<i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters

Cucurbitacins, oxygenated tetracyclic triterpenoids that are found mainly in the Cucurbitaceae family, play essential roles as defensive compounds, serving as allomones against herbivores and pathogens and as signals for insect–parasite recognition. These compounds also exhibit various pharmacologic...

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Main Authors: Xupo Ding, Zhuo Yang, Hao Wang, Jun Zeng, Haofu Dai, Wenli Mei
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/13/2/260
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author Xupo Ding
Zhuo Yang
Hao Wang
Jun Zeng
Haofu Dai
Wenli Mei
author_facet Xupo Ding
Zhuo Yang
Hao Wang
Jun Zeng
Haofu Dai
Wenli Mei
author_sort Xupo Ding
collection DOAJ
description Cucurbitacins, oxygenated tetracyclic triterpenoids that are found mainly in the Cucurbitaceae family, play essential roles as defensive compounds, serving as allomones against herbivores and pathogens and as signals for insect–parasite recognition. These compounds also exhibit various pharmacological effects. The biosynthesis of cucurbitacins is largely regulated by the bitter (<i>Bi</i>) gene, encoding an oxidosqualene cyclase, which catalyzes the conversion of 2,3-oxidosqualene into cucurbitadienol, a common precursor for cucurbitacin synthesis. Previous studies focused on uncovering the <i>Bi</i> gene clusters in Cucurbitaceae, but their presence in other cucurbitacin-producing plants remained unexplored. Here, the evolutionary history of <i>Bi</i> genes and their clusters were investigated in twenty-one plant genomes spanning three families based on chemotaxonomy. Nineteen <i>Bi</i> genes were identified in fourteen Cucurbitaceae, four Begoniaceae, and one <i>Aquilaria</i> species. Phylogenetic analysis suggested that the genome of <i>Aquilaria sinensis</i> contained the earliest <i>Bi</i> gene clusters in this dataset. Moreover, the genomic analysis revealed a conserved microsynteny of pivotal genes for cucurbitacin biosynthesis in Cucurbitaceae, while interspersed <i>Bi</i> gene clusters were observed in Begoniaceae, indicating rearrangements during plant <i>Bi</i> gene cluster formation. The bitter gene in <i>A. sinensis</i> was found to promote cucurbitadienol biosynthesis in the leaves of <i>Nicotiana benthamiana</i>. This comprehensive exploration of plant <i>Bi</i> genes and their clusters provides valuable insights into the genetic and evolutionary underpinnings of cucurbitacin biosynthesis. These findings offer prospects for a deeper understanding of cucurbitacin production and potential genetic resources for their enhancement in various plants.
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spelling doaj.art-22d38f2bf0d54fb3961a46c56e7e09062024-01-29T14:11:33ZengMDPI AGPlants2223-77472024-01-0113226010.3390/plants13020260<i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene ClustersXupo Ding0Zhuo Yang1Hao Wang2Jun Zeng3Haofu Dai4Wenli Mei5Key Laboratory of Research and Development of Natural Product from <i>Li Folk</i> Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Research and Development of Natural Product from <i>Li Folk</i> Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Research and Development of Natural Product from <i>Li Folk</i> Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Research and Development of Natural Product from <i>Li Folk</i> Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Research and Development of Natural Product from <i>Li Folk</i> Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaKey Laboratory of Research and Development of Natural Product from <i>Li Folk</i> Medicine of Hainan Province, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou 571101, ChinaCucurbitacins, oxygenated tetracyclic triterpenoids that are found mainly in the Cucurbitaceae family, play essential roles as defensive compounds, serving as allomones against herbivores and pathogens and as signals for insect–parasite recognition. These compounds also exhibit various pharmacological effects. The biosynthesis of cucurbitacins is largely regulated by the bitter (<i>Bi</i>) gene, encoding an oxidosqualene cyclase, which catalyzes the conversion of 2,3-oxidosqualene into cucurbitadienol, a common precursor for cucurbitacin synthesis. Previous studies focused on uncovering the <i>Bi</i> gene clusters in Cucurbitaceae, but their presence in other cucurbitacin-producing plants remained unexplored. Here, the evolutionary history of <i>Bi</i> genes and their clusters were investigated in twenty-one plant genomes spanning three families based on chemotaxonomy. Nineteen <i>Bi</i> genes were identified in fourteen Cucurbitaceae, four Begoniaceae, and one <i>Aquilaria</i> species. Phylogenetic analysis suggested that the genome of <i>Aquilaria sinensis</i> contained the earliest <i>Bi</i> gene clusters in this dataset. Moreover, the genomic analysis revealed a conserved microsynteny of pivotal genes for cucurbitacin biosynthesis in Cucurbitaceae, while interspersed <i>Bi</i> gene clusters were observed in Begoniaceae, indicating rearrangements during plant <i>Bi</i> gene cluster formation. The bitter gene in <i>A. sinensis</i> was found to promote cucurbitadienol biosynthesis in the leaves of <i>Nicotiana benthamiana</i>. This comprehensive exploration of plant <i>Bi</i> genes and their clusters provides valuable insights into the genetic and evolutionary underpinnings of cucurbitacin biosynthesis. These findings offer prospects for a deeper understanding of cucurbitacin production and potential genetic resources for their enhancement in various plants.https://www.mdpi.com/2223-7747/13/2/260cucurbitacin<i>Aquilaria sinensis</i><i>Begonia</i><i>Bi</i> genebitter gene clusterorigin
spellingShingle Xupo Ding
Zhuo Yang
Hao Wang
Jun Zeng
Haofu Dai
Wenli Mei
<i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters
Plants
cucurbitacin
<i>Aquilaria sinensis</i>
<i>Begonia</i>
<i>Bi</i> gene
bitter gene cluster
origin
title <i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters
title_full <i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters
title_fullStr <i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters
title_full_unstemmed <i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters
title_short <i>Aquilaria sinensis</i>: An Upstart Resource for Cucurbitacin Production Offers Insights into the Origin of Plant Bitter (<i>Bi</i>) Gene Clusters
title_sort i aquilaria sinensis i an upstart resource for cucurbitacin production offers insights into the origin of plant bitter i bi i gene clusters
topic cucurbitacin
<i>Aquilaria sinensis</i>
<i>Begonia</i>
<i>Bi</i> gene
bitter gene cluster
origin
url https://www.mdpi.com/2223-7747/13/2/260
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