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, 150 (1), 12-26

Evolutionary History and Stress Regulation of Plant Receptor-Like Kinase/Pelle Genes

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Evolutionary History and Stress Regulation of Plant Receptor-Like Kinase/Pelle Genes

Melissa D Lehti-Shiu et al. Plant Physiol.

Abstract

Receptor-Like Kinase (RLK)/Pelle genes play roles ranging from growth regulation to defense response, and the dramatic expansion of this family has been postulated to be crucial for plant-specific adaptations. Despite this, little is known about the history of or the factors that contributed to the dramatic expansion of this gene family. In this study, we show that expansion coincided with the establishment of land plants and that RLK/Pelle subfamilies were established early in land plant evolution. The RLK/Pelle family expanded at a significantly higher rate than other kinases, due in large part to expansion of a few subfamilies by tandem duplication. Interestingly, these subfamilies tend to have members with known roles in defense response, suggesting that their rapid expansion was likely a consequence of adaptation to fast-evolving pathogens. Arabidopsis (Arabidopsis thaliana) expression data support the importance of RLK/Pelles in biotic stress response. We found that hundreds of RLK/Pelles are up-regulated by biotic stress. Furthermore, stress responsiveness is correlated with the degree of tandem duplication in RLK/Pelle subfamilies. Our findings suggest a link between stress response and tandem duplication and provide an explanation for why a large proportion of the RLK/Pelle gene family is found in tandem repeats. In addition, our findings provide a useful framework for potentially predicting RLK/Pelle stress functions based on knowledge of expansion pattern and duplication mechanism. Finally, we propose that the detection of highly variable molecular patterns associated with specific pathogens/parasites is the main reason for the up-regulation of hundreds of RLK/Pelles under biotic stress.

Figures

Figure 1.
Figure 1.
Expansion of RLK/Pelle and other kinase families during land plant evolution. The phylogeny indicates the relationships between the four land plant species analyzed (A, Arabidopsis; P, poplar; R, rice; M, moss). The internal nodes are labeled indicating the common ancestors of the four plants (AP, APR, and APRM). The branches are labeled 1 to 6 to facilitate comparisons. The numbers of RLK/Pelle kinases (R) and other kinases (K), calculated based on subfamilies shared between all four species, at each node are shown in black boxes. Ancestral gene numbers were estimated by reconciling the ML gene tree of each kinase subfamily with the four-plant species tree (see “Materials and Methods”).
Figure 2.
Figure 2.
RLK/Pelle subfamily representation among four plant species and innovation in receptor kinase configuration. The first column shows subfamily names. The second column indicates the presence of an ECD found in most members of that subfamily. ECDs with known protein domains are indicated by symbols, with legends shown at the bottom. In the third column (species), the colored rectangles indicate the presence of subfamily member(s) in Arabidopsis (A), poplar (P), rice (R), and moss (M). A red rectangle indicates the gain of a protein domain. The identities of the novel domains are shown to the right. For the SD1 subfamily, poplar and rice RLK/Pelle genes gained novel ECDs independently, and these are labeled accordingly.
Figure 3.
Figure 3.
Heat map of subfamily expansion rates in different lineages. Relative expansion rate (defined as the log ratio of the number of genes at the nodes flanking each branch with the more recent node as the numerator) is shown for each subfamily at each branch. Shades of blue indicate the degree of loss, white indicates no net gain or loss, and shades of red indicate the degree of gain. The black box indicates the absence of a subfamily in the APRM-M (branch 1) and APRM-APR (branch 2) lineages. Branches are numbered as shown in the tree diagram.
Figure 4.
Figure 4.
RLK/Pelle subfamilies enriched in up- and down-regulated genes under abiotic and biotic stress conditions. Enrichment of stress-responsive members in each subfamily was determined by Fisher's exact test, with red shading indicating overrepresentation and blue shading indicating underrepresentation. A gray box indicates that no gene in that subfamily was up- or down-regulated. Red arrows indicate subfamilies with responsiveness to a broad range of biotic signals. The black arrow indicates the LRR-V subfamily whose members have functions in development, and the blue arrow indicates the LRR-II subfamily whose members function in both development and disease resistance. The green arrow indicates the LRR-XII subfamily. Two members in this family are MAMP receptors.
Figure 5.
Figure 5.
Relationship between tandem duplication and stress responsiveness. Average subfamily stress responsiveness (FS), as defined in the text, was plotted against the percentage of subfamily members found in tandem repeats for subfamilies with two or more tandem members. Responsiveness for up-regulated and down-regulated genes is shown by white and black circles, respectively. The best-fit lines, Spearman's ρ, and P values for up- and down-regulation are shown.

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