Cross species multi-omics reveals cell wall sequestration and elevated global transcript abundance as mechanisms of boron tolerance in plants
• Boron toxicity is a world-wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants. • We employed a cross-species comparison between boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte r...
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Veröffentlicht in: | The New phytologist 2021-06, Vol.230 (5), p.1985-2000 |
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container_issue | 5 |
container_start_page | 1985 |
container_title | The New phytologist |
container_volume | 230 |
creator | Wang, Guannan DiTusa, Sandra Feuer Oh, Dong-Ha Herrmann, Achim D. Mendoza-Cozatl, David G. O’Neill, Malcolm A. Smith, Aaron P. Dassanayake, Maheshi |
description | • Boron toxicity is a world-wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants.
• We employed a cross-species comparison between boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula, and a multiomics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.
• Schrenkiella parvula maintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron. Schrenkiella parvula excludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyte S. parvula facilitates critical cellular processes while maintaining the pool of ribose-containing compounds that can bind with boric acid.
• The S. parvula transcriptome is pre-adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron-stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity. |
doi_str_mv | 10.1111/nph.17295 |
format | Article |
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• We employed a cross-species comparison between boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula, and a multiomics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.
• Schrenkiella parvula maintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron. Schrenkiella parvula excludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyte S. parvula facilitates critical cellular processes while maintaining the pool of ribose-containing compounds that can bind with boric acid.
• The S. parvula transcriptome is pre-adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron-stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.17295</identifier><identifier>PMID: 33629348</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Abundance ; Adaptation ; Adaptation, Physiological - genetics ; Arabidopsis ; Arabidopsis - genetics ; Boric acid ; Boron ; Boron - toxicity ; boron tolerance ; boron transporters ; Brassicaceae ; Cell Wall ; Cell walls ; Cytoplasm ; extremophyte ; Gene expression ; Metabolism ; Metabolomics ; Plant growth ; Ribose ; RNA metabolism ; Schrenkiella parvula ; Species ; stress‐preparedness ; Toxicity ; Transcription ; Transcriptomes ; Transcriptomics</subject><ispartof>The New phytologist, 2021-06, Vol.230 (5), p.1985-2000</ispartof><rights>2021 The Authors © 2021 New Phytologist Foundation</rights><rights>2021 The Authors © 2021 New Phytologist Foundation</rights><rights>2021 The Authors New Phytologist © 2021 New Phytologist Foundation.</rights><rights>Copyright © 2021 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5035-d80a0080fc99b63365b4dc93a2fb8efdaa3fed05bd84fe066ccda6006e057d53</citedby><cites>FETCH-LOGICAL-c5035-d80a0080fc99b63365b4dc93a2fb8efdaa3fed05bd84fe066ccda6006e057d53</cites><orcidid>0000-0001-5277-1921 ; 0000-0003-4422-6012 ; 0000-0003-3123-3731 ; 0000-0002-1739-075X ; 0000-0003-1526-9814 ; 0000-0002-9616-0791 ; 0000000315269814 ; 0000000296160791 ; 0000000344226012 ; 0000000331233731 ; 0000000152771921 ; 000000021739075X</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%2Fnph.17295$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.17295$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,1427,27903,27904,45553,45554,46387,46811</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33629348$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1787150$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Guannan</creatorcontrib><creatorcontrib>DiTusa, Sandra Feuer</creatorcontrib><creatorcontrib>Oh, Dong-Ha</creatorcontrib><creatorcontrib>Herrmann, Achim D.</creatorcontrib><creatorcontrib>Mendoza-Cozatl, David G.</creatorcontrib><creatorcontrib>O’Neill, Malcolm A.</creatorcontrib><creatorcontrib>Smith, Aaron P.</creatorcontrib><creatorcontrib>Dassanayake, Maheshi</creatorcontrib><title>Cross species multi-omics reveals cell wall sequestration and elevated global transcript abundance as mechanisms of boron tolerance in plants</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>• Boron toxicity is a world-wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants.
• We employed a cross-species comparison between boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula, and a multiomics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.
• Schrenkiella parvula maintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron. Schrenkiella parvula excludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyte S. parvula facilitates critical cellular processes while maintaining the pool of ribose-containing compounds that can bind with boric acid.
