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Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid
The development of Agrobacterium tumefaciens-induced plant tumors primarily depends on the excessive production of auxin and cytokinin by enzymes encoded on T-DNA genes integrated into the plant genome. The aim of the present study was to investigate the involvement of additional phytohormone signal...
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Published in: | Planta 2003-01, Vol.216 (3), p.512-522 |
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creator | Veselov, Dmitry Langhans, Markus Hartung, Wolfram Aloni, Roni Feussner, Ivo Götz, Claudia Veselova, Svetlana Schlomski, Stefan Dickler, Christoph Bächmann, Knut Ullrich, Cornelia I. |
description | The development of Agrobacterium tumefaciens-induced plant tumors primarily depends on the excessive production of auxin and cytokinin by enzymes encoded on T-DNA genes integrated into the plant genome. The aim of the present study was to investigate the involvement of additional phytohormone signals in the vascularization required for rapid tumor proliferation. In stem tumors of Ricinus communis L., free auxin and zeatin riboside concentrations increased within 2 weeks to 15-fold the concentrations in control stem tissue. Auxin and cytokinin immunolocalization revealed the highest concentrations within and around tumor vascular bundles with concentration gradients. The time-course of changes in free auxin concentration in roots was inversely correlated with that in the tumors. The high ethylene emission induced by increased auxin- and cytokinin correlated with a 36-fold accumulation of abscisic acid in tumors. Ethylene emitted from tumors and exogenously applied ethylene caused an increase in abscisic acid concentrations also in the host leaves, with a diminution in leaf water vapor conductance. Jasmonic acid concentration reached a maximum already within the first week of bacterial infection. A wound effect could be excluded. The results demonstrate the concerted interaction of a cascade of transiently induced, non-T-DNA-encoded phytohormones jasmonic acid, ethylene and abscisic acid with T-DNA-encoded auxin and zeatin riboside plus trans-zeatin, all of which are required for successful plant tumor vascularization and development together with inhibition of host plant growth. |
doi_str_mv | 10.1007/s00425-002-0883-5 |
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The aim of the present study was to investigate the involvement of additional phytohormone signals in the vascularization required for rapid tumor proliferation. In stem tumors of Ricinus communis L., free auxin and zeatin riboside concentrations increased within 2 weeks to 15-fold the concentrations in control stem tissue. Auxin and cytokinin immunolocalization revealed the highest concentrations within and around tumor vascular bundles with concentration gradients. The time-course of changes in free auxin concentration in roots was inversely correlated with that in the tumors. The high ethylene emission induced by increased auxin- and cytokinin correlated with a 36-fold accumulation of abscisic acid in tumors. Ethylene emitted from tumors and exogenously applied ethylene caused an increase in abscisic acid concentrations also in the host leaves, with a diminution in leaf water vapor conductance. Jasmonic acid concentration reached a maximum already within the first week of bacterial infection. A wound effect could be excluded. The results demonstrate the concerted interaction of a cascade of transiently induced, non-T-DNA-encoded phytohormones jasmonic acid, ethylene and abscisic acid with T-DNA-encoded auxin and zeatin riboside plus trans-zeatin, all of which are required for successful plant tumor vascularization and development together with inhibition of host plant growth.