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

Lingfeng Mao, Hiroshi Kawaide, Toshiya Higuchi, Meihong Chen, Koji Miyamoto, Yoshiki Hirata, Honoka Kimura, Sho Miyazaki, Miyu Teruya, Kaoru Fujiwara, Keisuke Tomita, Hisakazu Yamane, Ken Ichiro Hayashi, Hideaki Nojiri, Lei Jia, Jie Qiu, Chuyu Ye, Michael P. Timko, Longjiang Fan, Kazunori Okada

Research output: Contribution to journalArticle

2 Citations (Scopus)

Abstract

Momilactones are bioactive diterpenoids that contribute to plant defense against pathogens and allelopathic interactions between plants. Both cultivated and wild grass species of Oryza and Echinochloa crus-galli (barnyard grass) produce momilactones using a biosynthetic gene cluster (BGC) in their genomes. The bryophyte Calohypnum plumiforme (formerly Hypnum plumaeforme) also produces momilactones, and the bifunctional diterpene cyclase gene CpDTC1/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 the C. plumiforme genome. The data revealed a 150-kb genomic region that contains two cytochrome P450 genes, the CpDTC1/HpDTC1 gene 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 in Nicotiana benthamiana suggest 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 (Oryza and Echinochloa) and C. plumiforme, with no synteny among these genomes. These results indicate that while the gene cluster in C. plumiforme is 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.

Original languageEnglish
Pages (from-to)12472-12480
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number22
DOIs
Publication statusPublished - 2020 Jun 2

Keywords

  • Bryophytes
  • Convergent evolution
  • Diterpene momilactones
  • Gene cluster
  • Specialized metabolites

ASJC Scopus subject areas

  • General

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  • Cite this

    Mao, L., Kawaide, H., Higuchi, T., Chen, M., Miyamoto, K., Hirata, Y., Kimura, H., Miyazaki, S., Teruya, M., Fujiwara, K., Tomita, K., Yamane, H., Hayashi, K. I., Nojiri, H., Jia, L., Qiu, J., Ye, C., Timko, M. P., Fan, L., & Okada, K. (2020). Genomic evidence for convergent evolution of gene clusters for momilactone biosynthesis in land plants. Proceedings of the National Academy of Sciences of the United States of America, 117(22), 12472-12480. https://doi.org/10.1073/pnas.1914373117