proteins and the two types of conserved intron splice sites suggest their evolutionary conservation. The evolutionary divergence time estimation of Group III proteins indicated that the divergence of Group III occurred during the Neogene period. Further, we focused on the roles of maize WRKYs in pathogen responses based on publicly available microarray experiments. The result suggested that some ZmWRKYs are expressed specifically under the infection of certain fungus, among which some are up-regulated and some are down-regulated, indicating their positive or negative roles in pathogen response. Also, some genes remain unchanged upon fungal infection. Pearson correlation coefficient (PCC) analysis was performed using 62 fungal infection experiments to calculate the correlation between each pair of genes. A PCC value higher than 0.6 was regarded as strong correlation - in these circumstances, ninety pairs of genes showed a strong positive correlation, while fifteen pairs of genes displayed a strong negative correlation. These correlated genes form a co-regulatory network and help us investigate the existence of interactions between WRKY proteins.

[1]  Diqiu Yu,et al.  Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. , 2012, Plant science : an international journal of experimental plant biology.

[2]  T. Eulgem,et al.  SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato , 2012, Planta.

[3]  Peer Bork,et al.  Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy , 2011, Nucleic Acids Res..

[4]  H. Yoshioka,et al.  Phosphorylation of the Nicotiana benthamiana WRKY8 Transcription Factor by MAPK Functions in the Defense Response[C][W][OA] , 2011, Plant Cell.

[5]  Q. Shen,et al.  WRKY transcription factors. , 2010, Trends in plant science.

[6]  T. Graves,et al.  The Physical and Genetic Framework of the Maize B73 Genome , 2009, PLoS genetics.

[7]  M. Nei,et al.  Evolution of F-box genes in plants: Different modes of sequence divergence and their relationships with functional diversification , 2009, Proceedings of the National Academy of Sciences.

[8]  Marta T. Bokowiec,et al.  Tobacco Transcription Factors: Novel Insights into Transcriptional Regulation in the Solanaceae1[C][W][OA] , 2008, Plant Physiology.

[9]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[10]  An-Yuan Guo,et al.  [GSDS: a gene structure display server]. , 2007, Yi chuan = Hereditas.

[11]  I. Somssich,et al.  Nuclear Activity of MLA Immune Receptors Links Isolate-Specific and Basal Disease-Resistance Responses , 2007, Science.

[12]  L. Lai,et al.  DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein , 2007, Nucleic acids research.

[13]  I. Somssich,et al.  The Transcription Factors WRKY11 and WRKY17 Act as Negative Regulators of Basal Resistance in Arabidopsis thaliana[W][OA] , 2006, The Plant Cell Online.

[14]  N. Amornsiripanitch,et al.  A Genomic Approach to Identify Regulatory Nodes in the Transcriptional Network of Systemic Acquired Resistance in Plants , 2006, PLoS pathogens.

[15]  Kang-Chang Kim,et al.  Pathogen-Induced Arabidopsis WRKY7 Is a Transcriptional Repressor and Enhances Plant Susceptibility to Pseudomonas syringae1[W] , 2006, Plant Physiology.

[16]  Chunhong Chen,et al.  Physical and Functional Interactions between Pathogen-Induced Arabidopsis WRKY18, WRKY40, and WRKY60 Transcription Factors[W] , 2006, The Plant Cell Online.

[17]  R. Henderson,et al.  Kinetics of the reactions between [S2MoS2Cu(SC6H4R-4)]2−(R = MeO, H, Cl or NO2) and CN−: substitution mechanism at a 3-coordinate CuI site , 2005 .

[18]  O. Pybus,et al.  Bayesian coalescent inference of past population dynamics from molecular sequences. , 2005, Molecular biology and evolution.

[19]  K. Shinozaki,et al.  Solution Structure of an Arabidopsis WRKY DNA Binding Domainw⃞ , 2005, The Plant Cell Online.

[20]  M. Cho,et al.  WRKY group IId transcription factors interact with calmodulin , 2005, FEBS letters.

[21]  Liangjiang Wang,et al.  The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants , 2005, BMC Evolutionary Biology.

