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PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway

BACKGROUND: In flowering plants, apomixis (asexual reproduction via seeds) is widely believed to result from failure of key regulators of the sexual female reproductive pathway. In the past few years, both differential display and RNA-seq comparative approaches involving reproductive organs of sexua...

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Autores principales: Siena, Lorena A, Ortiz, Juan Pablo A, Leblanc, Olivier, Pessino, Silvina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4243328/
https://www.ncbi.nlm.nih.gov/pubmed/25404464
http://dx.doi.org/10.1186/s12870-014-0297-0
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author Siena, Lorena A
Ortiz, Juan Pablo A
Leblanc, Olivier
Pessino, Silvina
author_facet Siena, Lorena A
Ortiz, Juan Pablo A
Leblanc, Olivier
Pessino, Silvina
author_sort Siena, Lorena A
collection PubMed
description BACKGROUND: In flowering plants, apomixis (asexual reproduction via seeds) is widely believed to result from failure of key regulators of the sexual female reproductive pathway. In the past few years, both differential display and RNA-seq comparative approaches involving reproductive organs of sexual plants and their apomictic counterparts have yielded extensive lists of candidate genes. Nevertheless, only a limited number of these genes have been functionally characterized, with few clues consequently available for understanding the molecular control of apomixis. We have previously identified several cDNA fragments with high similarity to genes involved in RNA biology and with differential amplification between sexual and apomictic Paspalum notatum plants. Here, we report the characterization of one of these candidates, namely, N69 encoding a protein of the S-adenosyl-L-methionine-dependent methyltransferases superfamily. The purpose of this work was to extend the N69 cDNA sequence and to characterize its expression at different developmental stages in both sexual and apomictic individuals. RESULTS: Molecular characterization of the N69 cDNA revealed homology with genes encoding proteins similar to yeast and mammalian trimethylguanosine synthase/PRIP-interacting proteins. These proteins play a dual role as ERK2-controlled transcriptional coactivators and mediators of sn(o)RNA and telomerase RNA cap trimethylation, and participate in mammals and yeast development. The N69-extended sequence was consequently renamed PnTgs1-like. Expression of PnTgs1-like during reproductive development was significantly higher in floral organs of sexual genotypes compared with apomicts. This difference was not detected in vegetative tissues. In addition, expression levels in reproductive tissues of several genotypes were negatively correlated with facultative apomixis rates. Moreover, in situ hybridization observations revealed that PnTgs1-like expression is relatively higher in ovules of sexual plants throughout development, from premeiosis to maturity. Tissues where differential expression is detected include nucellar cells, the site of aposporous initials differentiation in apomictic genotypes. CONCLUSIONS: Our results indicate that PnTgs1-like (formerly N69) encodes a trimethylguanosine synthase-like protein whose function in mammals and yeast is critical for development, including reproduction. Our findings also suggest a pivotal role for this candidate gene in nucellar cell fate, as its diminished expression is correlated with initiation of the apomictic pathway in plants. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0297-0) contains supplementary material, which is available to authorized users.
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spelling pubmed-42433282014-11-26 PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway Siena, Lorena A Ortiz, Juan Pablo A Leblanc, Olivier Pessino, Silvina BMC Plant Biol Research Article BACKGROUND: In flowering plants, apomixis (asexual reproduction via seeds) is widely believed to result from failure of key regulators of the sexual female reproductive pathway. In the past few years, both differential display and RNA-seq comparative approaches involving reproductive organs of sexual plants and their apomictic counterparts have yielded extensive lists of candidate genes. Nevertheless, only a limited number of these genes have been functionally characterized, with few clues consequently available for understanding the molecular control of apomixis. We have previously identified several cDNA fragments with high similarity to genes involved in RNA biology and with differential amplification between sexual and apomictic Paspalum notatum plants. Here, we report the characterization of one of these candidates, namely, N69 encoding a protein of the S-adenosyl-L-methionine-dependent methyltransferases superfamily. The purpose of this work was to extend the N69 cDNA sequence and to characterize its expression at different developmental stages in both sexual and apomictic individuals. RESULTS: Molecular characterization of the N69 cDNA revealed homology with genes encoding proteins similar to yeast and mammalian trimethylguanosine synthase/PRIP-interacting proteins. These proteins play a dual role as ERK2-controlled transcriptional coactivators and mediators of sn(o)RNA and telomerase RNA cap trimethylation, and participate in mammals and yeast development. The N69-extended sequence was consequently renamed PnTgs1-like. Expression of PnTgs1-like during reproductive development was significantly higher in floral organs of sexual genotypes compared with apomicts. This difference was not detected in vegetative tissues. In addition, expression levels in reproductive tissues of several genotypes were negatively correlated with facultative apomixis rates. Moreover, in situ hybridization observations revealed that PnTgs1-like expression is relatively higher in ovules of sexual plants throughout development, from premeiosis to maturity. Tissues where differential expression is detected include nucellar cells, the site of aposporous initials differentiation in apomictic genotypes. CONCLUSIONS: Our results indicate that PnTgs1-like (formerly N69) encodes a trimethylguanosine synthase-like protein whose function in mammals and yeast is critical for development, including reproduction. Our findings also suggest a pivotal role for this candidate gene in nucellar cell fate, as its diminished expression is correlated with initiation of the apomictic pathway in plants. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0297-0) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-18 /pmc/articles/PMC4243328/ /pubmed/25404464 http://dx.doi.org/10.1186/s12870-014-0297-0 Text en © Siena et al.; licensee BioMed Central Ltd. 2014 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 work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Siena, Lorena A
Ortiz, Juan Pablo A
Leblanc, Olivier
Pessino, Silvina
PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway
title PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway
title_full PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway
title_fullStr PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway
title_full_unstemmed PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway
title_short PnTgs1-like expression during reproductive development supports a role for RNA methyltransferases in the aposporous pathway
title_sort pntgs1-like expression during reproductive development supports a role for rna methyltransferases in the aposporous pathway
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4243328/
https://www.ncbi.nlm.nih.gov/pubmed/25404464
http://dx.doi.org/10.1186/s12870-014-0297-0
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