Abstract
Plants deploy distinct secondary metabolisms to cope with environment pressure and to face bio-aggressors notably through the production of biologically active alkaloids. This metabolism-type is particularly elaborated in Catharanthus roseus that synthesizes more than a hundred different monoterpene indole alkaloids (MIAs). While the characterization of their biosynthetic pathway now reaches completion, still little is known about the role of MIAs during biotic attacks. As a consequence, we developed a new plant/herbivore interaction system by challenging C. roseus leaves with Manduca sexta larvae. Transcriptomic and metabolic analyses demonstrated that C. roseus respond to folivory by both local and systemic processes relying on the activation of specific gene sets and biosynthesis of distinct MIAs following jasmonate production. While a huge local accumulation of strictosidine was monitored in attacked leaves that could repel caterpillars through its protein reticulation properties, newly developed leaves displayed an increased biosynthesis of the toxic strictosidine-derived MIAs, vindoline and catharanthine, produced by up-regulation of MIA biosynthetic genes. In this context, leaf consumption resulted in a rapid death of caterpillars that could be linked to the MIA dimerization observed in intestinal tracts. Furthermore, this study also highlights the overall transcriptomic control of the plant defense processes occurring during herbivory.
Highlights
For several decades, these cytotoxic monoterpene indole alkaloids (MIAs) have been valorized as pharmaceutical compounds used to treat human diseases such as the antineoplastic vinblastine and vincristine inhibiting tubulin polymerization, or the antihypertensive ajmalicine[7]
By combining targeted metabolic analyses and RNA sequencing, we demonstrated that folivory of C. roseus caused both local and systemic induction of MIA biosynthesis resulting from the induction of specific MIA biosynthetic gene expression
To determine whether an efficient interaction can be established between C. roseus and M. sexta, caterpillars were placed on leaves of C. roseus and its host plant N. tabacum
Summary
These cytotoxic MIAs have been valorized as pharmaceutical compounds used to treat human diseases such as the antineoplastic vinblastine and vincristine inhibiting tubulin polymerization, or the antihypertensive ajmalicine[7]. The complexity in the number of steps is overlaid by the spatial organization of the pathway which is distributed in at least three different cell-types and five distinct subcellular compartments[16] (Fig. 1) This multi-site organization implies potential inter- and intra-cellular transport of metabolites and involves the evolution of distinct enzyme isoforms harboring specific functions in MIAs synthesis, as exemplified with two recently identified secologanin synthase (SLS) isoforms displaying specific and complementary gene expression profiles within plant organs[17]. In the light of those data, the use of biotic agents combining several of these signals could lead to a strong and robust modulation of the MIA pathway, constituting a valuable tool to decipher MIA metabolism[46] This postulate is supported by the prominent results retrieved from the herbivory of the tobacco hornworm Manduca sexta on Nicotiana sp, enabling notably the elucidation of nicotine alkaloid metabolism[47]. By combining targeted metabolic analyses and RNA sequencing, we demonstrated that folivory of C. roseus caused both local and systemic induction of MIA biosynthesis resulting from the induction of specific MIA biosynthetic gene expression
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