[22]  Imre E Somssich,et al.  WRKY transcription factors: from DNA binding towards biological function. , 2004, Current opinion in plant biology.

[23]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[24]  K. Kogel,et al.  Identification of powdery mildew-induced barley genes by cDNA-AFLP: functional assessment of an early expressed MAP kinase , 2004, Plant Molecular Biology.

[25]  Gordon K Smyth,et al.  Statistical Applications in Genetics and Molecular Biology Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments , 2011 .

[26]  Benjamin M. Bolstad,et al.  affy - analysis of Affymetrix GeneChip data at the probe level , 2004, Bioinform..

[27]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[28]  Imre E Somssich,et al.  Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. , 2003, Molecular plant-microbe interactions : MPMI.

[29]  Alexei J Drummond,et al.  Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. , 2002, Genetics.

[30]  T. Eulgem,et al.  Leucine zipper-containing WRKY proteins widen the spectrum of immediate early elicitor-induced WRKY transcription factors in parsley. , 2002, Biochimica et biophysica acta.

[31]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[32]  Mark W. Chase,et al.  Evolution of the angiosperms: calibrating the family tree , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[33]  L. Sloan,et al.  Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present , 2001, Science.

[34]  A. Sharrocks,et al.  Docking domains and substrate-specificity determination for MAP kinases. , 2000, Trends in biochemical sciences.

[35]  I. Somssich,et al.  A novel regulatory element involved in rapid activation of parsley ELI7 gene family members by fungal elicitor or pathogen infection. , 2000, Molecular plant pathology.

[36]  B. Gaut,et al.  Maize as a model for the evolution of plant nuclear genomes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  T. Eulgem,et al.  The WRKY superfamily of plant transcription factors. , 2000, Trends in plant science.

[38]  H. Sano,et al.  Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding , 2000, Molecular and General Genetics MGG.

[39]  M. Long,et al.  Association of intron phases with conservation at splice site sequences and evolution of spliceosomal introns. , 1999, Molecular biology and evolution.

[40]  T. Eulgem,et al.  Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors , 1999, The EMBO journal.

[41]  Arlin Stoltzfus,et al.  Molecular evolution: Recent cases of spliceosomal intron gain? , 1998, Current Biology.

[42]  R F Doolittle,et al.  Determining divergence times with a protein clock: update and reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Memelink,et al.  Characterization of a zinc-dependent transcriptional activator from Arabidopsis. , 1996, Nucleic acids research.

[44]  I. Somssich,et al.  Interaction of elicitor‐induced DNA‐binding proteins with elicitor response elements in the promoters of parsley PR1 genes. , 1996, The EMBO journal.

[45]  J. Chappell,et al.  Identifying functional domains within terpene cyclases using a domain-swapping strategy. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[46]  S J de Souza,et al.  Evolution of the intron-exon structure of eukaryotic genes. , 1995, Current opinion in genetics & development.

[47]  P. Rushton,et al.  Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of α-Amy2 genes , 1995, Plant Molecular Biology.

[48]  S. Ishiguro,et al.  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 , 1994, Molecular and General Genetics MGG.

[49]  Peer Bork,et al.  Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation , 2007, Bioinform..

[50]  Jing Li,et al.  The WRKY family of transcription factors in rice and Arabidopsis and their origins. , 2005, DNA research : an international journal for rapid publication of reports on genes and genomes.

[51]  Zhixiang Chen,et al.  Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response , 2004, Plant Molecular Biology.

[52]  Michael Gribskov,et al.  Combining evidence using p-values: application to sequence homology searches , 1998, Bioinform..

[53]  N. Guex,et al.  SWISS‐MODEL and the Swiss‐Pdb Viewer: An environment for comparative protein modeling , 1997, Electrophoresis.

[54]  S. McKnight,et al.  Diversity and specificity in transcriptional regulation: the benefits of heterotypic dimerization. , 1991, Trends in biochemical sciences.

[55]  M. Kimura Estimation of evolutionary distances between homologous nucleotide sequences. , 1981, Proceedings of the National Academy of Sciences of the United States of America.