A Chromosome-Scale Assembly of the Garden Orach (Atriplex hortensis L.) Genome Using Oxford Nanopore Sequencing

Atriplex hortensis (2n = 2x = 18, 1C genome size similar to 1.1 gigabases), also known as garden orach and mountain-spinach, is a highly nutritious, broadleaf annual of the Amaranthaceae-Chenopodiaceae alliance (Chenopodiaceae sensu stricto, subfam. Chenopodioideae) that has spread in cultivation fr...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Frontiers in plant science 2020-05, Vol.11, p.624, Article 624
Hauptverfasser: Hunt, Spencer P., Jarvis, David E., Larsen, Dallas J., Mosyakin, Sergei L., Kolano, Bozena A., Jackson, Eric W., Martin, Sara L., Jellen, Eric N., Maughan, Peter J.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue
container_start_page 624
container_title Frontiers in plant science
container_volume 11
creator Hunt, Spencer P.
Jarvis, David E.
Larsen, Dallas J.
Mosyakin, Sergei L.
Kolano, Bozena A.
Jackson, Eric W.
Martin, Sara L.
Jellen, Eric N.
Maughan, Peter J.
description Atriplex hortensis (2n = 2x = 18, 1C genome size similar to 1.1 gigabases), also known as garden orach and mountain-spinach, is a highly nutritious, broadleaf annual of the Amaranthaceae-Chenopodiaceae alliance (Chenopodiaceae sensu stricto, subfam. Chenopodioideae) that has spread in cultivation from its native primary domestication area in Eurasia to other temperate and subtropical regions worldwide. Atriplex L. is a highly complex but, as understood now, a monophyletic group of mainly halophytic and/or xerophytic plants, of which A. hortensis has been a vegetable of minor importance in some areas of Eurasia (from Central Asia to the Mediterranean) at least since antiquity. Nonetheless, it is a crop with tremendous nutritional potential due primarily to its exceptional leaf and seed protein quantities (approaching 30%) and quality (high levels of lysine). Although there is some literature describing the taxonomy and production of A. hortensis, there is a general lack of genetic and genomic data that would otherwise help elucidate the genetic variation, phylogenetic positioning, and future potential of the species. Here, we report the assembly of the first high-quality, chromosome-scale reference genome for A. hortensis cv. "Golden." Long-read data from Oxford Nanopore's MinION DNA sequencer was assembled with the program Canu and polished with Illumina short reads. Contigs were scaffolded to chromosome scale using chromatin-proximity maps (Hi-C) yielding a final assembly containing 1,325 scaffolds with a N50 of 98.9 Mb - with 94.7% of the assembly represented in the nine largest, chromosome-scale scaffolds. Sixty-six percent of the genome was classified as highly repetitive DNA, with the most common repetitive elements being Gypsy-(32%) and Copia-like (11%) long-terminal repeats. The annotation was completed using MAKER which identified 37,083 gene models and 2,555 tRNA genes. Completeness of the genome, assessed using the Benchmarking Universal Single Copy Orthologs (BUSCO) metric, identified 97.5% of the conserved orthologs as complete, with only 2.2% being duplicated, reflecting the diploid nature of A. hortensis. A resequencing panel of 21 wild, unimproved and cultivated A. hortensis accessions revealed three distinct populations with little variation within subpopulations. These resources provide vital information to better understand A. hortensis and facilitate future study.
