Molecular, Biochemical, and Organismal Analyses of Tomato Plants Simultaneously Attacked by Herbivores from Two Feeding Guilds

Abstract

Previous work identified aphids and caterpillars as having distinct effects on plant responses to herbivory. We sought to decipher these interactions across different levels of biological organization, i.e., molecular, biochemical, and organismal, with tomato plants either damaged by one 3rd-instar beet armyworm caterpillar (Spodoptera exigua), damaged by 40 adult potato aphids (Macrosiphum euphorbiae), simultaneous damaged by both herbivores, or left undamaged (controls). After placing insects on plants, plants were transferred to a growth chamber for 5 d to induce a systemic response. Subsequently, individual leaflets from non-damaged parts of plants were excised and used for gene expression analysis (microarrays and quantitative real-time PCR), C/N analysis, total protein analysis, proteinase inhibitor (PI) analysis, and for performance assays. At the molecular level, caterpillars up-regulated 56 and down-regulated 29 genes systemically, while aphids up-regulated 93 and downregulated 146 genes, compared to controls. Although aphids induced more genes than caterpillars, the magnitude of caterpillar-induced gene accumulation, particularly for those associated with plant defenses, was often greater. In dualdamaged plants, aphids suppressed 27% of the genes regulated by caterpillars, while caterpillars suppressed 66% of the genes regulated by aphids. At the biochemical level, caterpillars induced three-fold higher PI activity compared to controls, while aphids had no effects on PIs either alone or when paired with caterpillars. Aphid feeding alone reduced the foliar C/N ratio, but not when caterpillars also fed on the plants. Aphid and caterpillar feeding alone had no effect on the amount of protein in systemic leaves; however, both herbivores feeding on the plant reduced the amount of protein compared to aphid-damaged plants. At the organismal level, S. exigua neonate performance was negatively affected by prior caterpillar feeding, regardless of whether aphids were present or absent. This study highlights areas of concordance and disjunction between molecular, biochemical, and organismal measures of induced plant resistance when plants are attacked by multiple herbivores. In general, our data produced consistent results when considering each herbivore separately but not when considering them together.

Loss of Function of FATTY ACID DESATURASE7 in Tomato Enhances Basal Aphid Resistance in a Salicylate-Dependent Manner

“…Application of the SA analog benzothiadiazole also reduces aphid population growth on the Moneymaker cultivar (Cooper et al, 2004;Boughton et al, 2006;. Furthermore, tobacco mosaic virus infection reduces plant susceptibility to aphids in wild-type tomato but not in transgenic plants impaired in SA accumulation, which suggests that the SA-mediated defense responses against pathogens in tomato are also effective against aphids (Rodriguez-Saona et al, 2010).…”

Plant‐mediated interactions between two herbivores differentially affect a subsequently arriving third herbivore in populations of wild cabbage

“…For example, in Nicotiana attenuata plants crosstalk between the JA and SA signalling pathways resulted in optimisation of defence responses (Rayapuram & Baldwin 2007). However, insect herbivores can also interfere with JAand SA-induced defences, which can affect the outcome of interactions between plants and multiple attackers (Voelckel & Baldwin 2004;Rodriguez-Saona et al 2010;Mathur et al 2013). Through these indirect plant-mediated interactions, competition between attacking herbivores is commonly found in nature, in which induced plant responses to a first herbivore may affect the resistance of plants to subsequent herbivores (Denno et al 1995;Kaplan & Denno 2007).…”

The HERBIVORE ELICITOR-REGULATED1 Gene Enhances Abscisic Acid Levels and Defenses against Herbivores in Nicotiana attenuata Plants

“…This ability allows plants to tailor their defense responses to the attack of specific herbivores and thereby attain higher fitness and survival rates in natural environments in which defense-growth tradeoffs frequently determine plant performance (Reymond et al, 2000;Howe and Jander, 2008). Some plants have been shown to discriminate between the attack of generalist and specialist herbivores, or insects from different feeding guilds, through the perception of specific herbivore elicitors associated with the particular insect species (Heidel and Baldwin, 2004;Diezel et al, 2009;Rodriguez-Saona et al, 2010;Bidart-Bouzat and Kliebenstein, 2011;Chung and Felton, 2011;Ali and Agrawal, 2012;Kawazu et al, 2012). A number of herbivore-associated elicitors that mediate these specific recognition responses have already been identified: fatty acid-amino acid conjugates (FACs), caeliferins, Glc oxidase, b-glucosidase, inceptin, oligouronides, and lipases (Alborn et al, 1997;Schäfer et al, 2011;Bonaventure, 2012;Erb et al, 2012).…”