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1. An important role of l ‐fucose biosynthesis and protein fucosylation genes in Arabidopsis immunity

   https://doi.org/10.1111/nph.15639  

   Zhang, Li ; Paasch, Bradley C. ; Chen, Jin ; Day, Brad ; He, Sheng Yang ( January 2019 , New Phytologist)

   Plants mount coordinated immune responses to defend themselves against pathogens. However, the cellular components required for plant immunity are not fully understood. The jasmonate‐mimicking coronatine (COR) toxin produced byPseudomonas syringaepv.tomato(Pst)DC3000 functions to overcome plant immunity. We previously isolated eight Arabidopsis (scord) mutants that exhibit increased susceptibility to aCOR‐deficient mutant ofPstDC3000. Among them, thescord6mutant exhibits defects both in stomatal closure response and in restricting bacterial multiplication inside the apoplast. However, the identity ofSCORD6remained elusive.

   In this study, we aim to identify theSCORD6gene.

   We identifiedSCORD6via next‐generation sequencing and found it to beMURUS1(MUR1), which is involved in the biosynthesis ofGDP‐l‐fucose.

   Discovery ofSCORD6asMUR1led to a series of experiments that revealed a multi‐faceted role ofl‐fucose biosynthesis in stomatal and apoplastic defenses as well as in pattern‐triggered immunity and effector‐triggered immunity, including glycosylation of pattern‐recognition receptors. Furthermore, compromised stomatal and/or apoplastic defenses were observed in mutants of several fucosyltransferases with specific substrates (e.g.O‐glycan,N‐glycan or theDELLAtranscriptional repressors). Collectively, these results uncover a novel and broad role ofl‐fucose and protein fucosylation in plant immunity.

    

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2. A natural diversity screen in Arabidopsis thaliana reveals determinants for HopZ1a recognition in the ZAR1‐ZED1 immune complex

   https://doi.org/10.1111/pce.13927  

   Baudin, Maël ; Martin, Eliza C. ; Sass, Chodon ; Hassan, Jana A. ; Bendix, Claire ; Sauceda, Rolin ; Diplock, Nathan ; Specht, Chelsea D. ; Petrescu, Andrei J. ; Lewis, Jennifer D. ( November 2020 , Plant, Cell & Environment)

   Pathogen pressure on hosts can lead to the evolution of genes regulating the innate immune response. By characterizing naturally occurring polymorphisms in immune receptors, we can better understand the molecular determinants of pathogen recognition. ZAR1 is an ancientArabidopsis thalianaNLR (Nucleotide‐binding [NB] Leucine‐rich‐repeat [LRR] Receptor) that recognizes multiple secreted effector proteins from the pathogenic bacteriaPseudomonas syringaeandXanthomonas campestristhrough its interaction with receptor‐like cytoplasmic kinases (RLCKs). ZAR1 was first identified for its role in recognizingP. syringaeeffector HopZ1a, through its interaction with the RLCK ZED1. To identify additional determinants of HopZ1a recognition, we performed a computational screen for ecotypes from the 1001 Genomes project that were likely to lack HopZ1a recognition, and tested ~300 ecotypes. We identified ecotypes containing polymorphisms in ZAR1 and ZED1. Using our previously establishedNicotiana benthamianatransient assay and Arabidopsis ecotypes, we tested for the effect of naturally occurring polymorphisms on ZAR1 interactions and the immune response. We identified key residues in the NB or LRR domain of ZAR1 that impact the interaction with ZED1. We demonstrate that natural diversity combined with functional assays can help define the molecular determinants and interactions necessary to regulate immune induction in response to pathogens.

    

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3. The tomato Pto gene confers resistance to Pseudomonas floridensis , an emergent plant pathogen with just nine type III effectors

   https://doi.org/10.1111/ppa.12995  

   Eckshtain‐Levi, N. ; Lindeberg, M. ; Vallad, G. E. ; Martin, G. B. ( February 2019 , Plant Pathology)

   A newly discovered bacterial species,Pseudomonas floridensis, has emerged as a pathogen of tomato in Florida. This study compares the virulence and other attributes ofP. floridensistoPseudomonas syringaepv.tomato, which causes bacterial speck disease of tomato.Pseudomonas floridensisreached lower population levels in leaves of tomato as compared to theP. syringaepv.tomatostrainsDC3000 andNYT1. Analysis of the genome sequence of theP. floridensistype strainGEV388 revealed that it has just nine typeIIIeffectors including AvrPtoB_GEV388, which is 66% identical to AvrPtoB inDC3000. Five of these effectors have been previously reported to be members of a ‘minimal effector repertoire’ required for fullDC3000 virulence onNicotiana benthamiana; however,GEV388 grew poorly on leaves of this plant species compared to theDC3000 minimal effector strain. The tomatoPtogene recognizes AvrPtoB in race 0P. syringaepv.tomatostrains, thereby conferring resistance to bacterial speck disease.Ptowas also found to confer resistance toP. floridensis, indicating this gene will be useful in the protection of tomato against this newly emerged pathogen.