doi_str_mv 10.3389/fpls.2020.00624
format Article
fullrecord <record><control><sourceid>proquest_doaj_</sourceid><recordid>TN_cdi_proquest_miscellaneous_2412219340</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_8c5f65535ee84f8bb6ed9ea275768090</doaj_id><sourcerecordid>2412219340</sourcerecordid><originalsourceid>FETCH-LOGICAL-c459t-743ef00cc514d90db9467d5a68bde26640160a72c37000e95d0ed83c298e8e673</originalsourceid><addsrcrecordid>eNqNkk1vEzEQhlcIRKvSMzfkYxFK6vXX2hekKIJQKSKHUomb5bVnG1e7drA30P57vE2J2hu-2PK884zH71TV-xrPKZXqstv1eU4wwXOMBWGvqtNaCDZjgvx8_ex8Up3nfIfL4hgr1bytTijhhHJFT6u4QMttikPMcYDZtTU9oEXOMLT9A4odGreAViY5CGiTjN2ii8WY_K6He7SNaYSQfUbr-Ue0glAI6Cb7cIs2911MDn03Ie5iAnQNv_YQbAm9q950ps9w_rSfVTdfv_xYfputN6ur5WI9s4yrcdYwCh3G1vKaOYVdq5hoHDdCtg5I6QzXApuGWNqUvkBxh8FJaomSIEE09Ky6OnBdNHd6l_xg0oOOxuvHi5hutUmjtz1oaXknOKccQLJOtq0Ap8CQhjdCYoUL6_OBtdu3AzgLYUymfwF9GQl-q2_jb90QUUtaF8DFEyDF8hF51IPPFvreBIj7rAmrCakVZVOty4PUpphzgu5YpsZ6cl1PruvJdf3oesn48Px1R_0_j4tAHgR_oI1dtr44AUfZNBYM89LtNCH10o9m9DEs4z6MJfXT_6fSv7FOyWc</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2412219340</pqid></control><display><type>article</type><title>A Chromosome-Scale Assembly of the Garden Orach (Atriplex hortensis L.) Genome Using Oxford Nanopore Sequencing</title><source>DOAJ Directory of Open Access Journals</source><source>PubMed Central Open Access</source><source>Web of Science - Science Citation Index Expanded - 2020&lt;img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" /&gt;</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Hunt, Spencer P. ; Jarvis, David E. ; Larsen, Dallas J. ; Mosyakin, Sergei L. ; Kolano, Bozena A. ; Jackson, Eric W. ; Martin, Sara L. ; Jellen, Eric N. ; Maughan, Peter J.</creator><creatorcontrib>Hunt, Spencer P. ; Jarvis, David E. ; Larsen, Dallas J. ; Mosyakin, Sergei L. ; Kolano, Bozena A. ; Jackson, Eric W. ; Martin, Sara L. ; Jellen, Eric N. ; Maughan, Peter J.</creatorcontrib><description>Atriplex hortensis (2n = 2x = 18, 1C genome size similar to 1.1 gigabases), also known as garden orach and mountain-spinach, is a highly nutritious, broadleaf annual of the Amaranthaceae-Chenopodiaceae alliance (Chenopodiaceae sensu stricto, subfam. Chenopodioideae) that has spread in cultivation from its native primary domestication area in Eurasia to other temperate and subtropical regions worldwide. Atriplex L. is a highly complex but, as understood now, a monophyletic group of mainly halophytic and/or xerophytic plants, of which A. hortensis has been a vegetable of minor importance in some areas of Eurasia (from Central Asia to the Mediterranean) at least since antiquity. Nonetheless, it is a crop with tremendous nutritional potential due primarily to its exceptional leaf and seed protein quantities (approaching 30%) and quality (high levels of lysine). Although there is some literature describing the taxonomy and production of A. hortensis, there is a general lack of genetic and genomic data that would otherwise help elucidate the genetic variation, phylogenetic positioning, and future potential of the species. Here, we report the assembly of the first high-quality, chromosome-scale reference genome for A. hortensis cv. "Golden." Long-read data from Oxford Nanopore's MinION DNA sequencer was assembled with the program Canu and polished with Illumina short reads. Contigs were scaffolded to chromosome scale using chromatin-proximity maps (Hi-C) yielding a final assembly containing 1,325 scaffolds with a N50 of 98.9 Mb - with 94.7% of the assembly represented in the nine largest, chromosome-scale scaffolds. Sixty-six percent of the genome was classified as highly repetitive DNA, with the most common repetitive elements being Gypsy-(32%) and Copia-like (11%) long-terminal repeats. The annotation was completed using MAKER which identified 37,083 gene models and 2,555 tRNA genes. Completeness of the genome, assessed using the Benchmarking Universal Single Copy Orthologs (BUSCO) metric, identified 97.5% of the conserved orthologs as complete, with only 2.2% being duplicated, reflecting the diploid nature of A. hortensis. A resequencing panel of 21 wild, unimproved and cultivated A. hortensis accessions revealed three distinct populations with little variation within subpopulations. These resources provide vital information to better understand A. hortensis and facilitate future study.