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Implementation of CsLIS/NES in linalool biosynthesis involves transcript splicing regulation in Camellia sinensis

Volatile terpenoids produced in tea plants (Camellia sinensis) are airborne signals interacting against other ecosystem members, but also pleasant odorants of tea products. Transcription regulation (including transcript processing) is pivotal for plant volatile terpenoid production. In this study, a...

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Published in:Plant, cell and environment cell and environment, 2018-01, Vol.41 (1), p.176-186
Main Authors: Liu, Guo‐Feng, Liu, Jing‐Jing, He, Zhi‐Rong, Wang, Fu‐Min, Yang, Hua, Yan, Yi‐Feng, Gao, Ming‐Jun, Gruber, Margaret Y., Wan, Xiao‐Chun, Wei, Shu
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creator Liu, Guo‐Feng
Liu, Jing‐Jing
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Gruber, Margaret Y.
Wan, Xiao‐Chun
Wei, Shu
description Volatile terpenoids produced in tea plants (Camellia sinensis) are airborne signals interacting against other ecosystem members, but also pleasant odorants of tea products. Transcription regulation (including transcript processing) is pivotal for plant volatile terpenoid production. In this study, a terpene synthase gene CsLIS/NES was recovered from tea plants (C. sinensis cv. “Long‐Men Xiang”). CsLIS/NES transcription regulation resulted in 2 splicing forms: CsLIS/NES‐1 and CsLIS/NES‐2 lacking a 305 bp‐fragment at N‐terminus, both producing (E)‐nerolidol and linalool in vitro. Transgenic tobacco studies and a gene‐specific antisense oligo‐deoxynucleotide suppression applied in tea leaves indicated that CsLIS/NES‐1, localized in chloroplasts, acted as linalool synthase, whereas CsLIS/NES‐2 localized in cytosol, functioned as a potential nerolidol synthase, but not linalool synthase. Expression patterns of the 2 transcript isoforms in tea were distinctly different and responded differentially to the application of stress signal molecule methyl jasmonate. Leaf expression of CsLIS/NES‐1, but not CsLIS/NES‐2, was significantly induced by methyl jasmonate. Our data indicated that distinct transcript splicing regulation patterns, together with subcellular compartmentation of CsLIS/NE‐1 and CsLIS/NE‐2 implemented the linalool biosynthesis regulation in tea plants in responding to endogenous and exogenous regulatory factors. Linalool and nerolidol produced in tea plants are not only airborne signals interacting against other ecosystem members for better plant fitness but also floral scent determinants of tea products. A better understanding of the mechanisms underlying their biosynthesis in tea plants may provide effective approaches for tea aroma quality and tea productivity improvement. In this study, tea CsLIS/NES gene was found being differentially involved in linalool and nerolidol biosynthesis due to its 2 splicing transcripts with distinct expression patterns. Regulation at transcription (including transcript processing) and subcellular compartmentation of the 2 CsLIS/NES transcripts implement the biosynthesis regulation of linalool and nerolidol in tea plants in responding to endogenous and exogenous regulatory factors.
