Tomato Root Penetration in Soil Requires a Coaction between Ethylene and Auxin Signaling
During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and gre...
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Published in | Plant physiology (Bethesda) Vol. 156; no. 3; pp. 1424 - 1438 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
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Rockville, MD
American Society of Plant Biologists
01.07.2011
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Abstract | During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and grew in the air, forming loops. Time-lapse video imaging showed that 1-MCP-grown root tips retained positive gravitropism and made contact with the surface of Soilrite but failed to penetrate into the Soilrite. Time-course studies revealed that the effect of 1-MCP was most prominent when seed imbibition and germination were carried out in the continual presence of 1-MCP. Conversely, 1-MCP was ineffective when applied postgermination after penetration of roots in the Soilrite. Furthermore, treatment with 1-MCP caused a reduction in DRS::β-glucuronidase auxin-reporter activity and modified the expression of SIIAA3 and SIIAA9 transcripts, indicating interference with auxin signaling. The reduced ethylene perception mutant, Never-ripe, displayed decreased ability for root penetration, and the enhanced polar auxin transport mutant, polycotyledon, showed a nearly normal root penetration in the presence of 1-MCP, which could be reversed by application of auxin transport inhibitors. Our results indicate that during tomato seed germination, a coaction between ethylene and auxin is required for root penetration into the soil. |
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AbstractList | During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and grew in the air, forming loops. Time-lapse video imaging showed that 1-MCP-grown root tips retained positive gravitropism and made contact with the surface of Soilrite but failed to penetrate into the Soilrite. Time-course studies revealed that the effect of 1-MCP was most prominent when seed imbibition and germination were carried out in the continual presence of 1-MCP. Conversely, 1-MCP was ineffective when applied postgermination after penetration of roots in the Soilrite. Furthermore, treatment with 1-MCP caused a reduction in DR5::β-glucuronidase auxin-reporter activity and modified the expression of SlIAA3 and SlIAA9 transcripts, indicating interference with auxin signaling. The reduced ethylene perception mutant, Never-ripe, displayed decreased ability for root penetration, and the enhanced polar auxin transport mutant, polycotyledon, showed a nearly normal root penetration in the presence of 1-MCP, which could be reversed by application of auxin transport inhibitors. Our results indicate that during tomato seed germination, a coaction between ethylene and auxin is required for root penetration into the soil. During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato ( Solanum lycopersicum ) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and grew in the air, forming loops. Time-lapse video imaging showed that 1-MCP-grown root tips retained positive gravitropism and made contact with the surface of Soilrite but failed to penetrate into the Soilrite. Time-course studies revealed that the effect of 1-MCP was most prominent when seed imbibition and germination were carried out in the continual presence of 1-MCP. Conversely, 1-MCP was ineffective when applied postgermination after penetration of roots in the Soilrite. Furthermore, treatment with 1-MCP caused a reduction in DR5 :: β-glucuronidase auxin-reporter activity and modified the expression of SlIAA3 and SlIAA9 transcripts, indicating interference with auxin signaling. The reduced ethylene perception mutant, Never-ripe , displayed decreased ability for root penetration, and the enhanced polar auxin transport mutant, polycotyledon , showed a nearly normal root penetration in the presence of 1-MCP, which could be reversed by application of auxin transport inhibitors. Our results indicate that during tomato seed germination, a coaction between ethylene and auxin is required for root penetration into the soil. During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and grew in the air, forming loops. Time-lapse video imaging showed that 1-MCP-grown root tips retained positive gravitropism and made contact with the surface of Soilrite but failed to penetrate into the Soilrite. Time-course studies revealed that the effect of 1-MCP was most prominent when seed imbibition and germination were carried out in the continual presence of 1-MCP. Conversely, 1-MCP was ineffective when applied postgermination after penetration of roots in the Soilrite. Furthermore, treatment with 1-MCP caused a reduction in DRS::β-glucuronidase auxin-reporter activity and modified the expression of SIIAA3 and SIIAA9 transcripts, indicating interference with auxin signaling. The reduced ethylene perception mutant, Never-ripe, displayed decreased ability for root penetration, and the enhanced polar auxin transport mutant, polycotyledon, showed a nearly normal root penetration in the presence of 1-MCP, which could be reversed by application of auxin transport inhibitors. Our results indicate that during tomato seed germination, a coaction between ethylene and auxin is required for root penetration into the soil. During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and grew in the air, forming loops. Time-lapse video imaging showed that 1-MCP-grown root tips retained positive gravitropism and made contact with the surface of Soilrite but failed to penetrate into the Soilrite. Time-course studies revealed that the effect of 1-MCP was most prominent when seed imbibition and germination were carried out in the continual presence of 1-MCP. Conversely, 1-MCP was ineffective when applied postgermination after penetration of roots in the