The chemical compound ‘Heatin’ stimulates hypocotyl elongation and interferes with the Arabidopsis NIT1‐subfamily of nitrilases
SUMMARY Temperature passively affects biological processes involved in plant growth. Therefore, it is challenging to study the dedicated temperature signalling pathways that orchestrate thermomorphogenesis, a suite of elongation growth‐based adaptations that enhance leaf‐cooling capacity. We screene...
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Veröffentlicht in: | The Plant journal : for cell and molecular biology 2021-06, Vol.106 (6), p.1523-1540 |
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creator | Woude, Lennard Piotrowski, Markus Klaasse, Gruson Paulus, Judith K. Krahn, Daniel Ninck, Sabrina Kaschani, Farnusch Kaiser, Markus Novák, Ondřej Ljung, Karin Bulder, Suzanne Verk, Marcel Snoek, Basten L. Fiers, Martijn Martin, Nathaniel I. Hoorn, Renier A. L. Robert, Stéphanie Smeekens, Sjef Zanten, Martijn |
description | SUMMARY
Temperature passively affects biological processes involved in plant growth. Therefore, it is challenging to study the dedicated temperature signalling pathways that orchestrate thermomorphogenesis, a suite of elongation growth‐based adaptations that enhance leaf‐cooling capacity. We screened a chemical library for compounds that restored hypocotyl elongation in the pif4‐2–deficient mutant background at warm temperature conditions in Arabidopsis thaliana to identify modulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, containing 1‐iminomethyl‐2‐naphthol as a pharmacophore, was selected as an enhancer of elongation growth. We show that ARABIDOPSIS ALDEHYDE OXIDASES redundantly contribute to Heatin‐mediated hypocotyl elongation. Following a chemical proteomics approach, the members of the NITRILASE1‐subfamily of auxin biosynthesis enzymes were identified among the molecular targets of Heatin. Our data reveal that nitrilases are involved in promotion of hypocotyl elongation in response to high temperature and Heatin‐mediated hypocotyl elongation requires the NITRILASE1‐subfamily members, NIT1 and NIT2. Heatin inhibits NIT1‐subfamily enzymatic activity in vitro and the application of Heatin accordingly results in the accumulation of NIT1‐subfamily substrate indole‐3‐acetonitrile in vivo. However, levels of the NIT1‐subfamily product, bioactive auxin (indole‐3‐acetic acid), were also significantly increased. It is likely that the stimulation of hypocotyl elongation by Heatin might be independent of its observed interaction with NITRILASE1‐subfamily members. However, nitrilases may contribute to the Heatin response by stimulating indole‐3‐acetic acid biosynthesis in an indirect way. Heatin and its functional analogues present novel chemical entities for studying auxin biology.
Significance Statement
We identified the chemical compound Heatin that stimulates plant thermomorphogenesis and show that Heatin interferes with NIT1‐subfamily enzymatic activity and results in accumulation of auxin. The precise mechanism of action of Heatin requires further study but the investigations presented can contribute to knowledge‐based engineering of warm temperature‐resilient crops. Heatin is a promising agrochemical to steer plant growth and is a novel chemical tool for studying auxin biology. |
doi_str_mv | 10.1111/tpj.15250 |
format | Article |
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Temperature passively affects biological processes involved in plant growth. Therefore, it is challenging to study the dedicated temperature signalling pathways that orchestrate thermomorphogenesis, a suite of elongation growth‐based adaptations that enhance leaf‐cooling capacity. We screened a chemical library for compounds that restored hypocotyl elongation in the pif4‐2–deficient mutant background at warm temperature conditions in Arabidopsis thaliana to identify modulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, containing 1‐iminomethyl‐2‐naphthol as a pharmacophore, was selected as an enhancer of elongation growth. We show that ARABIDOPSIS ALDEHYDE OXIDASES redundantly contribute to Heatin‐mediated hypocotyl elongation. Following a chemical proteomics approach, the members of the NITRILASE1‐subfamily of auxin biosynthesis enzymes were identified among the molecular targets of Heatin. Our data reveal that nitrilases are involved in promotion of hypocotyl elongation in response to high temperature and Heatin‐mediated hypocotyl elongation requires the NITRILASE1‐subfamily members, NIT1 and NIT2. Heatin inhibits NIT1‐subfamily enzymatic activity in vitro and the application of Heatin accordingly results in the accumulation of NIT1‐subfamily substrate indole‐3‐acetonitrile in vivo. However, levels of the NIT1‐subfamily product, bioactive auxin (indole‐3‐acetic acid), were also significantly increased. It is likely that the stimulation of hypocotyl elongation by Heatin might be independent of its observed interaction with NITRILASE1‐subfamily members. However, nitrilases may contribute to the Heatin response by stimulating indole‐3‐acetic acid biosynthesis in an indirect way. Heatin and its functional analogues present novel chemical entities for studying auxin biology.
