title: The Arabidopsis microtubule-associated protein MAP65-3 supports infection by filamentous biotrophic pathogens by down-regulating salicylic acid-dependent defenses.
abstract: The oomycete Hyaloperonospora arabidopsidis and the ascomycete Erysiphe cruciferarum are obligate biotrophic pathogens causing downy mildew and powdery mildew, respectively, on Arabidopsis. Upon infection, the filamentous pathogens induce the formation of intracellular bulbous structures called haustoria, which are required for the biotrophic lifestyle. We previously showed that the microtubule-associated protein AtMAP65-3 plays a critical role in organizing cytoskeleton microtubule arrays during mitosis and cytokinesis. This renders the protein essential for the development of giant cells, which are the feeding sites induced by root knot nematodes. Here, we show that AtMAP65-3 expression is also induced in leaves upon infection by the downy mildew oomycete and the powdery mildew fungus. Loss of AtMAP65-3 function in the map65-3 mutant dramatically reduced infection by both pathogens, predominantly at the stages of leaf penetration. Whole-transcriptome analysis showed an over-represented, constitutive activation of genes involved in salicylic acid (SA) biosynthesis, signaling, and defense execution in map65-3, whereas jasmonic acid (JA)-mediated signaling was down-regulated. Preventing SA synthesis and accumulation in map65-3 rescued plant susceptibility to pathogens, but not the developmental phenotype caused by cytoskeleton defaults. AtMAP65-3 thus has a dual role. It positively regulates cytokinesis, thus plant growth and development, and negatively interferes with plant defense against filamentous biotrophs. Our data suggest that downy mildew and powdery mildew stimulate AtMAP65-3 expression to down-regulate SA signaling for infection.
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Michaël
authors.initials: M
authors.lastname: Quentin
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Isabelle
authors.initials: I
authors.lastname: Baurès
authors.affiliation: Lehrstuhl für Phytopathologie, Technische Universität München, D-85350 Freising-Weihenstephan, Germany.
authors.forename: Caroline
authors.initials: C
authors.lastname: Hoefle
authors.affiliation: The Sainsbury Laboratory, John Innes Centre, Norwich Research Park, Norwich NR4 7UH, UK.
authors.forename: Marie-Cécile
authors.initials: MC
authors.lastname: Caillaud
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Valérie
authors.initials: V
authors.lastname: Allasia
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Franck
authors.initials: F
authors.lastname: Panabières
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Pierre
authors.initials: P
authors.lastname: Abad
authors.affiliation: Lehrstuhl für Phytopathologie, Technische Universität München, D-85350 Freising-Weihenstephan, Germany.
authors.forename: Ralph
authors.initials: R
authors.lastname: Hückelhoven
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France favery@sophia.inra.fr keller@sophia.inra.fr.
authors.forename: Harald
authors.initials: H
authors.lastname: Keller
authors.affiliation: INRA, Université de Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France favery@sophia.inra.fr keller@sophia.inra.fr.
authors.forename: Bruno
authors.initials: B
authors.lastname: Favery
mesh_terms: D017360:Arabidopsis / Q000187:drug effects / Q000235:genetics / Q000276:immunology* / Q000382:microbiology*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D001203:Ascomycota / Q000187:drug effects / Q000502:physiology*; D015536:Down-Regulation / Q000187:drug effects*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D055786:Gene Knockout Techniques; D008869:Microtubule-Associated Proteins / Q000235:genetics / Q000378:metabolism*; D008870:Microtubules / Q000187:drug effects / Q000378:metabolism; D009154:Mutation / Q000235:genetics; D044742:Peronospora / Q000187:drug effects / Q000502:physiology*; D010935:Plant Diseases / Q000382:microbiology*; D020156:Salicylic Acid / Q000494:pharmacology*; D059467:Transcriptome / Q000187:drug effects / Q000235:genetics
chemical_list: D029681:Arabidopsis Proteins; C576219:MAP65-3 protein, Arabidopsis; D008869:Microtubule-Associated Proteins; D020156:Salicylic Acid
keywords: Cytoskeleton; fungus; microtubules; mildew; oomycete; plant defense; salicylic acid.