title: The bacterial effector HopX1 targets JAZ transcriptional repressors to activate jasmonate signaling and promote infection in Arabidopsis.
abstract: Pathogenicity of Pseudomonas syringae is dependent on a type III secretion system, which secretes a suite of virulence effector proteins into the host cytoplasm, and the production of a number of toxins such as coronatine (COR), which is a mimic of the plant hormone jasmonate-isoleuce (JA-Ile). Inside the plant cell, effectors target host molecules to subvert the host cell physiology and disrupt defenses. However, despite the fact that elucidating effector action is essential to understanding bacterial pathogenesis, the molecular function and host targets of the vast majority of effectors remain largely unknown. Here, we found that effector HopX1 from Pseudomonas syringae pv. tabaci (Pta) 11528, a strain that does not produce COR, interacts with and promotes the degradation of JAZ proteins, a key family of JA-repressors. We show that hopX1 encodes a cysteine protease, activity that is required for degradation of JAZs by HopX1. HopX1 associates with JAZ proteins through its central ZIM domain and degradation occurs in a COI1-independent manner. Moreover, ectopic expression of HopX1 in Arabidopsis induces the expression of JA-dependent genes, represses salicylic acid (SA)-induced markers, and complements the growth of a COR-deficient P. syringae pv. tomato (Pto) DC3000 strain during natural bacterial infections. Furthermore, HopX1 promoted susceptibility when delivered by the natural type III secretion system, to a similar extent as the addition of COR, and this effect was dependent on its catalytic activity. Altogether, our results indicate that JAZ proteins are direct targets of bacterial effectors to promote activation of JA-induced defenses and susceptibility in Arabidopsis. HopX1 illustrates a paradigm of an alternative evolutionary solution to COR with similar physiological outcome.
authors.affiliation: Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Madrid, Spain.
authors.forename: Selena
authors.initials: S
authors.lastname: Gimenez-Ibanez
authors.affiliation: Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Madrid, Spain.
authors.forename: Marta
authors.initials: M
authors.lastname: Boter
authors.affiliation: Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Madrid, Spain.
authors.forename: Gemma
authors.initials: G
authors.lastname: Fernández-Barbero
authors.affiliation: Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Madrid, Spain.
authors.forename: Andrea
authors.initials: A
authors.lastname: Chini
authors.affiliation: Research School of Biology, Australian National University, Canberra, Australia.
authors.forename: John P
authors.initials: JP
authors.lastname: Rathjen
authors.affiliation: Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Madrid, Spain.
authors.forename: Roberto
authors.initials: R
authors.lastname: Solano
mesh_terms: D017360:Arabidopsis / Q000378:metabolism* / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001426:Bacterial Proteins / Q000502:physiology*; D003517:Cyclopentanes / Q000378:metabolism*; D057056:Cysteine Proteases / Q000502:physiology*; D004268:DNA-Binding Proteins / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D054884:Host-Pathogen Interactions; D009687:Nuclear Proteins / Q000378:metabolism; D054883:Oxylipins / Q000378:metabolism*; D010935:Plant Diseases / Q000382:microbiology; D010937:Plant Growth Regulators / Q000378:metabolism; D059748:Proteolysis; D044224:Pseudomonas syringae / Q000201:enzymology*; D012097:Repressor Proteins / Q000378:metabolism*; D014157:Transcription Factors / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D001426:Bacterial Proteins; C092776:CONSTANS protein, Arabidopsis; D003517:Cyclopentanes; D004268:DNA-Binding Proteins; C525049:JAS1 protein, Arabidopsis; C554741:JAZ1 protein, Arabidopsis; C554742:JAZ6 protein, Arabidopsis; D009687:Nuclear Proteins; D054883:Oxylipins; D010937:Plant Growth Regulators; D012097:Repressor Proteins; D014157:Transcription Factors; C011006:jasmonic acid; D057056:Cysteine Proteases