Significance Statement
We identified the chemical compound Heatin that stimulates plant thermomorphogenesis and show that Heatin interferes with NIT1‐subfamily enzymatic activity and results in accumulation of auxin. The precise mechanism of action of Heatin requires further study but the investigations presented can contribute to knowledge‐based engineering of warm temperature‐resilient crops. Heatin is a promising agrochemical to steer plant growth and is a novel chemical tool for studying auxin biology.</description><identifier>ISSN: 0960-7412</identifier><identifier>ISSN: 1365-313X</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.15250</identifier><identifier>PMID: 33768644</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>1‐iminomethyl‐2‐naphthol ; Acetic acid ; Acetonitrile ; Adaptation ; aldehyde oxidase ; Aldehyde Oxidase - genetics ; Aldehyde Oxidase - metabolism ; Aldehydes ; Aminohydrolases - genetics ; Aminohydrolases - metabolism ; Apomorphine - analogs & derivatives ; Apomorphine - pharmacology ; Arabidopsis ; Arabidopsis - drug effects ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Aromatic compounds ; Auxins ; Biological activity ; Biosynthesis ; Chemical compounds ; chemical genetics ; Deficient mutant ; Elongation ; Enzymatic activity ; Enzyme Inhibitors - administration & dosage ; Enzyme Inhibitors - chemistry ; Enzyme Inhibitors - pharmacology ; Gene Expression Regulation, Plant - drug effects ; Genetics ; Genetik ; Heatin ; Herbicides - pharmacology ; High temperature ; Hypocotyl - drug effects ; Hypocotyl - growth & development ; IAN ; Indole-3-acetonitrile ; Indoleacetic acid ; Indoleacetic Acids ; Modulators ; Molecular Structure ; Naphthol ; NIT1‐subfamily ; nitrilases ; Original ; Picloram - pharmacology ; PIF4 ; Plant growth ; Proteomics ; Signal transduction ; Structure-Activity Relationship ; Substrates ; Target recognition ; Temperature requirements ; thermomorphogenesis ; Transcriptome - drug effects</subject><ispartof>The Plant journal : for cell and molecular biology, 2021-06, Vol.106 (6), p.1523-1540</ispartof><rights>2021 The Authors. published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2021 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</rights><rights>2021. This article 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-c4820-98c3bfa695b424ad36c4c18ddf13aee16a9b2080224ff8d840900e76c78e0c403</citedby><cites>FETCH-LOGICAL-c4820-98c3bfa695b424ad36c4c18ddf13aee16a9b2080224ff8d840900e76c78e0c403</cites><orcidid>0000-0002-2810-7374</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%2Ftpj.15250$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.15250$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,552,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33768644$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://res.slu.se/id/publ/111877$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Woude, Lennard</creatorcontrib><creatorcontrib>Piotrowski, Markus</creatorcontrib><creatorcontrib>Klaasse, Gruson</creatorcontrib><creatorcontrib>Paulus, Judith K.</creatorcontrib><creatorcontrib>Krahn, Daniel</creatorcontrib><creatorcontrib>Ninck, Sabrina</creatorcontrib><creatorcontrib>Kaschani, Farnusch</creatorcontrib><creatorcontrib>Kaiser, Markus</creatorcontrib><creatorcontrib>Novák, Ondřej</creatorcontrib><creatorcontrib>Ljung, Karin</creatorcontrib><creatorcontrib>Bulder, Suzanne</creatorcontrib><creatorcontrib>Verk, Marcel</creatorcontrib><creatorcontrib>Snoek, Basten L.</creatorcontrib><creatorcontrib>Fiers, Martijn</creatorcontrib><creatorcontrib>Martin, Nathaniel I.</creatorcontrib><creatorcontrib>Hoorn, Renier A. L.</creatorcontrib><creatorcontrib>Robert, Stéphanie</creatorcontrib><creatorcontrib>Smeekens, Sjef</creatorcontrib><creatorcontrib>Zanten, Martijn</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><title>The chemical compound ‘Heatin’ stimulates hypocotyl elongation and interferes with the Arabidopsis NIT1‐subfamily of nitrilases</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>SUMMARY
