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Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis
The biosynthesis of the recently identified novel class of plant hormones, strigolactones, is up-regulated upon phosphate deficiency in many plant species. It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates h...
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Published in: | Plant physiology (Bethesda) 2011-02, Vol.155 (2), p.974-987 |
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creator | Kohlen, Wouter Charnikhova, Tatsiana Liu, Qing Bours, Ralph Domagalska, Malgorzata A Beguerie, Sebastien Verstappen, Francel Leyser, Ottoline Bouwmeester, Harro Ruyter-Spira, Carolien |
description | The biosynthesis of the recently identified novel class of plant hormones, strigolactones, is up-regulated upon phosphate deficiency in many plant species. It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates hyphal branching of arbuscular mycorrhizal fungi. In this work, we demonstrate that this induction is conserved in Arabidopsis (Arabidopsis thaliana), although Arabidopsis is not a host for arbuscular mycorrhizal fungi. We demonstrate that the increase in strigolactone production contributes to the changes in shoot architecture observed in response to phosphate deficiency. Using high-performance liquid chromatography, column chromatography, and multiple reaction monitoring-liquid chromatography-tandem mass spectrometry analysis, we identified two strigolactones (orobanchol and orobanchyl acetate) in Arabidopsis and have evidence of the presence of a third (5-deoxystrigol). We show that at least one of them (orobanchol) is strongly reduced in the putative strigolactone biosynthetic mutants more axillary growth1 (max1) and max4 but not in the signal transduction mutant max2. Orobanchol was also detected in xylem sap and up-regulated under phosphate deficiency, which is consistent with the idea that root-derived strigolactones are transported to the shoot, where they regulate branching. Moreover, two additional putative strigolactone-like compounds were detected in xylem sap, one of which was not detected in root exudates. Together, these results show that xylem-transported strigolactones contribute to the regulation of shoot architectural response to phosphate-limiting conditions. |
doi_str_mv | 10.1104/pp.110.164640 |
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It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates hyphal branching of arbuscular mycorrhizal fungi. In this work, we demonstrate that this induction is conserved in Arabidopsis (Arabidopsis thaliana), although Arabidopsis is not a host for arbuscular mycorrhizal fungi. We demonstrate that the increase in strigolactone production contributes to the changes in shoot architecture observed in response to phosphate deficiency. Using high-performance liquid chromatography, column chromatography, and multiple reaction monitoring-liquid chromatography-tandem mass spectrometry analysis, we identified two strigolactones (orobanchol and orobanchyl acetate) in Arabidopsis and have evidence of the presence of a third (5-deoxystrigol). We show that at least one of them (orobanchol) is strongly reduced in the putative strigolactone biosynthetic mutants more axillary growth1 (max1) and max4 but not in the signal transduction mutant max2. Orobanchol was also detected in xylem sap and up-regulated under phosphate deficiency, which is consistent with the idea that root-derived strigolactones are transported to the shoot, where they regulate branching. Moreover, two additional putative strigolactone-like compounds were detected in xylem sap, one of which was not detected in root exudates. Together, these results show that xylem-transported strigolactones contribute to the regulation of shoot architectural response to phosphate-limiting conditions.</description><identifier>ISSN: 0032-0889</identifier><identifier>ISSN: 1532-2548</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.110.164640</identifier><identifier>PMID: 21119045</identifier><identifier>CODEN: PPHYA5</identifier><language>eng</language><publisher>Rockville, MD: American Society of Plant Biologists</publisher><subject>Acetates ; Agronomy. Soil science and plant productions ; am fungi ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis thaliana ; Architecture ; auxin transport ; Biological and medical sciences ; Biological Transport ; Biosynthesis ; Chromatography, High Pressure Liquid ; DEVELOPMENT AND HORMONE ACTION ; Economic plant physiology ; Fundamental and applied biological