Academic journal article Genetics

Arabidopsis Thaliana Genes Encoding Defense Signaling and Recognition Proteins Exhibit Contrasting Evolutionary Dynamics

Academic journal article Genetics

Arabidopsis Thaliana Genes Encoding Defense Signaling and Recognition Proteins Exhibit Contrasting Evolutionary Dynamics

Article excerpt

ABSTRACT

The interplay between pathogen effectors, their host targets, and cognate recognition proteins provides various opportunities for antagonistic cycles of selection acting on plant and pathogen to achieve or abrogate resistance, respectively. Selection has previously been shown to maintain diversity in plant proteins involved in pathogen recognition and some of their cognate pathogen effectors. We analyzed the signatures of selection on 10 Arabidopsis thaliana genes encoding defense signal transduction proteins in plants, which are potential targets of pathogen effectors. There was insufficient evidence to reject neutral evolution for 6 genes encoding signaling components consistent with these proteins not being targets of effectors and/or indicative of constraints on their ability to coevolve with pathogen effectors. Functional constraints on effector targets may have provided the driving selective force for the evolution of guard proteins. PBS1, a known target of an effector, showed little variation but is known to be monitored by a variable guard protein. Evidence of selection maintaining diversity was present at NPR1, PAD4, and EDS1. Differences in the signatures of selection observed may reflect the numbers of effectors that target a particular protein, the presence or absence of a cognate guard protein, as well as functional constraints imposed by biochemical activities or interactions with plant proteins.

NUMEROUS molecular events determine the outcome of interactions between plants and potential pathogens (Jones and Dangl 2006). On the plant side, these include proteins involved in the direct or indirect recognition of pathogens, signaling proteins that transduce recognition events, and response proteins that are induced and restrict pathogen growth as a result of their antimicrobial activity or inhibitory action on pathogenicity factors. These are matched in the pathogen by effector proteins that manipulate the host to the pathogen's advantage. Effectors may act by interfering with the resistance signaling pathway or as pathogenicity factors such as hydrolytic enzymes or inhibitors of response proteins. There are, therefore,multiple opportunities for antagonistic cycles of selection acting on plant and pathogen to affect or abrogate resistance.

The majority of host recognition genes cloned to date encode nucleotide binding site-leucine rich repeat (NBS-LRR) proteins. Analyses of NBS-LRR paralogs have revealed hypervariability in the predicted solvent exposed residues in the LRR region (e.g., Jones and Jones 1997; Kuang et al. 2004). This is consistent with diversifying selection indicative of simultaneous selection acting on both pathogen effectors and host recognition proteins in their respective attempts to avoid and maintain detection. Evolutionary analyses of NBS-LRR genes, however, are complicated by extensive gene duplication, variable rates of sequence exchange between paralogs, and indistinguishable orthologous relationships. Therefore, evolutionary analyses of individual genes in clusters are problematic. Strong diversifying selection has, however, been detected for at least two lowcopy genes, RPP13 in Arabidopsis thaliana and L in flax, in which sequence exchange between paralogs has been rare (Ellis et al. 1999; Rose et al. 2004; Dodds et al. 2006). Furthermore, several single-copy NBS-LRRencoding loci have presence-absence polymorphisms that correlate with resistance/susceptibility phenotypes, limited diversity within each allelic class, and ancient polymorphisms (Stahl et al. 1999; Tianet al. 2002; Shen et al. 2006). Frequency-dependent selection is thought to generate and maintain the diversity at R-gene loci exhibiting both patterns of variation (Michelmore and Meyers 1998; Stahl et al. 1999).

Only a few response genes have demonstrated strong evidence of selection (Tiffin and Moeller 2006). Positive selection has been detected at specific amino acid sites within cell wall degrading enzymes and inhibitors such as class I chitinases, endo-b-1,3-glucanases, and polygalacturonase inhibitor proteins (PGIPs) (Stotz et al. …

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