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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
Main Authors: Kohlen, Wouter, Charnikhova, Tatsiana, Liu, Qing, Bours, Ralph, Domagalska, Malgorzata A, Beguerie, Sebastien, Verstappen, Francel, Leyser, Ottoline, Bouwmeester, Harro, Ruyter-Spira, Carolien
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cited_by cdi_FETCH-LOGICAL-c611t-84cce7bcf8f39e0b1cb9d1bc041696ff15d0ec867175a0faa5370b7ed2d1b28a3
cites cdi_FETCH-LOGICAL-c611t-84cce7bcf8f39e0b1cb9d1bc041696ff15d0ec867175a0faa5370b7ed2d1b28a3
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container_title Plant physiology (Bethesda)
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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. 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Psychology ; Germination ; germination stimulants ; indole-3-acetic-acid levels ; Lactones - isolation &amp; purification ; Lactones - metabolism ; Mutation ; orobanche spp ; parasitic plants ; Parasitism and symbiosis ; Phosphates ; Phosphates - deficiency ; Phosphates - metabolism ; phosphorus deficiency ; Plant Growth Regulators - isolation &amp; purification ; Plant Growth Regulators - metabolism ; Plant physiology and development ; Plant roots ; Plant Roots - chemistry ; Plant Roots - metabolism ; Plant Shoots - growth &amp; 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 &amp; 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&amp;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). 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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 &amp; 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 &amp; 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 &amp; 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. 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Psychology</topic><topic>Germination</topic><topic>germination stimulants</topic><topic>indole-3-acetic-acid levels</topic><topic>Lactones - isolation &amp; 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 &amp; 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 &amp; 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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source JSTOR Archival Journals and Primary Sources Collection; Oxford Journals Online
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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