Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF‐mediated auxin responses
Summary We investigated the interaction between osmotic stress and auxin signaling in leaf growth regulation. Therefore, we grew Arabidopsis thaliana seedlings on agar media supplemented with mannitol to impose osmotic stress and 1‐naphthaleneacetic acid (NAA), a synthetic auxin. We performed kinema...
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creator | Kalve, Shweta Sizani, Bulelani L. Markakis, Marios Nektarios Helsmoortel, Céline Vandeweyer, Geert Laukens, Kris Sommen, Manou Naulaerts, Stefan Vissenberg, Kris Prinsen, Els Beemster, Gerrit T. S. |
description | Summary
We investigated the interaction between osmotic stress and auxin signaling in leaf growth regulation. Therefore, we grew Arabidopsis thaliana seedlings on agar media supplemented with mannitol to impose osmotic stress and 1‐naphthaleneacetic acid (NAA), a synthetic auxin.
We performed kinematic analysis and flow‐cytometry to quantify the effects on cell division and expansion in the first leaf pair, determined the effects on auxin homeostasis and response (DR5::β‐glucuronidase), performed a next‐generation sequencing transcriptome analysis and investigated the response of auxin‐related mutants.
Mannitol inhibited cell division and expansion. NAA increased the effect of mannitol on cell division, but ameliorated its effect on expansion. In proliferating cells, NAA and mannitol increased free IAA concentrations at the cost of conjugated IAA and stimulated DR5 promotor activity. Transcriptome analysis shows a large overlap between NAA and osmotic stress‐induced changes, including upregulation of auxin synthesis, conjugation, transport and TRANSPORT INHIBITOR RESPONSE1 (TIR1) and AUXIN RESPONSE FACTOR (ARF) response genes, but downregulation of Aux/IAA response inhibitors. Consistently, arf7/19 double mutant lack the growth response to auxin and show a significantly reduced sensitivity to osmotic stress.
Our results show that osmotic stress inhibits cell division during leaf growth of A. thaliana at least partly by inducing the auxin transcriptional response. |
doi_str_mv | 10.1111/nph.16490 |
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We investigated the interaction between osmotic stress and auxin signaling in leaf growth regulation. Therefore, we grew Arabidopsis thaliana seedlings on agar media supplemented with mannitol to impose osmotic stress and 1‐naphthaleneacetic acid (NAA), a synthetic auxin.
We performed kinematic analysis and flow‐cytometry to quantify the effects on cell division and expansion in the first leaf pair, determined the effects on auxin homeostasis and response (DR5::β‐glucuronidase), performed a next‐generation sequencing transcriptome analysis and investigated the response of auxin‐related mutants.
Mannitol inhibited cell division and expansion. NAA increased the effect of mannitol on cell division, but ameliorated its effect on expansion. In proliferating cells, NAA and mannitol increased free IAA concentrations at the cost of conjugated IAA and stimulated DR5 promotor activity. Transcriptome analysis shows a large overlap between NAA and osmotic stress‐induced changes, including upregulation of auxin synthesis, conjugation, transport and TRANSPORT INHIBITOR RESPONSE1 (TIR1) and AUXIN RESPONSE FACTOR (ARF) response genes, but downregulation of Aux/IAA response inhibitors. Consistently, arf7/19 double mutant lack the growth response to auxin and show a significantly reduced sensitivity to osmotic stress.
