Cargando…

RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias

BACKGROUND: Pollination reduces flower longevity in many angiosperms by accelerating corolla senescence. This response requires hormone signaling between the floral organs and results in the degradation of macromolecules and organelles within the petals to allow for nutrient remobilization to develo...

Descripción completa

Detalles Bibliográficos
Autores principales: Broderick, Shaun R, Wijeratne, Saranga, Wijeratn, Asela J, Chapin, Laura J, Meulia, Tea, Jones, Michelle L
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4245787/
https://www.ncbi.nlm.nih.gov/pubmed/25403317
http://dx.doi.org/10.1186/s12870-014-0307-2
_version_ 1782346423853907968
author Broderick, Shaun R
Wijeratne, Saranga
Wijeratn, Asela J
Chapin, Laura J
Meulia, Tea
Jones, Michelle L
author_facet Broderick, Shaun R
Wijeratne, Saranga
Wijeratn, Asela J
Chapin, Laura J
Meulia, Tea
Jones, Michelle L
author_sort Broderick, Shaun R
collection PubMed
description BACKGROUND: Pollination reduces flower longevity in many angiosperms by accelerating corolla senescence. This response requires hormone signaling between the floral organs and results in the degradation of macromolecules and organelles within the petals to allow for nutrient remobilization to developing seeds. To investigate early pollination-induced changes in petal gene expression, we utilized high-throughput sequencing to identify transcripts that were differentially expressed between corollas of pollinated Petunia × hybrida flowers and their unpollinated controls at 12, 18, and 24 hours after opening. RESULTS: In total, close to 0.5 billion Illumina 101 bp reads were generated, de novo assembled, and annotated, resulting in an EST library of approximately 33 K genes. Over 4,700 unique, differentially expressed genes were identified using comparisons between the pollinated and unpollinated libraries followed by pairwise comparisons of pollinated libraries to unpollinated libraries from the same time point (i.e. 12-P/U, 18-P/U, and 24-P/U) in the Bioconductor R package DESeq2. Over 500 gene ontology terms were enriched. The response to auxin stimulus and response to 1-aminocyclopropane-1-carboxylic acid terms were enriched by 12 hours after pollination (hap). Using weighted gene correlation network analysis (WGCNA), three pollination-specific modules were identified. Module I had increased expression across pollinated corollas at 12, 18, and 24 h, and modules II and III had a peak of expression in pollinated corollas at 18 h. A total of 15 enriched KEGG pathways were identified. Many of the genes from these pathways were involved in metabolic processes or signaling. More than 300 differentially expressed transcription factors were identified. CONCLUSIONS: Gene expression changes in corollas were detected within 12 hap, well before fertilization and corolla wilting or ethylene evolution. Significant changes in gene expression occurred at 18 hap, including the up-regulation of autophagy and down-regulation of ribosomal genes and genes involved in carbon fixation. This transcriptomic database will greatly expand the genetic resources available in petunia. Additionally, it will guide future research aimed at identifying the best targets for increasing flower longevity by delaying corolla senescence. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0307-2) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-4245787
institution National Center for Biotechnology Information
language English
publishDate 2014
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-42457872014-11-28 RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias Broderick, Shaun R Wijeratne, Saranga Wijeratn, Asela J Chapin, Laura J Meulia, Tea Jones, Michelle L BMC Plant Biol Research Article BACKGROUND: Pollination reduces flower longevity in many angiosperms by accelerating corolla senescence. This response requires hormone signaling between the floral organs and results in the degradation of macromolecules and organelles within the petals to allow for nutrient remobilization to developing seeds. To investigate early pollination-induced changes in petal gene expression, we utilized high-throughput sequencing to identify transcripts that were differentially expressed between corollas of pollinated Petunia × hybrida flowers and their unpollinated controls at 12, 18, and 24 hours after opening. RESULTS: In total, close to 0.5 billion Illumina 101 bp reads were generated, de novo assembled, and annotated, resulting in an EST library of approximately 33 K genes. Over 4,700 unique, differentially expressed genes were identified using comparisons between the pollinated and unpollinated libraries followed by pairwise comparisons of pollinated libraries to unpollinated libraries from the same time point (i.e. 12-P/U, 18-P/U, and 24-P/U) in the Bioconductor R package DESeq2. Over 500 gene ontology terms were enriched. The response to auxin stimulus and response to 1-aminocyclopropane-1-carboxylic acid terms were enriched by 12 hours after pollination (hap). Using weighted gene correlation network analysis (WGCNA), three pollination-specific modules were identified. Module I had increased expression across pollinated corollas at 12, 18, and 24 h, and modules II and III had a peak of expression in pollinated corollas at 18 h. A total of 15 enriched KEGG pathways were identified. Many of the genes from these pathways were involved in metabolic processes or signaling. More than 300 differentially expressed transcription factors were identified. CONCLUSIONS: Gene expression changes in corollas were detected within 12 hap, well before fertilization and corolla wilting or ethylene evolution. Significant changes in gene expression occurred at 18 hap, including the up-regulation of autophagy and down-regulation of ribosomal genes and genes involved in carbon fixation. This transcriptomic database will greatly expand the genetic resources available in petunia. Additionally, it will guide future research aimed at identifying the best targets for increasing flower longevity by delaying corolla senescence. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-014-0307-2) contains supplementary material, which is available to authorized users. BioMed Central 2014-11-18 /pmc/articles/PMC4245787/ /pubmed/25403317 http://dx.doi.org/10.1186/s12870-014-0307-2 Text en © Broderick 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
Broderick, Shaun R
Wijeratne, Saranga
Wijeratn, Asela J
Chapin, Laura J
Meulia, Tea
Jones, Michelle L
RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
title RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
title_full RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
title_fullStr RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
title_full_unstemmed RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
title_short RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
title_sort rna-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4245787/
https://www.ncbi.nlm.nih.gov/pubmed/25403317
http://dx.doi.org/10.1186/s12870-014-0307-2
work_keys_str_mv AT broderickshaunr rnasequencingrevealsearlydynamictranscriptomechangesinthecorollasofpollinatedpetunias
AT wijeratnesaranga rnasequencingrevealsearlydynamictranscriptomechangesinthecorollasofpollinatedpetunias
AT wijeratnaselaj rnasequencingrevealsearlydynamictranscriptomechangesinthecorollasofpollinatedpetunias
AT chapinlauraj rnasequencingrevealsearlydynamictranscriptomechangesinthecorollasofpollinatedpetunias
AT meuliatea rnasequencingrevealsearlydynamictranscriptomechangesinthecorollasofpollinatedpetunias
AT jonesmichellel rnasequencingrevealsearlydynamictranscriptomechangesinthecorollasofpollinatedpetunias