An ancestral oomycete locus contains late blight avirulence gene Avr3a , encoding a protein that is recognized in the host cytoplasm

Abstract

The oomycete Phytophthora infestans causes late blight, the potato disease that precipitated the Irish famines in 1846 and 1847. It represents a reemerging threat to potato production and is one of >70 species that are arguably the most devastating pathogens of dicotyledonous plants. Nevertheless, little is known about the molecular bases of pathogenicity in these algae-like organisms or of avirulence molecules that are perceived by host defenses. Disease resistance alleles, products of which recognize corresponding avirulence molecules in the pathogen, have been introgressed into the cultivated potato from a wild species, Solanum demissum, and R1 and R3a have been identified. We used association genetics to identify Avr3a and show that it encodes a protein that is recognized in the host cytoplasm, where it triggers R3a-dependent cell death. Avr3a resides in a region of the P. infestans genome that is colinear with the locus containing avirulence gene ATR1 NdWsB in Hyaloperonospora parasitica, an oomycete pathogen of Arabidopsis. Remarkably, distances between conserved genes in these avirulence loci were often similar, despite intervening genomic variation. We suggest that Avr3a has undergone gene duplication and that an allele evading recognition by R3a arose under positive selection.microsynteny ͉ Phytophthora infestans ͉ hypersensitive response ͉ linkage disequilibrium ͉ hemibiotroph

Evidence for intragenic recombination and selective sweep in an effector gene of Phytophthora infestans

“…This high evolutionary rate may well contribute to the rapid “breakdown” of many host resistances mediated by major genes (Cooke et al., 2012; Pilet et al., 2005). In previous studies, only two haplotypes formed by three SNPs were detected in 55 isolates of P. infestans (Armstrong et al., 2005) and six haplotypes generated by 12 SNPs were found in a different set of 88 sequences (Cárdenas et al., 2011). High haplotype diversity in the current study is unlikely due to artifacts generated by PCR amplification.…”

“…Large population size coupled with its continuing expansion creates optimal conditions for the generation and maintenance of genetic variation in the Chinese pathogen population. Interestingly, no shared AA sequences were found between the current and previous studies except the Avr3a EM virulent form (Armstrong et al., 2005; Cárdenas et al., 2011). In 2005, the frequency of Avr3a KI accounted for ~15% of the population (55 isolates, Armstrong et al., 2005) but its frequency reduced to ~7% in 2011 (88 isolates, Cárdenas et al., 2011).…”

“…These primers were originally designed for Pex147 (Armstrong et al., 2005) but were successfully used to amplify Avr3a in a previous study (Cárdenas et al., 2011). PCRs were carried out in a 25 μl reaction volume using Gene Cycler ™ (Bio‐Rad, Shanghai).…”

“…Avr3a, recognized by the corresponding resistance gene R3a in the host plant, was the first effector gene characterized in P. infestans (Armstrong et al., 2005). It is a RXLR effector containing conserved W, Y, and L motifs in C‐terminal domains.…”

“…Silencing Avr3a compromised the pathogenicity of P. infestans in a susceptible potato cultivar and Nicotiana benthamiana (Bos et al., 2010; Vetukuri et al., 2011). Although both virulent and avirulent types of Avr3a existed in P. infestans , the former are more frequent, accounting for 60%–100% of Avr3a in natural populations (Armstrong et al., 2005; Cárdenas et al., 2011; Wu et al., 2016). Recently, several main groups of isoforms have been functional analyzed.…”