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Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria
Methyl jasmonate (MeJA) is a known elicitor of plant specialized metabolism, including triterpenoid saponins. Saponaria vaccaria is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural simila...
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Published in: | Nature communications 2023-11, Vol.14 (1), p.7101-7101, Article 7101 |
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description | Methyl jasmonate (MeJA) is a known elicitor of plant specialized metabolism, including triterpenoid saponins.
Saponaria vaccaria
is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural similarities to the vaccine adjuvant QS-21. Leveraging the MeJA-elicited saponin biosynthesis, we identify multiple enzymes catalyzing the oxidation and glycosylation of triterpenoids in
S. vaccaria
. This exploration is aided by Pacbio full-length transcriptome sequencing and gene expression analysis. A cellulose synthase-like enzyme can not only glucuronidate triterpenoid aglycones but also alter the product profile of a cytochrome P450 monooxygenase via preference for the aldehyde intermediate. Furthermore, the discovery of a UDP-glucose 4,6-dehydratase and a UDP-4-keto-6-deoxy-glucose reductase reveals the biosynthetic pathway for the rare nucleotide sugar UDP-
d
-fucose, a likely sugar donor for fucosylation of plant natural products. Our work enables the production and optimization of high-value saponins in microorganisms and plants through synthetic biology approaches.
Methyl jasmonate triggers saponin production in
Saponaria vaccaria
. Using transcriptome data and heterologous expression, the authors identify P450s and glycosyltransferases that modify triterpenoids. They also discover the pathway for UDP-D-fucose biosynthesis. |
doi_str_mv | 10.1038/s41467-023-42877-0 |
format | article |
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Saponaria vaccaria
is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural similarities to the vaccine adjuvant QS-21. Leveraging the MeJA-elicited saponin biosynthesis, we identify multiple enzymes catalyzing the oxidation and glycosylation of triterpenoids in
S. vaccaria
. This exploration is aided by Pacbio full-length transcriptome sequencing and gene expression analysis. A cellulose synthase-like enzyme can not only glucuronidate triterpenoid aglycones but also alter the product profile of a cytochrome P450 monooxygenase via preference for the aldehyde intermediate. Furthermore, the discovery of a UDP-glucose 4,6-dehydratase and a UDP-4-keto-6-deoxy-glucose reductase reveals the biosynthetic pathway for the rare nucleotide sugar UDP-
d
-fucose, a likely sugar donor for fucosylation of plant natural products. Our work enables the production and optimization of high-value saponins in microorganisms and plants through synthetic biology approaches.
Methyl jasmonate triggers saponin production in
Saponaria vaccaria
. Using transcriptome data and heterologous expression, the authors identify P450s and glycosyltransferases that modify triterpenoids. They also discover the pathway for UDP-D-fucose biosynthesis.</description><identifier>ISSN: 2041-1723</identifier><identifier>EISSN: 2041-1723</identifier><identifier>DOI: 10.1038/s41467-023-42877-0</identifier><identifier>PMID: 37925486</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/39 ; 38/91 ; 631/449/2667 ; 631/449/447 ; 631/61/191/2018 ; 82/16 ; 82/58 ; 82/80 ; Aglycones ; Aldehydes ; Anticancer properties ; BASIC BIOLOGICAL SCIENCES ; Biosynthesis ; Cellulose ; Cellulose synthase ; Cytochrome P450 ; Cytochrome P450 monooxygenase ; Cytochromes P450 ; Dehydration ; Fucose ; Gene expression ; gene expression profiling ; Gene sequencing ; Glucose ; Glycosylation ; Herbal medicine ; Humanities and Social Sciences ; Methyl jasmonate ; Microorganisms ; multidisciplinary ; Natural products ; Nucleotides ; Optimization ; Oxidation ; plant biotechnology ; Reductases ; Saponaria ; Saponins ; Science ; Science (multidisciplinary) ; secondary metabolism ; Sugar ; Traditional Chinese medicine ; Transcriptomes ; Triterpenoids</subject><ispartof>Nature communications, 2023-11, Vol.14 (1), p.7101-7101, Article 7101</ispartof><rights>The Author(s) 2023</rights><rights>The Author(s) 2023. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c545t-4d03c5a2cb9aae9bd5c52f73990688f933f7f8fc3dbcb7e9db45fc4143c2b5b03</citedby><cites>FETCH-LOGICAL-c545t-4d03c5a2cb9aae9bd5c52f73990688f933f7f8fc3dbcb7e9db45fc4143c2b5b03</cites><orcidid>0000-0003-4170-6088 ; 0000-0002-6702-3560 ; 0000-0001-5614-1951 ; 0000000341706088 ; 0000000267023560 ; 0000000156141951</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2885955129/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2885955129?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.osti.gov/biblio/2204752$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Chen, Xiaoyue</creatorcontrib><creatorcontrib>Hudson, Graham A.</creatorcontrib><creatorcontrib>Mineo, Charlotte</creatorcontrib><creatorcontrib>Amer, Bashar</creatorcontrib><creatorcontrib>Baidoo, Edward E. K.</creatorcontrib><creatorcontrib>Crowe, Samantha A.</creatorcontrib><creatorcontrib>Liu, Yuzhong</creatorcontrib><creatorcontrib>Keasling, Jay D.</creatorcontrib><creatorcontrib>Scheller, Henrik V.</creatorcontrib><creatorcontrib>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</creatorcontrib><title>Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria</title><title>Nature communications</title><addtitle>Nat Commun</addtitle><description>Methyl jasmonate (MeJA) is a known elicitor of plant specialized metabolism, including triterpenoid saponins.