Our results show that osmotic stress inhibits cell division during leaf growth of A. thaliana at least partly by inducing the auxin transcriptional response.</description><identifier>ISSN: 0028-646X</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.16490</identifier><identifier>PMID: 32077108</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; auxin ; Auxins ; Cell division ; cell division and expansion ; Conjugation ; Cost analysis ; Cytometry ; Gene expression ; Gene Expression Regulation, Plant ; Growth ; Homeostasis ; Indoleacetic Acids ; kinematic analysis ; leaf growth ; Leaves ; Mannitol ; Mutants ; Naphthaleneacetic acid ; Osmosis ; Osmotic Pressure ; Osmotic stress ; Plant Growth Regulators ; Plant Leaves - metabolism ; RNA‐sequencing ; Seedlings ; Transcription ; Transport</subject><ispartof>The New phytologist, 2020-06, Vol.226 (6), p.1766-1780</ispartof><rights>2020 The Authors. New Phytologist © 2020 New Phytologist Trust</rights><rights>2020 The Authors. New Phytologist © 2020 New Phytologist Trust.</rights><rights>Copyright © 2020 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4540-3e0da82fda93aca5297267b21f010ba6287d08b46d64d4b4d26ff48131e5a4a13</citedby><cites>FETCH-LOGICAL-c4540-3e0da82fda93aca5297267b21f010ba6287d08b46d64d4b4d26ff48131e5a4a13</cites><orcidid>0000-0002-8293-6851 ; 0000-0003-0292-2095 ; 0000-0002-1880-6374 ; 0000-0003-4320-1585 ; 0000-0002-8217-2564 ; 0000-0001-7180-7707 ; 0000-0002-2187-3770 ; 0000-0002-6262-6522 ; 0000-0001-6014-053X</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.16490$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.16490$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32077108$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kalve, Shweta</creatorcontrib><creatorcontrib>Sizani, Bulelani L.</creatorcontrib><creatorcontrib>Markakis, Marios Nektarios</creatorcontrib><creatorcontrib>Helsmoortel, Céline</creatorcontrib><creatorcontrib>Vandeweyer, Geert</creatorcontrib><creatorcontrib>Laukens, Kris</creatorcontrib><creatorcontrib>Sommen, Manou</creatorcontrib><creatorcontrib>Naulaerts, Stefan</creatorcontrib><creatorcontrib>Vissenberg, Kris</creatorcontrib><creatorcontrib>Prinsen, Els</creatorcontrib><creatorcontrib>Beemster, Gerrit T. S.</creatorcontrib><title>Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF‐mediated auxin responses</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary
We investigated the interaction between osmotic stress and auxin signaling in leaf growth regulation. Therefore, we grew Arabidopsis thaliana seedlings on agar media supplemented with mannitol to impose osmotic stress and 1‐naphthaleneacetic acid (NAA), a synthetic auxin.
We performed kinematic analysis and flow‐cytometry to quantify the effects on cell division and expansion in the first leaf pair, determined the effects on auxin homeostasis and response (DR5::β‐glucuronidase), performed a next‐generation sequencing transcriptome analysis and investigated the response of auxin‐related mutants.
Mannitol inhibited cell division and expansion. NAA increased the effect of mannitol on cell division, but ameliorated its effect on expansion. In proliferating cells, NAA and mannitol increased free IAA concentrations at the cost of conjugated IAA and stimulated DR5 promotor activity. Transcriptome analysis shows a large overlap between NAA and osmotic stress‐induced changes, including upregulation of auxin synthesis, conjugation, transport and TRANSPORT INHIBITOR RESPONSE1 (TIR1) and AUXIN RESPONSE FACTOR (ARF) response genes, but downregulation of Aux/IAA response inhibitors. Consistently, arf7/19 double mutant lack the growth response to auxin and show a significantly reduced sensitivity to osmotic stress.
