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Marsdenia tenacissima genome reveals calcium adaptation and tenacissoside biosynthesis

SUMMARY Marsdenia tenacissima is a medicinal plant widely distributed in the calcium‐rich karst regions of southwest China. However, the lack of a reference genome has hampered the implementation of molecular techniques in its breeding, pharmacology and domestication. We generated the chromosome‐lev...

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Published in:The Plant journal : for cell and molecular biology 2023-03, Vol.113 (6), p.1146-1159
Main Authors: Zhou, Yanli, Fan, Wei, Zhang, Haoyue, Zhang, Jingling, Zhang, Guanghui, Wang, Ding, Xiang, Guisheng, Zhao, Changhong, Li, Lianhua, He, Simei, Lu, Yingchun, Zhao, Jiuxia, Meng, Zhengui, Zhang, Xianmin, Meng, Hengling, Yin, Xinhua, Yang, Shengchao, Long, Guangqiang
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cited_by cdi_FETCH-LOGICAL-c3531-b34db78ccb7a65040e604e67486fb6e55818b598af85da7e6c8e7b39ffef93783
cites cdi_FETCH-LOGICAL-c3531-b34db78ccb7a65040e604e67486fb6e55818b598af85da7e6c8e7b39ffef93783
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container_title The Plant journal : for cell and molecular biology
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creator Zhou, Yanli
Fan, Wei
Zhang, Haoyue
Zhang, Jingling
Zhang, Guanghui
Wang, Ding
Xiang, Guisheng
Zhao, Changhong
Li, Lianhua
He, Simei
Lu, Yingchun
Zhao, Jiuxia
Meng, Zhengui
Zhang, Xianmin
Meng, Hengling
Yin, Xinhua
Yang, Shengchao
Long, Guangqiang
description SUMMARY Marsdenia tenacissima is a medicinal plant widely distributed in the calcium‐rich karst regions of southwest China. However, the lack of a reference genome has hampered the implementation of molecular techniques in its breeding, pharmacology and domestication. We generated the chromosome‐level genome assembly in Apocynaceae using combined SMRT sequencing and Hi‐C. The genome length was 381.76 Mb, with 98.9% of it found on 11 chromosomes. The genome contained 222.63 Mb of repetitive sequences and 21 899 predicted gene models, with a contig N50 of 6.57 Mb. Phylogenetic analysis revealed that M. tenacissima diverged from Calotropis gigantea at least 13.43 million years ago. Comparative genomics showed that M. tenacissima underwent ancient shared whole‐genome duplication. This event, together with tandem duplication, contributed to 70.71% of gene‐family expansion. Both pseudogene analysis and selective pressure calculations suggested calcium‐related adaptive evolution in the M. tenacissima genome. Calcium‐induced differentially expressed genes (DEGs) were mainly enriched in cell‐wall‐related processes. Domains (e.g. Fasciclin and Amb_all) and cis‐elements (e.g. MYB and MYC) frequently occurred in the coding and promoter regions of cell‐wall DEGs, respectively, and the expression levels of these genes correlated significantly with those of calcium‐signal‐related transcription factors. Moreover, calcium addition increased tenacissoside I, G and H contents. The availability of this high‐quality genome provides valuable genomic information for genetic breeding and molecular design, and lends insights into the calcium adaptation of M. tenacissima in karst areas. Significance Statement This study provide chromosome‐level genome sequence of Marsdenia tenacissima. We provide insights into calcium adaptation of plant species in Karst areas. This study put forward putative tenacissoside biosynthesis.
