title: Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction.
abstract: Spider mites (Tetranychidae sp.) are widely occurring arthropod pests on cultivated plants. Feeding by the two-spotted spider mite T. urticae, a generalist herbivore, induces a defense response in plants that mainly depends on the phytohormones jasmonic acid and salicylic acid (SA). On tomato (Solanum lycopersicum), however, certain genotypes of T. urticae and the specialist species T. evansi were found to suppress these defenses. This phenomenon occurs downstream of phytohormone accumulation via an unknown mechanism. We investigated if spider mites possess effector-like proteins in their saliva that can account for this defense suppression. First we performed an in silico prediction of the T. urticae and the T. evansi secretomes, and subsequently generated a short list of candidate effectors based on additional selection criteria such as life stage-specific expression and salivary gland expression via whole mount in situ hybridization. We picked the top five most promising protein families and then expressed representatives in Nicotiana benthamiana using Agrobacterium tumefaciens transient expression assays to assess their effect on plant defenses. Four proteins from two families suppressed defenses downstream of the phytohormone SA. Furthermore, T. urticae performance on N. benthamiana improved in response to transient expression of three of these proteins and this improvement was similar to that of mites feeding on the tomato SA accumulation mutant nahG. Our results suggest that both generalist and specialist plant-eating mite species are sensitive to SA defenses but secrete proteins via their saliva to reduce the negative effects of these defenses.
authors.affiliation: Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.|Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Carlos A
authors.initials: CA
authors.lastname: Villarroel
authors.affiliation: Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Wim
authors.initials: W
authors.lastname: Jonckheere
authors.affiliation: Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Juan M
authors.initials: JM
authors.lastname: Alba
authors.affiliation: Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Joris J
authors.initials: JJ
authors.lastname: Glas
authors.affiliation: Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, B-9000, Ghent, Belgium.
authors.forename: Wannes
authors.initials: W
authors.lastname: Dermauw
authors.affiliation: Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Michel A
authors.initials: MA
authors.lastname: Haring
authors.affiliation: Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.|Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, B-9000, Ghent, Belgium.
authors.forename: Thomas
authors.initials: T
authors.lastname: Van Leeuwen
authors.affiliation: Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Robert C
authors.initials: RC
authors.lastname: Schuurink
authors.affiliation: Department of Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE, Amsterdam, The Netherlands.
authors.forename: Merijn R
authors.initials: MR
authors.lastname: Kant
mesh_terms: D000818:Animals; D060829:Arthropod Proteins / Q000378:metabolism*; D060434:Herbivory; D008925:Mites / Q000145:classification / Q000502:physiology*; D012098:Reproduction; D012471:Salivary Proteins and Peptides / Q000378:metabolism*; D014026:Nicotiana / Q000276:immunology*
chemical_list: D060829:Arthropod Proteins; D012471:Salivary Proteins and Peptides
keywords: Agrobacterium tumefaciens transient assay; Nicotiana benthamiana; Solanum lycopersicum; Tetranychus evansi; Tetranychus urticae; effector; jasmonic acid; nahG tomato; plant defense suppression; salicylic acid