Our results show that osmotic stress inhibits cell division during leaf growth of A. thaliana at least partly by inducing the auxin transcriptional response.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>auxin</subject><subject>Auxins</subject><subject>Cell division</subject><subject>cell division and expansion</subject><subject>Conjugation</subject><subject>Cost analysis</subject><subject>Cytometry</subject><subject>Gene expression</subject><subject>Gene Expression Regulation, Plant</subject><subject>Growth</subject><subject>Homeostasis</subject><subject>Indoleacetic Acids</subject><subject>kinematic analysis</subject><subject>leaf growth</subject><subject>Leaves</subject><subject>Mannitol</subject><subject>Mutants</subject><subject>Naphthaleneacetic acid</subject><subject>Osmosis</subject><subject>Osmotic Pressure</subject><subject>Osmotic stress</subject><subject>Plant Growth Regulators</subject><subject>Plant Leaves - metabolism</subject><subject>RNA‐sequencing</subject><subject>Seedlings</subject><subject>Transcription</subject><subject>Transport</subject><issn>0028-646X</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kMFu1DAQQC0EotvCgR-oLHGhh7S24zjJcbVqKdKKIgQSN2sSOxtXWTv1JCp74xP6jf2SuuzCAYm5zOXpaeYR8o6zc57mwo_9OVeyZi_IgktVZxXPy5dkwZioMiXVjyNyjHjLGKsLJV6To1ywsuSsWpDNDW7D5FqKU7SI1PneNW5COljo6CaG-6mnoaPLCI0zYUSHdOphcOCBNjtqfQ--dX5Dl1-vHn89bK1xMFlDYf7pPE3OMXi0-Ia86mBA-_awT8j3q8tvq-tsffPx02q5zlpZSJbllhmoRGegzqGFQtSlUGUjeMc4a0CJqjSsaqQyShrZSCNU18n0LrcFSOD5Cfmw944x3M0WJ7112NphAG_DjFrkRZ3XtSzKhL7_B70Nc_TpOi0kyyspSykSdban2hgQo-30GN0W4k5zpp_r61Rf_66f2NODcW5SiL_kn9wJuNgD926wu_-b9Ocv13vlExj7j4g</recordid><startdate>202006</startdate><enddate>202006</enddate><creator>Kalve, Shweta</creator><creator>Sizani, Bulelani L.</creator><creator>Markakis, Marios Nektarios</creator><creator>Helsmoortel, Céline</creator><creator>Vandeweyer, Geert</creator><creator>Laukens, Kris</creator><creator>Sommen, Manou</creator><creator>Naulaerts, Stefan</creator><creator>Vissenberg, Kris</creator><creator>Prinsen, Els</creator><creator>Beemster, Gerrit T. S.</creator><general>Wiley Subscription Services, Inc</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><orcidid>https://orcid.org/0000-0002-8293-6851</orcidid><orcidid>https://orcid.org/0000-0003-0292-2095</orcidid><orcidid>https://orcid.org/0000-0002-1880-6374</orcidid><orcidid>https://orcid.org/0000-0003-4320-1585</orcidid><orcidid>https://orcid.org/0000-0002-8217-2564</orcidid><orcidid>https://orcid.org/0000-0001-7180-7707</orcidid><orcidid>https://orcid.org/0000-0002-2187-3770</orcidid><orcidid>https://orcid.org/0000-0002-6262-6522</orcidid><orcidid>https://orcid.org/0000-0001-6014-053X</orcidid></search><sort><creationdate>202006</creationdate><title>Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF‐mediated auxin responses</title><author>Kalve, Shweta ; Sizani, Bulelani L. ; Markakis, Marios Nektarios ; Helsmoortel, Céline ; Vandeweyer, Geert ; Laukens, Kris ; Sommen, Manou ; Naulaerts, Stefan ; Vissenberg, Kris ; Prinsen, Els ; Beemster, Gerrit T. S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4540-3e0da82fda93aca5297267b21f010ba6287d08b46d64d4b4d26ff48131e5a4a13</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>auxin</topic><topic>Auxins</topic><topic>Cell division</topic><topic>cell division and expansion</topic><topic>Conjugation</topic><topic>Cost analysis</topic><topic>Cytometry</topic><topic>Gene expression</topic><topic>Gene Expression Regulation, Plant</topic><topic>Growth</topic><topic>Homeostasis</topic><topic>Indoleacetic Acids</topic><topic>kinematic analysis</topic><topic>leaf growth</topic><topic>Leaves</topic><topic>Mannitol</topic><topic>Mutants</topic><topic>Naphthaleneacetic acid</topic><topic>Osmosis</topic><topic>Osmotic Pressure</topic><topic>Osmotic stress</topic><topic>Plant Growth Regulators</topic><topic>Plant Leaves - metabolism</topic><topic>RNA‐sequencing</topic><topic>Seedlings</topic><topic>Transcription</topic><topic>Transport</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kalve, Shweta</creatorcontrib><creatorcontrib>Sizani, Bulelani L.