</description><identifier>ISSN: 1664-462X</identifier><identifier>EISSN: 1664-462X</identifier><identifier>DOI: 10.3389/fpls.2020.00624</identifier><identifier>PMID: 32523593</identifier><language>eng</language><publisher>LAUSANNE: Frontiers Media Sa</publisher><subject>Amaranthaceae ; Atriplex hortensis ; Hi-C ; Life Sciences &amp; Biomedicine ; orach ; orphan crop ; Plant Science ; Plant Sciences ; proximity-guided assembly ; Science &amp; Technology</subject><ispartof>Frontiers in plant science, 2020-05, Vol.11, p.624, Article 624</ispartof><rights>Copyright © 2020 Hunt, Jarvis, Larsen, Mosyakin, Kolano, Jackson, Martin, Jellen and Maughan.</rights><rights>Copyright © 2020 Hunt, Jarvis, Larsen, Mosyakin, Kolano, Jackson, Martin, Jellen and Maughan. 2020 Hunt, Jarvis, Larsen, Mosyakin, Kolano, Jackson, Martin, Jellen and Maughan</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>10</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000540527500001</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c459t-743ef00cc514d90db9467d5a68bde26640160a72c37000e95d0ed83c298e8e673</citedby><cites>FETCH-LOGICAL-c459t-743ef00cc514d90db9467d5a68bde26640160a72c37000e95d0ed83c298e8e673</cites><orcidid>0000-0002-4187-3807</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7261831/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7261831/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2115,27929,27930,28253,53796,53798</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32523593$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hunt, Spencer P.</creatorcontrib><creatorcontrib>Jarvis, David E.</creatorcontrib><creatorcontrib>Larsen, Dallas J.</creatorcontrib><creatorcontrib>Mosyakin, Sergei L.</creatorcontrib><creatorcontrib>Kolano, Bozena A.</creatorcontrib><creatorcontrib>Jackson, Eric W.</creatorcontrib><creatorcontrib>Martin, Sara L.</creatorcontrib><creatorcontrib>Jellen, Eric N.</creatorcontrib><creatorcontrib>Maughan, Peter J.</creatorcontrib><title>A Chromosome-Scale Assembly of the Garden Orach (Atriplex hortensis L.) Genome Using Oxford Nanopore Sequencing</title><title>Frontiers in plant science</title><addtitle>FRONT PLANT SCI</addtitle><addtitle>Front Plant Sci</addtitle><description>Atriplex hortensis (2n = 2x = 18, 1C genome size similar to 1.1 gigabases), also known as garden orach and mountain-spinach, is a highly nutritious, broadleaf annual of the Amaranthaceae-Chenopodiaceae alliance (Chenopodiaceae sensu stricto, subfam. Chenopodioideae) that has spread in cultivation from its native primary domestication area in Eurasia to other temperate and subtropical regions worldwide. Atriplex L. is a highly complex but, as understood now, a monophyletic group of mainly halophytic and/or xerophytic plants, of which A. hortensis has been a vegetable of minor importance in some areas of Eurasia (from Central Asia to the Mediterranean) at least since antiquity. Nonetheless, it is a crop with tremendous nutritional potential due primarily to its exceptional leaf and seed protein quantities (approaching 30%) and quality (high levels of lysine). Although there is some literature describing the taxonomy and production of A. hortensis, there is a general lack of genetic and genomic data that would otherwise help elucidate the genetic variation, phylogenetic positioning, and future potential of the species. Here, we report the assembly of the first high-quality, chromosome-scale reference genome for A. hortensis cv. "Golden." Long-read data from Oxford Nanopore's MinION DNA sequencer was assembled with the program Canu and polished with Illumina short reads. Contigs were scaffolded to chromosome scale using chromatin-proximity maps (Hi-C) yielding a final assembly containing 1,325 scaffolds with a N50 of 98.9 Mb - with 94.7% of the assembly represented in the nine largest, chromosome-scale scaffolds. Sixty-six percent of the genome was classified as highly repetitive DNA, with the most common repetitive elements being Gypsy-(32%) and Copia-like (11%) long-terminal repeats. The annotation was completed using MAKER which identified 37,083 gene models and 2,555 tRNA genes. Completeness of the genome, assessed using the Benchmarking Universal Single Copy Orthologs (BUSCO) metric, identified 97.5% of the conserved orthologs as complete, with only 2.2% being duplicated, reflecting the diploid nature of A. hortensis. A resequencing panel of 21 wild, unimproved and cultivated A. hortensis accessions revealed three distinct populations with little variation within subpopulations. These resources provide vital information to better understand A. hortensis and facilitate future study.