Temperature passively affects biological processes involved in plant growth. Therefore, it is challenging to study the dedicated temperature signalling pathways that orchestrate thermomorphogenesis, a suite of elongation growth‐based adaptations that enhance leaf‐cooling capacity. We screened a chemical library for compounds that restored hypocotyl elongation in the pif4‐2–deficient mutant background at warm temperature conditions in Arabidopsis thaliana to identify modulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, containing 1‐iminomethyl‐2‐naphthol as a pharmacophore, was selected as an enhancer of elongation growth. We show that ARABIDOPSIS ALDEHYDE OXIDASES redundantly contribute to Heatin‐mediated hypocotyl elongation. Following a chemical proteomics approach, the members of the NITRILASE1‐subfamily of auxin biosynthesis enzymes were identified among the molecular targets of Heatin. Our data reveal that nitrilases are involved in promotion of hypocotyl elongation in response to high temperature and Heatin‐mediated hypocotyl elongation requires the NITRILASE1‐subfamily members, NIT1 and NIT2. Heatin inhibits NIT1‐subfamily enzymatic activity in vitro and the application of Heatin accordingly results in the accumulation of NIT1‐subfamily substrate indole‐3‐acetonitrile in vivo. However, levels of the NIT1‐subfamily product, bioactive auxin (indole‐3‐acetic acid), were also significantly increased. It is likely that the stimulation of hypocotyl elongation by Heatin might be independent of its observed interaction with NITRILASE1‐subfamily members. However, nitrilases may contribute to the Heatin response by stimulating indole‐3‐acetic acid biosynthesis in an indirect way. Heatin and its functional analogues present novel chemical entities for studying auxin biology.
Significance Statement
We identified the chemical compound Heatin that stimulates plant thermomorphogenesis and show that Heatin interferes with NIT1‐subfamily enzymatic activity and results in accumulation of auxin. The precise mechanism of action of Heatin requires further study but the investigations presented can contribute to knowledge‐based engineering of warm temperature‐resilient crops. Heatin is a promising agrochemical to steer plant growth and is a novel chemical tool for studying auxin biology.</description><subject>1‐iminomethyl‐2‐naphthol</subject><subject>Acetic acid</subject><subject>Acetonitrile</subject><subject>Adaptation</subject><subject>aldehyde oxidase</subject><subject>Aldehyde Oxidase - genetics</subject><subject>Aldehyde Oxidase - metabolism</subject><subject>Aldehydes</subject><subject>Aminohydrolases - genetics</subject><subject>Aminohydrolases - metabolism</subject><subject>Apomorphine - analogs & derivatives</subject><subject>Apomorphine - pharmacology</subject><subject>Arabidopsis</subject><subject>Arabidopsis - drug effects</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Aromatic compounds</subject><subject>Auxins</subject><subject>Biological activity</subject><subject>Biosynthesis</subject><subject>Chemical compounds</subject><subject>chemical genetics</subject><subject>Deficient mutant</subject><subject>Elongation</subject><subject>Enzymatic activity</subject><subject>Enzyme Inhibitors - administration & dosage</subject><subject>Enzyme Inhibitors - chemistry</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>Gene Expression Regulation, Plant - drug effects</subject><subject>Genetics</subject><subject>Genetik</subject><subject>Heatin</subject><subject>Herbicides - pharmacology</subject><subject>High temperature</subject><subject>Hypocotyl - drug effects</subject><subject>Hypocotyl - growth & development</subject><subject>IAN</subject><subject>Indole-3-acetonitrile</subject><subject>Indoleacetic acid</subject><subject>Indoleacetic Acids</subject><subject>Modulators</subject><subject>Molecular Structure</subject><subject>Naphthol</subject><subject>NIT1‐subfamily</subject><subject>nitrilases</subject><subject>Original</subject><subject>Picloram - pharmacology</subject><subject>PIF4</subject><subject>Plant growth</subject><subject>Proteomics</subject><subject>Signal transduction</subject><subject>Structure-Activity