sciences. Psychology ; Germination ; germination stimulants ; indole-3-acetic-acid levels ; Lactones - isolation & purification ; Lactones - metabolism ; Mutation ; orobanche spp ; parasitic plants ; Parasitism and symbiosis ; Phosphates ; Phosphates - deficiency ; Phosphates - metabolism ; phosphorus deficiency ; Plant Growth Regulators - isolation & purification ; Plant Growth Regulators - metabolism ; Plant physiology and development ; Plant roots ; Plant Roots - chemistry ; Plant Roots - metabolism ; Plant Shoots - growth & development ; Plant Shoots - metabolism ; Plants ; rms1 mutant ; Root exudates ; root-system architecture ; seed-germination ; Starvation ; Symbiosis ; Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...) ; Tandem Mass Spectrometry ; Xylem ; Xylem - chemistry ; Xylem - metabolism</subject><ispartof>Plant physiology (Bethesda), 2011-02, Vol.155 (2), p.974-987</ispartof><rights>2011 American Society of Plant Biologists</rights><rights>2015 INIST-CNRS</rights><rights>2011 American Society of Plant Biologists 2011</rights><rights>Wageningen University & Research</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c611t-84cce7bcf8f39e0b1cb9d1bc041696ff15d0ec867175a0faa5370b7ed2d1b28a3</citedby><cites>FETCH-LOGICAL-c611t-84cce7bcf8f39e0b1cb9d1bc041696ff15d0ec867175a0faa5370b7ed2d1b28a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41434170$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41434170$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,885,27922,27923,58236,58469</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=23854988$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21119045$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kohlen, Wouter</creatorcontrib><creatorcontrib>Charnikhova, Tatsiana</creatorcontrib><creatorcontrib>Liu, Qing</creatorcontrib><creatorcontrib>Bours, Ralph</creatorcontrib><creatorcontrib>Domagalska, Malgorzata A</creatorcontrib><creatorcontrib>Beguerie, Sebastien</creatorcontrib><creatorcontrib>Verstappen, Francel</creatorcontrib><creatorcontrib>Leyser, Ottoline</creatorcontrib><creatorcontrib>Bouwmeester, Harro</creatorcontrib><creatorcontrib>Ruyter-Spira, Carolien</creatorcontrib><title>Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis</title><title>Plant physiology (Bethesda)</title><addtitle>Plant Physiol</addtitle><description>The biosynthesis of the recently identified novel class of plant hormones, strigolactones, is up-regulated upon phosphate deficiency in many plant species. It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates hyphal branching of arbuscular mycorrhizal fungi. In this work, we demonstrate that this induction is conserved in Arabidopsis (Arabidopsis thaliana), although Arabidopsis is not a host for arbuscular mycorrhizal fungi. We demonstrate that the increase in strigolactone production contributes to the changes in shoot architecture observed in response to phosphate deficiency. Using high-performance liquid chromatography, column chromatography, and multiple reaction monitoring-liquid chromatography-tandem mass spectrometry analysis, we identified two strigolactones (orobanchol and orobanchyl acetate) in Arabidopsis and have evidence of the presence of a third (5-deoxystrigol). We show that at least one of them (orobanchol) is strongly reduced in the putative strigolactone biosynthetic mutants more axillary growth1 (max1) and max4 but not in the signal transduction mutant max2. Orobanchol was also detected in xylem sap and up-regulated under phosphate deficiency, which is consistent with the idea that root-derived strigolactones are transported to the shoot, where they regulate branching. Moreover, two additional putative strigolactone-like compounds were detected in xylem sap, one of which was not detected in root exudates. Together, these results show that xylem-transported strigolactones contribute to the regulation of shoot architectural response to phosphate-limiting conditions.