</description><identifier>ISSN: 0032-0935</identifier><identifier>EISSN: 1432-2048</identifier><identifier>DOI: 10.1007/s00425-002-0883-5</identifier><identifier>PMID: 12520344</identifier><identifier>CODEN: PLANAB</identifier><language>eng</language><publisher>Berlin: Springer-Verlag</publisher><subject>Abscisic Acid - metabolism ; Abscisic Acid - pharmacology ; Agrobacterium tumefaciens - growth & development ; Auxins ; Bacterial diseases ; Cyclopentanes - metabolism ; Cytokinins ; Cytokinins - metabolism ; Cytokinins - pharmacology ; Deoxyribonucleic acid ; DNA ; Ethylenes - metabolism ; Immunohistochemistry ; Indoleacetic Acids - metabolism ; Insulin antibodies ; Leaves ; Microscopy, Immunoelectron ; Oxylipins ; Plant growth ; Plant growth regulators ; Plant Growth Regulators - metabolism ; Plant Growth Regulators - pharmacology ; Plant roots ; Plant Roots - drug effects ; Plant Roots - growth & development ; Plant Roots - microbiology ; Plant Shoots - chemistry ; Plant Shoots - growth & development ; Plant Shoots - microbiology ; Plant Tumors - microbiology ; Plants ; Ricinus - chemistry ; Ricinus - growth & development ; Ricinus - microbiology ; Sieve elements ; Time Factors ; Tumors ; Water vapor ; Xylem</subject><ispartof>Planta, 2003-01, Vol.216 (3), p.512-522</ispartof><rights>Springer-Verlag Berlin Heidelberg 2003</rights><rights>2003 INIST-CNRS</rights><rights>Springer-Verlag 2003</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c376t-19c898ceb2fe595be8a06a92e7c362edad1208668ddd8537a234a922a4a013fe3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23387350$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23387350$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,4024,27923,27924,27925,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=14580448$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/12520344$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Veselov, Dmitry</creatorcontrib><creatorcontrib>Langhans, Markus</creatorcontrib><creatorcontrib>Hartung, Wolfram</creatorcontrib><creatorcontrib>Aloni, Roni</creatorcontrib><creatorcontrib>Feussner, Ivo</creatorcontrib><creatorcontrib>Götz, Claudia</creatorcontrib><creatorcontrib>Veselova, Svetlana</creatorcontrib><creatorcontrib>Schlomski, Stefan</creatorcontrib><creatorcontrib>Dickler, Christoph</creatorcontrib><creatorcontrib>Bächmann, Knut</creatorcontrib><creatorcontrib>Ullrich, Cornelia I.</creatorcontrib><title>Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid</title><title>Planta</title><addtitle>Planta</addtitle><description>The development of Agrobacterium tumefaciens-induced plant tumors primarily depends on the excessive production of auxin and cytokinin by enzymes encoded on T-DNA genes integrated into the plant genome. The aim of the present study was to investigate the involvement of additional phytohormone signals in the vascularization required for rapid tumor proliferation. In stem tumors of Ricinus communis L., free auxin and zeatin riboside concentrations increased within 2 weeks to 15-fold the concentrations in control stem tissue. Auxin and cytokinin immunolocalization revealed the highest concentrations within and around tumor vascular bundles with concentration gradients. The time-course of changes in free auxin concentration in roots was inversely correlated with that in the tumors. The high ethylene emission induced by increased auxin- and cytokinin correlated with a 36-fold accumulation of abscisic acid in tumors. Ethylene emitted from tumors and exogenously applied ethylene caused an increase in abscisic acid concentrations also in the host leaves, with a diminution in leaf water vapor conductance. Jasmonic acid concentration reached a maximum already within the first week of bacterial infection. A wound effect could be excluded. The results demonstrate the concerted interaction of a cascade of transiently induced, non-T-DNA-encoded phytohormones jasmonic acid, ethylene and abscisic acid with T-DNA-encoded auxin and zeatin riboside plus trans-zeatin, all of which are required for successful plant tumor vascularization and development together with inhibition of host plant growth.