Contrasting defence mechanisms against spider mite infestation in cyanogenic and non-cyanogenic legumes.

Understanding the complex interactions between plants and herbivores is essential for improving crop resistance. Aiming to expand the role of cyanogenesis in plant defence, we investigated the response of the cyanogenic Phaseolus lunatus (lima bean) and the non-cyanogenic Phaseolus vulgaris (common bean) to Tetranychus urticae (spider mite) infestation. Despite mite infesting both legumes, leaf damage infringed by this feeder was reduced in lima bean. Comparative transcriptome analyses revealed that both species exhibited substantial metabolic and transcriptional changes upon infestation, although alterations in P. lunatus were significantly more pronounced. Specific differences in amino acid homeostasis and key genes associated with the cyanogenic pathway were observed in these species, as well as the upregulation of the mandelonitrile lyase gene (PlMNL1) following T. urticae feeding. Concomitantly, the PIMNL1 activity increased. Lima bean plants also displayed an induction of β-cyanoalanine synthase (PlCYSC1), a key enzyme for cyanide detoxification, suggesting an internal regulatory mechanism to manage the toxicity of their defence responses. These findings contribute to our understanding of the legume-herbivore interactions and underscore the potential role of cyanogenesis in the elaboration of specific defensive responses, even within the same genus, which may reflect distinctive evolutionary adaptations or varying metabolic capabilities between species. • Cyanogenesis is a plant defense strategy involving the emission of poisonous hydrogen cyanide when plant tissues are disrupted by an herbivore. • The goal of this study was to compare the differential defense mechanisms triggered by Tetranychus urticae in two legume species, the cyanogenic Phaseolus lunatus (lima bean) and the non-cyanogenic Phaseolus vulgaris (common bean), by identifying which genes and metabolites are similar and different in these species. • Our findings demonstrate: i) leaf damage mediated by mites in P. lunatus was smaller than in P. vulgaris ; ii) both species exhibited substantial metabolic and transcriptional changes upon infestation, although alterations in P. lunatus were significantly more pronounced; iii) specific induction of genes linked to terpenoid and thiamine metabolism, changes in amino acid content and the induction of key genes linked to cyanogenesis were differentially produced in infested P. lunatus , suggesting the participation of these processes in the differential defense response; iv) a previously unannotated gene, PlMNL1 , encoding for mandelonitrile lyase in P. lunatus , was identified. PlMNL1 was mite-upregulated and the corresponding protein had mandelonitrile lyase activity; and v) A P. lunatus β-cyanoalanine synthase (PlCYSC1) is induced upon T. urticae infestation, suggesting a fine tuning mechanism between Cyanogenesis and HCN detoxification. [ABSTRACT FROM AUTHOR]