Revealing the role of autotoxicity protection for defense metabolism innovations in Solanaceae using a multiomics approach

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Many plant specialized metabolites (PSMs) function as defenses and abrogating particular pathway steps can lead to the accumulation of toxic intermediates, indicating that in addition to defense-based functional selection, autotoxicity avoidance plays a key role in the evolution of the PSM biochemistry. However, we currently do not know to which extent and how autotoxicity protection mechanisms evolve in concert with defensive functions. These challenging questions require a multi-species and -organ approach integrating gene -and PSM-level information (multiomics atlases) to test, using both functional and evolutionary studies, three key predictions of autotoxicity avoidance-driven evolution: that 1) strong signatures of positive selection for a PSM pathway should be detected for genes participating in autotoxicity prevention; 2) expression of those genes should likely be enriched in specific cell types associated with cell growth and/or differentiation; and that 3) similar organ-level signatures of selection should be detected among closely-related species harboring a given PSM innovation, since the selection imposed by intrinsic cellular functions is likely to be less dynamic than ecological selections. Here, by building on our recent breakthrough on the biosynthesis and (auto)toxicity mechanisms of diterpene glycosides (DTG) in tobacco as well as on other groups’ work on the biosynthesis of steroidal glycoalkaloids (SGA), two prominent Solaneaceae PSM defenses, we will implement a state-of-the-art integration of computational metabolomics, transcriptomics, single-cell genomics and genetic manipulation tools to address this challenge. We aim to (i) establish integrated metabolomics-transcriptomics atlases for eight solanaceous species to pinpoint on biochemical innovations in the DTG and SGA pathways; (ii) retrace the molecular evolution of these pathways and characterize genes with signatures of strong positive selection; and (iii), as a case-study, functionally decipher the contribution of autotoxicity avoidance for SGAs’ evolution using a combination of single-cell genomics and genetic manipulations. The outcomes of this work will allow us to evaluate whether autotoxicity prevention is a key selection pressure driving the chemodiversification in Solanaceae. More broadly, EVOMET will address a paradigm shift in our understanding of plant defense evolution, provide key insights for the design of next-generation crop protection strategies, and implement new comparative single-cell sequencing tools in plant evolutionary biology.