doi_str_mv 10.1111/tpj.16081
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However, the lack of a reference genome has hampered the implementation of molecular techniques in its breeding, pharmacology and domestication. We generated the chromosome‐level genome assembly in Apocynaceae using combined SMRT sequencing and Hi‐C. The genome length was 381.76 Mb, with 98.9% of it found on 11 chromosomes. The genome contained 222.63 Mb of repetitive sequences and 21 899 predicted gene models, with a contig N50 of 6.57 Mb. Phylogenetic analysis revealed that M. tenacissima diverged from Calotropis gigantea at least 13.43 million years ago. Comparative genomics showed that M. tenacissima underwent ancient shared whole‐genome duplication. This event, together with tandem duplication, contributed to 70.71% of gene‐family expansion. Both pseudogene analysis and selective pressure calculations suggested calcium‐related adaptive evolution in the M. tenacissima genome. Calcium‐induced differentially expressed genes (DEGs) were mainly enriched in cell‐wall‐related processes. Domains (e.g. Fasciclin and Amb_all) and cis‐elements (e.g. MYB and MYC) frequently occurred in the coding and promoter regions of cell‐wall DEGs, respectively, and the expression levels of these genes correlated significantly with those of calcium‐signal‐related transcription factors. Moreover, calcium addition increased tenacissoside I, G and H contents. The availability of this high‐quality genome provides valuable genomic information for genetic breeding and molecular design, and lends insights into the calcium adaptation of M. tenacissima in karst areas. Significance Statement This study provide chromosome‐level genome sequence of Marsdenia tenacissima. We provide insights into calcium adaptation of plant species in Karst areas. This study put forward putative tenacissoside biosynthesis.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.16081</identifier><identifier>PMID: 36575579</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Adaptation ; Apocynaceae ; Biosynthesis ; Breeding ; Ca2+ adaptation ; Calcium ; Calcium signalling ; cell‐wall remodeling ; Chromosomes ; DNA sequencing ; Domestication ; Evolution &amp; development ; Evolutionary genetics ; Gene expression ; Genes ; genome assembly ; Genomes ; Genomics ; Herbal medicine ; Hi‐C ; Karst ; Marsdenia ; Marsdenia - genetics ; Marsdenia tenacissima ; Medicinal plants ; Myc protein ; Pharmacology ; Phylogeny ; Plant Breeding ; Plants, Medicinal ; Reproduction (copying) ; Transcription factors</subject><ispartof>The Plant journal : for cell and molecular biology, 2023-03, Vol.113 (6), p.1146-1159</ispartof><rights>2022 Society for Experimental Biology and John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2023 Society for Experimental Biology and John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3531-b34db78ccb7a65040e604e67486fb6e55818b598af85da7e6c8e7b39ffef93783</citedby><cites>FETCH-LOGICAL-c3531-b34db78ccb7a65040e604e67486fb6e55818b598af85da7e6c8e7b39ffef93783</cites><orcidid>0000-0001-9147-4399 ; 0000-0002-4008-4590</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/36575579$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhou, Yanli</creatorcontrib><creatorcontrib>Fan, Wei</creatorcontrib><creatorcontrib>Zhang, Haoyue</creatorcontrib><creatorcontrib>Zhang, Jingling</creatorcontrib><creatorcontrib>Zhang, Guanghui</creatorcontrib><creatorcontrib>Wang, Ding</creatorcontrib><creatorcontrib>Xiang, Guisheng</creatorcontrib><creatorcontrib>Zhao, Changhong</creatorcontrib><creatorcontrib>Li, Lianhua</creatorcontrib><creatorcontrib>He, Simei</creatorcontrib><creatorcontrib>Lu, Yingchun</creatorcontrib><creatorcontrib>Zhao, Jiuxia</creatorcontrib><creatorcontrib>Meng, Zhengui</creatorcontrib><creatorcontrib>Zhang, Xianmin</creatorcontrib><creatorcontrib>Meng, Hengling</creatorcontrib><creatorcontrib>Yin, Xinhua</creatorcontrib><creatorcontrib>Yang, Shengchao</creatorcontrib><creatorcontrib>Long, Guangqiang</creatorcontrib><title>Marsdenia tenacissima genome reveals calcium adaptation and tenacissoside biosynthesis</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY Marsdenia tenacissima is a medicinal plant widely distributed in the calcium‐rich karst regions of southwest China. However, the lack of a reference genome has hampered the implementation of molecular techniques in its breeding, pharmacology and domestication. We generated the chromosome‐level genome assembly in Apocynaceae using combined SMRT sequencing and Hi‐C. The genome length was 381.76 Mb, with 98.9% of it found on 11 chromosomes. The genome contained 222.63 Mb of repetitive sequences and 21 899 predicted gene models, with a contig N50 of 6.57 Mb. Phylogenetic analysis revealed that M. tenacissima diverged from Calotropis gigantea at least 13.43 million years ago. Comparative genomics showed that M. tenacissima underwent ancient shared whole‐genome duplication. This event, together with tandem duplication, contributed to 70.71% of gene‐family expansion. Both pseudogene analysis and selective pressure calculations suggested calcium‐related adaptive evolution in the M. tenacissima genome. Calcium‐induced differentially expressed genes (DEGs) were mainly enriched in cell‐wall‐related processes. Domains (e.g. Fasciclin and Amb_all) and cis‐elements (e.g. MYB and MYC) frequently occurred in the coding and promoter regions of cell‐wall DEGs, respectively, and the expression levels of these genes correlated significantly with those of calcium‐signal‐related transcription factors. Moreover, calcium addition increased tenacissoside I, G and H contents. The availability of this high‐quality genome provides valuable genomic information for genetic breeding and molecular design, and lends insights into the calcium adaptation of M. tenacissima in karst areas. Significance Statement This study provide chromosome‐level genome sequence of Marsdenia tenacissima. We provide insights into calcium adaptation of plant species in Karst areas. 