• The S. parvula transcriptome is pre-adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron-stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity.</description><subject>Abundance</subject><subject>Adaptation</subject><subject>Adaptation, Physiological - genetics</subject><subject>Arabidopsis</subject><subject>Arabidopsis - genetics</subject><subject>Boric acid</subject><subject>Boron</subject><subject>Boron - toxicity</subject><subject>boron tolerance</subject><subject>boron transporters</subject><subject>Brassicaceae</subject><subject>Cell Wall</subject><subject>Cell walls</subject><subject>Cytoplasm</subject><subject>extremophyte</subject><subject>Gene expression</subject><subject>Metabolism</subject><subject>Metabolomics</subject><subject>Plant growth</subject><subject>Ribose</subject><subject>RNA metabolism</subject><subject>Schrenkiella parvula</subject><subject>Species</subject><subject>stress‐preparedness</subject><subject>Toxicity</subject><subject>Transcription</subject><subject>Transcriptomes</subject><subject>Transcriptomics</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kc9u1DAQxi0EosvCgQcAWXCBQ9px_jjOsVoBRaqAQw_cLMeeUK8SO9hOqz4E74x30_aAhA_2wb_5Zr75CHnN4JTlc-bm61PWll3zhGxYzbtCsKp9SjYApSh4zX-ekBcx7gGga3j5nJxUFS-7qhYb8mcXfIw0zqgtRjotY7KFn6yONOANqjFSjeNIb1W-Iv5eMKagkvWOKmcojnijEhr6a_S9Gmn-c1EHOyeq-sUZ5TRSlXVRXytn4xSpH2jvQ65PfsRwBKyj86hcii_JsyG3xFf375Zcff50tbsoLr9_-bo7vyx0A1VTGAEKQMCgu67n2UzT10Z3lSqHXuBglKoGNND0RtQDAudaG8UBOELTmqbaknerrI_JyqhtyuNp7xzqJFkrWpbbbMmHFZqDP9qWk42HXSiHfomyrPMG604wkdH3_6B7vwSXHciyYV0JohQ8Ux9XSh9WHnCQc7CTCneSgTzkKHOO8phjZt_eKy79hOaRfAguA2crcGtHvPu_kvz24-JB8s1asY_Jh8eKsoUGgPHqL0pks4s</recordid><startdate>202106</startdate><enddate>202106</enddate><creator>Wang, Guannan</creator><creator>DiTusa, Sandra Feuer</creator><creator>Oh, Dong-Ha</creator><creator>Herrmann, Achim D.</creator><creator>Mendoza-Cozatl, David G.</creator><creator>O’Neill, Malcolm A.</creator><creator>Smith, Aaron P.</creator><creator>Dassanayake, Maheshi</creator><general>Wiley</general><general>Wiley Subscription Services, Inc</general><general>Wiley-Blackwell</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>7QO</scope><scope>7SN</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H95</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>OTOTI</scope><orcidid>https://orcid.org/0000-0001-5277-1921</orcidid><orcidid>https://orcid.org/0000-0003-4422-6012</orcidid><orcidid>https://orcid.org/0000-0003-3123-3731</orcidid><orcidid>https://orcid.org/0000-0002-1739-075X</orcidid><orcidid>https://orcid.org/0000-0003-1526-9814</orcidid><orcidid>https://orcid.org/0000-0002-9616-0791</orcidid><orcidid>https://orcid.org/0000000315269814</orcidid><orcidid>https://orcid.org/0000000296160791</orcidid><orcidid>https://orcid.org/0000000344226012</orcidid><orcidid>https://orcid.org/0000000331233731</orcidid><orcidid>https://orcid.org/0000000152771921</orcidid><orcidid>https://orcid.org/000000021739075X</orcidid></search><sort><creationdate>202106</creationdate><title>Cross species multi-omics reveals cell wall sequestration and elevated global transcript abundance as mechanisms of boron tolerance in plants</title><author>Wang, Guannan ; DiTusa, Sandra Feuer ; Oh, Dong-Ha ; Herrmann, Achim D. ; Mendoza-Cozatl, David G. ; O’Neill, Malcolm A. ; Smith, Aaron P. ; Dassanayake, Maheshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5035-d80a0080fc99b63365b4dc93a2fb8efdaa3fed05bd84fe066ccda6006e057d53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Abundance</topic><topic>Adaptation</topic><topic>Adaptation, Physiological - genetics</topic><topic>Arabidopsis</topic><topic>Arabidopsis - genetics</topic><topic>Boric acid</topic><topic>Boron</topic><topic>Boron - toxicity</topic><topic>boron tolerance</topic><topic>boron transporters</topic><topic>Brassicaceae</topic><topic>Cell Wall</topic><topic>Cell walls</topic><topic>Cytoplasm</topic><topic>extremophyte</topic><topic>Gene expression</topic><topic>Metabolism</topic><topic>Metabolomics</topic><topic>Plant growth</topic><topic>Ribose</topic><topic>RNA metabolism</topic><topic>Schrenkiella parvula</topic><topic>Species</topic><topic>stress‐preparedness</topic><topic>Toxicity</topic><topic>Transcription</topic><topic>Transcriptomes</topic><topic>Transcriptomics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Guannan</creatorcontrib><creatorcontrib>DiTusa, Sandra Feuer</creatorcontrib><creatorcontrib>Oh, Dong-Ha</creatorcontrib><creatorcontrib>Herrmann, Achim D.