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 inPlant physiology (Bethesda) Vol. 156; no. 3; pp. 1424 - 1438
Main Authors Santisree, Parankusam, Nongmaithem, Sapana, Vasuki, Himabindu, Sreelakshmi, Yellamaraju, Ivanchenko, Maria G., Sharma, Rameshwar
Format Journal Article
LanguageEnglish
Published 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.
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.)
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Issue 3
Keywords Auxin
Root
Ethylene
Tomato
Soils
Penetration
Vegetable crop
Plant physiology
Dicotyledones
Angiospermae
Lycopersicon esculentum
Spermatophyta
Solanaceae
Language English
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CC BY 4.0
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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.
OpenAccessLink http://www.plantphysiol.org/content/plantphysiol/156/3/1424.full.pdf
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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
URI https://www.jstor.org/stable/41435050
https://www.ncbi.nlm.nih.gov/pubmed/21571667
https://www.proquest.com/docview/1400127539
https://www.proquest.com/docview/874897521
https://pubmed.ncbi.nlm.nih.gov/PMC3135914
Volume 156
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