Genomic evidence for convergent evolution of gene clusters for momilactone biosynthesis in land plants

Abstract

Momilactones are bioactive diterpenoids that contribute to plant defense against pathogens and allelopathic interactions between plants. Both cultivated and wild grass species ofOryzaandEchinochloa crus-galli(barnyard grass) produce momilactones using a biosynthetic gene cluster (BGC) in their genomes. The bryophyteCalohypnum plumiforme(formerlyHypnum plumaeforme) also produces momilactones, and the bifunctional diterpene cyclase geneCpDTC1/HpDTC1,which is responsible for the production of the diterpene framework, has been characterized. To understand the molecular architecture of the momilactone biosynthetic genes in the moss genome and their evolutionary relationships with other momilactone-producing plants, we sequenced and annotated theC. plumiformegenome. The data revealed a 150-kb genomic region that contains two cytochrome P450 genes, theCpDTC1/HpDTC1gene and the “dehydrogenase momilactone A synthase” gene tandemly arranged and inductively transcribed following stress exposure. The predicted enzymatic functions in yeast and recombinant assay and the successful pathway reconstitution inNicotiana benthamianasuggest that it is a functional BGC responsible for momilactone production. Furthermore, in a survey of genomic sequences of a broad range of plant species, we found that momilactone BGC is limited to the two grasses (OryzaandEchinochloa) andC. plumiforme, with no synteny among these genomes. These results indicate that while the gene cluster inC. plumiformeis functionally similar to that in rice and barnyard grass, it is likely a product of convergent evolution. To the best of our knowledge, this report of a BGC for a specialized plant defense metabolite in bryophytes is unique.

Cytochrome P450 CYP81A10v7 in Lolium rigidum confers metabolic resistance to herbicides across at least five modes of action

“…As P450s normally cluster together on the same chromosome in plants (Nelson and Werck‐Reichhart, 2011; Liu et al , 2016), the existence of co‐regulated gene clusters involving different types of genes (such as P450s, GSTs and UGTs) in a metabolic pathway might occur, so that CYP72A71v1 could be potentially linked to these genes conferring herbicide resistance. Co‐ordinately regulated genes clusters have been reported for biosynthesis of allelochemicals such as DIMBOA and momilactone (see a recent paper by Batada et al ., 2007; Giacomini et al ., 2020; Mao et al ., 2020).…”

Polyploidy underlies co-option and diversification of biosynthetic triterpene pathways in the apple tribe

“…The genomic basis of this astounding metabolic complexity has been long proposed to arise via gene duplication, followed by subfunctionalization and neofunctionalization (39)(40)(41). Recently, genomic reorganizations, such as formation of diterpene and triterpene gene clusters, are also found as new genomic features associated with metabolic diversification in plants (42)(43)(44)(45). There are a wealth of cases tracing single gene duplication events to address the contribution of these local variants on diversification of metabolites (41,46,47).…”

Plant Metabolic Network: A multi-species resource of plant metabolic information

“…We therefore evaluated the performance of PMN’s metabolic reconstruction pipeline both in its entirety and using only computational prediction. The manual pathway validation revealed a number of pathways predicted to be present outside of their known taxonomic range, such as momilactone’s predicted presence across Poaceae despite being known to exist only in rice and a few other species, some outside of Poaceae (in which they appear to have evolved convergently) (Mao et al 2020). While some of these results may reflect compounds that are, in fact, more widely distributed than currently thought, many such cases likely result from inaccurate prediction of enzymatic function by E2P2.…”