Saponaria vaccaria
is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural similarities to the vaccine adjuvant QS-21. Leveraging the MeJA-elicited saponin biosynthesis, we identify multiple enzymes catalyzing the oxidation and glycosylation of triterpenoids in
S. vaccaria
. This exploration is aided by Pacbio full-length transcriptome sequencing and gene expression analysis. A cellulose synthase-like enzyme can not only glucuronidate triterpenoid aglycones but also alter the product profile of a cytochrome P450 monooxygenase via preference for the aldehyde intermediate. Furthermore, the discovery of a UDP-glucose 4,6-dehydratase and a UDP-4-keto-6-deoxy-glucose reductase reveals the biosynthetic pathway for the rare nucleotide sugar UDP-
d
-fucose, a likely sugar donor for fucosylation of plant natural products. Our work enables the production and optimization of high-value saponins in microorganisms and plants through synthetic biology approaches.
Methyl jasmonate triggers saponin production in
Saponaria vaccaria
. Using transcriptome data and heterologous expression, the authors identify P450s and glycosyltransferases that modify triterpenoids. They also discover the pathway for UDP-D-fucose biosynthesis.</description><subject>38/39</subject><subject>38/91</subject><subject>631/449/2667</subject><subject>631/449/447</subject><subject>631/61/191/2018</subject><subject>82/16</subject><subject>82/58</subject><subject>82/80</subject><subject>Aglycones</subject><subject>Aldehydes</subject><subject>Anticancer properties</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Biosynthesis</subject><subject>Cellulose</subject><subject>Cellulose synthase</subject><subject>Cytochrome P450</subject><subject>Cytochrome P450 monooxygenase</subject><subject>Cytochromes P450</subject><subject>Dehydration</subject><subject>Fucose</subject><subject>Gene expression</subject><subject>gene expression profiling</subject><subject>Gene sequencing</subject><subject>Glucose</subject><subject>Glycosylation</subject><subject>Herbal medicine</subject><subject>Humanities and Social Sciences</subject><subject>Methyl jasmonate</subject><subject>Microorganisms</subject><subject>multidisciplinary</subject><subject>Natural products</subject><subject>Nucleotides</subject><subject>Optimization</subject><subject>Oxidation</subject><subject>plant biotechnology</subject><subject>Reductases</subject><subject>Saponaria</subject><subject>Saponins</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>secondary metabolism</subject><subject>Sugar</subject><subject>Traditional Chinese medicine</subject><subject>Transcriptomes</subject><subject>Triterpenoids</subject><issn>2041-1723</issn><issn>2041-1723</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9ks2OFCEUhStG40zGeQFXRDduSil-qmBlzPg3ySQu1DUB6tJNpwpKoCfpN_CxpaYm6riQDTdw7gccTtM87_DrDlPxJrOO9UOLCW0ZEUOtHjXnBLOu7QZCH_9VnzWXOR9wHVR2grGnzRkdJOFM9OfNz_dg_bKH5MMOleQLpAVC9CPKeonBB2R8zKdQ9pB9RuaEJriFpHebXodsk19KnAElyLUjAyoRzVD2pwkddJ5j0AUQTN76oouPAVXo1xWuk9foVlu7Fs-aJ05PGS7v54vm-8cP364-tzdfPl1fvbtpLWe8tGzE1HJNrJFagzQjt5y4gUqJeyGcpNQNTjhLR2PNAHI0jDtbvaKWGG4wvWiuN-4Y9UEtyc86nVTUXt0txLRTOhVvJ1CEDpw67gyRmHFipXOjpHoQAmsp3Mp6u7GWo5lhtBCqI9MD6MOd4PdqF29Vh3vCuWCV8GIjxFy8ytUisHsbQwBbFKlfOHBSRa_uj0nxxxFyUbPPFqZJB4jHrIgQPSWCd32VvvxHeojHFKqhq4pLzjsiq4psKptizgnc7yt3WK3pUlu6VE2XukuXWh9Lt6a8rGGB9Af9n65f7tLUwg</recordid><startdate>20231104</startdate><enddate>20231104</enddate><creator>Chen, Xiaoyue</creator><creator>Hudson, Graham A.</creator><creator>Mineo, Charlotte</creator><creator>Amer, Bashar</creator><creator>Baidoo, Edward E. 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K.</au><au>Crowe, Samantha A.</au><au>Liu, Yuzhong</au><au>Keasling, Jay D.</au><au>Scheller, Henrik V.</au><aucorp>Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria</atitle><jtitle>Nature communications</jtitle><stitle>Nat Commun</stitle><date>2023-11-04</date><risdate>2023</risdate><volume>14</volume><issue>1</issue><spage>7101</spage><epage>7101</epage><pages>7101-7101</pages><artnum>7101</artnum><issn>2041-1723</issn><eissn>2041-1723</eissn><abstract>Methyl jasmonate (MeJA) is a known elicitor of plant specialized metabolism, including triterpenoid saponins.
