Alteration of plant primary metabolism in response to insect herbivory

Abstract

ORCID IDs: 0000-0002-3643-7875 (S.Z.); 0000-0002-4716-4323 (Y.-R.L.); 0000-0002-5912-779X (V.T.); 0000-0002-9675-934X (G.J.).Plants in nature, which are continuously challenged by diverse insect herbivores, produce constitutive and inducible defenses to reduce insect damage and preserve their own fitness. In addition to inducing pathways that are directly responsible for the production of toxic and deterrent compounds, insect herbivory causes numerous changes in plant primary metabolism. Whereas the functions of defensive metabolites such as alkaloids, terpenes, and glucosinolates have been studied extensively, the fitness benefits of changes in photosynthesis, carbon transport, and nitrogen allocation remain less well understood. Adding to the complexity of the observed responses, the feeding habits of different insect herbivores can significantly influence the induced changes in plant primary metabolism. In this review, we summarize experimental data addressing the significance of insect feeding habits, as related to herbivore-induced changes in plant primary metabolism. Where possible, we link these physiological changes with current understanding of their underlying molecular mechanisms. Finally, we discuss the potential fitness benefits that host plants receive from altering their primary metabolism in response to insect herbivory.

Trichoderma gamsii affected herbivore feeding behaviour on Arabidopsis thaliana by modifying the leaf metabolome and phytohormones

“…The biosynthesis of tryptophan, glutamine and glutamic acid are induced in herbivore‐infested plants. The overproduction of these amino acids seems to serve as precursors for inducible defence metabolites (Brotman et al ., 2012; Rojas et al ., 2014; Zhou et al ., 2015). In our study, the leaves of T. gamsii F18‐treated plants had more tyrosine, tryptophan, serine, oxoproline, ornithine, phenylalanine, lysine, glutamine, glutamic acid, cyanoalanine, citrulline, aspartic acid and asparagine compared to the control plants.…”

“…For example, tryptophan plays a critical role in regulating plant responses to biotic and abiotic stresses (Radwanski and Last, 1995; Zhao and Last, 1996; Sangha et al ., 2011). Transcript profiling data generally show herbivory‐induced changes in the expression of genes related to the production of glutamine, glutamic acid, asparagine and aspartic acid (Thompson and Goggin, 2006; Caldana et al ., 2011; Appel and Cocroft, 2014; Zhou et al ., 2015), which are involved in nitrogen assimilation (Coruzzi and Last, 2000). Amino acids also play a role in signal transduction to induce defence gene expression.…”

Focus Issue on Metabolism: Metabolites, Metabolites Everywhere

“…While the production of specialized metabolites as defensive molecules is well documented and at times considerable, with, for example, nicotine conditionally containing 6% of the nitrogen in Nicotiana attenuata (Baldwin et al, 1998) and benzoxazinoids constituting up to 2% of the dry matter of some Poaceae (Zuniga et al, 1983), the effects on constitutively abundant metabolites are less frequently considered. In their review, Zhou et al (2015) collate studies looking precisely at these metabolites and comparing specialist versus generalist herbivores (Steinbrenner et al, 2011). The metabolic data, when considered together with collated gene expression data, lead to the intriguing conclusion that, for specialist herbivores, tomato (Solanum lycopersicum) plants change resource allocation rather than produce chemical defense compounds, albeit in a manner that needs to be studied on an interaction-by-interaction basis.…”

“…They conclude with a perspective of current and anticipated developments of what are already becoming indispensable tools of the plant metabolism. The Updates by Soltis and Kliebenstein (2015) and Zhou et al (2015) cover the use of natural variance for the identification of key genes regulating the accumulation or degradation of metabolites and the lesser discussed effects of plantinsect interactions on primary metabolism of the plant, respectively. The first of these provides both mechanistic and evolutionary insights as well as discusses the predominance of the influence of organellar genomes (Joseph et al, 2013) and the sheer breadth of loci that combine to underlie the complex genetic architecture of the metabolome.…”

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

“…Indeed, they hypothesise that in the mite saliva there is a wide range of proteins that can act as effectors or elicitors, and its presence will determine the tomato defense outcome. In fact, the proteins present in the saliva of T. urticae vary depending on the host .To circumvent the deleterious effects of plant secondary metabolites and anti- Herbivore attack can also induce changes in plant primary metabolism, such as the reallocation of carbon and nitrogen resources (Steinbrenner et al, 2011;Zhou et al, 2015). The function of these changes for the plant is still not clear, but it has been suggested that they might be used by the plant as a source of energy, as precursors of defense compounds and to hamper herbivore performance by reducing the nutritive value of plant tissue (Zhou et al, 2015).…”