Integrated transcriptomic and metabolomic analysis reveals weak anti-feeding capability from submerged plant Ottelia alismoides to freshwater snails

The direct grazing of herbivores on submerged macrophytes has long been recognized as an important contributor to macrophyte loss in shallow lakes. The defense mechanism of aquatic plants against grazing laid a theoretical basis for the conservation of endangered submerged macrophytes against habitat change. Here, we aim to explore the response of the endangered macrophyte Ottelia alismoides to direct grazing by the freshwater snails Radix swinhoei by using physiological, transcriptomic and metabolomic analyses. Based on field observation, we hypothesize that O. alismoides may not have an effective grazing resistance mechanism. Our 48-h microcosm study revealed 739 differentially expressed genes (DEGs) between the grazed treatment and the control. GO annotation analysis identified DEGs with molecular functions such as signaling receptor activity and various enzyme activities, as well as biological processes including auxin signaling, responses to oxidative stress, and salicylic acid. DEGs related to phytohormones (especially jasmonic acid, JA) and antioxidant enzymes were significantly up-regulated. In addition, the 20 metabolites changed significantly after being grazed. For example, the up-regulation of the JA biosynthetic pathway led to a marginal increase of the JA content in leaves, and its signal transduction pathway was also up-regulated, consistent with that the precursor of secondary metabolism of flavonoids was up-regulated and that the transcriptome biosynthesis pathway of flavonoids was also up-regulated. Though evident defensive steps were found at the aspects of transcriptome and metabolome, leaf intactness and the photosynthetic parameters in the leaves were strongly negatively affected by snail grazing. We argued that the efficiency of those defensive strategies has probably been compromised due to the degenerative secondary metabolism in submerged leaves. Thus, to protect endangered submerged macrophytes, countermeasures for herbivory should be considered along with other important policies.