</creatorcontrib><creatorcontrib>Markakis, Marios Nektarios</creatorcontrib><creatorcontrib>Helsmoortel, Céline</creatorcontrib><creatorcontrib>Vandeweyer, Geert</creatorcontrib><creatorcontrib>Laukens, Kris</creatorcontrib><creatorcontrib>Sommen, Manou</creatorcontrib><creatorcontrib>Naulaerts, Stefan</creatorcontrib><creatorcontrib>Vissenberg, Kris</creatorcontrib><creatorcontrib>Prinsen, Els</creatorcontrib><creatorcontrib>Beemster, Gerrit T. 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S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF‐mediated auxin responses</atitle><jtitle>The New phytologist</jtitle><addtitle>New Phytol</addtitle><date>2020-06</date><risdate>2020</risdate><volume>226</volume><issue>6</issue><spage>1766</spage><epage>1780</epage><pages>1766-1780</pages><issn>0028-646X</issn><eissn>1469-8137</eissn><abstract>Summary
We investigated the interaction between osmotic stress and auxin signaling in leaf growth regulation. Therefore, we grew Arabidopsis thaliana seedlings on agar media supplemented with mannitol to impose osmotic stress and 1‐naphthaleneacetic acid (NAA), a synthetic auxin.
We performed kinematic analysis and flow‐cytometry to quantify the effects on cell division and expansion in the first leaf pair, determined the effects on auxin homeostasis and response (DR5::β‐glucuronidase), performed a next‐generation sequencing transcriptome analysis and investigated the response of auxin‐related mutants.
Mannitol inhibited cell division and expansion. NAA increased the effect of mannitol on cell division, but ameliorated its effect on expansion. In proliferating cells, NAA and mannitol increased free IAA concentrations at the cost of conjugated IAA and stimulated DR5 promotor activity. Transcriptome analysis shows a large overlap between NAA and osmotic stress‐induced changes, including upregulation of auxin synthesis, conjugation, transport and TRANSPORT INHIBITOR RESPONSE1 (TIR1) and AUXIN RESPONSE FACTOR (ARF) response genes, but downregulation of Aux/IAA response inhibitors. Consistently, arf7/19 double mutant lack the growth response to auxin and show a significantly reduced sensitivity to osmotic stress.
Our results show that osmotic stress inhibits cell division during leaf growth of A. thaliana at least partly by inducing the auxin transcriptional response.</abstract><cop>England</cop><pub>Wiley Subscription Services, Inc</pub><pmid>32077108</pmid><doi>10.1111/nph.16490</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-8293-6851</orcidid><orcidid>https://orcid.org/0000-0003-0292-2095</orcidid><orcidid>https://orcid.org/0000-0002-1880-6374</orcidid><orcidid>https://orcid.org/0000-0003-4320-1585</orcidid><orcidid>https://orcid.org/0000-0002-8217-2564</orcidid><orcidid>https://orcid.org/0000-0001-7180-7707</orcidid><orcidid>https://orcid.org/0000-0002-2187-3770</orcidid><orcidid>https://orcid.org/0000-0002-6262-6522</orcidid><orcidid>https://orcid.org/0000-0001-6014-053X</orcidid><oa>free_for_read</oa></addata></record> |
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source | Jstor Complete Legacy; Wiley Free Content; MEDLINE; Wiley Online Library Journals Frontfile Complete; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals |
subjects | Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana auxin Auxins Cell division cell division and expansion Conjugation Cost analysis Cytometry Gene expression Gene Expression Regulation, Plant Growth Homeostasis Indoleacetic Acids kinematic analysis leaf growth Leaves Mannitol Mutants Naphthaleneacetic acid Osmosis Osmotic Pressure Osmotic stress Plant Growth Regulators Plant Leaves - metabolism RNA‐sequencing Seedlings Transcription Transport |
title | Osmotic stress inhibits leaf growth of Arabidopsis thaliana by enhancing ARF‐mediated auxin responses |
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