Learning from methylomes: epigenomic correlates of Populus balsamifera traits based on deep learning models of natural DNA methylation

Summary Epigenomes have remarkable potential for the estimation of plant traits. This study tested the hypothesis that natural variation in DNA methylation can be used to estimate industrially important traits in a genetically diverse population of Populus balsamifera L. (balsam poplar) trees grown...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Plant biotechnology journal 2020-06, Vol.18 (6), p.1361-1375
Hauptverfasser: Champigny, Marc J., Unda, Faride, Skyba, Oleksandr, Soolanayakanahally, Raju Y., Mansfield, Shawn D., Campbell, Malcolm M.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1375
container_issue 6
container_start_page 1361
container_title Plant biotechnology journal
container_volume 18
creator Champigny, Marc J.
Unda, Faride
Skyba, Oleksandr
Soolanayakanahally, Raju Y.
Mansfield, Shawn D.
Campbell, Malcolm M.
description Summary Epigenomes have remarkable potential for the estimation of plant traits. This study tested the hypothesis that natural variation in DNA methylation can be used to estimate industrially important traits in a genetically diverse population of Populus balsamifera L. (balsam poplar) trees grown at two common garden sites. Statistical learning experiments enabled by deep learning models revealed that plant traits in novel genotypes can be modelled transparently using small numbers of methylated DNA predictors. Using this approach, tissue type, a nonheritable attribute, from which DNA methylomes were derived was assigned, and provenance, a purely heritable trait and an element of population structure, was determined. Significant proportions of phenotypic variance in quantitative wood traits, including total biomass (57.5%), wood density (40.9%), soluble lignin (25.3%) and cell wall carbohydrate (mannose: 44.8%) contents, were also explained from natural variation in DNA methylation. Modelling plant traits using DNA methylation can capture tissue‐specific epigenetic mechanisms underlying plant phenotypes in natural environments. DNA methylation‐based models offer new insight into natural epigenetic influence on plants and can be used as a strategy to validate the identity, provenance or quality of agroforestry products.
doi_str_mv 10.1111/pbi.13299
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7207000</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2315974011</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4439-76d319f3edefbd93f22cec9a34720a7f377396fa75ff0844301ac29d82dd4ce53</originalsourceid><addsrcrecordid>eNp1kc9uVCEUh2-Mja3VhS9gSNzoYlr-3cvgwqRWbZtMtAtdEwYOUxou3MK9mnkBn1umM51YE9lA4Dsfv5PTNK8IPiF1nQ5Lf0IYlfJJc0R4J2aia-nT_Znzw-Z5KbcYU9K13bPmkBHB6Zywo-b3AnSOPq6Qy6lHPYw365B6KO8RDH4FMfXeIJNyhqBHKCg5dJ2GKUwFLXUouvcOskZj1n7cXBWwKEVkAQYUHtx9shDua6Mep6wD-vT1bPeZHn2KL5oDV23wcrcfNz--fP5-fjlbfLu4Oj9bzAznTNZeLCPSMbDgllYyR6kBIzXjgmItHBOCyc5p0TqH57UEE22otHNqLTfQsuPmw9Y7TMserIFYgwc1ZN_rvFZJe_X4JfobtUo_VfULjHEVvN0JcrqboIyq98VACDpCmoqijLRScExIRd_8g96mKcfanqIcd1xILDeJ3m0pk1MpGdw-DMFqM11Vp6vup1vZ13-n35MP46zA6Rb45QOs_29S1x-vtso_a_Sx1A</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2406479095</pqid></control><display><type>article</type><title>Learning from methylomes: epigenomic correlates of Populus balsamifera traits based on deep learning models of natural DNA methylation</title><source>DOAJ Directory of Open Access Journals</source><source>Wiley Online Library Journals Frontfile Complete</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Wiley Online Library Open Access</source><creator>Champigny, Marc J. ; Unda, Faride ; Skyba, Oleksandr ; Soolanayakanahally, Raju Y. ; Mansfield, Shawn D. ; Campbell, Malcolm M.</creator><creatorcontrib>Champigny, Marc J. ; Unda, Faride ; Skyba, Oleksandr ; Soolanayakanahally, Raju Y. ; Mansfield, Shawn D. ; Campbell, Malcolm M.