Jasmonate‐dependent depletion of soluble sugars compromises plant resistance to Manduca sexta

Abstract

SummaryJasmonates regulate plant secondary metabolism and herbivore resistance. How they influence primary metabolites and how this may affect herbivore growth and performance are not well understood.We profiled sugars and starch of jasmonate biosynthesis-deficient and jasmonate-insensitive Nicotiana attenuata plants and manipulated leaf carbohydrates through genetic engineering and in vitro complementation to assess how jasmonate-dependent sugar accumulation affects the growth of Manduca sexta caterpillars.We found that jasmonates reduce the constitutive and herbivore-induced concentration of glucose and fructose in the leaves across different developmental stages. Diurnal, jasmonatedependent inhibition of invertase activity was identified as a likely mechanism for this phenomenon. Contrary to our expectation, both in planta and in vitro approaches showed that the lower sugar concentrations led to increased M. sexta growth. As a consequence, jasmonate-dependent depletion of sugars rendered N. attenuata plants more susceptible to M. sexta attack.In conclusion, jasmonates are important regulators of leaf carbohydrate accumulation and this determines herbivore growth. Jasmonate-dependent resistance is reduced rather than enhanced through the suppression of glucose and fructose concentrations, which may contribute to the evolution of divergent resistance strategies of plants in nature.

Alteration of plant primary metabolism in response to insect herbivory

“…Lu et al (2015), for example, found that herbivore-induced carbohydrate sequestration can still occur in the roots of jasmonate signaling-deficient rice mutants, whereas reallocation of carbohydrates toward herbivore-attacked leaves and away from roots in N. attenuata is modulated by both jasmonate and auxin signaling (Machado et al, 2013(Machado et al, , 2015. Following this same line of investigation, concomitant with the incorporation of less-studied signaling networks, one would expect the eventual union of defense signaling networks that control herbivore-induced changes in both primary and secondary metabolism.…”

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

“…Whereas early studies of AG-BG interactions between herbivores tended to focus on explanations based on resource alterations (e.g., 106), the advent of the molecular era resulted in a stronger emphasis on explanations based on specificity of induction and specificity of response to systemically induced defenses (e.g., 144). Studies simultaneously considering resource-and defense-based mechanisms (e.g., 104) are now emerging and promise to better explain and predict patterns of outcomes of plant-mediated AG-BG interactions among different types of phytophages.…”

“…N. attenuata plants upregulate CW-Inv in response to leaf herbivory, which is JA dependent and associated with both a reduced depletion of carbohydrates and with increased capacity to enhance secondary metabolite pools (40). JA-dependent inhibition of invertase activity results in a depletion of hexose levels but nevertheless enhances the performance of a leaf-chewing insect (104). Phytophages thus modulate source-sink relationships, which are intertwined with defense signaling.…”

Evolution of herbivore-induced early defense signaling was shaped by genome-wide duplications in Nicotiana

“…In comparison to VIGS-EV plants, VIGS- NaLRRK1 plants accumulated significantly higher transcript levels of FAC-induced NaMYB8, NaTD2 and NaTPI (Figure 7 i-o), consistent with the observed effects on JA signaling. In addition to NaMYB8 regulated genes, FAC induced JA signaling also induces changes in primary metabolism, in particular soluble sugars and soluble invertases activity in N. attenuata (Machado et al, 2015). Here, we also found that VIGS- NaLRRK1 plants showed higher levels of induced soluble sugars and invertases activity in comparison to those of VIGS-EV plants (Figure 7—figure supplement 2).…”