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Transcription regulation (including transcript processing) is pivotal for plant volatile terpenoid production. In this study, a terpene synthase gene CsLIS/NES was recovered from tea plants (C. sinensis cv. “Long‐Men Xiang”). CsLIS/NES transcription regulation resulted in 2 splicing forms: CsLIS/NES‐1 and CsLIS/NES‐2 lacking a 305 bp‐fragment at N‐terminus, both producing (E)‐nerolidol and linalool in vitro. Transgenic tobacco studies and a gene‐specific antisense oligo‐deoxynucleotide suppression applied in tea leaves indicated that CsLIS/NES‐1, localized in chloroplasts, acted as linalool synthase, whereas CsLIS/NES‐2 localized in cytosol, functioned as a potential nerolidol synthase, but not linalool synthase. Expression patterns of the 2 transcript isoforms in tea were distinctly different and responded differentially to the application of stress signal molecule methyl jasmonate. Leaf expression of CsLIS/NES‐1, but not CsLIS/NES‐2, was significantly induced by methyl jasmonate. Our data indicated that distinct transcript splicing regulation patterns, together with subcellular compartmentation of CsLIS/NE‐1 and CsLIS/NE‐2 implemented the linalool biosynthesis regulation in tea plants in responding to endogenous and exogenous regulatory factors. Linalool and nerolidol produced in tea plants are not only airborne signals interacting against other ecosystem members for better plant fitness but also floral scent determinants of tea products. A better understanding of the mechanisms underlying their biosynthesis in tea plants may provide effective approaches for tea aroma quality and tea productivity improvement. In this study, tea CsLIS/NES gene was found being differentially involved in linalool and nerolidol biosynthesis due to its 2 splicing transcripts with distinct expression patterns. Regulation at transcription (including transcript processing) and subcellular compartmentation of the 2 CsLIS/NES transcripts implement the biosynthesis regulation of linalool and nerolidol in tea plants in responding to endogenous and exogenous regulatory factors.</description><identifier>ISSN: 0140-7791</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.13080</identifier><identifier>PMID: 28963730</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Acetates - pharmacology ; Acyclic Monoterpenes ; Alkyl and Aryl Transferases - genetics ; Alkyl and Aryl Transferases - metabolism ; alternative splicing ; Antisense RNA ; Aroma ; Base Sequence ; Biosynthesis ; Camellia sinensis ; Camellia sinensis - drug effects ; Camellia sinensis - genetics ; Camellia sinensis - metabolism ; Chloroplasts ; Compartmentation ; CsLIS/NES ; Cyclopentanes - pharmacology ; Cytosol ; Data processing ; Ecosystems ; Fitness ; Flowers - drug effects ; Flowers - metabolism ; Gene Expression Regulation, Plant - drug effects ; Gene regulation ; Isoforms ; Leaves ; Linalool ; Methyl jasmonate ; Monoterpenes - metabolism ; N-Terminus ; Nerolidol ; Nicotiana - genetics ; Odorants ; Oxylipins - pharmacology ; Plant Leaves - drug effects ; Plant Leaves - metabolism ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants (botany) ; Plants, Genetically Modified ; Regulation ; RNA Splicing - drug effects ; RNA Splicing - genetics ; RNA, Messenger - genetics ; RNA, Messenger - metabolism ; Sesquiterpenes - metabolism ; Splicing ; Subcellular Fractions - metabolism ; Tea ; tea aroma ; Terpene synthase ; Terpenes ; Terpenes - metabolism ; Tobacco ; Transcription ; Transgenic plants ; volatile terpenoids</subject><ispartof>Plant, cell and environment, 2018-01, Vol.41 (1), p.176-186</ispartof><rights>2017 John Wiley &amp; Sons Ltd</rights><rights>2017 John Wiley &amp; Sons Ltd.</rights><rights>2018 John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3880-5f13714a56d6213d5e473ad88dd6a89764c512ee160070d0bebfa38872d65c0b3</citedby><cites>FETCH-LOGICAL-c3880-5f13714a56d6213d5e473ad88dd6a89764c512ee160070d0bebfa38872d65c0b3</cites><orcidid>0000-0002-8803-9625</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28963730$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Guo‐Feng</creatorcontrib><creatorcontrib>Liu, Jing‐Jing</creatorcontrib><creatorcontrib>He, Zhi‐Rong</creatorcontrib><creatorcontrib>Wang, Fu‐Min</creatorcontrib><creatorcontrib>Yang, Hua</creatorcontrib><creatorcontrib>Yan, Yi‐Feng</creatorcontrib><creatorcontrib>Gao, Ming‐Jun</creatorcontrib><creatorcontrib>Gruber, Margaret Y.