</description><subject>Amaranthaceae</subject><subject>Atriplex hortensis</subject><subject>Hi-C</subject><subject>Life Sciences &amp; Biomedicine</subject><subject>orach</subject><subject>orphan crop</subject><subject>Plant Science</subject><subject>Plant Sciences</subject><subject>proximity-guided assembly</subject><subject>Science &amp; Technology</subject><issn>1664-462X</issn><issn>1664-462X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>AOWDO</sourceid><sourceid>DOA</sourceid><recordid>eNqNkk1vEzEQhlcIRKvSMzfkYxFK6vXX2hekKIJQKSKHUomb5bVnG1e7drA30P57vE2J2hu-2PK884zH71TV-xrPKZXqstv1eU4wwXOMBWGvqtNaCDZjgvx8_ex8Up3nfIfL4hgr1bytTijhhHJFT6u4QMttikPMcYDZtTU9oEXOMLT9A4odGreAViY5CGiTjN2ii8WY_K6He7SNaYSQfUbr-Ue0glAI6Cb7cIs2911MDn03Ie5iAnQNv_YQbAm9q950ps9w_rSfVTdfv_xYfputN6ur5WI9s4yrcdYwCh3G1vKaOYVdq5hoHDdCtg5I6QzXApuGWNqUvkBxh8FJaomSIEE09Ky6OnBdNHd6l_xg0oOOxuvHi5hutUmjtz1oaXknOKccQLJOtq0Ap8CQhjdCYoUL6_OBtdu3AzgLYUymfwF9GQl-q2_jb90QUUtaF8DFEyDF8hF51IPPFvreBIj7rAmrCakVZVOty4PUpphzgu5YpsZ6cl1PruvJdf3oesn48Px1R_0_j4tAHgR_oI1dtr44AUfZNBYM89LtNCH10o9m9DEs4z6MJfXT_6fSv7FOyWc</recordid><startdate>20200525</startdate><enddate>20200525</enddate><creator>Hunt, Spencer P.</creator><creator>Jarvis, David E.</creator><creator>Larsen, Dallas J.</creator><creator>Mosyakin, Sergei L.</creator><creator>Kolano, Bozena A.</creator><creator>Jackson, Eric W.</creator><creator>Martin, Sara L.</creator><creator>Jellen, Eric N.</creator><creator>Maughan, Peter J.</creator><general>Frontiers Media Sa</general><general>Frontiers Media S.A</general><scope>AOWDO</scope><scope>BLEPL</scope><scope>DTL</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4187-3807</orcidid></search><sort><creationdate>20200525</creationdate><title>A Chromosome-Scale Assembly of the Garden Orach (Atriplex hortensis L.) Genome Using Oxford Nanopore Sequencing</title><author>Hunt, Spencer P. ; Jarvis, David E. ; Larsen, Dallas J. ; Mosyakin, Sergei L. ; Kolano, Bozena A. ; Jackson, Eric W. ; Martin, Sara L. ; Jellen, Eric N. ; Maughan, Peter J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c459t-743ef00cc514d90db9467d5a68bde26640160a72c37000e95d0ed83c298e8e673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Amaranthaceae</topic><topic>Atriplex hortensis</topic><topic>Hi-C</topic><topic>Life Sciences &amp; Biomedicine</topic><topic>orach</topic><topic>orphan crop</topic><topic>Plant Science</topic><topic>Plant Sciences</topic><topic>proximity-guided assembly</topic><topic>Science &amp; Technology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hunt, Spencer P.</creatorcontrib><creatorcontrib>Jarvis, David E.</creatorcontrib><creatorcontrib>Larsen, Dallas J.</creatorcontrib><creatorcontrib>Mosyakin, Sergei L.</creatorcontrib><creatorcontrib>Kolano, Bozena A.</creatorcontrib><creatorcontrib>Jackson, Eric W.</creatorcontrib><creatorcontrib>Martin, Sara L.</creatorcontrib><creatorcontrib>Jellen, Eric N.</creatorcontrib><creatorcontrib>Maughan, Peter J.</creatorcontrib><collection>Web of Science - Science Citation Index Expanded - 2020</collection><collection>Web of Science Core Collection</collection><collection>Science Citation Index Expanded</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Frontiers in plant science</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hunt, Spencer P.</au><au>Jarvis, David E.</au><au>Larsen, Dallas J.</au><au>Mosyakin, Sergei L.</au><au>Kolano, Bozena A.</au><au>Jackson, Eric W.</au><au>Martin, Sara L.</au><au>Jellen, Eric N.