</description><subject>Acetates</subject><subject>Agronomy. Soil science and plant productions</subject><subject>am fungi</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Architecture</subject><subject>auxin transport</subject><subject>Biological and medical sciences</subject><subject>Biological Transport</subject><subject>Biosynthesis</subject><subject>Chromatography, High Pressure Liquid</subject><subject>DEVELOPMENT AND HORMONE ACTION</subject><subject>Economic plant physiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Germination</subject><subject>germination stimulants</subject><subject>indole-3-acetic-acid levels</subject><subject>Lactones - isolation & purification</subject><subject>Lactones - metabolism</subject><subject>Mutation</subject><subject>orobanche spp</subject><subject>parasitic plants</subject><subject>Parasitism and symbiosis</subject><subject>Phosphates</subject><subject>Phosphates - deficiency</subject><subject>Phosphates - metabolism</subject><subject>phosphorus deficiency</subject><subject>Plant Growth Regulators - isolation & purification</subject><subject>Plant Growth Regulators - metabolism</subject><subject>Plant physiology and development</subject><subject>Plant roots</subject><subject>Plant Roots - chemistry</subject><subject>Plant Roots - metabolism</subject><subject>Plant Shoots - growth & development</subject><subject>Plant Shoots - metabolism</subject><subject>Plants</subject><subject>rms1 mutant</subject><subject>Root exudates</subject><subject>root-system architecture</subject><subject>seed-germination</subject><subject>Starvation</subject><subject>Symbiosis</subject><subject>Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...)</subject><subject>Tandem Mass Spectrometry</subject><subject>Xylem</subject><subject>Xylem - chemistry</subject><subject>Xylem - metabolism</subject><issn>0032-0889</issn><issn>1532-2548</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNqFks1u1DAUhSMEosPAkiXgDWI1xY6didMFUlV-iihQdVqJneU4NxNXHjvYDlV4JJ4SRxlGsGKTE_l-99i-Pln2lOBjQjB73feTHpM1WzN8L1uQguarvGD8frbAOP1jzquj7FEItxhjQgl7mB3lhJAKs2KR_dpEr7fOSBWdhYBOPaBrL23onY_QoNh5N2y7pIC-jQZ2SNoGXRo5Iok-wYiunAGkLdp0zsXUrjodQcXBS4OuINnYACg6dNm50HcyAnoLrVYarBqnvi_OSl8PQQ1GevR5VM77Tv9M3ecuTIay1o3rgw6PswetNAGe7HWZ3bx_d312vrr4-uHj2enFSq0JiSvOlIKyVi1vaQW4JqquGlIrzMi6WrctKRoMiq9LUhYSt1IWtMR1CU2eqJxLusxOZt87uQWrbfqIdEalg3BSC6NrL_0o7gYvrJmkH-ogGKZFmvcyezM3p8UdNApsTJMQvde7qWky-LdidSe27oeg6a0YJ8ng1d7Au-8DhCh2OigwRlpwQxAVLkmBywL_l-SsYjTnJU_kaiaVdyF4aA_nIVhMKRJ9P6mYU5T4539f4kD_iU0CXu4BGZQ0bQrMNJ4DR3nBKj5t_GzmbkN0_lBnhFFGymmjF3O9lU7IrU8eN5s8pRSTivI0TvobH2LpGA</recordid><startdate>20110201</startdate><enddate>20110201</enddate><creator>Kohlen, Wouter</creator><creator>Charnikhova, Tatsiana</creator><creator>Liu, Qing</creator><creator>Bours, Ralph</creator><creator>Domagalska, Malgorzata A</creator><creator>Beguerie, Sebastien</creator><creator>Verstappen, Francel</creator><creator>Leyser, Ottoline</creator><creator>Bouwmeester, Harro</creator><creator>Ruyter-Spira, Carolien</creator><general>American Society of Plant Biologists</general><scope>FBQ</scope><scope>IQODW</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>7X8</scope><scope>M7N</scope><scope>5PM</scope><scope>QVL</scope></search><sort><creationdate>20110201</creationdate><title>Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis</title><author>Kohlen, Wouter ; Charnikhova, Tatsiana ; Liu, Qing ; Bours, Ralph ; Domagalska, Malgorzata A ; Beguerie, Sebastien ; Verstappen, Francel ; Leyser, Ottoline ; Bouwmeester, Harro ; Ruyter-Spira, Carolien</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c611t-84cce7bcf8f39e0b1cb9d1bc041696ff15d0ec867175a0faa5370b7ed2d1b28a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Acetates</topic><topic>Agronomy. Soil science and plant productions</topic><topic>am fungi</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Architecture</topic><topic>auxin transport</topic><topic>Biological and medical sciences</topic><topic>Biological Transport</topic><topic>Biosynthesis</topic><topic>Chromatography, High Pressure Liquid</topic><topic>DEVELOPMENT AND HORMONE ACTION</topic><topic>Economic plant physiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Germination</topic><topic>germination stimulants</topic><topic>indole-3-acetic-acid levels</topic><topic>Lactones - isolation & purification</topic><topic>Lactones - metabolism</topic><topic>Mutation</topic><topic>orobanche spp</topic><topic>parasitic plants</topic><topic>Parasitism and symbiosis</topic><topic>Phosphates</topic><topic>Phosphates - deficiency</topic><topic>Phosphates - metabolism</topic><topic>phosphorus deficiency</topic><topic>Plant Growth Regulators - isolation & purification</topic><topic>Plant Growth Regulators - metabolism</topic><topic>Plant physiology and development</topic><topic>Plant roots</topic><topic>Plant Roots - chemistry</topic><topic>Plant Roots - metabolism</topic><topic>Plant Shoots - growth & development</topic><topic>Plant Shoots - metabolism</topic><topic>Plants</topic><topic>rms1 mutant</topic><topic>Root exudates</topic><topic>root-system architecture</topic><topic>seed-germination</topic><topic>Starvation</topic><topic>Symbiosis</topic><topic>Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...)