Relationship</subject><subject>Substrates</subject><subject>Target recognition</subject><subject>Temperature requirements</subject><subject>thermomorphogenesis</subject><subject>Transcriptome - drug effects</subject><issn>0960-7412</issn><issn>1365-313X</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><sourceid>D8T</sourceid><recordid>eNp1kT9v1DAYhy0Eokdh4AsgS0wMufpfHGdBqiqgRRUwHBKb5ThO41MSB9vhlO0Wdkb4evdJ8JFS0QEv7-Dn9_h9_QLwHKM1Tucsjts1zkmOHoAVpjzPKKZfHoIVKjnKCobJCXgSwhYhXFDOHoMTSgsuOGMr8H3TGqhb01utOqhdP7ppqOFh__PSqGiHw_4XDNH2U6eiCbCdR6ddnDtoOjfcJMINUKWAHaLxjfGJ2dnYwpi0515VtnZjsAF-uNrgw_5HmKpG9baboWvgYKO3nQomPAWPGtUF8-y2noLPb99sLi6z64_vri7OrzPNBEFZKTRNeV7mFSNM1ZRrprGo6wZTZQzmqqwIEogQ1jSiFgyVCJmC60IYpBmip2C9eMPOjFMlR2975WfplJWhmyrlj0UGI9O3iqJIgddLING9qbUZolfdvdz9m8G28sZ9k4JyhPOj4OWtwLuvkwlRbt3khzSkJHnOCCrygiTq1UJp70Lwprl7AaNjK1imFcs_K07si39buiP_7jQBZwuws52Z_2-Sm0_vF-Vvz_63lg</recordid><startdate>202106</startdate><enddate>202106</enddate><creator>Woude, Lennard</creator><creator>Piotrowski, Markus</creator><creator>Klaasse, Gruson</creator><creator>Paulus, Judith K.</creator><creator>Krahn, Daniel</creator><creator>Ninck, Sabrina</creator><creator>Kaschani, Farnusch</creator><creator>Kaiser, Markus</creator><creator>Novák, Ondřej</creator><creator>Ljung, Karin</creator><creator>Bulder, Suzanne</creator><creator>Verk, Marcel</creator><creator>Snoek, Basten L.</creator><creator>Fiers, Martijn</creator><creator>Martin, Nathaniel I.</creator><creator>Hoorn, Renier A. L.</creator><creator>Robert, Stéphanie</creator><creator>Smeekens, Sjef</creator><creator>Zanten, Martijn</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><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>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope><orcidid>https://orcid.org/0000-0002-2810-7374</orcidid></search><sort><creationdate>202106</creationdate><title>The chemical compound ‘Heatin’ stimulates hypocotyl elongation and interferes with the Arabidopsis NIT1‐subfamily of nitrilases</title><author>Woude, Lennard ; Piotrowski, Markus ; Klaasse, Gruson ; Paulus, Judith K. ; Krahn, Daniel ; Ninck, Sabrina ; Kaschani, Farnusch ; Kaiser, Markus ; Novák, Ondřej ; Ljung, Karin ; Bulder, Suzanne ; Verk, Marcel ; Snoek, Basten L. ; Fiers, Martijn ; Martin, Nathaniel I. ; Hoorn, Renier A. L. ; Robert, Stéphanie ; Smeekens, Sjef ; Zanten, Martijn</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4820-98c3bfa695b424ad36c4c18ddf13aee16a9b2080224ff8d840900e76c78e0c403</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>1‐iminomethyl‐2‐naphthol</topic><topic>Acetic acid</topic><topic>Acetonitrile</topic><topic>Adaptation</topic><topic>aldehyde oxidase</topic><topic>Aldehyde Oxidase - genetics</topic><topic>Aldehyde Oxidase - metabolism</topic><topic>Aldehydes</topic><topic>Aminohydrolases - genetics</topic><topic>Aminohydrolases - metabolism</topic><topic>Apomorphine - analogs & derivatives</topic><topic>Apomorphine - pharmacology</topic><topic>Arabidopsis</topic><topic>Arabidopsis - drug effects</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Aromatic compounds</topic><topic>Auxins</topic><topic>Biological activity</topic><topic>Biosynthesis</topic><topic>Chemical compounds</topic><topic>chemical genetics</topic><topic>Deficient mutant</topic><topic>Elongation</topic><topic>Enzymatic activity</topic><topic>Enzyme Inhibitors - administration & dosage</topic><topic>Enzyme Inhibitors - chemistry</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>Gene Expression Regulation, Plant - drug effects</topic><topic>Genetics</topic><topic>Genetik</topic><topic>Heatin</topic><topic>Herbicides - pharmacology</topic><topic>High temperature</topic><topic>Hypocotyl - drug effects</topic><topic>Hypocotyl - growth & development</topic><topic>IAN</topic><topic>Indole-3-acetonitrile</topic><topic>Indoleacetic acid</topic><topic>Indoleacetic Acids</topic><topic>Modulators</topic><topic>Molecular Structure</topic><topic>Naphthol</topic><topic>NIT1‐subfamily</topic><topic>nitrilases</topic><topic>Original</topic><topic>Picloram - pharmacology</topic><topic>PIF4</topic><topic>Plant growth</topic><topic>Proteomics</topic><topic>Signal transduction</topic><topic>Structure-Activity Relationship</topic><topic>Substrates</topic><topic>Target recognition</topic><topic>Temperature requirements</topic><topic>thermomorphogenesis</topic><topic>Transcriptome - drug effects</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Woude, Lennard</creatorcontrib><creatorcontrib>Piotrowski, Markus</creatorcontrib><creatorcontrib>Klaasse, Gruson</creatorcontrib><creatorcontrib>Paulus, Judith K.