An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores

Abstract

A general prediction of the specialist/generalist paradigm indicates that plant responses to insect herbivores may depend on the degree of ecological specialization of the insect attacker. However, results from a single greenhouse experiment evaluating the responses of the model plant Arabidopsis thaliana to three specialist (Plutella xylostella, Pieris rapae, and Brevicoryne brassicae) and three generalist (Trichoplusia ni, Spodoptera exigua, and Myzus persicae) insect species did not support the previous prediction. Using an ecological genomic approach, we assessed plant responses in terms of herbivore-induced changes in genome-wide gene expression, defense-related pathways, and concentrations of glucosinolates (i.e., secondary metabolites that are ubiquitously present in cruciferous plants). Our results showed that plant responses were not influenced by the degree of specialization of insect herbivores. In contrast, responses were more strongly shaped by insect taxa (i.e., aphid vs. lepidopteran species), likely due to their different feeding modes. Interestingly, similar patterns of plant responses were induced by the same insect herbivore species in terms of defense signaling (jasmonic acid pathway), aliphatic glucosinolate metabolism (at both the gene expression and phenotypic levels) and genome-wide responses. Furthermore, plant responses to insect herbivores belonging to the same taxon (i.e., four lepidopteran species) were not explained by herbivore specialization or phylogenetic history. Overall, this study suggests that different feeding modes of insect taxa as well as herbivore-specific plant responses, which may result from distinct ecological/evolutionary interactions between A. thaliana (or a close relative) and each of the lepidopteran species, may explain why observed responses deviate from those predicted by the specialist/generalist paradigm.

Intraspecific variation in defense against a generalist lepidopteran herbivore in populations of Eruca sativa (Mill.)

“…2004; Bidart‐Bouzat and Kliebenstein 2011). However, specialist insects (e.g., Pieris sp., Pluttela xylostella ) have evolved physiological means to overcome the toxic effects of GS; the deterrent and toxic properties of these metabolites are therefore mostly effective against generalists (Ratzka et al.…”

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

“…Furthermore, plants show defence responses induced by herbivores, for example by producing compounds that deter or repel the attackers (Schoonhoven et al 2005), which may also affect subsequently feeding herbivores (Kessler & Halitschke 2007). Depending on the feeding guild of the attacking insect, changes in phytohormone production, gene transcription and protein production can occur, which lead to a different regulation of plant defences (Heidel & Baldwin 2004;de Vos et al 2005;Bidart-Bouzat & Kliebenstein 2011;Koo et al 2013) and, thus to expression of a herbivore species-specific induced plant phenotype.…”

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).…”