Soilrite. Furthermore, treatment with 1-MCP caused a reduction in DR5::β-glucuronidase auxin-reporter activity and modified the expression of SlIAA3 and SlIAA9 transcripts, indicating interference with auxin signaling. The reduced ethylene perception mutant, Never-ripe, displayed decreased ability for root penetration, and the enhanced polar auxin transport mutant, polycotyledon, showed a nearly normal root penetration in the presence of 1-MCP, which could be reversed by application of auxin transport inhibitors. Our results indicate that during tomato seed germination, a coaction between ethylene and auxin is required for root penetration into the soil.During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum) seeds germinated in the presence of 1-methylcyclopropene (1-MCP), an inhibitor of ethylene action, failed to insert roots into Soilrite and grew in the air, forming loops. Time-lapse video imaging showed that 1-MCP-grown root tips retained positive gravitropism and made contact with the surface of Soilrite but failed to penetrate into the Soilrite. Time-course studies revealed that the effect of 1-MCP was most prominent when seed imbibition and germination were carried out in the continual presence of 1-MCP. Conversely, 1-MCP was ineffective when applied postgermination after penetration of roots in the Soilrite. Furthermore, treatment with 1-MCP caused a reduction in DR5::β-glucuronidase auxin-reporter activity and modified the expression of SlIAA3 and SlIAA9 transcripts, indicating interference with auxin signaling. The reduced ethylene perception mutant, Never-ripe, displayed decreased ability for root penetration, and the enhanced polar auxin transport mutant, polycotyledon, showed a nearly normal root penetration in the presence of 1-MCP, which could be reversed by application of auxin transport inhibitors. Our results indicate that during tomato seed germination, a coaction between ethylene and auxin is required for root penetration into the soil. |
Author | Sharma, Rameshwar Santisree, Parankusam Vasuki, Himabindu Sreelakshmi, Yellamaraju Nongmaithem, Sapana Ivanchenko, Maria G. |
AuthorAffiliation | School of Life Sciences, University of Hyderabad, Hyderabad 500046, India (P.S., S.N., H.V., Y.S., R.S.); Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331 (M.G.I.) |
AuthorAffiliation_xml | – name: School of Life Sciences, University of Hyderabad, Hyderabad 500046, India (P.S., S.N., H.V., Y.S., R.S.); Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331 (M.G.I.) |
Author_xml | – sequence: 1 givenname: Parankusam surname: Santisree fullname: Santisree, Parankusam – sequence: 2 givenname: Sapana surname: Nongmaithem fullname: Nongmaithem, Sapana – sequence: 3 givenname: Himabindu surname: Vasuki fullname: Vasuki, Himabindu – sequence: 4 givenname: Yellamaraju surname: Sreelakshmi fullname: Sreelakshmi, Yellamaraju – sequence: 5 givenname: Maria G. surname: Ivanchenko fullname: Ivanchenko, Maria G. – sequence: 6 givenname: Rameshwar surname: Sharma fullname: Sharma, Rameshwar |
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Keywords | Auxin Root Ethylene Tomato Soils Penetration Vegetable crop Plant physiology Dicotyledones Angiospermae Lycopersicon esculentum Spermatophyta Solanaceae |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Some figures in this article are displayed in color online but in black and white in the print edition. This work was supported by the International Atomic Energy Agency, by the Department of Biotechnology, New Delhi, India (grants to R.S. and Y.S.), by the University Grants Commission, New Delhi, by the Department of Biotechnology-Center for Education and Research in Biology and Biotechnology (fellowship to P.S.), by a University of Hyderabad fellowship to N.S., and by the U.S. Department of Agriculture National Research Initiative Competitive Grants Program (grant no. 2006–03434 to M.G.I.). The online version of this article contains Web-only data. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Rameshwar Sharma (rameshwar.sharma@gmail.com). www.plantphysiol.org/cgi/doi/10.1104/pp.111.177014 Open Access articles can be viewed online without a subscription. |
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Snippet | During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato (Solanum lycopersicum)... During seed germination, emerging roots display positive gravitropism and penetrate into the soil for nutrition and anchorage. Tomato ( Solanum lycopersicum )... |
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SubjectTerms | 1-methylcyclopropene Auxins Biological and medical sciences Biological Transport Biological Transport - drug effects Cyclopropanes Cyclopropanes - pharmacology DEVELOPMENT AND HORMONE ACTION drug effects ethylene ethylene inhibitors Ethylenes Ethylenes - metabolism Fundamental and applied biological sciences. Psychology Gene expression regulation Gene Expression Regulation, Plant Gene Expression Regulation, Plant - drug effects Genes, Plant Genes, Plant - genetics genetics Gravitropism Gravitropism - drug effects growth & development Hypocotyls Indoleacetic Acids Indoleacetic Acids - metabolism Lycopersicon esculentum - drug effects Lycopersicon esculentum - growth & development Mechanotransduction, Cellular Mechanotransduction, Cellular - drug effects Mechanotransduction, Cellular - genetics Meristem Meristem - drug effects Meristem - metabolism metabolism Mutation Mutation - genetics nutrition pharmacology Plant growth regulators Plant physiology and development Plant Roots Plant Roots - drug effects Plant Roots - growth & development Plants Receptors Root growth Root tips seed germination Seedlings Seedlings - drug effects Seedlings - growth & development seeds Signal Transduction Signal Transduction - drug effects Soil Solanum lycopersicum tomatoes |
Title | Tomato Root Penetration in Soil Requires a Coaction between Ethylene and Auxin Signaling |
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