</creatorcontrib><creatorcontrib>Krahn, Daniel</creatorcontrib><creatorcontrib>Ninck, Sabrina</creatorcontrib><creatorcontrib>Kaschani, Farnusch</creatorcontrib><creatorcontrib>Kaiser, Markus</creatorcontrib><creatorcontrib>Novák, Ondřej</creatorcontrib><creatorcontrib>Ljung, Karin</creatorcontrib><creatorcontrib>Bulder, Suzanne</creatorcontrib><creatorcontrib>Verk, Marcel</creatorcontrib><creatorcontrib>Snoek, Basten L.</creatorcontrib><creatorcontrib>Fiers, Martijn</creatorcontrib><creatorcontrib>Martin, Nathaniel I.</creatorcontrib><creatorcontrib>Hoorn, Renier A. L.</creatorcontrib><creatorcontrib>Robert, Stéphanie</creatorcontrib><creatorcontrib>Smeekens, Sjef</creatorcontrib><creatorcontrib>Zanten, Martijn</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (Open Access Collection)</collection><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 & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Woude, Lennard</au><au>Piotrowski, Markus</au><au>Klaasse, Gruson</au><au>Paulus, Judith K.</au><au>Krahn, Daniel</au><au>Ninck, Sabrina</au><au>Kaschani, Farnusch</au><au>Kaiser, Markus</au><au>Novák, Ondřej</au><au>Ljung, Karin</au><au>Bulder, Suzanne</au><au>Verk, Marcel</au><au>Snoek, Basten L.</au><au>Fiers, Martijn</au><au>Martin, Nathaniel I.</au><au>Hoorn, Renier A. L.</au><au>Robert, Stéphanie</au><au>Smeekens, Sjef</au><au>Zanten, Martijn</au><aucorp>Sveriges lantbruksuniversitet</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The chemical compound ‘Heatin’ stimulates hypocotyl elongation and interferes with the Arabidopsis NIT1‐subfamily of nitrilases</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2021-06</date><risdate>2021</risdate><volume>106</volume><issue>6</issue><spage>1523</spage><epage>1540</epage><pages>1523-1540</pages><issn>0960-7412</issn><issn>1365-313X</issn><eissn>1365-313X</eissn><abstract>SUMMARY
Temperature passively affects biological processes involved in plant growth. Therefore, it is challenging to study the dedicated temperature signalling pathways that orchestrate thermomorphogenesis, a suite of elongation growth‐based adaptations that enhance leaf‐cooling capacity. We screened a chemical library for compounds that restored hypocotyl elongation in the pif4‐2–deficient mutant background at warm temperature conditions in Arabidopsis thaliana to identify modulators of thermomorphogenesis. The small aromatic compound ‘Heatin’, containing 1‐iminomethyl‐2‐naphthol as a pharmacophore, was selected as an enhancer of elongation growth. We show that ARABIDOPSIS ALDEHYDE OXIDASES redundantly contribute to Heatin‐mediated hypocotyl elongation. Following a chemical proteomics approach, the members of the NITRILASE1‐subfamily of auxin biosynthesis enzymes were identified among the molecular targets of Heatin. Our data reveal that nitrilases are involved in promotion of hypocotyl elongation in response to high temperature and Heatin‐mediated hypocotyl elongation requires the NITRILASE1‐subfamily members, NIT1 and NIT2. Heatin inhibits NIT1‐subfamily enzymatic activity in vitro and the application of Heatin accordingly results in the accumulation of NIT1‐subfamily substrate indole‐3‐acetonitrile in vivo. However, levels of the NIT1‐subfamily product, bioactive auxin (indole‐3‐acetic acid), were also significantly increased. It is likely that the stimulation of hypocotyl elongation by Heatin might be independent of its observed interaction with NITRILASE1‐subfamily members. However, nitrilases may contribute to the Heatin response by stimulating indole‐3‐acetic acid biosynthesis in an indirect way. Heatin and its functional analogues present novel chemical entities for studying auxin biology.