</topic><topic>Tandem Mass Spectrometry</topic><topic>Xylem</topic><topic>Xylem - chemistry</topic><topic>Xylem - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kohlen, Wouter</creatorcontrib><creatorcontrib>Charnikhova, Tatsiana</creatorcontrib><creatorcontrib>Liu, Qing</creatorcontrib><creatorcontrib>Bours, Ralph</creatorcontrib><creatorcontrib>Domagalska, Malgorzata A</creatorcontrib><creatorcontrib>Beguerie, Sebastien</creatorcontrib><creatorcontrib>Verstappen, Francel</creatorcontrib><creatorcontrib>Leyser, Ottoline</creatorcontrib><creatorcontrib>Bouwmeester, Harro</creatorcontrib><creatorcontrib>Ruyter-Spira, Carolien</creatorcontrib><collection>AGRIS</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>NARCIS:Publications</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kohlen, Wouter</au><au>Charnikhova, Tatsiana</au><au>Liu, Qing</au><au>Bours, Ralph</au><au>Domagalska, Malgorzata A</au><au>Beguerie, Sebastien</au><au>Verstappen, Francel</au><au>Leyser, Ottoline</au><au>Bouwmeester, Harro</au><au>Ruyter-Spira, Carolien</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis</atitle><jtitle>Plant physiology (Bethesda)</jtitle><addtitle>Plant Physiol</addtitle><date>2011-02-01</date><risdate>2011</risdate><volume>155</volume><issue>2</issue><spage>974</spage><epage>987</epage><pages>974-987</pages><issn>0032-0889</issn><issn>1532-2548</issn><eissn>1532-2548</eissn><coden>PPHYA5</coden><abstract>The biosynthesis of the recently identified novel class of plant hormones, strigolactones, is up-regulated upon phosphate deficiency in many plant species. It is generally accepted that the evolutionary origin of strigolactone up-regulation is their function as a rhizosphere signal that stimulates hyphal branching of arbuscular mycorrhizal fungi. In this work, we demonstrate that this induction is conserved in Arabidopsis (Arabidopsis thaliana), although Arabidopsis is not a host for arbuscular mycorrhizal fungi. We demonstrate that the increase in strigolactone production contributes to the changes in shoot architecture observed in response to phosphate deficiency. Using high-performance liquid chromatography, column chromatography, and multiple reaction monitoring-liquid chromatography-tandem mass spectrometry analysis, we identified two strigolactones (orobanchol and orobanchyl acetate) in Arabidopsis and have evidence of the presence of a third (5-deoxystrigol). We show that at least one of them (orobanchol) is strongly reduced in the putative strigolactone biosynthetic mutants more axillary growth1 (max1) and max4 but not in the signal transduction mutant max2. Orobanchol was also detected in xylem sap and up-regulated under phosphate deficiency, which is consistent with the idea that root-derived strigolactones are transported to the shoot, where they regulate branching. Moreover, two additional putative strigolactone-like compounds were detected in xylem sap, one of which was not detected in root exudates. Together, these results show that xylem-transported strigolactones contribute to the regulation of shoot architectural response to phosphate-limiting conditions.</abstract><cop>Rockville, MD</cop><pub>American Society of Plant Biologists</pub><pmid>21119045</pmid><doi>10.1104/pp.110.164640</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acetates Agronomy. Soil science and plant productions am fungi Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis thaliana Architecture auxin transport Biological and medical sciences Biological Transport Biosynthesis Chromatography, High Pressure Liquid DEVELOPMENT AND HORMONE ACTION Economic plant physiology Fundamental and applied biological sciences. Psychology Germination germination stimulants indole-3-acetic-acid levels Lactones - isolation & purification Lactones - metabolism Mutation orobanche spp parasitic plants Parasitism and symbiosis Phosphates Phosphates - deficiency Phosphates - metabolism phosphorus deficiency Plant Growth Regulators - isolation & purification Plant Growth Regulators - metabolism Plant physiology and development Plant roots Plant Roots - chemistry Plant Roots - metabolism Plant Shoots - growth & development Plant Shoots - metabolism Plants rms1 mutant Root exudates root-system architecture seed-germination Starvation Symbiosis Symbiosis (nodules, symbiotic nitrogen fixation, mycorrhiza...) Tandem Mass Spectrometry Xylem Xylem - chemistry Xylem - metabolism |
title | Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis |
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