Drought stress promotes the colonization success of a herbivorous mite that manipulates plant defenses

Miguel G Ximénez-Embún,Juan M Alba,Felix Ortego,Joris J Glas,Pedro Castañera,Merijn R Kant

doi:10.1007/s10493-017-0200-4

Abstract

Climate change is expected to bring longer periods of drought and this may affect the plant’s ability to resist pests. We assessed if water deficit affects the tomato russet mite (TRM; Aculops lycopersici), a key tomato-pest. TRM thrives on tomato by suppressing the plant’s jamonate defenses while these defenses typically are modulated by drought stress. We observed that the TRM population grows faster and causes more damage on drought-stressed plants. To explain this observation we measured several nutrients, phytohormones, defense-gene expression and the activity of defensive proteins in plants with or without drought stress or TRM. TRM increased the levels of total protein and several free amino acids. It also promoted the SA-response and upregulated the accumulation of jasmonates but down-regulated the downstream marker genes while promoting the activity of cysteine—but not serine—protease inhibitors, polyphenol oxidase and of peroxidase (POD). Drought stress, in turn, retained the down regulation of JA-marker genes and reduced the activity of serine protease inhibitors and POD, and altered the levels of some free-amino acids. When combined, drought stress antagonized the accumulation of POD and JA by TRM and synergized accumulation of free sugars and SA. Our data show that drought stress interacts with pest-induced primary and secondary metabolic changes and promotes pest performance.

Highlights

Global agriculture faces a big challenge as climate change will affect crop production in the near future
Plant stress responses are regulated by a complex network of phytohormones, with jasmonic acid (JA) and salicylic acid (SA) as the central players assisted by ancillary hormones such as abscisic acid (ABA), auxins and ethylene
Our data show that tomatoes infested with tomato russet mite (TRM) increase their levels of total protein and of several free amino acids while promoting SA-responses and upregulating the activity of cysteine protease inhibitors, polyphenol oxidases and peroxidases

Summary

Introduction

Global agriculture faces a big challenge as climate change will affect crop production in the near future. In order to prevent desiccation, cells undergo an osmotic adjustment, increasing the amount of free sugars and free amino acids, especially proline (Hummel et al 2010; Showler 2013) These metabolic changes in the plant, have as consequence an increase on plant nutritional value for herbivores and can promote their performance (Huberty and Denno 2004; White 2009). Herbivores such as mites appear not to be passive and may themselves manipulate the plant’s primary metabolism (Zhou et al 2015) and secondary metabolism i.e., defenses (Kant et al 2015) to their own benefit. Phytohormones can crosstalk and thereby modulate each other’s actions (Pieterse et al 2009; Berens et al 2017)

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