Lateral transfers lead to the birth of momilactone biosynthetic gene clusters in grass

SUMMARY

Momilactone A, an important plant labdane‐related diterpenoid, functions as a phytoalexin against pathogens and an allelochemical against neighboring plants. The genes involved in the biosynthesis of momilactone A are found in clusters, i.e., momilactone A biosynthetic gene clusters (MABGCs), in the rice and barnyardgrass genomes. In addition, we know little about the origin and evolution of MABGCs. Here, we integrated results from comprehensive phylogeny and comparative genomic analyses of the core genes of MABGC‐like clusters and MABGCs in 40 monocot plant genomes, providing convincing evidence for the birth and evolution of MABGCs in grass species. The MABGCs found in the PACMAD clade of the core grass lineage (including Panicoideae and Chloridoideae) originated from a MABGC‐like cluster in Triticeae (BOP clade) via lateral gene transfer (LGT) and followed by recruitment of MAS1/2 and CYP76L1 genes. The MABGCs in Oryzoideae originated from PACMAD through another LGT event and lost CYP76L1 afterwards. The Oryza MABGC and another Oryza diterpenoid cluster c2BGC are two distinct clusters, with the latter originating from gene duplication and relocation within Oryzoideae. Further comparison of the expression patterns of the MABGC genes between rice and barnyardgrass in response to pathogen infection and allelopathy provides novel insights into the functional innovation of MABGCs in plants. Our results demonstrate LGT‐mediated origination of MABGCs in grass and shed lights into the evolutionary innovation and optimization of plant biosynthetic pathways.

Significance Statement

How biosynthetic gene clusters (BGCs) originate and evolve is less known in eukaryotes. Momilactone A, an important defensive and allelopathic secondary chemical in plants, is synthesized by momilactone A BGCs (MABGCs). By exploiting the phylogeny and comparative genomics of the core genes of MABGC‐like clusters and MABGCs across 40 plant species, we reconstruct the evolutionary trajectory of MABGCs in grass, i.e., the PACMAD clade (including Panicoideae and Chloridoideae) acquired MABGCs from Triticeae via lateral gene transfer (LGT) of a MABGC‐like cluster and another LGT event passed the PACMAD MABGC on to Oryza. The composition of MABGCs is dynamic with gain and/or loss of genes in the recipient species after LGT. The study demonstrates that, like prokaryotes, plants are capable of moving a cluster of genes involved in the same biosynthesis pathway by LGT. The results shed light into the evolutionary innovation of BGCs and optimization of a biosynthetic pathway via synthetic biology.