Drought-stressed tomato plants trigger bottom-up effects on key mite pests

Abstract

Abstract The increase on drought periods as consequence of climate change will affect crops sensitive to drought, like tomato whose production in Mediterranean areas is expected to be under deficit irrigation schedules. In this thesis, it has been established the effect of both abiotic (drought) and biotic (mite infestation) stresses on tomato plant, specifically: 1) the effect of drought-stressed tomato plants (cv. Moneymaker) on the performance of three key mite pests, the spider mites Tetranychus urticae and T. evansi, and the eriophyid mite Aculops lycopersici; 2) the morphological, physiological and molecular changes induced in tomato plants in response to both stresses (either alone or in combination) and their effects on the mite’s performance; and 3) the plant-mediated effects of water deficit on the performance of T. evansi on tomato drought-adapted accessions. Our data reveal that T. evansi caused more leaf damage (1.5 fold) to drought-stressed tomato plants. Mite performance was also enhanced, as revealed by significant increases of eggs laid (2 fold) at 4 days post infestation (dpi), and of mobile forms (1.5-2 fold) at 10 dpi. The levels of several essential amino acids (histidine, isoleucine, leucine, tyrosine, valine) and free sugars in tomato leaves were significantly induced by drought in combination with mites. A non-essential amino acid, the osmolite proline, was strongly induced and stimulated mite feeding and egg laying when added to tomato leaf disks at levels recorded at 10 dpi. Tomato plant defense proteins were also affected by drought and/or mite infestation, but T. evansi was capable of circumventing their potential adverse effects. Both, tomato adapted (TA) and non-adapted (TNA) strains of T. urticae benefit from the improved nutritional value of tomato plants induced by drought stress (increased concentrations of essential amino acids and free sugars). Mite infestation alone had almost no effect on the nutritional composition of tomato leaves, with the exception of an increase of free sugars. Tomato plant defense proteins were induced by both drought stress and mite infestation. However, the induction of protease inhibitors was higher in tomatoes exposed to mites from the TNA strain than from the TA strain. The better performance of the TA strain could be associated to both changes in the digestive (cysteine and aspartyl protease and α-amylase activities) and detoxification (esterase activity) physiology of the mites and the attenuation of some of the plant´s defenses (protease inhibitors). A. lycopersici population grew faster and caused more damage on drought-stressed tomato plants. This finding can be related to the increased levels of total protein and several free amino acids in tomato-infested plants. Mite infestation promoted the salicylic acid (SA) response and up-regulated the expression of jasmonic acid (JA) and derivates, as well as the activity of cysteine protease inhibitors, polyphenol oxidase and peroxidase (POD). Drought stress, in turn, reduced the expression of JA marker genes and 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 mite infestation and synergized accumulation of free sugars and SA. Finally, it has been tested the effect on T. evansi performance of four accessions of the drought-adapted tomatoes, ‘Tomàtiga de Ramellet’ (TR) under water shortage. In the accessions TR61 and TR154 it was observed an enhancement of mite performance by drought, but not in the TR58 and TR126. A clear link could be established between changes in plant nutritional value and mite performance. Soluble free essential amino were accumulated on tomato plants where mite performance was enhanced under drought stress (TR154 and Moneymaker). This induction did not occur in TR126, where mite performance was not altered. Furthermore, the induction of plant defences in response to T. evansi infestation was stronger in TR126 and TR154 than in Moneymaker, which might be a factor contributing to its lower performance on these TR accessions.. These data reveal that the changes induced in the plant by drought and mite infestation increase plant nutritional value and mite performance. Furthermore, it provides an experimental framework to screening for drought-resistant tomato accessions that will be at the same time resistant to herbivore mites, depending on the metabolic changes on the plant. These findings are especially important in the task of adapting area-wide tomato production to mitigate the effects of climate change, and for the management and prediction of herbivore mite proliferation.