2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants
Strigolactones (SLs), a class of plant apocarotenoids, serve dual roles as rhizosphere-signaling molecules and plant hormones. Orobanchol, a major naturally occurring SL, along with its various derivatives, has been detected in the root exudates of plants of the Fabaceae family. Medicaol, fabacyl ac...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-04-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2024.1392212/full |
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| author | Masato Homma Kiyono Uchida Takatoshi Wakabayashi Takatoshi Wakabayashi Masaharu Mizutani Hirosato Takikawa Yukihiro Sugimoto |
| author_facet | Masato Homma Kiyono Uchida Takatoshi Wakabayashi Takatoshi Wakabayashi Masaharu Mizutani Hirosato Takikawa Yukihiro Sugimoto |
| author_sort | Masato Homma |
| collection | DOAJ |
| description | Strigolactones (SLs), a class of plant apocarotenoids, serve dual roles as rhizosphere-signaling molecules and plant hormones. Orobanchol, a major naturally occurring SL, along with its various derivatives, has been detected in the root exudates of plants of the Fabaceae family. Medicaol, fabacyl acetate, and orobanchyl acetate were identified in the root exudates of barrel medic (Medicago truncatula), pea (Pisum sativum), and cowpea (Vigna unguiculata), respectively. Although the biosynthetic pathway leading to orobanchol production has been elucidated, the biosynthetic pathways of the orobanchol derivatives have not yet been fully elucidated. Here, we report the identification of 2-oxoglutarate-dependent dioxygenases (DOXs) and BAHD acyltransferases responsible for converting orobanchol to these derivatives in Fabaceae plants. First, the metabolic pathways downstream of orobanchol were analyzed using substrate feeding experiments. Prohexadione, an inhibitor of DOX inhibits the conversion of orobanchol to medicaol in barrel medic. The DOX inhibitor also reduced the formation of fabacyl acetate and fabacol, a precursor of fabacyl acetate, in pea. Subsequently, we utilized a dataset based on comparative transcriptome analysis to select a candidate gene encoding DOX for medicaol synthase in barrel medic. Recombinant proteins of the gene converted orobanchol to medicaol. The candidate genes encoding DOX and BAHD acyltransferase for fabacol synthase and fabacol acetyltransferase, respectively, were selected by co-expression analysis in pea. The recombinant proteins of the candidate genes converted orobanchol to fabacol and acetylated fabacol. Furthermore, fabacol acetyltransferase and its homolog in cowpea acetylated orobanchol. The kinetics and substrate specificity analyses revealed high affinity and strict recognition of the substrates of the identified enzymes. These findings shed light on the molecular mechanisms underlying the structural diversity of SLs. |
| first_indexed | 2024-04-24T07:58:12Z |
| format | Article |
| id | doaj.art-65e3a16eedcc4174a013728e9ff7e72e |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-04-24T07:58:12Z |
| publishDate | 2024-04-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Plant Science |
| spelling | doaj.art-65e3a16eedcc4174a013728e9ff7e72e2024-04-18T04:40:02ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-04-011510.3389/fpls.2024.139221213922122-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plantsMasato Homma0Kiyono Uchida1Takatoshi Wakabayashi2Takatoshi Wakabayashi3Masaharu Mizutani4Hirosato Takikawa5Yukihiro Sugimoto6Department of Agrobioscience, Graduate School of Agricultural Science, Kobe University, Kobe, JapanDepartment of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanDepartment of Agrobioscience, Graduate School of Agricultural Science, Kobe University, Kobe, JapanDepartment of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanDepartment of Agrobioscience, Graduate School of Agricultural Science, Kobe University, Kobe, JapanDepartment of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, JapanDepartment of Agrobioscience, Graduate School of Agricultural Science, Kobe University, Kobe, JapanStrigolactones (SLs), a class of plant apocarotenoids, serve dual roles as rhizosphere-signaling molecules and plant hormones. Orobanchol, a major naturally occurring SL, along with its various derivatives, has been detected in the root exudates of plants of the Fabaceae family. Medicaol, fabacyl acetate, and orobanchyl acetate were identified in the root exudates of barrel medic (Medicago truncatula), pea (Pisum sativum), and cowpea (Vigna unguiculata), respectively. Although the biosynthetic pathway leading to orobanchol production has been elucidated, the biosynthetic pathways of the orobanchol derivatives have not yet been fully elucidated. Here, we report the identification of 2-oxoglutarate-dependent dioxygenases (DOXs) and BAHD acyltransferases responsible for converting orobanchol to these derivatives in Fabaceae plants. First, the metabolic pathways downstream of orobanchol were analyzed using substrate feeding experiments. Prohexadione, an inhibitor of DOX inhibits the conversion of orobanchol to medicaol in barrel medic. The DOX inhibitor also reduced the formation of fabacyl acetate and fabacol, a precursor of fabacyl acetate, in pea. Subsequently, we utilized a dataset based on comparative transcriptome analysis to select a candidate gene encoding DOX for medicaol synthase in barrel medic. Recombinant proteins of the gene converted orobanchol to medicaol. The candidate genes encoding DOX and BAHD acyltransferase for fabacol synthase and fabacol acetyltransferase, respectively, were selected by co-expression analysis in pea. The recombinant proteins of the candidate genes converted orobanchol to fabacol and acetylated fabacol. Furthermore, fabacol acetyltransferase and its homolog in cowpea acetylated orobanchol. The kinetics and substrate specificity analyses revealed high affinity and strict recognition of the substrates of the identified enzymes. These findings shed light on the molecular mechanisms underlying the structural diversity of SLs.https://www.frontiersin.org/articles/10.3389/fpls.2024.1392212/fullstrigolactonebiosynthesisorobanchol diversification2-oxoglutarate-dependent dioxygenaseBAHD acyltransferase |
| spellingShingle | Masato Homma Kiyono Uchida Takatoshi Wakabayashi Takatoshi Wakabayashi Masaharu Mizutani Hirosato Takikawa Yukihiro Sugimoto 2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants Frontiers in Plant Science strigolactone biosynthesis orobanchol diversification 2-oxoglutarate-dependent dioxygenase BAHD acyltransferase |
| title | 2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants |
| title_full | 2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants |
| title_fullStr | 2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants |
| title_full_unstemmed | 2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants |
| title_short | 2-oxoglutarate-dependent dioxygenases and BAHD acyltransferases drive the structural diversification of orobanchol in Fabaceae plants |
| title_sort | 2 oxoglutarate dependent dioxygenases and bahd acyltransferases drive the structural diversification of orobanchol in fabaceae plants |
| topic | strigolactone biosynthesis orobanchol diversification 2-oxoglutarate-dependent dioxygenase BAHD acyltransferase |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2024.1392212/full |
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