    

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4. Phytonematode peptide effectors exploit a host post‐translational trafficking mechanism to the ER using a novel translocation signal

   https://doi.org/10.1111/nph.16765  

   Wang, Jianying ; Dhroso, Andi ; Liu, Xunliang ; Baum, Thomas J. ; Hussey, Richard S. ; Davis, Eric L. ; Wang, Xiaohong ; Korkin, Dmitry ; Mitchum, Melissa G. ( July 2020 , New Phytologist)

   Cyst nematodes induce a multicellular feeding site within roots called a syncytium. It remains unknown how root cells are primed for incorporation into the developing syncytium. Furthermore, it is unclear how CLAVATA3/EMBRYO SURROUNDING REGION (CLE) peptide effectors secreted into the cytoplasm of the initial feeding cell could have an effect on plant cells so distant from where the nematode is feeding as the syncytium expands.

   Here we describe a novel translocation signal within nematode CLE effectors that is recognized by plant cell secretory machinery to redirect these peptides from the cytoplasm to the apoplast of plant cells.

   We show that the translocation signal is functionally conserved across CLE effectors identified in nematode species spanning three genera and multiple plant species, operative across plant cell types, and can traffic other unrelated small peptides from the cytoplasm to the apoplast of host cells via a previously unknown post‐translational mechanism of endoplasmic reticulum (ER) translocation.

   Our results uncover a mechanism of effector trafficking that is unprecedented in any plant pathogen to date, andthey illustrate how phytonematodes can deliver effector proteins into host cells and then hijack plant cellular processes for their export back out of the cell to function as external signaling molecules to distant cells.

    

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5. Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1– tomato PTO immune complex via acetylation

   Jeleńska, J. ; Lee, J. ; Manning, A.J. ; Wolfgeher, D.J. ; Ahn, Y. ; Walters-Marrah, G. ; Lopez, I.E. ; Garcia, L. ; Sheri A. McClerklin, S.A. ; Michelmore, R.W. ; et al ( January 2021 , PLOS pathogens)

   null (Ed.)

   The plant pathogen Pseudomonas syringae secretes multiple effectors that modulate plant defenses. Some effectors trigger defenses due to specific recognition by plant immune complexes, whereas others can suppress the resulting immune responses. The HopZ3 effector of P. syringae pv. syringae B728a (PsyB728a) is an acetyltransferase that modifies not only components of plant immune complexes, but also the Psy effectors that activate these complexes. In Arabidopsis, HopZ3 acetylates the host RPM1 complex and the Psy effectors AvrRpm1 and AvrB3. This study focuses on the role of HopZ3 during tomato infection. In Psy-resistant tomato, the main immune complex includes PRF and PTO, a RIPK-family kinase that recognizes the AvrPto effector. HopZ3 acts as avirulence factor on tomato by suppressing AvrPto1Psy-triggered immunity. HopZ3acetylates AvrPto1Psy and the host proteins PTO, SlRIPK and SlRIN4s. Biochemical reconstruction and site-directed mutagenesis experiments suggest that acetylation acts in multiple ways to suppress immune signaling in tomato. First, acetylation disrupts the critical AvrPto1Psy-PTO interaction needed to initiate the immune response. Unmodified residues at the binding interface of both proteins and at other residues needed for binding are acetylated. Second, acetylation occurs at residues important for AvrPto1Psy function but not for binding to PTO. Finally, acetylation reduces specific phosphorylations needed for promoting the immune-inducing activity of HopZ3’s targets such as AvrPto1Psy and PTO. In some cases, acetylation competes with phosphorylation. HopZ3-mediated acetylation suppresses the kinase activity of SlRIPK and the phosphorylation of its SlRIN4 substrate previously implicated in PTO-signaling. Thus, HopZ3 disrupts the functions of multiple immune components and the effectors that trigger them, leading to increased susceptibility to infection. Finally, mass 44 spectrometry used to map specific acetylated residues confirmed HopZ3’s unusual capacity to modify histidine in addition to serine, threonine and lysine residues. 

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