Salivary proteins of spider mites suppress defenses in Nicotiana benthamiana and promote mite reproduction. (April 2016)

• Record Type: Journal Article
• Authors: Villarroel, Carlos A.; Jonckheere, Wim; Alba, Juan M.; Glas, Joris J.; Dermauw, Wannes; Haring, Michel A.; Van Leeuwen, Thomas; Schuurink, Robert C.; Kant, Merijn R.
• Is Part Of: Plant journal. Volume 86:Number 2(2016:Apr.)
• Page Start: 119
• Page End: 131
• Publication Date: 2016-04
• Subjects: Tetranychus urticae -- Tetranychus evansi -- Nicotiana benthamiana -- Solanum lycopersicum -- effector -- plant defense suppression -- salicylic acid -- jasmonic acid -- Agrobacterium tumefaciens transient assay -- nahG tomato; Plant molecular biology -- Periodicals; Plant cells and tissues -- Periodicals; Botany -- Periodicals; 580
• DOI: 10.1111/tpj.13152
• Languages: English
• ISSNs: 0960-7412

Abstract

Summary: 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. Significance Statement: Effector proteins from microbial, insect and nematode pathogens suppress plant defense responses, but whether mites used a similar strategy has been poorly studied. Here we used bioinformatics, in situ hybridization, gene‐expression analysis, and bioassays to provide evidence that spider mite saliva has effector proteins which suppress plant salicylic acid defenses.