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Oomycete pathogens secrete hundreds of effectors, including avirulence proteins that trigger host genotype-specific resistance response, to manipulate host immunity and facilitate infection. Sequence and expression variations of avirulence genes in pathogens are well known to be responsible for loss of host genotype-specific disease resistance. However, little is known on the underlying mechanisms associated with virulence variation in the diploid Phytophthora pathogens. We report in this study that the endogenous small RNAs (sRNAs) are involved in the variation of expression of avirulence gene Avr1b in P. sojae. The sRNAs were originated from the natural antisense transcripts of Avr1b. We further showed that the sense and antisense expression of Avr1b were programmed by the 10-base deletions in their promoter regions. Expanded analysis showed that up to 31% of the P. sojae RXLR effector genes were associated with sRNAs. Genome analysis further showed that the 9-bp and 10-bp insertion/deletion variants were significantly enriched in the regulatory regions of RXLR effector genes. These results indicate that the expression of RXLR effector genes are programmed by significantly enriched variations in their regulatory regions that lead to the variations in bidirectional transcription, which likely further affect production of endogenous sRNAs and silencing of homologous RXLR effector genes of Phytophthora pathogens.

Small RNAs generated by bidirectional transcription mediate silencing of RXLR effector genes in the oomycete Phytophthora sojae