</description><subject>Abscisic Acid - metabolism</subject><subject>Abscisic Acid - pharmacology</subject><subject>Agrobacterium tumefaciens - growth & development</subject><subject>Auxins</subject><subject>Bacterial diseases</subject><subject>Cyclopentanes - metabolism</subject><subject>Cytokinins</subject><subject>Cytokinins - metabolism</subject><subject>Cytokinins - pharmacology</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>Ethylenes - metabolism</subject><subject>Immunohistochemistry</subject><subject>Indoleacetic Acids - metabolism</subject><subject>Insulin antibodies</subject><subject>Leaves</subject><subject>Microscopy, Immunoelectron</subject><subject>Oxylipins</subject><subject>Plant growth</subject><subject>Plant growth regulators</subject><subject>Plant Growth Regulators - metabolism</subject><subject>Plant Growth Regulators - pharmacology</subject><subject>Plant roots</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - growth & development</subject><subject>Plant Roots - microbiology</subject><subject>Plant Shoots - chemistry</subject><subject>Plant Shoots - growth & development</subject><subject>Plant Shoots - microbiology</subject><subject>Plant Tumors - microbiology</subject><subject>Plants</subject><subject>Ricinus - chemistry</subject><subject>Ricinus - growth & development</subject><subject>Ricinus - microbiology</subject><subject>Sieve elements</subject><subject>Time Factors</subject><subject>Tumors</subject><subject>Water vapor</subject><subject>Xylem</subject><issn>0032-0935</issn><issn>1432-2048</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><recordid>eNpdkU2O1DAQhSMEYnoGDsACZCENqwlU7Dh2lqPmVxqJDawjx67QbhI72A6iL8b5cOiIkVi5pPe9qnK9onhWwesKQLyJADXlJQAtQUpW8gfFrqoZLSnU8mGxA8g1tIxfFJcxHgGyKMTj4qKinAKr613x-y3-xNHPE7pE_EBuvwXfK50w2GUiaZlwUNqii2TPZWmdWTQaMo8q41n1IRLlDLHTnE3EO3LwMZF48D5lJSDR3qXgxzG7-hNRRKuolcF11lHFyTurSZ5gbohafll3Q_Qp-e_WrSWmw2lEh39HqD5qGzf6SfFoUGPEp9t7VXx9_-7L_mN59_nDp_3tXamZaFJZtVq2UmNPB-Qt71EqaFRLUWjWUDTKVBRk00hjjORMKMrqLFNVK6jYgOyqeHXuOwf_Y8GYuslGjWP-P_oldoK2NW9EncGX_4FHvwSXd-tEPrQE1ooMVWdIBx9jwKGbg51UOHUVdGui3TnRLifarYl2PHtebI2XfkJz79gizMD1BqyXHYegXL7TPVdzCXmBzD0_c8eYfPinU8akYBzYH_lytMs</recordid><startdate>20030101</startdate><enddate>20030101</enddate><creator>Veselov, Dmitry</creator><creator>Langhans, Markus</creator><creator>Hartung, Wolfram</creator><creator>Aloni, Roni</creator><creator>Feussner, Ivo</creator><creator>Götz, Claudia</creator><creator>Veselova, Svetlana</creator><creator>Schlomski, Stefan</creator><creator>Dickler, Christoph</creator><creator>Bächmann, Knut</creator><creator>Ullrich, Cornelia I.</creator><general>Springer-Verlag</general><general>Springer</general><general>Springer Nature B.V</general><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>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20030101</creationdate><title>Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid</title><author>Veselov, Dmitry ; Langhans, Markus ; Hartung, Wolfram ; Aloni, Roni ; Feussner, Ivo ; Götz, Claudia ; Veselova, Svetlana ; Schlomski, Stefan ; Dickler, Christoph ; Bächmann, Knut ; Ullrich, Cornelia I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c376t-19c898ceb2fe595be8a06a92e7c362edad1208668ddd8537a234a922a4a013fe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Abscisic Acid - metabolism</topic><topic>Abscisic Acid - pharmacology</topic><topic>Agrobacterium tumefaciens - growth & development</topic><topic>Auxins</topic><topic>Bacterial diseases</topic><topic>Cyclopentanes - metabolism</topic><topic>Cytokinins</topic><topic>Cytokinins - metabolism</topic><topic>Cytokinins - pharmacology</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>Ethylenes - metabolism</topic><topic>Immunohistochemistry</topic><topic>Indoleacetic Acids - metabolism</topic><topic>Insulin