The grapevine kinome: annotation, classification and expression patterns in developmental processes and stress responses

Abstract

Protein kinases (PKs) have evolved as the largest family of molecular switches that regulate protein activities associated with almost all essential cellular functions. Only a fraction of plant PKs, however, have been functionally characterized even in model plant species. In the present study, the entire grapevine kinome was identified and annotated using the most recent version of the grapevine genome. A total of 1168 PK-encoding genes were identified and classified into 20 groups and 121 families, with the RLK-Pelle group being the largest, with 872 members. The 1168 kinase genes were unevenly distributed over all 19 chromosomes, and both tandem and segmental duplications contributed to the expansion of the grapevine kinome, especially of the RLK-Pelle group. Ka/Ks values indicated that most of the tandem and segmental duplication events were under purifying selection. The grapevine kinome families exhibited different expression patterns during plant development and in response to various stress treatments, with many being coexpressed. The comprehensive annotation of grapevine kinase genes, their patterns of expression and coexpression, and the related information facilitate a more complete understanding of the roles of various grapevine kinases in growth and development, responses to abiotic stress, and evolutionary history.

Fig. 1. Comparison of grapevine protein kinase families with those in Arabidopsis (eudicot species) and rice (monocot species).

The grapevine PKs were classified into 20 groups and 121 families

Fig. 2. Chromosomal locations of tandemly duplicated kinase genes in grapevine.

A total of 395 tandemly duplicated kinase genes representing 19 families were distributed unevenly among 18 chromosomes. Gene IDs and related family names are presented to the right of each chromosome, and related information on gene location is listed on the left

Fig. 3. Gene Ontology (GO) analysis of tandemly duplicated grapevine PK genes.

The size of each slice in the pie chart indicates the relative abundance of that GO term in the grapevine kinome. GO terms were collected from the CRIBI database

Fig. 4. A heatmap illustrating the expression data of 120 different grapevine kinase families in 54 different grapevine tissues at various stages of development.

The heatmap was generated using the R package pheatmap. The color scale represents expression levels, with red indicating high expression levels and blue indicating low levels

Fig. 5. A heatmap of the expression data of 56 different grapevine kinase families in response to salt, PEG, cold, drought, heat, and ABA.

The heatmap was generated using the R package pheatmap. The color scale represents expression levels, with red indicating high expression levels and blue indicating low levels

Fig. 6. The coexpression network of grapevine PK families in response to salt, PEG, cold, drought, heat and ABA treatments.

The nodes represent families, and the edges between nodes represent coexpression correlations of family pairs. Different edge line colors represent either positive (blue) or negative (red) correlations

Fig. 7. The expression patterns of grapevine PK genes under drought and salt stresses.

a qRT–PCR expression data of 12 selected PK genes subjected to drought stress by withholding water for 0 (control), 2, 4, and 8 d after full water saturation. The RNA-Seq data of related grapevine PK genes are shown as FPKM values. b Quantification of expression levels of 12 grapevine PK genes in response to salt stress using qRT–PCR. Plants were subjected to salt stress by irrigating with 200 mM NaCl, and leaves were collected at 0 (control), 6, 12, and 24 h post salt treatment. The actin gene (VIT_212s0178g00200) was used as a reference gene to normalize gene expression levels. Values are the means ± SE of three replicates for each, and bars with different letters are significantly different at P < 0.05 according to Duncan’s multiple range test