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Open AccessArticle

Distinct Signatures of Host Defense Suppression by Plant-Feeding Mites

1
Department of Evolutionary and Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. Box 94240, 1090 GE Amsterdam, The Netherlands
2
Department of Plants and Crops, Faculty of Bioscience Engineering, Ghent University, B-9000 Ghent, Belgium
3
Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, P.O. Box 94215, 1090 GE Amsterdam, The Netherlands
*
Author to whom correspondence should be addressed.
These authors contributed equally to this work.
Current address: Institute of Plant Sciences, University of Bern, 3013 Bern, Switzerland.
§
Current address: Rijk Zwaan Breeding BV, P.O. Box 40, 2678 ZG De Lier, The Netherlands.
Int. J. Mol. Sci. 2018, 19(10), 3265; https://doi.org/10.3390/ijms19103265
Received: 8 August 2018 / Revised: 12 October 2018 / Accepted: 14 October 2018 / Published: 20 October 2018
(This article belongs to the Special Issue Plant Defense Genes Against Biotic Stresses)
Tomato plants are attacked by diverse herbivorous arthropods, including by cell-content-feeding mites, such as the extreme generalist Tetranychus urticae and specialists like Tetranychus evansi and Aculops lycopersici. Mite feeding induces plant defense responses that reduce mite performance. However, T. evansi and A. lycopersici suppress plant defenses via poorly understood mechanisms and, consequently, maintain a high performance on tomato. On a shared host, T. urticae can be facilitated by either of the specialist mites, likely due to the suppression of plant defenses. To better understand defense suppression and indirect plant-mediated interactions between herbivorous mites, we used gene-expression microarrays to analyze the transcriptomic changes in tomato after attack by either a single mite species (T. urticae, T. evansi, A. lycopersici) or two species simultaneously (T. urticae plus T. evansi or T. urticae plus A. lycopersici). Additionally, we assessed mite-induced changes in defense-associated phytohormones using LC-MS/MS. Compared to non-infested controls, jasmonates (JAs) and salicylate (SA) accumulated to higher amounts upon all mite-infestation treatments, but the response was attenuated after single infestations with defense-suppressors. Strikingly, whereas 8 to 10% of tomato genes were differentially expressed upon single infestations with T. urticae or A. lycopersici, respectively, only 0.1% was altered in T. evansi-infested plants. Transcriptome analysis of dual-infested leaves revealed that A. lycopersici primarily suppressed T. urticae-induced JA defenses, while T. evansi dampened T. urticae-triggered host responses on a transcriptome-wide scale. The latter suggests that T. evansi not solely down-regulates plant gene expression, but rather directs it back towards housekeeping levels. Our results provide valuable new insights into the mechanisms underlying host defense suppression and the plant-mediated facilitation of competing herbivores. View Full-Text
Keywords: comparative transcriptomics; defense suppression; dual infestation; facilitation; herbivore; plant defense; plant-mediated interactions; tomato red spider mite (Tetranychus evansi); tomato russet mite (Aculops lycopersici); two-spotted spider mite (Tetranychus urticae) comparative transcriptomics; defense suppression; dual infestation; facilitation; herbivore; plant defense; plant-mediated interactions; tomato red spider mite (Tetranychus evansi); tomato russet mite (Aculops lycopersici); two-spotted spider mite (Tetranychus urticae)
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MDPI and ACS Style

Schimmel, B.C.J.; Alba, J.M.; Wybouw, N.; Glas, J.J.; Meijer, T.T.; Schuurink, R.C.; Kant, M.R. Distinct Signatures of Host Defense Suppression by Plant-Feeding Mites. Int. J. Mol. Sci. 2018, 19, 3265.

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