Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize
Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induce...
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creator | Oliveira, Dyoni M. Mota, Thatiane R. Salatta, Fábio V. Sinzker, Renata C. Končitíková, Radka Kopečný, David Simister, Rachael Silva, Mariana Goeminne, Geert Morreel, Kris Rencoret, Jorge Gutiérrez, Ana Tryfona, Theodora Marchiosi, Rogério Dupree, Paul del Río, José C. Boerjan, Wout McQueen‐Mason, Simon J. Gomez, Leonardo D. Ferrarese‐Filho, Osvaldo dos Santos, Wanderley D. |
description | Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity.
We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. Based on these findings, we propose a model of grass cell wall remodeling in response to salinity. |
doi_str_mv | 10.1111/pce.13805 |
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We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. Based on these findings, we propose a model of grass cell wall remodeling in response to salinity.</description><identifier>ISSN: 0140-7791</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.13805</identifier><identifier>PMID: 32441772</identifier><language>eng</language><publisher>Chichester, UK: John Wiley & Sons, Ltd</publisher><subject>Abiotic stress ; Arabinoxylans ; Biosynthesis ; Carbohydrates ; cell wall ; Cell walls ; Cellulose ; Composition ; Corn ; Electrophoresis ; ferulic acid ; Gel electrophoresis ; Gene expression ; lignification ; Lignin ; Magnetic resonance spectroscopy ; Metabolism ; Metabolites ; Nitrobenzene ; NMR ; NMR spectroscopy ; Nuclear magnetic resonance ; Oxidation ; Phenolic compounds ; Phenols ; Plant extracts ; Plant roots ; Polymers ; Polysaccharides ; p‐coumaric acid ; Roots ; Saccharides ; Salinity ; Salinity effects ; Salts ; Seedlings ; Stress ; xylan ; Zea mays</subject><ispartof>Plant, cell and environment, 2020-09, Vol.43 (9), p.2172-2191</ispartof><rights>2020 John Wiley & Sons Ltd.</rights><rights>2020 John Wiley & Sons, Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3885-c3fa99a4b1a2fade5c2e50be12141d4bc92770f9e70843749ba4dc46fd6b7d8b3</citedby><cites>FETCH-LOGICAL-c3885-c3fa99a4b1a2fade5c2e50be12141d4bc92770f9e70843749ba4dc46fd6b7d8b3</cites><orcidid>0000-0002-8386-2524 ; 0000-0002-4309-4284 ; 0000-0002-6072-2860 ; 0000-0002-7537-3368 ; 0000-0003-1495-510X ; 0000-0001-9270-6286 ; 0000-0002-3040-6787 ; 0000-0002-4398-8982 ; 0000-0002-8823-9029 ; 0000-0001-6382-9447 ; 0000-0002-3477-4544 ; 0000-0003-2728-7331 ; 0000-0002-1618-3521 ; 0000-0002-4871-098X ; 0000-0002-6781-4768</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%2Fpce.13805$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpce.13805$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32441772$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Oliveira, Dyoni M.</creatorcontrib><creatorcontrib>Mota, Thatiane R.</creatorcontrib><creatorcontrib>Salatta, Fábio V.</creatorcontrib><creatorcontrib>Sinzker, Renata C.</creatorcontrib><creatorcontrib>Končitíková, Radka</creatorcontrib><creatorcontrib>Kopečný, David</creatorcontrib><creatorcontrib>Simister, Rachael</creatorcontrib><creatorcontrib>Silva, Mariana</creatorcontrib><creatorcontrib>Goeminne, Geert</creatorcontrib><creatorcontrib>Morreel, Kris</creatorcontrib><creatorcontrib>Rencoret, Jorge</creatorcontrib><creatorcontrib>Gutiérrez, Ana</creatorcontrib><creatorcontrib>Tryfona, Theodora</creatorcontrib><creatorcontrib>Marchiosi, Rogério</creatorcontrib><creatorcontrib>Dupree, Paul</creatorcontrib><creatorcontrib>del Río, José C.</creatorcontrib><creatorcontrib>Boerjan, Wout</creatorcontrib><creatorcontrib>McQueen‐Mason, Simon J.</creatorcontrib><creatorcontrib>Gomez, Leonardo D.</creatorcontrib><creatorcontrib>Ferrarese‐Filho, Osvaldo</creatorcontrib><creatorcontrib>dos Santos, Wanderley D.</creatorcontrib><title>Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity.
