Drivers of metabolic diversification: how dynamic genomic neighbourhoods generate new biosynthetic pathways in the Brassicaceae

Liu, Zhenhua, Suarez Duran, Hernando G., Harnvanichvech, Yosapol, Stephenson, Michael J. ORCID: https://orcid.org/0000-0002-2594-1806, Schranz, M. Eric, Nelson, David, Medema, Marnix H. and Osbourn, Anne (2020) Drivers of metabolic diversification: how dynamic genomic neighbourhoods generate new biosynthetic pathways in the Brassicaceae. New Phytologist, 227 (4). pp. 1109-1123. ISSN 0028-646X

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Abstract

Plants produce an array of specialized metabolites with important ecological functions. The mechanisms underpinning the evolution of new biosynthetic pathways are not well-understood. Here, we exploit available genome sequence resources to investigate triterpene biosynthesis across the Brassicaceae. Oxidosqualene cyclases (OSCs) catalyze the first committed step in triterpene biosynthesis. Systematic analysis of 13 sequenced Brassicaceae genomes was performed to identify all OSC genes. The genome neighbourhoods (GNs) around a total of 163 OSC genes were investigated to identify Pfam domains significantly enriched in these regions. All-vs-all comparisons of OSC neighbourhoods and phylogenomic analysis were used to investigate the sequence similarity and evolutionary relationships of the numerous candidate triterpene biosynthetic gene clusters (BGCs) observed. Functional analysis of three representative BGCs was carried out and their triterpene pathway products were elucidated. Our results indicate that plant genomes are remarkably plastic, and that dynamic GNs generate new biosynthetic pathways in different Brassicaceae lineages by shuffling the genes encoding a core palette of triterpene-diversifying enzymes, presumably in response to strong environmental selection pressure. These results illuminate a genomic basis for diversification of plant-specialized metabolism through natural combinatorics of enzyme families, which can be mimicked using synthetic biology to engineer diverse bioactive molecules.

Item Type: Article
Additional Information: Research Funding: Biological Sciences Research Council (BBSRC). Grant Numbers: BB/L014130/1, BB/P012523/1; John Innes Foundation; National Institutes of Health. Grant Number: U101GM110699; The Netherlands Organization for Scientific Research. Grant Number: 863.15.002
Uncontrolled Keywords: brassicaceae,biosynthetic gene clusters,metabolic pathway evolution,plant interactions,specialized metabolism,terpenes,physiology,plant science ,/dk/atira/pure/subjectarea/asjc/1300/1314
Faculty \ School: Faculty of Science > School of Chemistry
Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 26 Sep 2022 12:32
Last Modified: 24 Oct 2022 06:53
URI: https://ueaeprints.uea.ac.uk/id/eprint/88648
DOI: 10.1111/nph.16338

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