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RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways

BACKGROUND: In cereal crops such as wheat, an optimal timing of developmental transitions is required to maximize grain yield. Many of these developmental changes are precisely regulated by changes in the duration, intensity or quality of light. Phytochromes are dimeric photoreceptors that absorb li...

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Autores principales: Pearce, Stephen, Kippes, Nestor, Chen, Andrew, Debernardi, Juan Manuel, Dubcovsky, Jorge
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915087/
https://www.ncbi.nlm.nih.gov/pubmed/27329140
http://dx.doi.org/10.1186/s12870-016-0831-3
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author Pearce, Stephen
Kippes, Nestor
Chen, Andrew
Debernardi, Juan Manuel
Dubcovsky, Jorge
author_facet Pearce, Stephen
Kippes, Nestor
Chen, Andrew
Debernardi, Juan Manuel
Dubcovsky, Jorge
author_sort Pearce, Stephen
collection PubMed
description BACKGROUND: In cereal crops such as wheat, an optimal timing of developmental transitions is required to maximize grain yield. Many of these developmental changes are precisely regulated by changes in the duration, intensity or quality of light. Phytochromes are dimeric photoreceptors that absorb light maximally in the red and far-red wavelengths and induce large-scale transcriptional changes in response to variation in light quality. In wheat, PHYC is required for early flowering under long days. However, it is currently unknown whether this function requires the presence of PHYB. In this study, we characterized the role of PHYB in wheat development and used RNA-seq to analyze and compare the transcriptomes of phyB-null and phyC-null TILLING mutants. RESULTS: Under long-day photoperiods, phyB-null plants exhibit a severe delay in flowering comparable to the delay observed in phyC-null plants. These results demonstrate that both genes are required for the induction of wheat flowering under long days. Using replicated RNA-seq studies we identified 82 genes that are significantly up or down regulated in both the phyB-null and phyC-null mutant relative to their respective wild-type controls. Among these genes are several well-characterized positive regulators of flowering, including PPD1, FT1 and VRN1. Eight-fold more genes were differentially regulated only in the phyB-null mutant (2202) than only in the phyC-null mutant (261). The PHYB-regulated genes were enriched in components of the auxin, gibberellin and brassinosteroid biosynthesis and signaling pathways, and in transcription factors with putative roles in regulating vegetative development and shade-avoidance responses. Several genes involved in abiotic stress tolerance pathways were also found to be regulated by PHYB. CONCLUSIONS: PHYB and PHYC are both required for the photoperiodic induction of wheat flowering, whereas PHYB alone regulates a large number of genes involved in hormone biosynthesis and signaling, shade-avoidance response, and abiotic stress tolerance. Our analysis provides a comprehensive overview of the PHYB- and PHYC-mediated transcriptional changes during light signaling, and an initial step towards the dissection of this regulatory gene network in wheat. This further dissection will be required to explore the individual phytochrome-mediated developmental responses and to evaluate their potential to improve wheat adaptation to changing environments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0831-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-49150872016-06-22 RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways Pearce, Stephen Kippes, Nestor Chen, Andrew Debernardi, Juan Manuel Dubcovsky, Jorge BMC Plant Biol Research Article BACKGROUND: In cereal crops such as wheat, an optimal timing of developmental transitions is required to maximize grain yield. Many of these developmental changes are precisely regulated by changes in the duration, intensity or quality of light. Phytochromes are dimeric photoreceptors that absorb light maximally in the red and far-red wavelengths and induce large-scale transcriptional changes in response to variation in light quality. In wheat, PHYC is required for early flowering under long days. However, it is currently unknown whether this function requires the presence of PHYB. In this study, we characterized the role of PHYB in wheat development and used RNA-seq to analyze and compare the transcriptomes of phyB-null and phyC-null TILLING mutants. RESULTS: Under long-day photoperiods, phyB-null plants exhibit a severe delay in flowering comparable to the delay observed in phyC-null plants. These results demonstrate that both genes are required for the induction of wheat flowering under long days. Using replicated RNA-seq studies we identified 82 genes that are significantly up or down regulated in both the phyB-null and phyC-null mutant relative to their respective wild-type controls. Among these genes are several well-characterized positive regulators of flowering, including PPD1, FT1 and VRN1. Eight-fold more genes were differentially regulated only in the phyB-null mutant (2202) than only in the phyC-null mutant (261). The PHYB-regulated genes were enriched in components of the auxin, gibberellin and brassinosteroid biosynthesis and signaling pathways, and in transcription factors with putative roles in regulating vegetative development and shade-avoidance responses. Several genes involved in abiotic stress tolerance pathways were also found to be regulated by PHYB. CONCLUSIONS: PHYB and PHYC are both required for the photoperiodic induction of wheat flowering, whereas PHYB alone regulates a large number of genes involved in hormone biosynthesis and signaling, shade-avoidance response, and abiotic stress tolerance. Our analysis provides a comprehensive overview of the PHYB- and PHYC-mediated transcriptional changes during light signaling, and an initial step towards the dissection of this regulatory gene network in wheat. This further dissection will be required to explore the individual phytochrome-mediated developmental responses and to evaluate their potential to improve wheat adaptation to changing environments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12870-016-0831-3) contains supplementary material, which is available to authorized users. BioMed Central 2016-06-21 /pmc/articles/PMC4915087/ /pubmed/27329140 http://dx.doi.org/10.1186/s12870-016-0831-3 Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Pearce, Stephen
Kippes, Nestor
Chen, Andrew
Debernardi, Juan Manuel
Dubcovsky, Jorge
RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
title RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
title_full RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
title_fullStr RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
title_full_unstemmed RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
title_short RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
title_sort rna-seq studies using wheat phytochrome b and phytochrome c mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4915087/
https://www.ncbi.nlm.nih.gov/pubmed/27329140
http://dx.doi.org/10.1186/s12870-016-0831-3
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