Convergent and divergent evolution of plant chemical defenses

Negin, Boaz; Jander, Georg

doi:10.1016/j.pbi.2023.102368

Cited by 11 publications

(4 citation statements)

References 56 publications

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“…In principle, BXDs could have arisen early in the history of the angiosperms and then been lost in multiple taxa, or alternatively, BXDs could have arisen independently several times during angiosperm evolution. Examples for both evolutionary trajectories have already been reported for specialized metabolites in plants ( 22 – 27 ). Previous studies using radiolabeled BXD precursors have shown that the BXD pathway in dicotyledonous plants most likely starts from indole, as in maize ( 28 ).…”

mentioning

confidence: 79%

Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants

Florean,

Luck,

Hong

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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Benzoxazinoids (BXDs) form a class of indole-derived specialized plant metabolites with broad antimicrobial and antifeedant properties. Unlike most specialized metabolites, which are typically lineage-specific, BXDs occur sporadically in a number of distantly related plant orders. This observation suggests that BXD biosynthesis arose independently numerous times in the plant kingdom. However, although decades of research in the grasses have led to the elucidation of the BXD pathway in the monocots, the biosynthesis of BXDs in eudicots is unknown. Here, we used a metabolomic and transcriptomic-guided approach, in combination with pathway reconstitution in Nicotiana benthamiana, to identify and characterize the BXD biosynthetic pathways from both Aphelandra squarrosa and Lamium galeobdolon , two phylogenetically distant eudicot species. We show that BXD biosynthesis in A. squarrosa and L. galeobdolon utilize a dual-function flavin-containing monooxygenase in place of two distinct cytochrome P450s, as is the case in the grasses. In addition, we identified evolutionarily unrelated cytochrome P450s, a 2-oxoglutarate-dependent dioxygenase, a UDP-glucosyltransferase, and a methyltransferase that were also recruited into these BXD biosynthetic pathways. Our findings constitute the discovery of BXD pathways in eudicots. Moreover, the biosynthetic enzymes of these pathways clearly demonstrate that BXDs independently arose in the plant kingdom at least three times. The heterogeneous pool of identified BXD enzymes represents a remarkable example of metabolic plasticity, in which BXDs are synthesized according to a similar chemical logic, but with an entirely different set of metabolic enzymes.

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confidence: 79%

Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants

Florean,

Luck,

Hong

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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“…They can be classified by the source of their nitrogen and the type of ring it is found in. However, these classes are not necessarily evolutionarily related and have emerged convergently 39 . The LDCs found in piperidine alkaloid biosynthesis are an example of this, with legume LDC and lycopodium LDC emerging from ODCs independently 20 .…”

Section: Discussionmentioning

confidence: 99%

Nonsymmetric formation of Δ¹-piperideine from lysine in plants via a bacterial-like PLP-dependent enzyme

Wood,

Daza,

Newling

et al. 2024

Preprint

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Piperidine alkaloids in plants derive from lysine via Δ1-piperideine. We investigated the alkaloid biosynthesis inFlueggea suffruticosa, a plant that produces diverse piperidine alkaloids, including securinine. Until now, pathways leading to the formation of Δ1-piperideine have involved two enzymatic steps: a decarboxylase and an oxidase, proceeding via free cadaverine. We discovered Δ1-piperideine synthase (PS), a PLP-dependent enzyme that forms Δ1-piperideine directly from lysine via an oxidative deamination. We demonstrate that PS catalyses this transformation in a non-symmetric manner, and show it is positioned within the group III decarboxylase family, which is typically associated with prokaryotes. We also identified a paralog gene exhibiting decarboxylase activity. This work delineates the first enzymatic step in the biosynthesis of securinine as an unprecedented oxidative deamination of lysine. It also marks the identification of the first eukaryotic group III decarboxylase and resolves the longstanding question of non-symmetric nitrogen incorporation in piperidine alkaloids.

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“…Both plants and their herbivore pests have evolved various strategies to avoid each other’s defense systems during the coevolutionary arms race. Plants employ efficient biochemical defensive systems, such as specialized metabolites, that are critical to overcoming intense herbivore attacks (Ehrlich & Raven, 1964; Mithöfer & Boland, 2012; Negin & Jander, 2023; Speed, Fenton, Jones, Ruxton, & Brockhurst, 2015; War et al, 2012). Our results revealed a TIA “timebomb” in C. roseus leaves that effectively influences the survival of a chewing insect, M. sexta, as a resistance-proof and sustainable chemical defensive strategy against herbivory (Figure 1).…”

Section: Discussionmentioning

confidence: 99%

Transcriptional reprogramming deploys a compartmentalized “timebomb” inCatharanthus roseusto fend off chewing herbivores

Liu,

Shi,

Patra

et al. 2024

Preprint

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The evolutionary arms-race between plants and insects has led to key adaptive innovations that drive diversification. Alkaloids are well-documented anti-herbivory compounds in plant chemical defenses, but how these specialized metabolites are allocated to cope with both biotic and abiotic stresses concomitantly is largely unknown. To examine how plants prioritize their metabolic resources responding to herbivory and cold, we integrated dietary toxicity bioassay in insects with co-expression analysis, hierarchical clustering, promoter assay, and protein-protein interaction in plants.Catharanthus roseus,a medicinal plant known for its insecticidal property against chewing herbivores, produces two terpenoid indole alkaloid monomers, vindoline and catharanthine. Individually, they exhibited negligible toxicity againstManduca sexta,a chewing herbivore; their condensed product, anhydrovinblastine, however, was highly toxic. Such unique insecticidal mode of action demonstrates that terpenoid indole alkaloid “timebomb” can only be activated when the two spatially isolated monomeric precursors are dimerized by herbivory. Without initial selection pressure and apparent fitness costs, this adaptive chemical defense against herbivory is innovative and sustainable.The biosynthesis of insecticidal terpenoid indole alkaloids is induced by herbivory but suppressed by cold. Here, we identified a transcription factor,Herbivore InducedVindoline-geneExpression (HIVE), that coordinates the production of terpenoid indole alkaloids in response to herbivory and cold stress. The HIVE-mediated transcriptional reprogramming allows this herbaceous perennial to allocate their metabolic resources for chemical defense at a normal temperature, when herbivory pressure is high, but switches to cold tolerance under a cooler temperature, when insect infestation is secondary.

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Convergent and divergent evolution of plant chemical defenses

Cited by 11 publications

References 56 publications

Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants

Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants

Nonsymmetric formation of Δ¹-piperideine from lysine in plants via a bacterial-like PLP-dependent enzyme

Transcriptional reprogramming deploys a compartmentalized “timebomb” inCatharanthus roseusto fend off chewing herbivores

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Convergent and divergent evolution of plant chemical defenses

Cited by 11 publications

References 56 publications

Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants

Reinventing metabolic pathways: Independent evolution of benzoxazinoids in flowering plants

Nonsymmetric formation of Δ1-piperideine from lysine in plants via a bacterial-like PLP-dependent enzyme

Transcriptional reprogramming deploys a compartmentalized “timebomb” inCatharanthus roseusto fend off chewing herbivores

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Nonsymmetric formation of Δ¹-piperideine from lysine in plants via a bacterial-like PLP-dependent enzyme