Terminating rice innate immunity induction requires a network of antagonistic and redox-responsive E3 ubiquitin ligases targeting a fungal sirtuin

Gang Li, Xiaobo Qi, Guangchao Sun, Raquel O. Rocha, Lauren M. Segal, Katherine S. Downey, Janet D. Wright, Richard A. Wilson

Research output: Contribution to journalArticle

Abstract

Fungal phytopathogens can suppress plant immune mechanisms in order to colonize living host cells. Identifying all the molecular components involved is critical for elaborating a detailed systems-level model of plant infection probing pathogen weaknesses; yet, the hierarchy of molecular events controlling fungal responses to the plant cell is not clear. Here we show how, in the blast fungus Magnaporthe oryzae, terminating rice innate immunity requires a dynamic network of redox-responsive E3 ubiquitin ligases targeting fungal sirtuin 2 (Sir2), an antioxidation regulator required for suppressing the host oxidative burst. Immunoblotting, immunopurification, mass spectrometry and gene functional analyses showed that Sir2 levels responded to oxidative stress via a mechanism involving ubiquitination and three antagonistic E3 ubiquitin ligases: Grr1 and Ptr1 maintained basal Sir2 levels in the absence of oxidative stress; Upl3 facilitated Sir2 accumulation in response to oxidative stress. Grr1 and Upl3 interacted directly with Sir2 in a manner that decreased and scaled with oxidative stress, respectively. Deleting UPL3 depleted Sir2 during growth in rice cells, triggering host immunity and preventing infection. Overexpressing SIR2 in the Δupl3 mutant remediated pathogenicity. Our work reveals how redox-responsive E3 ubiquitin ligases in M. oryzae mediate Sir2 accumulation-dependent antioxidation to modulate plant innate immunity and host susceptibility.

Original languageEnglish (US)
Pages (from-to)523-540
Number of pages18
JournalNew Phytologist
Volume226
Issue number2
DOIs
StatePublished - Apr 1 2020

Keywords

  • E3 ubiquitin ligase
  • Magnaporthe oryzae
  • Pyricularia oryzae
  • redox stress
  • rice blast
  • rice innate immunity
  • sirtuin

ASJC Scopus subject areas

  • Physiology
  • Plant Science

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