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High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes

Sexual reproduction is a critical process in the life-cycle of plants and very sensitive to environmental perturbations. To better understand the effect of high temperature on plant reproduction, we cultivated tomato (Solanum lycopersicum) plants in continuous mild heat. Under this condition we obse...

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Autores principales: Müller, Florian, Xu, Jiemeng, Kristensen, Lieke, Wolters-Arts, Mieke, de Groot, Peter F. M., Jansma, Stuart Y., Mariani, Celestina, Park, Sunghun, Rieu, Ivo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5147909/
https://www.ncbi.nlm.nih.gov/pubmed/27936079
http://dx.doi.org/10.1371/journal.pone.0167614
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author Müller, Florian
Xu, Jiemeng
Kristensen, Lieke
Wolters-Arts, Mieke
de Groot, Peter F. M.
Jansma, Stuart Y.
Mariani, Celestina
Park, Sunghun
Rieu, Ivo
author_facet Müller, Florian
Xu, Jiemeng
Kristensen, Lieke
Wolters-Arts, Mieke
de Groot, Peter F. M.
Jansma, Stuart Y.
Mariani, Celestina
Park, Sunghun
Rieu, Ivo
author_sort Müller, Florian
collection PubMed
description Sexual reproduction is a critical process in the life-cycle of plants and very sensitive to environmental perturbations. To better understand the effect of high temperature on plant reproduction, we cultivated tomato (Solanum lycopersicum) plants in continuous mild heat. Under this condition we observed a simultaneous reduction in pollen viability and appearance of anthers with pistil-like structures, while in a more thermotolerant genotype, both traits were improved. Ectopic expression of two pistil-specific genes, TRANSMITTING TISSUE SPECIFIC and TOMATO AGAMOUS LIKE11, in the anthers confirmed that the anthers had gained partial pistil identity. Concomitantly, expression of the B-class genes TOMATO APETALA3, TOMATO MADS BOX GENE6 (TM6) and LePISTILLATA was reduced in anthers under continuous mild heat. Plants in which TM6 was partially silenced reacted hypersensitively to temperature elevation with regard to the frequency of pistilloid anthers, pollen viability and pollen quantity. Taken together, these results suggest that high-temperature-induced down-regulation of tomato B-class genes contributes to anther deformations and reduced male fertility. Improving our understanding of how temperature perturbs the molecular mechanisms of anther and pollen development will be important in the view of maintaining agricultural output under current climate changes.
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spelling pubmed-51479092016-12-28 High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes Müller, Florian Xu, Jiemeng Kristensen, Lieke Wolters-Arts, Mieke de Groot, Peter F. M. Jansma, Stuart Y. Mariani, Celestina Park, Sunghun Rieu, Ivo PLoS One Research Article Sexual reproduction is a critical process in the life-cycle of plants and very sensitive to environmental perturbations. To better understand the effect of high temperature on plant reproduction, we cultivated tomato (Solanum lycopersicum) plants in continuous mild heat. Under this condition we observed a simultaneous reduction in pollen viability and appearance of anthers with pistil-like structures, while in a more thermotolerant genotype, both traits were improved. Ectopic expression of two pistil-specific genes, TRANSMITTING TISSUE SPECIFIC and TOMATO AGAMOUS LIKE11, in the anthers confirmed that the anthers had gained partial pistil identity. Concomitantly, expression of the B-class genes TOMATO APETALA3, TOMATO MADS BOX GENE6 (TM6) and LePISTILLATA was reduced in anthers under continuous mild heat. Plants in which TM6 was partially silenced reacted hypersensitively to temperature elevation with regard to the frequency of pistilloid anthers, pollen viability and pollen quantity. Taken together, these results suggest that high-temperature-induced down-regulation of tomato B-class genes contributes to anther deformations and reduced male fertility. Improving our understanding of how temperature perturbs the molecular mechanisms of anther and pollen development will be important in the view of maintaining agricultural output under current climate changes. Public Library of Science 2016-12-09 /pmc/articles/PMC5147909/ /pubmed/27936079 http://dx.doi.org/10.1371/journal.pone.0167614 Text en © 2016 Müller et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Müller, Florian
Xu, Jiemeng
Kristensen, Lieke
Wolters-Arts, Mieke
de Groot, Peter F. M.
Jansma, Stuart Y.
Mariani, Celestina
Park, Sunghun
Rieu, Ivo
High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes
title High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes
title_full High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes
title_fullStr High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes
title_full_unstemmed High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes
title_short High-Temperature-Induced Defects in Tomato (Solanum lycopersicum) Anther and Pollen Development Are Associated with Reduced Expression of B-Class Floral Patterning Genes
title_sort high-temperature-induced defects in tomato (solanum lycopersicum) anther and pollen development are associated with reduced expression of b-class floral patterning genes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5147909/
https://www.ncbi.nlm.nih.gov/pubmed/27936079
http://dx.doi.org/10.1371/journal.pone.0167614
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