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Fan, Wei ; Zhang, Haoyue ; Zhang, Jingling ; Zhang, Guanghui ; Wang, Ding ; Xiang, Guisheng ; Zhao, Changhong ; Li, Lianhua ; He, Simei ; Lu, Yingchun ; Zhao, Jiuxia ; Meng, Zhengui ; Zhang, Xianmin ; Meng, Hengling ; Yin, Xinhua ; Yang, Shengchao ; Long, Guangqiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3531-b34db78ccb7a65040e604e67486fb6e55818b598af85da7e6c8e7b39ffef93783</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Adaptation</topic><topic>Apocynaceae</topic><topic>Biosynthesis</topic><topic>Breeding</topic><topic>Ca2+ adaptation</topic><topic>Calcium</topic><topic>Calcium signalling</topic><topic>cell‐wall remodeling</topic><topic>Chromosomes</topic><topic>DNA sequencing</topic><topic>Domestication</topic><topic>Evolution &amp; development</topic><topic>Evolutionary genetics</topic><topic>Gene expression</topic><topic>Genes</topic><topic>genome assembly</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Herbal medicine</topic><topic>Hi‐C</topic><topic>Karst</topic><topic>Marsdenia</topic><topic>Marsdenia - genetics</topic><topic>Marsdenia tenacissima</topic><topic>Medicinal plants</topic><topic>Myc protein</topic><topic>Pharmacology</topic><topic>Phylogeny</topic><topic>Plant Breeding</topic><topic>Plants, Medicinal</topic><topic>Reproduction (copying)</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhou, Yanli</creatorcontrib><creatorcontrib>Fan, Wei</creatorcontrib><creatorcontrib>Zhang, Haoyue</creatorcontrib><creatorcontrib>Zhang, Jingling</creatorcontrib><creatorcontrib>Zhang, Guanghui</creatorcontrib><creatorcontrib>Wang, Ding</creatorcontrib><creatorcontrib>Xiang, Guisheng</creatorcontrib><creatorcontrib>Zhao, Changhong</creatorcontrib><creatorcontrib>Li, Lianhua</creatorcontrib><creatorcontrib>He, Simei</creatorcontrib><creatorcontrib>Lu, Yingchun</creatorcontrib><creatorcontrib>Zhao, Jiuxia</creatorcontrib><creatorcontrib>Meng, Zhengui</creatorcontrib><creatorcontrib>Zhang, Xianmin</creatorcontrib><creatorcontrib>Meng, Hengling</creatorcontrib><creatorcontrib>Yin, Xinhua</creatorcontrib><creatorcontrib>Yang, Shengchao</creatorcontrib><creatorcontrib>Long, Guangqiang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium &amp; 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However, the lack of a reference genome has hampered the implementation of molecular techniques in its breeding, pharmacology and domestication. We generated the chromosome‐level genome assembly in Apocynaceae using combined SMRT sequencing and Hi‐C. The genome length was 381.76 Mb, with 98.9% of it found on 11 chromosomes. The genome contained 222.63 Mb of repetitive sequences and 21 899 predicted gene models, with a contig N50 of 6.57 Mb. Phylogenetic analysis revealed that M. tenacissima diverged from Calotropis gigantea at least 13.43 million years ago. Comparative genomics showed that M. tenacissima underwent ancient shared whole‐genome duplication. This event, together with tandem duplication, contributed to 70.71% of gene‐family expansion. Both pseudogene analysis and selective pressure calculations suggested calcium‐related adaptive evolution in the M. tenacissima genome. Calcium‐induced differentially expressed genes (DEGs) were mainly enriched in cell‐wall‐related processes. Domains (e.g. Fasciclin and Amb_all) and cis‐elements (e.g. MYB and MYC) frequently occurred in the coding and promoter regions of cell‐wall DEGs, respectively, and the expression levels of these genes correlated significantly with those of calcium‐signal‐related transcription factors. Moreover, calcium addition increased tenacissoside I, G and H contents. The availability of this high‐quality genome provides valuable genomic information for genetic breeding and molecular design, and lends insights into the calcium adaptation of M. tenacissima in karst areas. Significance Statement This study provide chromosome‐level genome sequence of Marsdenia tenacissima. We provide insights into calcium adaptation of plant species in Karst areas. This study put forward putative tenacissoside biosynthesis.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>36575579</pmid><doi>10.1111/tpj.16081</doi><tpages>1159</tpages><orcidid>https://orcid.org/0000-0001-9147-4399</orcidid><orcidid>https://orcid.org/0000-0002-4008-4590</orcidid></addata></record>
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subjects Adaptation
Apocynaceae
Biosynthesis
Breeding
Ca2+ adaptation
Calcium
Calcium signalling
cell‐wall remodeling
Chromosomes
DNA sequencing
Domestication
Evolution & development
Evolutionary genetics
Gene expression
Genes
genome assembly
Genomes
Genomics
Herbal medicine
Hi‐C
Karst
Marsdenia
Marsdenia - genetics
Marsdenia tenacissima
Medicinal plants
Myc protein
Pharmacology
Phylogeny
Plant Breeding
Plants, Medicinal
Reproduction (copying)
Transcription factors
title Marsdenia tenacissima genome reveals calcium adaptation and tenacissoside biosynthesis
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