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Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes

BACKGROUND: Plant gametophytes play central roles in sexual reproduction. A hallmark of the plant life cycle is that gene expression is required in the haploid gametophytes. Consequently, many mutant phenotypes are expressed in this phase. RESULTS: We perform a quantitative RNA-seq analysis of embry...

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Autores principales: Chettoor, Antony M, Givan, Scott A, Cole, Rex A, Coker, Clayton T, Unger-Wallace, Erica, Vejlupkova, Zuzana, Vollbrecht, Erik, Fowler, John E, Evans, Matthew MS
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4309534/
https://www.ncbi.nlm.nih.gov/pubmed/25084966
http://dx.doi.org/10.1186/s13059-014-0414-2
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author Chettoor, Antony M
Givan, Scott A
Cole, Rex A
Coker, Clayton T
Unger-Wallace, Erica
Vejlupkova, Zuzana
Vollbrecht, Erik
Fowler, John E
Evans, Matthew MS
author_facet Chettoor, Antony M
Givan, Scott A
Cole, Rex A
Coker, Clayton T
Unger-Wallace, Erica
Vejlupkova, Zuzana
Vollbrecht, Erik
Fowler, John E
Evans, Matthew MS
author_sort Chettoor, Antony M
collection PubMed
description BACKGROUND: Plant gametophytes play central roles in sexual reproduction. A hallmark of the plant life cycle is that gene expression is required in the haploid gametophytes. Consequently, many mutant phenotypes are expressed in this phase. RESULTS: We perform a quantitative RNA-seq analysis of embryo sacs, comparator ovules with the embryo sacs removed, mature pollen, and seedlings to assist the identification of gametophyte functions in maize. Expression levels were determined for annotated genes in both gametophytes, and novel transcripts were identified from de novo assembly of RNA-seq reads. Transposon-related transcripts are present in high levels in both gametophytes, suggesting a connection between gamete production and transposon expression in maize not previously identified in any female gametophytes. Two classes of small signaling proteins and several transcription factor gene families are enriched in gametophyte transcriptomes. Expression patterns of maize genes with duplicates in subgenome 1 and subgenome 2 indicate that pollen-expressed genes in subgenome 2 are retained at a higher rate than subgenome 2 genes with other expression patterns. Analysis of available insertion mutant collections shows a statistically significant deficit in insertions in gametophyte-expressed genes. CONCLUSIONS: This analysis, the first RNA-seq study to compare both gametophytes in a monocot, identifies maize gametophyte functions, gametophyte expression of transposon-related sequences, and unannotated, novel transcripts. Reduced recovery of mutations in gametophyte-expressed genes is supporting evidence for their function in the gametophytes. Expression patterns of extant, duplicated maize genes reveals that selective pressures based on male gametophytic function have likely had a disproportionate effect on plant genomes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-014-0414-2) contains supplementary material, which is available to authorized users.
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spelling pubmed-43095342015-01-29 Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes Chettoor, Antony M Givan, Scott A Cole, Rex A Coker, Clayton T Unger-Wallace, Erica Vejlupkova, Zuzana Vollbrecht, Erik Fowler, John E Evans, Matthew MS Genome Biol Research BACKGROUND: Plant gametophytes play central roles in sexual reproduction. A hallmark of the plant life cycle is that gene expression is required in the haploid gametophytes. Consequently, many mutant phenotypes are expressed in this phase. RESULTS: We perform a quantitative RNA-seq analysis of embryo sacs, comparator ovules with the embryo sacs removed, mature pollen, and seedlings to assist the identification of gametophyte functions in maize. Expression levels were determined for annotated genes in both gametophytes, and novel transcripts were identified from de novo assembly of RNA-seq reads. Transposon-related transcripts are present in high levels in both gametophytes, suggesting a connection between gamete production and transposon expression in maize not previously identified in any female gametophytes. Two classes of small signaling proteins and several transcription factor gene families are enriched in gametophyte transcriptomes. Expression patterns of maize genes with duplicates in subgenome 1 and subgenome 2 indicate that pollen-expressed genes in subgenome 2 are retained at a higher rate than subgenome 2 genes with other expression patterns. Analysis of available insertion mutant collections shows a statistically significant deficit in insertions in gametophyte-expressed genes. CONCLUSIONS: This analysis, the first RNA-seq study to compare both gametophytes in a monocot, identifies maize gametophyte functions, gametophyte expression of transposon-related sequences, and unannotated, novel transcripts. Reduced recovery of mutations in gametophyte-expressed genes is supporting evidence for their function in the gametophytes. Expression patterns of extant, duplicated maize genes reveals that selective pressures based on male gametophytic function have likely had a disproportionate effect on plant genomes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13059-014-0414-2) contains supplementary material, which is available to authorized users. BioMed Central 2014-07-31 2014 /pmc/articles/PMC4309534/ /pubmed/25084966 http://dx.doi.org/10.1186/s13059-014-0414-2 Text en © Chettoor 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/2.0), 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
Chettoor, Antony M
Givan, Scott A
Cole, Rex A
Coker, Clayton T
Unger-Wallace, Erica
Vejlupkova, Zuzana
Vollbrecht, Erik
Fowler, John E
Evans, Matthew MS
Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes
title Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes
title_full Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes
title_fullStr Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes
title_full_unstemmed Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes
title_short Discovery of novel transcripts and gametophytic functions via RNA-seq analysis of maize gametophytic transcriptomes
title_sort discovery of novel transcripts and gametophytic functions via rna-seq analysis of maize gametophytic transcriptomes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4309534/
https://www.ncbi.nlm.nih.gov/pubmed/25084966
http://dx.doi.org/10.1186/s13059-014-0414-2
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