</creatorcontrib><description>Summary Epigenomes have remarkable potential for the estimation of plant traits. This study tested the hypothesis that natural variation in DNA methylation can be used to estimate industrially important traits in a genetically diverse population of Populus balsamifera L. (balsam poplar) trees grown at two common garden sites. Statistical learning experiments enabled by deep learning models revealed that plant traits in novel genotypes can be modelled transparently using small numbers of methylated DNA predictors. Using this approach, tissue type, a nonheritable attribute, from which DNA methylomes were derived was assigned, and provenance, a purely heritable trait and an element of population structure, was determined. Significant proportions of phenotypic variance in quantitative wood traits, including total biomass (57.5%), wood density (40.9%), soluble lignin (25.3%) and cell wall carbohydrate (mannose: 44.8%) contents, were also explained from natural variation in DNA methylation. Modelling plant traits using DNA methylation can capture tissue‐specific epigenetic mechanisms underlying plant phenotypes in natural environments. DNA methylation‐based models offer new insight into natural epigenetic influence on plants and can be used as a strategy to validate the identity, provenance or quality of agroforestry products.</description><identifier>ISSN: 1467-7644</identifier><identifier>EISSN: 1467-7652</identifier><identifier>DOI: 10.1111/pbi.13299</identifier><identifier>PMID: 31742813</identifier><language>eng</language><publisher>England: John Wiley &amp; Sons, Inc</publisher><subject>Agriculture ; Agroforestry ; authentication ; Biomass ; Carbohydrates ; Cell walls ; Deep learning ; Deoxyribonucleic acid ; DNA ; DNA methylation ; Epigenetics ; epigenomics ; Gardens &amp; gardening ; Genomes ; Genomics ; Genotype &amp; phenotype ; Genotypes ; Hardwoods ; Lignin ; Machine learning ; Mannose ; Natural environment ; Neural networks ; Phenotypes ; Phenotypic variations ; Plant diseases ; Poplar ; Population genetics ; Population structure ; Populus balsamifera ; Provenance ; Statistical analysis ; Trees ; Wood</subject><ispartof>Plant biotechnology journal, 2020-06, Vol.18 (6), p.1361-1375</ispartof><rights>2019 The Authors. published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley &amp; Sons Ltd.</rights><rights>2019 The Authors. Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley &amp; Sons Ltd.</rights><rights>2020. 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-c4439-76d319f3edefbd93f22cec9a34720a7f377396fa75ff0844301ac29d82dd4ce53</citedby><cites>FETCH-LOGICAL-c4439-76d319f3edefbd93f22cec9a34720a7f377396fa75ff0844301ac29d82dd4ce53</cites><orcidid>0000-0002-0175-554X ; 0000-0002-1396-6651</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpbi.13299$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpbi.13299$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,860,881,1411,11542,27903,27904,45553,45554,46030,46454</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31742813$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Champigny, Marc J.</creatorcontrib><creatorcontrib>Unda, Faride</creatorcontrib><creatorcontrib>Skyba, Oleksandr</creatorcontrib><creatorcontrib>Soolanayakanahally, Raju Y.</creatorcontrib><creatorcontrib>Mansfield, Shawn D.</creatorcontrib><creatorcontrib>Campbell, Malcolm M.</creatorcontrib><title>Learning from methylomes: epigenomic correlates of Populus balsamifera traits based on deep learning models of natural DNA methylation</title><title>Plant biotechnology journal</title><addtitle>Plant Biotechnol J</addtitle><description>Summary Epigenomes have remarkable potential for the estimation of plant traits. This study tested the hypothesis that natural variation in DNA methylation can be used to estimate industrially important traits in a genetically diverse population of Populus balsamifera L. (balsam poplar) trees grown at two common garden sites. Statistical learning experiments enabled by deep learning models revealed that plant traits in novel genotypes can be modelled transparently using small numbers of methylated DNA predictors. Using this approach, tissue type, a nonheritable attribute, from which DNA methylomes were derived was assigned, and provenance, a purely heritable trait and an element of population structure, was determined. Significant proportions of phenotypic variance in quantitative wood traits, including total biomass (57.5%), wood density (40.9%), soluble lignin (25.3%) and cell wall carbohydrate (mannose: 44.8%) contents, were also explained from natural variation in DNA methylation. Modelling plant traits using DNA methylation can capture tissue‐specific epigenetic mechanisms underlying plant phenotypes in natural environments. DNA methylation‐based models offer new insight into natural epigenetic influence on plants and can be used as a strategy to validate the identity, provenance or quality of agroforestry products.