title: A Subset of Ubiquitin-Conjugating Enzymes Is Essential for Plant Immunity.
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 UBIQUITIN-CONJUGATING11 (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.
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Bangjun
authors.identifier: 0000-0003-2986-6310
authors.initials: B
authors.lastname: Zhou
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Ravi V
authors.identifier: 0000-0002-1173-0493
authors.initials: RV
authors.lastname: Mural
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Xuanyang
authors.identifier: 0000-0002-3977-5554
authors.initials: X
authors.lastname: Chen
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Matt E
authors.identifier: 0000-0002-0001-3675
authors.initials: ME
authors.lastname: Oates
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Richard A
authors.initials: RA
authors.lastname: Connor
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Gregory B
authors.identifier: 0000-0003-0044-6830
authors.initials: GB
authors.lastname: Martin
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.).|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.).|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.).|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.).
authors.forename: Julian
authors.identifier: 0000-0002-1965-4982
authors.initials: J
authors.lastname: Gough
authors.affiliation: Plant Science Innovation Center and Plant Pathology Department, University of Nebraska, Lincoln, Nebraska 68583 (B.Z., L.Z.); lzeng3@unl.edu.|Biology Department, University of Arkansas, Little Rock, Arkansas 72204 (B.Z., R.V.M., X.C., R.A.C., L.Z.); lzeng3@unl.edu.|Department of Computer Science, University of Bristol, Bristol BS8 1UB, United Kingdom (M.E.O., J.G.); lzeng3@unl.edu.|Boyce Thompson Institute for Plant Research and Department of Plant Pathology and Plant-Microbe Biology, School of Integrative Plant Science, Cornell University, Ithaca, New York 14853 (G.B.M.); and lzeng3@unl.edu.|Southern Regional Collaborative Innovation Center for Grain and Oil Crops, Hunan Agricultural University, Changsha 410128, China (L.Z.) lzeng3@unl.edu.
authors.forename: Lirong
authors.identifier: 0000-0001-8802-4872
authors.initials: L
authors.lastname: Zeng
mesh_terms: D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D016923:Cell Death; D020868:Gene Silencing; D018745:Genome, Plant; D054884:Host-Pathogen Interactions / Q000276:immunology; D018551:Solanum lycopersicum / Q000166:cytology / Q000235:genetics* / Q000276:immunology / Q000382:microbiology; D010802:Phylogeny; D057865:Plant Immunity / Q000502:physiology*; D010940:Plant Proteins / Q000235:genetics / Q000276:immunology* / Q000378:metabolism; D030821:Plants, Genetically Modified; D017346:Protein Serine-Threonine Kinases / Q000235:genetics / Q000378:metabolism; D044224:Pseudomonas syringae / Q000472:pathogenicity; D014026:Nicotiana / Q000235:genetics / Q000378:metabolism; D044763:Ubiquitin-Conjugating Enzymes / Q000235:genetics / Q000276:immunology* / Q000378:metabolism; D054875:Ubiquitination
chemical_list: D001426:Bacterial Proteins; D010940:Plant Proteins; C081695:avrPto protein, Pseudomonas syringae; D044763:Ubiquitin-Conjugating Enzymes; C091599:Fen protein, Lycopersicon esculentum; D017346:Protein Serine-Threonine Kinases