We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. Based on these findings, we propose a model of grass cell wall remodeling in response to salinity.</description><subject>Abiotic stress</subject><subject>Arabinoxylans</subject><subject>Biosynthesis</subject><subject>Carbohydrates</subject><subject>cell wall</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Composition</subject><subject>Corn</subject><subject>Electrophoresis</subject><subject>ferulic acid</subject><subject>Gel electrophoresis</subject><subject>Gene expression</subject><subject>lignification</subject><subject>Lignin</subject><subject>Magnetic resonance spectroscopy</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Nitrobenzene</subject><subject>NMR</subject><subject>NMR spectroscopy</subject><subject>Nuclear magnetic resonance</subject><subject>Oxidation</subject><subject>Phenolic compounds</subject><subject>Phenols</subject><subject>Plant extracts</subject><subject>Plant roots</subject><subject>Polymers</subject><subject>Polysaccharides</subject><subject>p‐coumaric acid</subject><subject>Roots</subject><subject>Saccharides</subject><subject>Salinity</subject><subject>Salinity effects</subject><subject>Salts</subject><subject>Seedlings</subject><subject>Stress</subject><subject>xylan</subject><subject>Zea mays</subject><issn>0140-7791</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNp1kcFq3DAQhkVpaTZJD3mBIuilgWwiWbJl91aWJA0E2kNzNrI03lWQJVdjE7ZPkUeOtrvNoVAdRprh45PQT8gZZ5c8r6vRwCUXNSvfkAUXVbkUTLK3ZMG4ZEulGn5EjhEfGcsD1bwnR6KQkitVLMjzCrynTzqXBEO04F1Y0zlYSBS1nyhOCRC_0LuAbr2ZkLowRWo2Oqxh19Ax-i1qkyfJWcAL2kOafdx6PbkYLqh36-B6Zw6tDpaOGwjRO0MHmHSXTzjsTIN2v-GUvOu1R_hw2E_Iw831z9W35f3327vV1_ulEXVd5trrptGy47rotYXSFFCyDnjBJbeyM02hFOsbUKyWQsmm09IaWfW26pStO3FCPu-9Y4q_ZsCpHRya_Bk6QJyxLSSrBFOlqDL66R_0Mc4p5NdlSpQVr_JVmTrfUyZFxAR9OyY36LRtOWt3MbU5pvZPTJn9eDDO3QD2lfybSwau9sCT87D9v6n9sbreK18Aogqegw</recordid><startdate>202009</startdate><enddate>202009</enddate><creator>Oliveira, Dyoni M.</creator><creator>Mota, Thatiane R.</creator><creator>Salatta, Fábio V.</creator><creator>Sinzker, Renata C.</creator><creator>Končitíková, Radka</creator><creator>Kopečný, David</creator><creator>Simister, Rachael</creator><creator>Silva, Mariana</creator><creator>Goeminne, Geert</creator><creator>Morreel, Kris</creator><creator>Rencoret, Jorge</creator><creator>Gutiérrez, Ana</creator><creator>Tryfona, Theodora</creator><creator>Marchiosi, Rogério</creator><creator>Dupree, Paul</creator><creator>del Río, José C.</creator><creator>Boerjan, Wout</creator><creator>McQueen‐Mason, Simon J.</creator><creator>Gomez, Leonardo D.</creator><creator>Ferrarese‐Filho, Osvaldo</creator><creator>dos Santos, Wanderley D.</creator><general>John Wiley & Sons, Ltd</general><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-8386-2524</orcidid><orcidid>https://orcid.org/0000-0002-4309-4284</orcidid><orcidid>https://orcid.org/0000-0002-6072-2860</orcidid><orcidid>https://orcid.org/0000-0002-7537-3368</orcidid><orcidid>https://orcid.org/0000-0003-1495-510X</orcidid><orcidid>https://orcid.org/0000-0001-9270-6286</orcidid><orcidid>https://orcid.org/0000-0002-3040-6787</orcidid><orcidid>https://orcid.org/0000-0002-4398-8982</orcidid><orcidid>https://orcid.org/0000-0002-8823-9029</orcidid><orcidid>https://orcid.org/0000-0001-6382-9447</orcidid><orcidid>https://orcid.org/0000-0002-3477-4544</orcidid><orcidid>https://orcid.org/0000-0003-2728-7331</orcidid><orcidid>https://orcid.org/0000-0002-1618-3521</orcidid><orcidid>https://orcid.org/0000-0002-4871-098X</orcidid><orcidid>https://orcid.org/0000-0002-6781-4768</orcidid></search><sort><creationdate>202009</creationdate><title>Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize</title><author>Oliveira, Dyoni M. ; Mota, Thatiane R. ; Salatta, Fábio V. ; Sinzker, Renata C. ; Končitíková, Radka ; Kopečný, David ; Simister, Rachael ; Silva, Mariana ; Goeminne, Geert ; Morreel, Kris ; Rencoret, Jorge ; Gutiérrez, Ana ; Tryfona, Theodora ; Marchiosi, Rogério ; Dupree, Paul ; del Río, José C. ; Boerjan, Wout ; McQueen‐Mason, Simon J. ; Gomez, Leonardo D. ; Ferrarese‐Filho, Osvaldo ; dos Santos, Wanderley D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3885-c3fa99a4b1a2fade5c2e50be12141d4bc92770f9e70843749ba4dc46fd6b7d8b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Abiotic stress</topic><topic>Arabinoxylans</topic><topic>Biosynthesis</topic><topic>Carbohydrates</topic><topic>cell