</description><subject>Agriculture</subject><subject>Agroforestry</subject><subject>authentication</subject><subject>Biomass</subject><subject>Carbohydrates</subject><subject>Cell walls</subject><subject>Deep learning</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA methylation</subject><subject>Epigenetics</subject><subject>epigenomics</subject><subject>Gardens &amp; gardening</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Genotype &amp; phenotype</subject><subject>Genotypes</subject><subject>Hardwoods</subject><subject>Lignin</subject><subject>Machine learning</subject><subject>Mannose</subject><subject>Natural environment</subject><subject>Neural networks</subject><subject>Phenotypes</subject><subject>Phenotypic variations</subject><subject>Plant diseases</subject><subject>Poplar</subject><subject>Population genetics</subject><subject>Population structure</subject><subject>Populus balsamifera</subject><subject>Provenance</subject><subject>Statistical analysis</subject><subject>Trees</subject><subject>Wood</subject><issn>1467-7644</issn><issn>1467-7652</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp1kc9uVCEUh2-Mja3VhS9gSNzoYlr-3cvgwqRWbZtMtAtdEwYOUxou3MK9mnkBn1umM51YE9lA4Dsfv5PTNK8IPiF1nQ5Lf0IYlfJJc0R4J2aia-nT_Znzw-Z5KbcYU9K13bPmkBHB6Zywo-b3AnSOPq6Qy6lHPYw365B6KO8RDH4FMfXeIJNyhqBHKCg5dJ2GKUwFLXUouvcOskZj1n7cXBWwKEVkAQYUHtx9shDua6Mep6wD-vT1bPeZHn2KL5oDV23wcrcfNz--fP5-fjlbfLu4Oj9bzAznTNZeLCPSMbDgllYyR6kBIzXjgmItHBOCyc5p0TqH57UEE22otHNqLTfQsuPmw9Y7TMserIFYgwc1ZN_rvFZJe_X4JfobtUo_VfULjHEVvN0JcrqboIyq98VACDpCmoqijLRScExIRd_8g96mKcfanqIcd1xILDeJ3m0pk1MpGdw-DMFqM11Vp6vup1vZ13-n35MP46zA6Rb45QOs_29S1x-vtso_a_Sx1A</recordid><startdate>202006</startdate><enddate>202006</enddate><creator>Champigny, Marc J.</creator><creator>Unda, Faride</creator><creator>Skyba, Oleksandr</creator><creator>Soolanayakanahally, Raju Y.</creator><creator>Mansfield, Shawn D.</creator><creator>Campbell, Malcolm M.</creator><general>John Wiley &amp; Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>L6V</scope><scope>LK8</scope><scope>M7P</scope><scope>M7S</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-0175-554X</orcidid><orcidid>https://orcid.org/0000-0002-1396-6651</orcidid></search><sort><creationdate>202006</creationdate><title>Learning from methylomes: epigenomic correlates of Populus balsamifera traits based on deep learning models of natural DNA methylation</title><author>Champigny, Marc J. ; Unda, Faride ; Skyba, Oleksandr ; Soolanayakanahally, Raju Y. ; Mansfield, Shawn D. ; Campbell, Malcolm M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4439-76d319f3edefbd93f22cec9a34720a7f377396fa75ff0844301ac29d82dd4ce53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Agriculture</topic><topic>Agroforestry</topic><topic>authentication</topic><topic>Biomass</topic><topic>Carbohydrates</topic><topic>Cell walls</topic><topic>Deep learning</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA methylation</topic><topic>Epigenetics</topic><topic>epigenomics</topic><topic>Gardens &amp; gardening</topic><topic>Genomes</topic><topic>Genomics</topic><topic>Genotype &amp; phenotype</topic><topic>Genotypes</topic><topic>Hardwoods</topic><topic>Lignin</topic><topic>Machine learning</topic><topic>Mannose</topic><topic>Natural environment</topic><topic>Neural networks</topic><topic>Phenotypes</topic><topic>Phenotypic variations</topic><topic>Plant diseases</topic><topic>Poplar</topic><topic>Population genetics</topic><topic>Population structure</topic><topic>Populus balsamifera</topic><topic>Provenance</topic><topic>Statistical analysis</topic><topic>Trees</topic><topic>Wood</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Champigny, Marc J.</creatorcontrib><creatorcontrib>Unda, Faride</creatorcontrib><creatorcontrib>Skyba, Oleksandr</creatorcontrib><creatorcontrib>Soolanayakanahally, Raju Y.