</creatorcontrib><creatorcontrib>Mendoza-Cozatl, David G.</creatorcontrib><creatorcontrib>O’Neill, Malcolm A.</creatorcontrib><creatorcontrib>Smith, Aaron P.</creatorcontrib><creatorcontrib>Dassanayake, Maheshi</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>Ecology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Engineering Research Database</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV</collection><jtitle>The New phytologist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Guannan</au><au>DiTusa, Sandra Feuer</au><au>Oh, Dong-Ha</au><au>Herrmann, Achim D.</au><au>Mendoza-Cozatl, David G.</au><au>O’Neill, Malcolm A.</au><au>Smith, Aaron P.</au><au>Dassanayake, Maheshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cross species multi-omics reveals cell wall sequestration and elevated global transcript abundance as mechanisms of boron tolerance in plants</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2021-06</date><risdate>2021</risdate><volume>230</volume><issue>5</issue><spage>1985</spage><epage>2000</epage><pages>1985-2000</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>• Boron toxicity is a world-wide problem for crops, yet we have a limited understanding of the genetic responses and adaptive mechanisms to this stress in plants.
• We employed a cross-species comparison between boron stress-sensitive Arabidopsis thaliana and its boron stress-tolerant extremophyte relative Schrenkiella parvula, and a multiomics approach integrating genomics, transcriptomics, metabolomics and ionomics to assess plant responses and adaptations to boron stress.
• Schrenkiella parvula maintains lower concentrations of total boron and free boric acid than Arabidopsis when grown with excess boron. Schrenkiella parvula excludes excess boron more efficiently than Arabidopsis, which we propose is partly driven by SpBOR5, a boron transporter that we functionally characterize in this study. Both species use cell walls as a partial sink for excess boron. When accumulated in the cytoplasm, excess boron appears to interrupt RNA metabolism. The extremophyte S. parvula facilitates critical cellular processes while maintaining the pool of ribose-containing compounds that can bind with boric acid.
• The S. parvula transcriptome is pre-adapted to boron toxicity. It exhibits substantial overlaps with the Arabidopsis boron-stress responsive transcriptome. Cell wall sequestration and increases in global transcript levels under excess boron conditions emerge as key mechanisms for sustaining plant growth under boron toxicity.</abstract><cop>England</cop><pub>Wiley</pub><pmid>33629348</pmid><doi>10.1111/nph.17295</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-5277-1921</orcidid><orcidid>https://orcid.org/0000-0003-4422-6012</orcidid><orcidid>https://orcid.org/0000-0003-3123-3731</orcidid><orcidid>https://orcid.org/0000-0002-1739-075X</orcidid><orcidid>https://orcid.org/0000-0003-1526-9814</orcidid><orcidid>https://orcid.org/0000-0002-9616-0791</orcidid><orcidid>https://orcid.org/0000000315269814</orcidid><orcidid>https://orcid.org/0000000296160791</orcidid><orcidid>https://orcid.org/0000000344226012</orcidid><orcidid>https://orcid.org/0000000331233731</orcidid><orcidid>https://orcid.org/0000000152771921</orcidid><orcidid>https://orcid.org/000000021739075X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Abundance Adaptation Adaptation, Physiological - genetics Arabidopsis Arabidopsis - genetics Boric acid Boron Boron - toxicity boron tolerance boron transporters Brassicaceae Cell Wall Cell walls Cytoplasm extremophyte Gene expression Metabolism Metabolomics Plant growth Ribose RNA metabolism Schrenkiella parvula Species stress‐preparedness Toxicity Transcription Transcriptomes Transcriptomics |
title | Cross species multi-omics reveals cell wall sequestration and elevated global transcript abundance as mechanisms of boron tolerance in plants |
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