</au><au>Maughan, Peter J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Chromosome-Scale Assembly of the Garden Orach (Atriplex hortensis L.) Genome Using Oxford Nanopore Sequencing</atitle><jtitle>Frontiers in plant science</jtitle><stitle>FRONT PLANT SCI</stitle><addtitle>Front Plant Sci</addtitle><date>2020-05-25</date><risdate>2020</risdate><volume>11</volume><spage>624</spage><pages>624-</pages><artnum>624</artnum><issn>1664-462X</issn><eissn>1664-462X</eissn><abstract>Atriplex hortensis (2n = 2x = 18, 1C genome size similar to 1.1 gigabases), also known as garden orach and mountain-spinach, is a highly nutritious, broadleaf annual of the Amaranthaceae-Chenopodiaceae alliance (Chenopodiaceae sensu stricto, subfam. Chenopodioideae) that has spread in cultivation from its native primary domestication area in Eurasia to other temperate and subtropical regions worldwide. Atriplex L. is a highly complex but, as understood now, a monophyletic group of mainly halophytic and/or xerophytic plants, of which A. hortensis has been a vegetable of minor importance in some areas of Eurasia (from Central Asia to the Mediterranean) at least since antiquity. Nonetheless, it is a crop with tremendous nutritional potential due primarily to its exceptional leaf and seed protein quantities (approaching 30%) and quality (high levels of lysine). Although there is some literature describing the taxonomy and production of A. hortensis, there is a general lack of genetic and genomic data that would otherwise help elucidate the genetic variation, phylogenetic positioning, and future potential of the species. Here, we report the assembly of the first high-quality, chromosome-scale reference genome for A. hortensis cv. "Golden." Long-read data from Oxford Nanopore's MinION DNA sequencer was assembled with the program Canu and polished with Illumina short reads. Contigs were scaffolded to chromosome scale using chromatin-proximity maps (Hi-C) yielding a final assembly containing 1,325 scaffolds with a N50 of 98.9 Mb - with 94.7% of the assembly represented in the nine largest, chromosome-scale scaffolds. Sixty-six percent of the genome was classified as highly repetitive DNA, with the most common repetitive elements being Gypsy-(32%) and Copia-like (11%) long-terminal repeats. The annotation was completed using MAKER which identified 37,083 gene models and 2,555 tRNA genes. Completeness of the genome, assessed using the Benchmarking Universal Single Copy Orthologs (BUSCO) metric, identified 97.5% of the conserved orthologs as complete, with only 2.2% being duplicated, reflecting the diploid nature of A. hortensis. A resequencing panel of 21 wild, unimproved and cultivated A. hortensis accessions revealed three distinct populations with little variation within subpopulations. These resources provide vital information to better understand A. hortensis and facilitate future study.</abstract><cop>LAUSANNE</cop><pub>Frontiers Media Sa</pub><pmid>32523593</pmid><doi>10.3389/fpls.2020.00624</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-4187-3807</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1664-462X
ispartof Frontiers in plant science, 2020-05, Vol.11, p.624, Article 624
issn 1664-462X
1664-462X
language eng
recordid cdi_proquest_miscellaneous_2412219340
source DOAJ Directory of Open Access Journals; PubMed Central Open Access; Web of Science - Science Citation Index Expanded - 2020<img src="https://exlibris-pub.s3.amazonaws.com/fromwos-v2.jpg" />; EZB-FREE-00999 freely available EZB journals; PubMed Central
subjects Amaranthaceae
Atriplex hortensis
Hi-C
Life Sciences & Biomedicine
orach
orphan crop
Plant Science
Plant Sciences
proximity-guided assembly
Science & Technology
title A Chromosome-Scale Assembly of the Garden Orach (Atriplex hortensis L.) Genome Using Oxford Nanopore Sequencing
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-14T04%3A02%3A26IST&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=A%20Chromosome-Scale%20Assembly%20of%20the%20Garden%20Orach%20(Atriplex%20hortensis%20L.)%20Genome%20Using%20Oxford%20Nanopore%20Sequencing&rft.jtitle=Frontiers%20in%20plant%20science&rft.au=Hunt,%20Spencer%20P.&rft.date=2020-05-25&rft.volume=11&rft.spage=624&rft.pages=624-&rft.artnum=624&rft.issn=1664-462X&rft.eissn=1664-462X&rft_id=info:doi/10.3389/fpls.2020.00624&rft_dat=%3Cproquest_doaj_%3E2412219340%3C/proquest_doaj_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2412219340&rft_id=info:pmid/32523593&rft_doaj_id=oai_doaj_org_article_8c5f65535ee84f8bb6ed9ea275768090&rfr_iscdi=true