Early Molecular Responses of Tomato to Combined Moderate Water Stress and Tomato Red Spider Mite Tetranychus evansi Attack

Interaction between plants and their environment is changing as a consequence of the climate change and global warming, increasing the performance and dispersal of some pest species which become invasive species. Tetranychus evansi also known as the tomato red spider mite, is an invasive species which has been reported to increase its performance when feeding in the tomato cultivar Moneymaker (MM) under water deficit conditions. In order to clarify the underlying molecular events involved, we examined early plant molecular changes occurring on MM during T. evansi infestation alone or in combination with moderate drought stress. Hormonal profiling of MM plants showed an increase in abscisic acid (ABA) levels in drought-stressed plants while salicylic acid (SA) levels were higher in drought-stressed plants infested with T. evansi, indicating that SA is involved in the regulation of plant responses to this stress combination. Changes in the expression of ABA-dependent DREB2, NCED1, and RAB18 genes confirmed the presence of drought-dependent molecular responses in tomato plants and indicated that these responses could be modulated by the tomato red spider mite. Tomato metabolic profiling identified 42 differentially altered compounds produced by T. evansi attack, moderate drought stress, and/or their combination, reinforcing the idea of putative manipulation of tomato plant responses by tomato red spider mite. Altogether, these results indicate that the tomato red spider mite acts modulating plant responses to moderate drought stress by interfering with the ABA and SA hormonal responses, providing new insights into the early events occurring on plant biotic and abiotic stress interaction

Performance of <i>T</i>. <i>evansi</i> with regard to the number of eggs laid (a) and leaf damaged area (b), on leaf disks treated with L-proline.

<p>Concentrations applied are equivalent to the one estimated on drought-stressed tomato plants at 4 and 10 days post infestation. Data are mean ±SE. Different letters indicate significant differences (One-way ANOVA, Bonferroni <i>post hoc</i> test, <i>P</i><0.05).</p

Water stress status (well watered, mild and moderate drought) of tomato plant.

<p>Drought induction was started 7 days before mite infestation and was continued until the end of the experiment [10 days post infestation (dpi)]. It is expressed as percentages of saturation weight (SW) and volumetric soil water content (Ɵ). The turgor loss point was established as 40% of SW.</p

Effect of moderate drought at mite infestation and at 4 and 10 days post infestation (dpi) on: a) tomato stomatal conductance (gs); b) maximum quantum yield of PSII photochemistry (Fv/Fm); c) stem length; d) plant aerial dry weight.

<p>Data are mean ± SE. * indicates a statistically significant difference within each time (Three-way ANOVA, Bonferroni post hoc test, P<0.05).</p

Levels of free amino acids in tomato leaves subjected to moderate drought stress and <i>T</i>. <i>evansi</i> infestation at 10 days post infestation (dpi).

<p>Data represent the ratio ± SE of the different treatments with respect to non-infested control plants at 10 dpi. = [(Treatment−Control 10dpi) / Control 10dpi]. The division between essential and nonessential amino acids is based on a study with the closely related species <i>Tetranychus urticae</i> [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0145275#pone.0145275.ref032" target="_blank">32</a>]. * Indicates significant difference of the treatment with the control determined by Dunnet <i>post hoc</i> test p<0.05.</p

Plant-Mediated Effects of Water Deficit on the Performance of Tetranychus evansi on Tomato Drought-Adapted Accessions

Climate change is expected to increase drought periods and the performance and dispersal of some invasive species such as Tetranychus evansi, which has been reported to take advantage of the nutritional changes induced by water-shortage on the tomato cultivar Moneymaker (MM). We have examined the implications for mite’s biology of four accessions of the drought-adapted tomatoes, “Tomàtiga de Ramellet” (TR), under moderate drought stress. Mite performance was enhanced by drought in two accessions (TR61 and TR154), but not in the other two accessions (TR58 and TR126). We selected one accession of each outcome (i.e., TR154 and TR126) to further analyze plant nutritional parameters. We found that free sugars and most essential amino acids for mites were induced by drought and/or mite infestation on MM and TR154 plants, whereas sugars were not altered and a reduced number of essential amino acids were induced by drought in TR126. Remarkably, mite performance was enhanced by leaf infiltration of free sugars, essential amino acids mixture, and L-proline on well-watered MM and by free sugars on drought-stressed TR126 plants. These results indicate a positive link between the induction of soluble carbohydrates and amino acids used by the plant for osmotic adjustment and mite performance. The effects of drought and/or mite infestation on the defense response of plants was analyzed at three levels: phytohormone accumulation, the transcript levels of marker genes linked to jasmonates (JAs), salicylic acid (SA), and abscisic acid (ABA) pathways, and the activity of defense proteins. The ability of T. evansi to downregulate the accumulation of defense-related phytohormones was noted on MM and the two TR accessions analyzed (TR126 and TR154), though differences in the induction of protein defense genes and activities by drought and/or mite infestation were observed among them. These results emphasize the importance of studying plant biotic and abiotic stress factors in combination and provides an experimental framework for screening drought-tolerant tomato accessions that will be also resistant to herbivore mites

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

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