</creatorcontrib><creatorcontrib>Mansfield, Shawn D.</creatorcontrib><creatorcontrib>Campbell, Malcolm M.</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Wiley Free Content</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Materials Science &amp; Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant biotechnology journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Champigny, Marc J.</au><au>Unda, Faride</au><au>Skyba, Oleksandr</au><au>Soolanayakanahally, Raju Y.</au><au>Mansfield, Shawn D.</au><au>Campbell, Malcolm M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Learning from methylomes: epigenomic correlates of Populus balsamifera traits based on deep learning models of natural DNA methylation</atitle><jtitle>Plant biotechnology journal</jtitle><addtitle>Plant Biotechnol J</addtitle><date>2020-06</date><risdate>2020</risdate><volume>18</volume><issue>6</issue><spage>1361</spage><epage>1375</epage><pages>1361-1375</pages><issn>1467-7644</issn><eissn>1467-7652</eissn><abstract>Summary Epigenomes have remarkable potential for the estimation of plant traits. This study tested the hypothesis that natural variation in DNA methylation can be used to estimate industrially important traits in a genetically diverse population of Populus balsamifera L. (balsam poplar) trees grown at two common garden sites. Statistical learning experiments enabled by deep learning models revealed that plant traits in novel genotypes can be modelled transparently using small numbers of methylated DNA predictors. Using this approach, tissue type, a nonheritable attribute, from which DNA methylomes were derived was assigned, and provenance, a purely heritable trait and an element of population structure, was determined. Significant proportions of phenotypic variance in quantitative wood traits, including total biomass (57.5%), wood density (40.9%), soluble lignin (25.3%) and cell wall carbohydrate (mannose: 44.8%) contents, were also explained from natural variation in DNA methylation. Modelling plant traits using DNA methylation can capture tissue‐specific epigenetic mechanisms underlying plant phenotypes in natural environments. DNA methylation‐based models offer new insight into natural epigenetic influence on plants and can be used as a strategy to validate the identity, provenance or quality of agroforestry products.</abstract><cop>England</cop><pub>John Wiley &amp; Sons, Inc</pub><pmid>31742813</pmid><doi>10.1111/pbi.13299</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-0175-554X</orcidid><orcidid>https://orcid.org/0000-0002-1396-6651</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1467-7644
ispartof Plant biotechnology journal, 2020-06, Vol.18 (6), p.1361-1375
issn 1467-7644
1467-7652
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7207000
source DOAJ Directory of Open Access Journals; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Wiley Online Library Open Access
subjects Agriculture
Agroforestry
authentication
Biomass
Carbohydrates
Cell walls
Deep learning
Deoxyribonucleic acid
DNA
DNA methylation
Epigenetics
epigenomics
Gardens & gardening
Genomes
Genomics
Genotype & phenotype
Genotypes
Hardwoods
Lignin
Machine learning
Mannose
Natural environment
Neural networks
Phenotypes
Phenotypic variations
Plant diseases
Poplar
Population genetics
Population structure
Populus balsamifera
Provenance
Statistical analysis
Trees
Wood
title Learning from methylomes: epigenomic correlates of Populus balsamifera traits based on deep learning models of natural DNA methylation
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-23T14%3A09%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Learning%20from%20methylomes:%20epigenomic%20correlates%20of%20Populus%20balsamifera%20traits%20based%20on%20deep%20learning%20models%20of%20natural%20DNA%20methylation&rft.jtitle=Plant%20biotechnology%20journal&rft.au=Champigny,%20Marc%20J.&rft.date=2020-06&rft.volume=18&rft.issue=6&rft.spage=1361&rft.epage=1375&rft.pages=1361-1375&rft.issn=1467-7644&rft.eissn=1467-7652&rft_id=info:doi/10.1111/pbi.13299&rft_dat=%3Cproquest_pubme%3E2315974011%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2406479095&rft_id=info:pmid/31742813&rfr_iscdi=true