Saponaria vaccaria
is an annual herb used in traditional Chinese medicine, containing large quantities of oleanane-type triterpenoid saponins with anticancer properties and structural similarities to the vaccine adjuvant QS-21. Leveraging the MeJA-elicited saponin biosynthesis, we identify multiple enzymes catalyzing the oxidation and glycosylation of triterpenoids in
S. vaccaria
. This exploration is aided by Pacbio full-length transcriptome sequencing and gene expression analysis. A cellulose synthase-like enzyme can not only glucuronidate triterpenoid aglycones but also alter the product profile of a cytochrome P450 monooxygenase via preference for the aldehyde intermediate. Furthermore, the discovery of a UDP-glucose 4,6-dehydratase and a UDP-4-keto-6-deoxy-glucose reductase reveals the biosynthetic pathway for the rare nucleotide sugar UDP-
d
-fucose, a likely sugar donor for fucosylation of plant natural products. Our work enables the production and optimization of high-value saponins in microorganisms and plants through synthetic biology approaches.
Methyl jasmonate triggers saponin production in
Saponaria vaccaria
. Using transcriptome data and heterologous expression, the authors identify P450s and glycosyltransferases that modify triterpenoids. They also discover the pathway for UDP-D-fucose biosynthesis.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>37925486</pmid><doi>10.1038/s41467-023-42877-0</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-4170-6088</orcidid><orcidid>https://orcid.org/0000-0002-6702-3560</orcidid><orcidid>https://orcid.org/0000-0001-5614-1951</orcidid><orcidid>https://orcid.org/0000000341706088</orcidid><orcidid>https://orcid.org/0000000267023560</orcidid><orcidid>https://orcid.org/0000000156141951</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 38/39 38/91 631/449/2667 631/449/447 631/61/191/2018 82/16 82/58 82/80 Aglycones Aldehydes Anticancer properties BASIC BIOLOGICAL SCIENCES Biosynthesis Cellulose Cellulose synthase Cytochrome P450 Cytochrome P450 monooxygenase Cytochromes P450 Dehydration Fucose Gene expression gene expression profiling Gene sequencing Glucose Glycosylation Herbal medicine Humanities and Social Sciences Methyl jasmonate Microorganisms multidisciplinary Natural products Nucleotides Optimization Oxidation plant biotechnology Reductases Saponaria Saponins Science Science (multidisciplinary) secondary metabolism Sugar Traditional Chinese medicine Transcriptomes Triterpenoids |
title | Deciphering triterpenoid saponin biosynthesis by leveraging transcriptome response to methyl jasmonate elicitation in Saponaria vaccaria |
url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-29T00%3A03%3A21IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Deciphering%20triterpenoid%20saponin%20biosynthesis%20by%20leveraging%20transcriptome%20response%20to%20methyl%20jasmonate%20elicitation%20in%20Saponaria%20vaccaria&rft.jtitle=Nature%20communications&rft.au=Chen,%20Xiaoyue&rft.aucorp=Lawrence%20Berkeley%20National%20Laboratory%20(LBNL),%20Berkeley,%20CA%20(United%20States)&rft.date=2023-11-04&rft.volume=14&rft.issue=1&rft.spage=7101&rft.epage=7101&rft.pages=7101-7101&rft.artnum=7101&rft.issn=2041-1723&rft.eissn=2041-1723&rft_id=info:doi/10.1038/s41467-023-42877-0&rft_dat=%3Cproquest_doaj_%3E2885955129%3C/proquest_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c545t-4d03c5a2cb9aae9bd5c52f73990688f933f7f8fc3dbcb7e9db45fc4143c2b5b03%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2885955129&rft_id=info:pmid/37925486&rfr_iscdi=true |