Significance Statement
We identified the chemical compound Heatin that stimulates plant thermomorphogenesis and show that Heatin interferes with NIT1‐subfamily enzymatic activity and results in accumulation of auxin. The precise mechanism of action of Heatin requires further study but the investigations presented can contribute to knowledge‐based engineering of warm temperature‐resilient crops. Heatin is a promising agrochemical to steer plant growth and is a novel chemical tool for studying auxin biology.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>33768644</pmid><doi>10.1111/tpj.15250</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-2810-7374</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0960-7412 |
ispartof | The Plant journal : for cell and molecular biology, 2021-06, Vol.106 (6), p.1523-1540 |
issn | 0960-7412 1365-313X 1365-313X |
language | eng |
recordid | cdi_swepub_primary_oai_slubar_slu_se_111877 |
source | MEDLINE; Wiley Journals; SWEPUB Freely available online; IngentaConnect Free/Open Access Journals; EZB-FREE-00999 freely available EZB journals; Wiley Online Library (Open Access Collection) |
subjects | 1‐iminomethyl‐2‐naphthol Acetic acid Acetonitrile Adaptation aldehyde oxidase Aldehyde Oxidase - genetics Aldehyde Oxidase - metabolism Aldehydes Aminohydrolases - genetics Aminohydrolases - metabolism Apomorphine - analogs & derivatives Apomorphine - pharmacology Arabidopsis Arabidopsis - drug effects Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Aromatic compounds Auxins Biological activity Biosynthesis Chemical compounds chemical genetics Deficient mutant Elongation Enzymatic activity Enzyme Inhibitors - administration & dosage Enzyme Inhibitors - chemistry Enzyme Inhibitors - pharmacology Gene Expression Regulation, Plant - drug effects Genetics Genetik Heatin Herbicides - pharmacology High temperature Hypocotyl - drug effects Hypocotyl - growth & development IAN Indole-3-acetonitrile Indoleacetic acid Indoleacetic Acids Modulators Molecular Structure Naphthol NIT1‐subfamily nitrilases Original Picloram - pharmacology PIF4 Plant growth Proteomics Signal transduction Structure-Activity Relationship Substrates Target recognition Temperature requirements thermomorphogenesis Transcriptome - drug effects |
title | The chemical compound ‘Heatin’ stimulates hypocotyl elongation and interferes with the Arabidopsis NIT1‐subfamily of nitrilases |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T00%3A45%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_swepu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20chemical%20compound%20%E2%80%98Heatin%E2%80%99%20stimulates%20hypocotyl%20elongation%20and%20interferes%20with%20the%20Arabidopsis%20NIT1%E2%80%90subfamily%20of%20nitrilases&rft.jtitle=The%20Plant%20journal%20:%20for%20cell%20and%20molecular%20biology&rft.au=Woude,%20Lennard&rft.aucorp=Sveriges%20lantbruksuniversitet&rft.date=2021-06&rft.volume=106&rft.issue=6&rft.spage=1523&rft.epage=1540&rft.pages=1523-1540&rft.issn=0960-7412&rft.eissn=1365-313X&rft_id=info:doi/10.1111/tpj.15250&rft_dat=%3Cproquest_swepu%3E2554207572%3C/proquest_swepu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2554207572&rft_id=info:pmid/33768644&rfr_iscdi=true |