Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants

© 2019 Levsh et al. As a means to maintain their sessile lifestyle amid challenging environments, plants produce an enormous diversity of compounds as chemical defenses against biotic and abiotic insults. The underpinning metabolic pathways that support the biosynthesis of these specialized chemical...

Full description

Bibliographic Details
Main Authors: Levsh, Olesya, Pluskal, Tomáš, Carballo, Valentina, Mitchell, Andrew J, Weng, Jing-Ke
Other Authors: Massachusetts Institute of Technology. Department of Biology
Format: Article
Language:English
Published: Elsevier BV 2021
Online Access:https://hdl.handle.net/1721.1/133380
_version_ 1811079861494611968
author Levsh, Olesya
Pluskal, Tomáš
Carballo, Valentina
Mitchell, Andrew J
Weng, Jing-Ke
author2 Massachusetts Institute of Technology. Department of Biology
author_facet Massachusetts Institute of Technology. Department of Biology
Levsh, Olesya
Pluskal, Tomáš
Carballo, Valentina
Mitchell, Andrew J
Weng, Jing-Ke
author_sort Levsh, Olesya
collection MIT
description © 2019 Levsh et al. As a means to maintain their sessile lifestyle amid challenging environments, plants produce an enormous diversity of compounds as chemical defenses against biotic and abiotic insults. The underpinning metabolic pathways that support the biosynthesis of these specialized chemicals in divergent plant species provide a rich arena for understanding the molecular evolution of complex metabolic traits. Rosmarinic acid (RA) is a phenolic natural product first discovered in plants of the mint family (Lamiaceae) and is recognized for its wide range of medicinal properties and potential applications in human dietary and medical interventions. Interestingly, the RA chemotype is present sporadically in multiple taxa of flowering plants as well as some hornworts and ferns, prompting the question whether its biosynthesis arose independently across different lineages. Here we report the elucidation of the RA biosynthetic pathway in Phacelia campanularia (desert bells). This species represents the borage family (Boraginaceae), an RA-producing family closely related to the Lamiaceae within the Lamiids clade. Using a multi-omics approach in combination with functional characterization of candidate genes both in vitro and in vivo, we found that RA biosynthesis in P. campanularia involves specific activities of a BAHD acyltransferase and two cytochrome P450 hydroxylases. Further phylogenetic and comparative structure–function analyses of the P. campanularia RA biosynthetic enzymes clearly indicate that RA biosynthesis has evolved independently at least twice in the Lamiids, an exemplary case of chemotypic convergence through disparate evolutionary trajectories.
first_indexed 2024-09-23T11:21:45Z
format Article
id mit-1721.1/133380
institution Massachusetts Institute of Technology
language English
last_indexed 2024-09-23T11:21:45Z
publishDate 2021
publisher Elsevier BV
record_format dspace
spelling mit-1721.1/1333802023-09-27T20:11:37Z Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants Levsh, Olesya Pluskal, Tomáš Carballo, Valentina Mitchell, Andrew J Weng, Jing-Ke Massachusetts Institute of Technology. Department of Biology Whitehead Institute for Biomedical Research © 2019 Levsh et al. As a means to maintain their sessile lifestyle amid challenging environments, plants produce an enormous diversity of compounds as chemical defenses against biotic and abiotic insults. The underpinning metabolic pathways that support the biosynthesis of these specialized chemicals in divergent plant species provide a rich arena for understanding the molecular evolution of complex metabolic traits. Rosmarinic acid (RA) is a phenolic natural product first discovered in plants of the mint family (Lamiaceae) and is recognized for its wide range of medicinal properties and potential applications in human dietary and medical interventions. Interestingly, the RA chemotype is present sporadically in multiple taxa of flowering plants as well as some hornworts and ferns, prompting the question whether its biosynthesis arose independently across different lineages. Here we report the elucidation of the RA biosynthetic pathway in Phacelia campanularia (desert bells). This species represents the borage family (Boraginaceae), an RA-producing family closely related to the Lamiaceae within the Lamiids clade. Using a multi-omics approach in combination with functional characterization of candidate genes both in vitro and in vivo, we found that RA biosynthesis in P. campanularia involves specific activities of a BAHD acyltransferase and two cytochrome P450 hydroxylases. Further phylogenetic and comparative structure–function analyses of the P. campanularia RA biosynthetic enzymes clearly indicate that RA biosynthesis has evolved independently at least twice in the Lamiids, an exemplary case of chemotypic convergence through disparate evolutionary trajectories. 2021-10-27T19:52:26Z 2021-10-27T19:52:26Z 2019 2021-08-04T12:12:08Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/133380 en 10.1074/JBC.RA119.010454 Journal of Biological Chemistry Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Elsevier BV American Society for Biochemistry & Molecular Biology (ASBMB)
spellingShingle Levsh, Olesya
Pluskal, Tomáš
Carballo, Valentina
Mitchell, Andrew J
Weng, Jing-Ke
Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants
title Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants
title_full Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants
title_fullStr Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants
title_full_unstemmed Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants
title_short Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants
title_sort independent evolution of rosmarinic acid biosynthesis in two sister families under the lamiids clade of flowering plants
url https://hdl.handle.net/1721.1/133380
work_keys_str_mv AT levsholesya independentevolutionofrosmarinicacidbiosynthesisintwosisterfamiliesunderthelamiidscladeoffloweringplants
AT pluskaltomas independentevolutionofrosmarinicacidbiosynthesisintwosisterfamiliesunderthelamiidscladeoffloweringplants
AT carballovalentina independentevolutionofrosmarinicacidbiosynthesisintwosisterfamiliesunderthelamiidscladeoffloweringplants
AT mitchellandrewj independentevolutionofrosmarinicacidbiosynthesisintwosisterfamiliesunderthelamiidscladeoffloweringplants
AT wengjingke independentevolutionofrosmarinicacidbiosynthesisintwosisterfamiliesunderthelamiidscladeoffloweringplants