Trehalose-mediated reprograming: metabolic crosstalk in plant-insect interactions

In nature, plants often face multiple attackers simultaneously, giving rise to complex three-way interactions that can reshape defense outcomes in unexpected ways. An intriguing example comes from observations that prior aphid infestation, or even pretreatment with aphid honeydew, suppresses the jasmonic acid (JA) burst typically triggered by herbivory, thereby increasing plant susceptibility to subsequent insect attack. Yu and colleagues dissected this phenomenon by identifying the active components in aphid honeydew and uncovering the underlying mechanism. Using mass spectrometry, they revealed a complex mixture containing saccharides (notably trehalose), amino acids (including theanine, γ-aminobutyric acid, arginine, glutamic acid, glutamine, and alanine), and several phytohormones (JA, salicylic acid, abscisic acid, and JA-Ile). Functionally, plants subjected to mechanical damage plus trehalose treatment supported significantly greater larval growth. Feeding caterpillars an equivalent amount of trehalose directly, however, did not enhance their weight, demonstrating that trehalose acts by suppressing plant resistance rather than serving as a nutritional supplement. Surprisingly, trehalose treatment did not reduce JA or JA-Ile levels; instead, these hormones increased. The key effect lay elsewhere: catechins, specialized defense metabolites induced by drought stress, were suppressed. Consistent with this, trehalose enhanced plant water retention, whereas dehydration promoted catechin accumulation and herbivory resistance. Together, these findings highlight how insect-derived metabolites can reprogram plant water status and secondary metabolism, uncoupling hormonal signaling from effective defense. Looking ahead, this work opens new avenues for understanding how ecological context and metabolic cross-talk shape plant resistance, contributing to improved design of sustainable crop protection strategies. (Summary by Ching Chan @ntnuchanlab) Plant Cell Environ. 10.1111/pce.70270