antibodies</topic><topic>Leaves</topic><topic>Microscopy, Immunoelectron</topic><topic>Oxylipins</topic><topic>Plant growth</topic><topic>Plant growth regulators</topic><topic>Plant Growth Regulators - metabolism</topic><topic>Plant Growth Regulators - pharmacology</topic><topic>Plant roots</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - growth & development</topic><topic>Plant Roots - microbiology</topic><topic>Plant Shoots - chemistry</topic><topic>Plant Shoots - 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Academic</collection><jtitle>Planta</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Veselov, Dmitry</au><au>Langhans, Markus</au><au>Hartung, Wolfram</au><au>Aloni, Roni</au><au>Feussner, Ivo</au><au>Götz, Claudia</au><au>Veselova, Svetlana</au><au>Schlomski, Stefan</au><au>Dickler, Christoph</au><au>Bächmann, Knut</au><au>Ullrich, Cornelia I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid</atitle><jtitle>Planta</jtitle><addtitle>Planta</addtitle><date>2003-01-01</date><risdate>2003</risdate><volume>216</volume><issue>3</issue><spage>512</spage><epage>522</epage><pages>512-522</pages><issn>0032-0935</issn><eissn>1432-2048</eissn><coden>PLANAB</coden><abstract>The development of Agrobacterium tumefaciens-induced plant tumors primarily depends on the excessive production of auxin and cytokinin by enzymes encoded on T-DNA genes integrated into the plant genome. The aim of the present study was to investigate the involvement of additional phytohormone signals in the vascularization required for rapid tumor proliferation. In stem tumors of Ricinus communis L., free auxin and zeatin riboside concentrations increased within 2 weeks to 15-fold the concentrations in control stem tissue. Auxin and cytokinin immunolocalization revealed the highest concentrations within and around tumor vascular bundles with concentration gradients. The time-course of changes in free auxin concentration in roots was inversely correlated with that in the tumors. The high ethylene emission induced by increased auxin- and cytokinin correlated with a 36-fold accumulation of abscisic acid in tumors. Ethylene emitted from tumors and exogenously applied ethylene caused an increase in abscisic acid concentrations also in the host leaves, with a diminution in leaf water vapor conductance. Jasmonic acid concentration reached a maximum already within the first week of bacterial infection. A wound effect could be excluded. The results demonstrate the concerted interaction of a cascade of transiently induced, non-T-DNA-encoded phytohormones jasmonic acid, ethylene and abscisic acid with T-DNA-encoded auxin and zeatin riboside plus trans-zeatin, all of which are required for successful plant tumor vascularization and development together with inhibition of host plant growth.</abstract><cop>Berlin</cop><pub>Springer-Verlag</pub><pmid>12520344</pmid><doi>10.1007/s00425-002-0883-5</doi><tpages>11</tpages></addata></record> |
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source | Springer Link; JSTOR |
subjects | Abscisic Acid - metabolism Abscisic Acid - pharmacology Agrobacterium tumefaciens - growth & development Auxins Bacterial diseases Cyclopentanes - metabolism Cytokinins Cytokinins - metabolism Cytokinins - pharmacology Deoxyribonucleic acid DNA Ethylenes - metabolism Immunohistochemistry Indoleacetic Acids - metabolism Insulin antibodies Leaves Microscopy, Immunoelectron Oxylipins Plant growth Plant growth regulators Plant Growth Regulators - metabolism Plant Growth Regulators - pharmacology Plant roots Plant Roots - drug effects Plant Roots - growth & development Plant Roots - microbiology Plant Shoots - chemistry Plant Shoots - growth & development Plant Shoots - microbiology Plant Tumors - microbiology Plants Ricinus - chemistry Ricinus - growth & development Ricinus - microbiology Sieve elements Time Factors Tumors Water vapor Xylem |
title | Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid |
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