title: A Secreted MIF Cytokine Enables Aphid Feeding and Represses Plant Immune Responses.
abstract: Aphids attack virtually all plant species and cause serious crop damages in agriculture. Despite their dramatic impact on food production, little is known about the molecular processes that allow aphids to exploit their host plants. To date, few aphid salivary proteins have been identified that are essential for aphid feeding, and their nature and function remain largely unknown. Here, we show that a macrophage migration inhibitory factor (MIF) is secreted in aphid saliva. In vertebrates, MIFs are important pro-inflammatory cytokines regulating immune responses. MIF proteins are also secreted by parasites of vertebrates, including nematodes, ticks, and protozoa, and participate in the modulation of host immune responses. The finding that a plant parasite secretes a MIF protein prompted us to question the role of the cytokine in the plant-aphid interaction. We show here that expression of MIF genes is crucial for aphid survival, fecundity, and feeding on a host plant. The ectopic expression of aphid MIFs in leaf tissues inhibits major plant immune responses, such as the expression of defense-related genes, callose deposition, and hypersensitive cell death. Functional complementation analyses in vivo allowed demonstrating that MIF1 is the member of the MIF protein family that allows aphids to exploit their host plants. To our knowledge, this is the first report of a cytokine that is secreted by a parasite to modulate plant immune responses. Our findings suggest a so-far unsuspected conservation of infection strategies among parasites of animal and plant species.
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Elodie
authors.initials: E
authors.lastname: Naessens
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Géraldine
authors.initials: G
authors.lastname: Dubreuil
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France; Université de Picardie Jules Verne, 33 rue Saint Leu, 80039 Amiens, France.
authors.forename: Philippe
authors.initials: P
authors.lastname: Giordanengo
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Olga Lucia
authors.initials: OL
authors.lastname: Baron
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France.
authors.forename: Naïma
authors.initials: N
authors.lastname: Minet-Kebdani
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France. Electronic address: harald.keller@sophia.inra.fr.
authors.forename: Harald
authors.initials: H
authors.lastname: Keller
authors.affiliation: INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France. Electronic address: christine.coustau@sophia.inra.fr.
authors.forename: Christine
authors.initials: C
authors.lastname: Coustau
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001042:Aphids / Q000235:genetics* / Q000378:metabolism; D005786:Gene Expression Regulation; D060434:Herbivory; D019476:Insect Proteins / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D008263:Macrophage Migration-Inhibitory Factors / Q000737:chemistry / Q000235:genetics* / Q000378:metabolism; D008969:Molecular Sequence Data; D057865:Plant Immunity; D018515:Plant Leaves; D012463:Saliva / Q000737:chemistry; D016415:Sequence Alignment; D031307:Vicia faba / Q000276:immunology*
chemical_list: D019476:Insect Proteins; D008263:Macrophage Migration-Inhibitory Factors