wall</topic><topic>Cell walls</topic><topic>Cellulose</topic><topic>Composition</topic><topic>Corn</topic><topic>Electrophoresis</topic><topic>ferulic acid</topic><topic>Gel electrophoresis</topic><topic>Gene expression</topic><topic>lignification</topic><topic>Lignin</topic><topic>Magnetic resonance spectroscopy</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Nitrobenzene</topic><topic>NMR</topic><topic>NMR spectroscopy</topic><topic>Nuclear magnetic resonance</topic><topic>Oxidation</topic><topic>Phenolic compounds</topic><topic>Phenols</topic><topic>Plant extracts</topic><topic>Plant roots</topic><topic>Polymers</topic><topic>Polysaccharides</topic><topic>p‐coumaric acid</topic><topic>Roots</topic><topic>Saccharides</topic><topic>Salinity</topic><topic>Salinity effects</topic><topic>Salts</topic><topic>Seedlings</topic><topic>Stress</topic><topic>xylan</topic><topic>Zea mays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Oliveira, Dyoni M.</creatorcontrib><creatorcontrib>Mota, Thatiane R.</creatorcontrib><creatorcontrib>Salatta, Fábio V.</creatorcontrib><creatorcontrib>Sinzker, Renata C.</creatorcontrib><creatorcontrib>Končitíková, Radka</creatorcontrib><creatorcontrib>Kopečný, David</creatorcontrib><creatorcontrib>Simister, Rachael</creatorcontrib><creatorcontrib>Silva, Mariana</creatorcontrib><creatorcontrib>Goeminne, Geert</creatorcontrib><creatorcontrib>Morreel, Kris</creatorcontrib><creatorcontrib>Rencoret, Jorge</creatorcontrib><creatorcontrib>Gutiérrez, Ana</creatorcontrib><creatorcontrib>Tryfona, Theodora</creatorcontrib><creatorcontrib>Marchiosi, Rogério</creatorcontrib><creatorcontrib>Dupree, Paul</creatorcontrib><creatorcontrib>del Río, José C.</creatorcontrib><creatorcontrib>Boerjan, Wout</creatorcontrib><creatorcontrib>McQueen‐Mason, Simon J.</creatorcontrib><creatorcontrib>Gomez, Leonardo D.</creatorcontrib><creatorcontrib>Ferrarese‐Filho, Osvaldo</creatorcontrib><creatorcontrib>dos Santos, Wanderley D.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Environment Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Plant, cell and environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Oliveira, Dyoni M.</au><au>Mota, Thatiane R.</au><au>Salatta, Fábio V.</au><au>Sinzker, Renata C.</au><au>Končitíková, Radka</au><au>Kopečný, David</au><au>Simister, Rachael</au><au>Silva, Mariana</au><au>Goeminne, Geert</au><au>Morreel, Kris</au><au>Rencoret, Jorge</au><au>Gutiérrez, Ana</au><au>Tryfona, Theodora</au><au>Marchiosi, Rogério</au><au>Dupree, Paul</au><au>del Río, José C.</au><au>Boerjan, Wout</au><au>McQueen‐Mason, Simon J.</au><au>Gomez, Leonardo D.</au><au>Ferrarese‐Filho, Osvaldo</au><au>dos Santos, Wanderley D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize</atitle><jtitle>Plant, cell and environment</jtitle><addtitle>Plant Cell Environ</addtitle><date>2020-09</date><risdate>2020</risdate><volume>43</volume><issue>9</issue><spage>2172</spage><epage>2191</epage><pages>2172-2191</pages><issn>0140-7791</issn><eissn>1365-3040</eissn><abstract>Although cell wall polymers play important roles in the tolerance of plants to abiotic stress, the effects of salinity on cell wall composition and metabolism in grasses remain largely unexplored. Here, we conducted an in‐depth study of changes in cell wall composition and phenolic metabolism induced upon salinity in maize seedlings and plants. Cell wall characterization revealed that salt stress modulated the deposition of cellulose, matrix polysaccharides and lignin in seedling roots, plant roots and stems. The extraction and analysis of arabinoxylans by size‐exclusion chromatography, 2D‐NMR spectroscopy and carbohydrate gel electrophoresis showed a reduction of arabinoxylan content in salt‐stressed roots. Saponification and mild acid hydrolysis revealed that salinity also reduced the feruloylation of arabinoxylans in roots of seedlings and plants. Determination of lignin content and composition by nitrobenzene oxidation and 2D‐NMR confirmed the increased incorporation of syringyl units in lignin of maize roots. Salt stress also induced the expression of genes and the activity of enzymes enrolled in phenylpropanoid biosynthesis. The UHPLC–MS‐based metabolite profiling confirmed the modulation of phenolic profiling by salinity and the accumulation of ferulate and its derivatives 3‐ and 4‐O‐feruloyl quinate. In conclusion, we present a model for explaining cell wall remodeling in response to salinity.
