RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members - PubMed (original) (raw)

RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members

Rays H Y Jiang et al. Proc Natl Acad Sci U S A. 2008.

Abstract

Pathogens secrete effector molecules that facilitate the infection of their hosts. A number of effectors identified in plant pathogenic Phytophthora species possess N-terminal motifs (RXLR-dEER) required for targeting these effectors into host cells. Here, we bioinformatically identify >370 candidate effector genes in each of the genomes of P. sojae and P. ramorum. A single superfamily, termed avirulence homolog (Avh) genes, accounts for most of the effectors. The Avh proteins show extensive sequence divergence but are all related and likely evolved from a common ancestor by rapid duplication and divergence. More than half of the Avh proteins contain conserved C-terminal motifs (termed W, Y, and L) that are usually arranged as a module that can be repeated up to eight times. The Avh genes belong to the most rapidly evolving part of the genome, and they are nearly always located at synteny breakpoints. The superfamily includes all experimentally identified oomycete effector and avirulence genes, and its rapid pace of evolution is consistent with a role for Avh proteins in interaction with plant hosts.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Relationship between Avh proteins. (A) Pairwise similarity of Avh groups (AGs). For every pair of groups, the two most similar Avh proteins were used for the sequence similarity analysis. The AGs from left to right and from top to bottom are AG_1_1 to AG_1_9, AG_2 to AG_78, and AG_83. (B) Pairwise similarity of randomly selected 1,000 P. sojae proteins. (C) Phylogram constructed with several AGs. The P. sojae Avh proteins are shaded in gray. The unrooted phylogram is based on NJ analysis. All major clades (indicated by black dots) are consistent with similarity groupings. Confidence of groupings was estimated by using 1,000 bootstrap replicates; numbers next to the branching point indicate the percentage of replicates supporting each branch. On the branch tip, the individual Avh proteins are indicated.

Fig. 2.

Fig. 2.

Conserved C-terminal motifs. (A) Motifs in Avh proteins; 36% of the Avh proteins have a combination of W, Y, and L motifs, 22% have only W motifs, and the remaining 42% do not have identifiable W, Y, or L motifs. SP, signal peptide. (B) The correlation between the number of W motifs and the size of the protein. (C) The consensus sequence of W, Y, and L motifs. The size of the histograms indicates the frequency of the occurrence of the amino acid residue. The most abundant four residues are shown if their frequencies are >2%. The most frequent amino acid at each position is shaded if the frequency is >20%. The most abundant W, Y, and L residues are shaded in black.

Fig. 3.

Fig. 3.

High level of sequence divergence and polymorphisms. (A) Sequence divergence of Avh proteins. Sequence divergence is defined as one sequence identity. PsAvh and PrAvh proteins were compared against P. ramorum and P. sojae proteins, respectively. Each radius ranges from 0 (center) to 80 (outer circle) representing 100–20% (or less) identity. The distribution along each circumference is random. A set of 1,000 randomly selected P. sojae proteins was compared against P. ramorum. (B) Positively selected sites in Avh proteins. Codeml model 2a was used to detect positively selected sites (shaded in black). The motifs are indicated by asterisks underneath. The analysis was performed on alleles of Avr1b (9) and close paralogs of PrAvh302.

Fig. 4.

Fig. 4.

Synteny breakpoints at the locations of Avh genes. (A) Distribution of Avh genes represented as indels. Six scaffolds containing more than two PsAvh genes are shown. PsScaffold_36 and PrScaffold_50 contain the largest clusters of Avh genes in P. sojae and P. ramorum, respectively. Paralogs belonging to the same family are indicated by lines. (B) One deletion and one rearrangement of PsAvh genes in the P. sojae scaffold_23. Orthologs are connected by thin lines.

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