A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’

Lily is a popular flower worldwide due to its elegant appearance and pleasant fragrance. Floral volatiles of lily are predominated by monoterpenes and benzenoids. While a number of genes for monoterpene biosynthesis have been characterized, the molecular mechanism underlying floral benzenoid formati...

Full description

Bibliographic Details
Main Authors: Yuechong Yue, Lan Wang, Manyi Li, Fang Liu, Junle Yin, Lijun Huang, Bin Zhou, Xinyue Li, Yunyi Yu, Feng Chen, Rangcai Yu, Yanping Fan
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1275960/full
_version_ 1797670014114856960
author Yuechong Yue
Yuechong Yue
Lan Wang
Manyi Li
Fang Liu
Junle Yin
Lijun Huang
Bin Zhou
Xinyue Li
Xinyue Li
Yunyi Yu
Yunyi Yu
Feng Chen
Rangcai Yu
Yanping Fan
Yanping Fan
author_facet Yuechong Yue
Yuechong Yue
Lan Wang
Manyi Li
Fang Liu
Junle Yin
Lijun Huang
Bin Zhou
Xinyue Li
Xinyue Li
Yunyi Yu
Yunyi Yu
Feng Chen
Rangcai Yu
Yanping Fan
Yanping Fan
author_sort Yuechong Yue
collection DOAJ
description Lily is a popular flower worldwide due to its elegant appearance and pleasant fragrance. Floral volatiles of lily are predominated by monoterpenes and benzenoids. While a number of genes for monoterpene biosynthesis have been characterized, the molecular mechanism underlying floral benzenoid formation in lily remains unclear. Here, we report on the identification and characterization of a novel BAHD acyltransferase gene that contributes to the biosynthesis of two related floral scent benzoate esters, ethyl benzoate and methyl benzoate, in the scented Lilium oriental hybrid ‘Siberia’. The emission of both methyl benzoate and ethyl benzoate in L. ‘Siberia’ was found to be tepal-specific, floral development-regulated and rhythmic. Through transcriptome profiling and bioinformatic analysis, a BAHD acyltransferase gene designated LoAAT1 was identified as the top candidate gene for the production of ethyl benzoate. In vitro enzyme assays and substrate feeding assays provide substantial evidence that LoAAT1 is responsible for the biosynthesis of ethyl benzoate. It was interesting to note that in in vitro enzyme assay, LoAAT1 can also catalyze the formation of methyl benzoate, which is typically formed by the action of benzoic acid methyltransferase (BAMT). The lack of an expressed putative BAMT gene in the flower transcriptome of L. ‘Siberia’, together with biochemical and expression evidence, led us to conclude that LoAAT1 is also responsible for, or at least contributes to, the biosynthesis of the floral scent compound methyl benzoate. This is the first report that a member of the plant BAHD acyltransferase family contributes to the production of both ethyl benzoate and methyl benzoate, presenting a new mechanism for the biosynthesis of benzoate esters.
first_indexed 2024-03-11T20:53:22Z
format Article
id doaj.art-1a019193a5014f4bb99b78fc72e0a889
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-03-11T20:53:22Z
publishDate 2023-09-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-1a019193a5014f4bb99b78fc72e0a8892023-09-30T21:26:50ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-09-011410.3389/fpls.2023.12759601275960A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’Yuechong Yue0Yuechong Yue1Lan Wang2Manyi Li3Fang Liu4Junle Yin5Lijun Huang6Bin Zhou7Xinyue Li8Xinyue Li9Yunyi Yu10Yunyi Yu11Feng Chen12Rangcai Yu13Yanping Fan14Yanping Fan15The Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaGuangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaCollege of Life Sciences, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaCollege of Life Sciences, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaGuangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaGuangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural University, Guangzhou, ChinaDepartment of Plant Sciences, University of Tennessee, Knoxville, TN, United StatesCollege of Life Sciences, South China Agricultural University, Guangzhou, ChinaThe Research Center for Ornamental Plants, College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou, ChinaGuangdong Key Laboratory for Innovative Development and Utilization of Forest Plant Germplasm, South China Agricultural University, Guangzhou, ChinaLily is a popular flower worldwide due to its elegant appearance and pleasant fragrance. Floral volatiles of lily are predominated by monoterpenes and benzenoids. While a number of genes for monoterpene biosynthesis have been characterized, the molecular mechanism underlying floral benzenoid formation in lily remains unclear. Here, we report on the identification and characterization of a novel BAHD acyltransferase gene that contributes to the biosynthesis of two related floral scent benzoate esters, ethyl benzoate and methyl benzoate, in the scented Lilium oriental hybrid ‘Siberia’. The emission of both methyl benzoate and ethyl benzoate in L. ‘Siberia’ was found to be tepal-specific, floral development-regulated and rhythmic. Through transcriptome profiling and bioinformatic analysis, a BAHD acyltransferase gene designated LoAAT1 was identified as the top candidate gene for the production of ethyl benzoate. In vitro enzyme assays and substrate feeding assays provide substantial evidence that LoAAT1 is responsible for the biosynthesis of ethyl benzoate. It was interesting to note that in in vitro enzyme assay, LoAAT1 can also catalyze the formation of methyl benzoate, which is typically formed by the action of benzoic acid methyltransferase (BAMT). The lack of an expressed putative BAMT gene in the flower transcriptome of L. ‘Siberia’, together with biochemical and expression evidence, led us to conclude that LoAAT1 is also responsible for, or at least contributes to, the biosynthesis of the floral scent compound methyl benzoate. This is the first report that a member of the plant BAHD acyltransferase family contributes to the production of both ethyl benzoate and methyl benzoate, presenting a new mechanism for the biosynthesis of benzoate esters.https://www.frontiersin.org/articles/10.3389/fpls.2023.1275960/fulllilyfloral scentBAHD acyltransferasemethyl benzoateethyl benzoatebiosynthesis
spellingShingle Yuechong Yue
Yuechong Yue
Lan Wang
Manyi Li
Fang Liu
Junle Yin
Lijun Huang
Bin Zhou
Xinyue Li
Xinyue Li
Yunyi Yu
Yunyi Yu
Feng Chen
Rangcai Yu
Yanping Fan
Yanping Fan
A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’
Frontiers in Plant Science
lily
floral scent
BAHD acyltransferase
methyl benzoate
ethyl benzoate
biosynthesis
title A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’
title_full A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’
title_fullStr A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’
title_full_unstemmed A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’
title_short A BAHD acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of Lilium oriental hybrid ‘Siberia’
title_sort bahd acyltransferase contributes to the biosynthesis of both ethyl benzoate and methyl benzoate in the flowers of lilium oriental hybrid siberia
topic lily
floral scent
BAHD acyltransferase
methyl benzoate
ethyl benzoate
biosynthesis
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1275960/full
work_keys_str_mv AT yuechongyue abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yuechongyue abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT lanwang abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT manyili abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT fangliu abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT junleyin abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT lijunhuang abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT binzhou abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT xinyueli abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT xinyueli abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yunyiyu abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yunyiyu abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT fengchen abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT rangcaiyu abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yanpingfan abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yanpingfan abahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yuechongyue bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yuechongyue bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT lanwang bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT manyili bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT fangliu bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT junleyin bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT lijunhuang bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT binzhou bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT xinyueli bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT xinyueli bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yunyiyu bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yunyiyu bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT fengchen bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT rangcaiyu bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yanpingfan bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia
AT yanpingfan bahdacyltransferasecontributestothebiosynthesisofbothethylbenzoateandmethylbenzoateintheflowersofliliumorientalhybridsiberia