We demonstrate the modulations induced by salt stress in the amounts of crystalline cellulose, matrix polysaccharides and lignin in roots of maize seedlings and roots, stems and leaves of maize plants. Salt stress reduced the feruloylation of arabinoxylan, increased the incorporation of syringyl lignin, and induced the biosynthesis and accumulation of ferulic acid and its derivatives. Based on these findings, we propose a model of grass cell wall remodeling in response to salinity.</abstract><cop>Chichester, UK</cop><pub>John Wiley & Sons, Ltd</pub><pmid>32441772</pmid><doi>10.1111/pce.13805</doi><tpages>20</tpages><orcidid>https://orcid.org/0000-0002-8386-2524</orcidid><orcidid>https://orcid.org/0000-0002-4309-4284</orcidid><orcidid>https://orcid.org/0000-0002-6072-2860</orcidid><orcidid>https://orcid.org/0000-0002-7537-3368</orcidid><orcidid>https://orcid.org/0000-0003-1495-510X</orcidid><orcidid>https://orcid.org/0000-0001-9270-6286</orcidid><orcidid>https://orcid.org/0000-0002-3040-6787</orcidid><orcidid>https://orcid.org/0000-0002-4398-8982</orcidid><orcidid>https://orcid.org/0000-0002-8823-9029</orcidid><orcidid>https://orcid.org/0000-0001-6382-9447</orcidid><orcidid>https://orcid.org/0000-0002-3477-4544</orcidid><orcidid>https://orcid.org/0000-0003-2728-7331</orcidid><orcidid>https://orcid.org/0000-0002-1618-3521</orcidid><orcidid>https://orcid.org/0000-0002-4871-098X</orcidid><orcidid>https://orcid.org/0000-0002-6781-4768</orcidid><oa>free_for_read</oa></addata></record> |
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source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Access via Wiley Online Library; Wiley Online Library (Open Access Collection) |
subjects | Abiotic stress Arabinoxylans Biosynthesis Carbohydrates cell wall Cell walls Cellulose Composition Corn Electrophoresis ferulic acid Gel electrophoresis Gene expression lignification Lignin Magnetic resonance spectroscopy Metabolism Metabolites Nitrobenzene NMR NMR spectroscopy Nuclear magnetic resonance Oxidation Phenolic compounds Phenols Plant extracts Plant roots Polymers Polysaccharides p‐coumaric acid Roots Saccharides Salinity Salinity effects Salts Seedlings Stress xylan Zea mays |
title | Cell wall remodeling under salt stress: Insights into changes in polysaccharides, feruloylation, lignification, and phenolic metabolism in maize |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-19T20%3A35%3A32IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Cell%20wall%20remodeling%20under%20salt%20stress:%20Insights%20into%20changes%20in%20polysaccharides,%20feruloylation,%20lignification,%20and%20phenolic%20metabolism%20in%20maize&rft.jtitle=Plant,%20cell%20and%20environment&rft.au=Oliveira,%20Dyoni%20M.&rft.date=2020-09&rft.volume=43&rft.issue=9&rft.spage=2172&rft.epage=2191&rft.pages=2172-2191&rft.issn=0140-7791&rft.eissn=1365-3040&rft_id=info:doi/10.1111/pce.13805&rft_dat=%3Cproquest_cross%3E2435616770%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2435616770&rft_id=info:pmid/32441772&rfr_iscdi=true |