Interdependent evolution of biosynthetic gene clusters for momilactone production in rice

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Date
2021-02-01
Authors
Kitaoka, Naoki
Zhang, Juan
Oyagbenro, Richard
Brown, Benjamin
Wu, Yisheng
Yang, Bing
Li, Zhaohu
Peters, Reuben
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Abstract

Plants can contain biosynthetic gene clusters (BGCs) that nominally resemble those found in microbes. However, while horizontal gene transmission is often observed in microbes, plants are limited to vertical gene transmission, implying that their BGCs may exhibit distinct inheritance patterns. Rice (Oryza sativa) contains two unlinked BGCs involved in diterpenoid phytoalexin metabolism, with one clearly required for momilactone biosynthesis, while the other is associated with production of phytocassanes. Here, in the process of elucidating momilactone biosynthesis, genetic evidence was found demonstrating a role for a cytochrome P450 (CYP) from the other ‘phytocassane’ BGC. This CYP76M8 acts after the CYP99A2/3 from the ‘momilactone’ BGC, producing a hemiacetal intermediate that is oxidized to the eponymous lactone by a short-chain alcohol dehydrogenase also from this BGC. Thus, the ‘momilactone’ BGC is not only incomplete, but also fractured by the need for CYP76M8 to act in between steps catalyzed by enzymes from this BGC. Moreover, as supported by similar activity observed with orthologs from the momilactone-producing wild-rice species Oryza punctata, the presence of CYP76M8 in the other ‘phytocassane’ BGC indicates interdependent evolution of these two BGCs, highlighting the distinct nature of BGC assembly in plants.

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This is a manuscript of an article published as Kitaoka, Naoki, Juan Zhang, Richard K. Oyagbenro, Benjamin Brown, Yisheng Wu, Bing Yang, Zhaohu Li, and Reuben J. Peters. "Interdependent evolution of biosynthetic gene clusters for momilactone production in rice." The Plant Cell 33 (2020): 290-305. doi:10.1093/plcell/koaa023. Posted with permission.

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