</creatorcontrib><creatorcontrib>Wan, Xiao‐Chun</creatorcontrib><creatorcontrib>Wei, Shu</creatorcontrib><title>Implementation of CsLIS/NES in linalool biosynthesis involves transcript splicing regulation in Camellia sinensis</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>Volatile terpenoids produced in tea plants (Camellia sinensis) are airborne signals interacting against other ecosystem members, but also pleasant odorants of tea products. Transcription regulation (including transcript processing) is pivotal for plant volatile terpenoid production. In this study, a terpene synthase gene CsLIS/NES was recovered from tea plants (C. sinensis cv. “Long‐Men Xiang”). CsLIS/NES transcription regulation resulted in 2 splicing forms: CsLIS/NES‐1 and CsLIS/NES‐2 lacking a 305 bp‐fragment at N‐terminus, both producing (E)‐nerolidol and linalool in vitro. Transgenic tobacco studies and a gene‐specific antisense oligo‐deoxynucleotide suppression applied in tea leaves indicated that CsLIS/NES‐1, localized in chloroplasts, acted as linalool synthase, whereas CsLIS/NES‐2 localized in cytosol, functioned as a potential nerolidol synthase, but not linalool synthase. Expression patterns of the 2 transcript isoforms in tea were distinctly different and responded differentially to the application of stress signal molecule methyl jasmonate. Leaf expression of CsLIS/NES‐1, but not CsLIS/NES‐2, was significantly induced by methyl jasmonate. Our data indicated that distinct transcript splicing regulation patterns, together with subcellular compartmentation of CsLIS/NE‐1 and CsLIS/NE‐2 implemented the linalool biosynthesis regulation in tea plants in responding to endogenous and exogenous regulatory factors. Linalool and nerolidol produced in tea plants are not only airborne signals interacting against other ecosystem members for better plant fitness but also floral scent determinants of tea products. A better understanding of the mechanisms underlying their biosynthesis in tea plants may provide effective approaches for tea aroma quality and tea productivity improvement. In this study, tea CsLIS/NES gene was found being differentially involved in linalool and nerolidol biosynthesis due to its 2 splicing transcripts with distinct expression patterns. Regulation at transcription (including transcript processing) and subcellular compartmentation of the 2 CsLIS/NES transcripts implement the biosynthesis regulation of linalool and nerolidol in tea plants in responding to endogenous and exogenous regulatory factors.</description><subject>Acetates - pharmacology</subject><subject>Acyclic Monoterpenes</subject><subject>Alkyl and Aryl Transferases - genetics</subject><subject>Alkyl and Aryl Transferases - metabolism</subject><subject>alternative splicing</subject><subject>Antisense RNA</subject><subject>Aroma</subject><subject>Base Sequence</subject><subject>Biosynthesis</subject><subject>Camellia sinensis</subject><subject>Camellia sinensis - drug effects</subject><subject>Camellia sinensis - genetics</subject><subject>Camellia sinensis - metabolism</subject><subject>Chloroplasts</subject><subject>Compartmentation</subject><subject>CsLIS/NES</subject><subject>Cyclopentanes - pharmacology</subject><subject>Cytosol</subject><subject>Data processing</subject><subject>Ecosystems</subject><subject>Fitness</subject><subject>Flowers - drug effects</subject><subject>Flowers - metabolism</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Gene regulation</subject><subject>Isoforms</subject><subject>Leaves</subject><subject>Linalool</subject><subject>Methyl jasmonate</subject><subject>Monoterpenes - metabolism</subject><subject>N-Terminus</subject><subject>Nerolidol</subject><subject>Nicotiana - genetics</subject><subject>Odorants</subject><subject>Oxylipins - pharmacology</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Leaves - metabolism</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants (botany)</subject><subject>Plants, Genetically Modified</subject><subject>Regulation</subject><subject>RNA Splicing - drug effects</subject><subject>RNA Splicing - genetics</subject><subject>RNA, Messenger - genetics</subject><subject>RNA, Messenger - metabolism</subject><subject>Sesquiterpenes - metabolism</subject><subject>Splicing</subject><subject>Subcellular Fractions - metabolism</subject><subject>Tea</subject><subject>tea aroma</subject><subject>Terpene synthase</subject><subject>Terpenes</subject><subject>Terpenes - metabolism</subject><subject>Tobacco</subject><subject>Transcription</subject><subject>Transgenic plants</subject><subject>volatile terpenoids</subject><issn>0140-7791</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1kMFq3DAQhkVp6G7SHvoCRdBTDs6OVrYkH4vZNAtLEkhyNrI93irIkiN5t-zbR6nT3jqXgZlvPpifkK8Mrliq1djiFeOg4ANZMi6KjEMOH8kSWA6ZlCVbkPMYnwHSQJafyGKtSsElhyV52Q6jxQHdpCfjHfU9reJu-7C63TxQ46g1TlvvLW2Mjyc3_cJoYlocvT1ipFPQLrbBjBONozWtcXsacH-wsy0JKj2gtUbTaBy6dPyZnPXaRvzy3i_I0_XmsbrJdnc_t9WPXdZypSAresYly3UhOrFmvCswl1x3SnWd0KqUIm8LtkZkAkBCBw02vU6Xct2JooWGX5Dvs3cM_uWAcaqf_SGkb2LNSqkKBUUuEnU5U23wMQbs6zGYQYdTzaB-C7dO4dZ_wk3st3fjoRmw-0f-TTMBqxn4bSye_m-q76vNrHwFL6KEOg</recordid><startdate>201801</startdate><enddate>201801</enddate><creator>Liu, Guo‐Feng</creator><creator>Liu, Jing‐Jing</creator><creator>He, Zhi‐Rong</creator><creator>Wang, Fu‐Min</creator><creator>Yang, Hua</creator><creator>Yan, Yi‐Feng</creator><creator>Gao, Ming‐Jun</creator><creator>Gruber, Margaret Y.</creator><creator>Wan, Xiao‐Chun</creator><creator>Wei, Shu</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><orcidid>https://orcid.org/0000-0002-8803-9625</orcidid></search><sort><creationdate>201801</creationdate><title>Implementation of CsLIS/NES in linalool biosynthesis involves transcript splicing regulation in Camellia sinensis</title><author>Liu, Guo‐Feng ; Liu, Jing‐Jing ; He, Zhi‐Rong ; Wang, Fu‐Min ; Yang, Hua ; Yan, Yi‐Feng ; Gao, Ming‐Jun ; Gruber, Margaret Y. ; Wan, Xiao‐Chun ; Wei, Shu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3880-5f13714a56d6213d5e473ad88dd6a89764c512ee160070d0bebfa38872d65c0b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Acetates - pharmacology</topic><topic>Acyclic Monoterpenes</topic><topic>Alkyl and Aryl Transferases - genetics</topic><topic>Alkyl and Aryl Transferases - metabolism</topic><topic>alternative splicing</topic><topic>Antisense RNA</topic><topic>Aroma</topic><topic>Base Sequence</topic><topic>Biosynthesis</topic><topic>Camellia sinensis</topic><topic>Camellia sinensis - drug effects</topic><topic>Camellia sinensis - genetics</topic><topic>Camellia sinensis - metabolism</topic><topic>Chloroplasts</topic><topic>Compartmentation</topic><topic>CsLIS/NES</topic><topic>Cyclopentanes - pharmacology</topic><topic>Cytosol</topic><topic>Data processing</topic><topic>Ecosystems</topic><topic>Fitness</topic><topic>Flowers - drug effects</topic><topic>Flowers - metabolism</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Gene regulation</topic><topic>Isoforms</topic><topic>Leaves</topic><topic>Linalool</topic><topic>Methyl jasmonate</topic><topic>Monoterpenes - metabolism</topic><topic>N-Terminus</topic><topic>Nerolidol</topic><topic>Nicotiana - genetics</topic><topic>Odorants</topic><topic>Oxylipins - pharmacology</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Leaves - metabolism</topic><topic>Plant Proteins - genetics</topic><topic>Plant Proteins - metabolism</topic><topic>Plants (botany)</topic><topic>Plants, Genetically Modified</topic><topic>Regulation</topic><topic>RNA Splicing - drug effects</topic><topic>RNA Splicing - genetics</topic><topic>RNA, Messenger - genetics</topic><topic>RNA, Messenger - metabolism</topic><topic>Sesquiterpenes - metabolism</topic><topic>Splicing</topic><topic>Subcellular Fractions - metabolism</topic><topic>Tea</topic><topic>tea aroma</topic><topic>Terpene synthase</topic><topic>Terpenes</topic><topic>Terpenes - metabolism</topic><topic>Tobacco</topic><topic>Transcription</topic><topic>Transgenic plants</topic><topic>volatile terpenoids</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Guo‐Feng</creatorcontrib><creatorcontrib>Liu, Jing‐Jing</creatorcontrib><creatorcontrib>He, Zhi‐Rong</creatorcontrib><creatorcontrib>Wang, Fu‐Min</creatorcontrib><creatorcontrib>Yang, Hua</creatorcontrib><creatorcontrib>Yan, Yi‐Feng</creatorcontrib><creatorcontrib>Gao, Ming‐Jun</creatorcontrib><creatorcontrib>Gruber, Margaret Y.