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

Qinhu Wang,Shizhi Luo,Brett M Tyler,Ke Xu,Chengcheng Zhong,Tingting Li,Biao Gu,Yuling Meng,Weixing Shan

doi:10.1186/s42483-019-0026-6

Abstract

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.

Highlights

Oomycetes are eukaryotic pathogens causing severe damages to crops (Kamoun et al 2015)
We show that the silencing of Avr1b in P. sojae is associated with small RNA (sRNA) derived from its natural antisense transcripts (NATs)
Identification of Avr1b-associated sRNAs Avr1b of P. sojae is the first avirulence gene cloned from oomycete pathogens and is recognized by soybeans carrying Rps1b (Shan et al 2004)

Summary

Introduction

Oomycetes are eukaryotic pathogens causing severe damages to crops (Kamoun et al 2015). The losses caused by soybean root and stem rot pathogen Phytophthora sojae is estimated at $1–2 billion per year (Wrather and Koenning 2006; Tyler 2007). Oomycete pathogens secrete a large array of effector proteins to manipulate host immunity and facilitate infection (Kamoun 2006; Stassen and Van den Ackerveken 2011). Many effectors, such as the RXLR family effectors (Jiang et al 2008; Haas et al.2009), are able to trigger or suppress programmed cell death in planta (Oh et al 2009; Wang et al 2011). Most the avirulence genes identified in oomycetes encode RXLR effectors (Jiang and Tyler 2012; Anderson et al 2015)

Methods

Results

Conclusion