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

Shumei Wang, Hazel McLellan, Tatyana Bukharova, Qin He, Fraser Murphy, Jiayang Shi, Shaohui Sun, Pauline van Weymers, Yajuan Ren, Gaetan Thilliez, Haixia Wang, Xinwei Chen, Stefan Engelhardt, Vivianne Vleeshouwers, Eleanor M. Gilroy, Stephen C. Whisson, Ingo Hein, Xiaodan Wang, Zhendong Tian, Paul R. J. BirchPetra C. Boevink

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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.

Original languageEnglish
Pages (from-to)343-356
Number of pages14
JournalJournal of Experimental Botany
Volume70
Issue number1
Early online date16 Oct 2018
DOIs
Publication statusPublished - 1 Jan 2019

Keywords

  • Avirulence
  • biotrophy
  • effector-triggered susceptibility
  • pathogenicity
  • Phytophthora
  • RXLR effector
  • virulence

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  • Projects

    Student Theses

    Secretion and delivery of virulence proteins from Phytophthora infestans to its host

    Author: Wang, S., 2019

    Supervisor: Birch, P. (Supervisor), Boevink, P. (Supervisor) & Whisson, S. (Supervisor)

    Student thesis: Doctoral ThesisDoctor of Philosophy

    Cite this

    Wang, S., McLellan, H., Bukharova, T., He, Q., Murphy, F., Shi, J., Sun, S., van Weymers, P., Ren, Y., Thilliez, G., Wang, H., Chen, X., Engelhardt, S., Vleeshouwers, V., Gilroy, E. M., Whisson, S. C., Hein, I., Wang, X., Tian, Z., ... Boevink, P. C. (2019). Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization. Journal of Experimental Botany, 70(1), 343-356. https://doi.org/10.1093/jxb/ery360