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In silico study of wall-associated kinase family reveals large-scale genomic expansion potentially connected with functional diversification in Populus

Abstract

The wall-associated kinases (WAKs) are a family of transmembrane proteins involved in pathogen responses and cell elongation in Arabidopsis. They belong to the major receptor-like kinase (RLK) family in plants. Given their architecture and connection to the cell wall, WAKs are thought to perceive and propagate extracellular signals. This study reports the characterization of the WAK family in a woody species based on the v3.0 genome assembly of Populus trichocarpa. In silico analysis revealed a total of 175 PtWAK sequences classified into four groups based on protein domains. Of the PtWAKs, 91.5 % were found in tandem-duplicated clusters contributing to the expansion of the family in poplar. Microarray and EST expression data mining revealed contrasting temporal and spatial expression patterns in stress treatments for several WAK members. The WAKs in poplar form the largest WAK family encountered to date in plants. The combination of phylogenetic and transcriptional data showed that members in nonexpanded clusters were mainly expressed in developmental processes, whereas PtWAKs that had evolved independently in a species-specific way were structured in clusters and were involved in resistance responses. This paper offers an overview of WAK family structure in P. trichocarpa, which will be useful for further functional analysis of the PtWAK family.

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Acknowledgments

This work was supported by the French Ministery of Higher Education and Research (doctoral contract). Editing and proofreading were done by Auvergne Traduction Technique.

Data archiving statement

A full list of the Phytozome gene sequences used for this paper is included in Online ressource 1. Data used for transcriptomic analyses are referenced on GEO database (accession numbers: GSE13990, GSM412653, GSE9673, GSE17223, GSE15242, GSE17226, GSE17230, GSE21171, GSE19297, and GSE13109).

Author information

Correspondence to Patricia Roeckel-Drevet.

Additional information

Communicated by J. L. Wegrzyn

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1

P. trichocarpa WAKs. PtWAKs were classified based on their chromosomal location. Alias names of v1 and v2 of poplar genome annotation are indicated. Domain structure, EST names and numbers per sequence, and WAK genomic, transcript, CDS, and protein sequences are given (PDF 29 kb)

Online resource 2

Alignment of EGF-Ca2+ domains (PDF 51 kb)

Online resource 3

Phylogenetic tree of PtWAKs containing the WAKassoc domain. The phylogenetic tree of PtWAKs using conserved WAKassoc domain is represented. The tree obtained by the BI method is represented, and posterior probability and bootstrap values of >50 are indicated at nodes as BI/NJ/MP (PDF 33 kb)

Online resource 4

Heatmap representation of all PtWAK expression patterns among different poplar tissues/environmental conditions/genotypes. PtWAK v3.0 gene model names are indicated. For each tissue/environmental condition/genotype, mean relative expression values (three to four replicates) are displayed. Sample and WAK, relative expression value was calculated by dividing the absolute value (RMA normalized) by the median of absolute values of all samples, except for the apex assay. In this case, relative expression was obtained by dividing each array-normalized expression value by the median of absolute values of all samples, and was then log2-transformed. An asterisk indicates significant tissue/environmental condition/genotype effect on PtWAK expression according to Welch’s t test/one-way ANOVA for two or more samples followed by adjusted Bonferroni correction (*p < 0.05). Blue-, red-, and green-shaded PtWAK names belong to PtWAK-RLK, PtWAK-RLCK, and PtWAK-RLP gene groups, respectively (PDF 144 kb)

Online resource 5

Expression pattern comparison of PtWAK and randomly selected genes;Seventy-two PtWAK genes or randomly selected genes were used for this analysis. a Box-plot representation of PtWAK and random gene expression level distribution. Expression values are RMA-normalized data from all experiments performed in this work (see “Methods”). The significant PtWAK effect on expression level was detected with Welch’s t test (***p < 0.001). For the Shannon entropy calculation, see “Methods.” b Tissue specificity of PtWAK and random genes as measured by Shannon entropy distribution. Low entropy values indicate high tissue specificity. χ2 value is given (not significant, p = 0.064). c Condition specificity of PtWAK and random genes as measured by Shannon entropy distribution. Low entropy values indicate high condition specificity. χ2 value is given (**p < 0.01). d Genotype specificity of PtWAK and random genes as measured by Shannon entropy distribution. Low entropy values indicate high genotype specificity. χ2 value is given (*p < 0.05) (PDF 55 kb)

Online resource 6

PtWAKs whose apex expression is affected depending on water availability. The mean relative expression values (three samples per condition) and their standard errors shown here were significantly affected by water availability variations according to one-way ANOVA followed by adjusted Bonferroni correction (*p < 0.05). Relative expression was obtained by dividing each array-normalized expression value by the median of absolute values of all samples for the PtWAK, and was then log2-transformed. Values for control (black charts), drought (grey charts) and rewatering after drought (white charts) are given (PDF 24 kb)

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Tocquard, K., Lafon-Placette, C., Auguin, D. et al. In silico study of wall-associated kinase family reveals large-scale genomic expansion potentially connected with functional diversification in Populus . Tree Genetics & Genomes 10, 1135–1147 (2014). https://doi.org/10.1007/s11295-014-0748-7

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Keywords

  • WAK
  • Populus
  • Phylogeny
  • Microarray data mining
  • Abiotic biotic stress