A subset of Ubiquitin-conjugating Enzymes is essential for Plant Immunity

Bangjun Zhou, Ravi V. Mural, Xuanyang Chen, Matt E. Oates, Richard A. Connor, Gregory B. Martin, Julian Gough, Lirong Zeng

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20 Scopus citations

Abstract

Of the three classes of enzymes involved in ubiquitination, ubiquitin-conjugating enzymes (E2) have been often incorrectly considered to play merely an auxiliary role in the process, and few E2 enzymes have been investigated in plants. To reveal the role of E2 in plant innate immunity, we identified and cloned 40 tomato genes encoding ubiquitin E2 proteins. Thioester assays indicated that the majority of the genes encode enzymatically active E2. Phylogenetic analysis classified the 40 tomato E2 enzymes into 13 groups, of which members of group III were found to interact and act specifically with AvrPtoB, a Pseudomonas syringae pv tomato effector that uses its ubiquitin ligase (E3) activity to suppress host immunity. Knocking down the expression of group III E2 genes in Nicotiana benthamiana diminished the AvrPtoB-promoted degradation of the Fen kinase and the AvrPtoB suppression of host immunity-associated programmed cell death. Importantly, silencing group III E2 genes also resulted in reduced pattern-triggered immunity (PTI). By contrast, programmed cell death induced by several effector-triggered immunity elicitors was not affected on group III-silenced plants. Functional characterization suggested redundancy among group III members for their role in the suppression of plant immunity by AvrPtoB and in PTI and identified UBIQUITINCONJUGATING11 (UBC11), UBC28, UBC29, UBC39, and UBC40 as playing a more significant role in PTI than other group III members. Our work builds a foundation for the further characterization of E2s in plant immunity and reveals that AvrPtoB has evolved a strategy for suppressing host immunity that is difficult for the plant to thwart.

Original languageEnglish (US)
Pages (from-to)1371-1390
Number of pages20
JournalPlant physiology
Volume173
Issue number2
DOIs
Publication statusPublished - Feb 2017

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ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

Cite this

Zhou, B., Mural, R. V., Chen, X., Oates, M. E., Connor, R. A., Martin, G. B., ... Zeng, L. (2017). A subset of Ubiquitin-conjugating Enzymes is essential for Plant Immunity. Plant physiology, 173(2), 1371-1390. https://doi.org/10.1104/pp.16.01190