</creatorcontrib><creatorcontrib>Wan, Xiao‐Chun</creatorcontrib><creatorcontrib>Wei, Shu</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium &amp; 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Transcription regulation (including transcript processing) is pivotal for plant volatile terpenoid production. In this study, a terpene synthase gene CsLIS/NES was recovered from tea plants (C. sinensis cv. “Long‐Men Xiang”). CsLIS/NES transcription regulation resulted in 2 splicing forms: CsLIS/NES‐1 and CsLIS/NES‐2 lacking a 305 bp‐fragment at N‐terminus, both producing (E)‐nerolidol and linalool in vitro. Transgenic tobacco studies and a gene‐specific antisense oligo‐deoxynucleotide suppression applied in tea leaves indicated that CsLIS/NES‐1, localized in chloroplasts, acted as linalool synthase, whereas CsLIS/NES‐2 localized in cytosol, functioned as a potential nerolidol synthase, but not linalool synthase. Expression patterns of the 2 transcript isoforms in tea were distinctly different and responded differentially to the application of stress signal molecule methyl jasmonate. Leaf expression of CsLIS/NES‐1, but not CsLIS/NES‐2, was significantly induced by methyl jasmonate. Our data indicated that distinct transcript splicing regulation patterns, together with subcellular compartmentation of CsLIS/NE‐1 and CsLIS/NE‐2 implemented the linalool biosynthesis regulation in tea plants in responding to endogenous and exogenous regulatory factors. Linalool and nerolidol produced in tea plants are not only airborne signals interacting against other ecosystem members for better plant fitness but also floral scent determinants of tea products. A better understanding of the mechanisms underlying their biosynthesis in tea plants may provide effective approaches for tea aroma quality and tea productivity improvement. In this study, tea CsLIS/NES gene was found being differentially involved in linalool and nerolidol biosynthesis due to its 2 splicing transcripts with distinct expression patterns. Regulation at transcription (including transcript processing) and subcellular compartmentation of the 2 CsLIS/NES transcripts implement the biosynthesis regulation of linalool and nerolidol in tea plants in responding to endogenous and exogenous regulatory factors.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>28963730</pmid><doi>10.1111/pce.13080</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0002-8803-9625</orcidid><oa>free_for_read</oa></addata></record>
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subjects Acetates - pharmacology
Acyclic Monoterpenes
Alkyl and Aryl Transferases - genetics
Alkyl and Aryl Transferases - metabolism
alternative splicing
Antisense RNA
Aroma
Base Sequence
Biosynthesis
Camellia sinensis
Camellia sinensis - drug effects
Camellia sinensis - genetics
Camellia sinensis - metabolism
Chloroplasts
Compartmentation
CsLIS/NES
Cyclopentanes - pharmacology
Cytosol
Data processing
Ecosystems
Fitness
Flowers - drug effects
Flowers - metabolism
Gene Expression Regulation, Plant - drug effects
Gene regulation
Isoforms
Leaves
Linalool
Methyl jasmonate
Monoterpenes - metabolism
N-Terminus
Nerolidol
Nicotiana - genetics
Odorants
Oxylipins - pharmacology
Plant Leaves - drug effects
Plant Leaves - metabolism
Plant Proteins - genetics
Plant Proteins - metabolism
Plants (botany)
Plants, Genetically Modified
Regulation
RNA Splicing - drug effects
RNA Splicing - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
Sesquiterpenes - metabolism
Splicing
Subcellular Fractions - metabolism
Tea
tea aroma
Terpene synthase
Terpenes
Terpenes - metabolism
Tobacco
Transcription
Transgenic plants
volatile terpenoids
title Implementation of CsLIS/NES in linalool biosynthesis involves transcript splicing regulation in Camellia sinensis
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