Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization.

Shumei Wang,Xinwei Chen,Hazel Mclellan,Ingo Hein,Yajuan Ren,Stefan Engelhardt,Tatyana Bukharova,Jiayang Shi,Haixia Wang,Pauline Van Weymers,Fraser Murphy,Xiaodan Wang,Zhendong Tian,Gaëtan Thilliez ,Vivianne G A A Vleeshouwers ,Paul R J Birch ,Eleanor M Gilroy ,Stephen C Whisson ,Shi‐Gang Sun ,Qiaojun He ,Petra C Boevink

doi:10.1093/jxb/ery360

Abstract

Oomycetes such as the potato blight pathogen Phytophthora infestans deliver RXLR effectors into plant cells to manipulate host processes and promote disease. Knowledge of where they localize inside host cells is important in understanding their function. Fifty-two P. infestans RXLR effectors (PiRXLRs) up-regulated during early stages of infection were expressed as fluorescent protein (FP) fusions inside cells of the model host Nicotiana benthamiana. FP-PiRXLR fusions were predominantly nucleo-cytoplasmic, nuclear, or plasma membrane-associated. Some also localized to the endoplasmic reticulum, mitochondria, peroxisomes, or microtubules, suggesting diverse sites of subcellular activity. Seven of the 25 PiRXLRs examined during infection accumulated at sites of haustorium penetration, probably due to co-localization with host target processes; Pi16663 (Avr1), for example, localized to Sec5-associated mobile bodies which showed perihaustorial accumulation. Forty-five FP-RXLR fusions enhanced pathogen leaf colonization when expressed in Nicotiana benthamiana, revealing that their presence was beneficial to infection. Co-expression of PiRXLRs that target and suppress different immune pathways resulted in an additive enhancement of colonization, indicating the potential to study effector combinations using transient expression assays. We provide a broad platform of high confidence P. infestans effector candidates from which to investigate the mechanisms, singly and in combination, by which this pathogen causes disease.

Highlights

Oomycetes are amongst the most successful groups of plant Phytophthora sojae causes severe damage to soybean, P. ramopathogens
Using the N. benthamiana–P.infestans pathosystem, which has been widely used for host–P. infestans interaction studies (Whisson et al, 2016), we found that transient expression of the majority of P. infestans RXLR effectors (PiRXLRs) effector candidates promoted P. infestans colonization
Fifty-two PiRXLR effector candidates were selected based on those reported to be induced during infection

Summary

Introduction

Oomycetes are amongst the most successful groups of plant Phytophthora sojae causes severe damage to soybean, P. ramopathogens They cause destructive diseases of economic- rum is responsible for Sudden Oak Death, P. palmivora infects a ally important crops (Kamoun et al, 2015). Many filamentous pathogens exert their virulence through effector proteins which are thought to promote pathogen colonization by modulating plant innate immunity (e.g. Whisson et al, 2016; Lanver et al, 2017) Phytophthora infestans produces both cytoplasmic and apoplastic effectors.Apoplastic effectors act outside the plant cell and include inhibitors of host hydrolases and proteases (Tian et al, 2007; Damasceno et al, 2008), whereas cytoplasmic effectors function within host cells and have a diverse range of targets and activities (Whisson et al, 2016)

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Conclusion