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Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b

BACKGROUND: As central regulators of the gibberellic acid (GA) signaling pathway in plants, DELLA proteins function as growth repressors and affect diverse biological processes. The wheat RHT-B1b and RHT-D1b semi-dwarfing alleles, which encode GA-insensitive DELLA proteins, have been widely adopted...

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Autores principales: Mo, Youngjun, Pearce, Stephen, Dubcovsky, Jorge
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6196432/
https://www.ncbi.nlm.nih.gov/pubmed/30348083
http://dx.doi.org/10.1186/s12870-018-1465-4
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author Mo, Youngjun
Pearce, Stephen
Dubcovsky, Jorge
author_facet Mo, Youngjun
Pearce, Stephen
Dubcovsky, Jorge
author_sort Mo, Youngjun
collection PubMed
description BACKGROUND: As central regulators of the gibberellic acid (GA) signaling pathway in plants, DELLA proteins function as growth repressors and affect diverse biological processes. The wheat RHT-B1b and RHT-D1b semi-dwarfing alleles, which encode GA-insensitive DELLA proteins, have been widely adopted in modern wheat varieties to improve lodging tolerance and harvest index. However, the molecular mechanisms by which DELLA modulates these responses in wheat remain largely unknown. RESULTS: We identified a tall tetraploid wheat mutant line carrying an induced missense mutation (E529K) in the PFYRE motif of RHT-B1b that partially suppressed the semi-dwarf phenotype. The height-increasing effect of RHT-B1b(E529K) relative to RHT-B1b (19 cm or 21% increase) was significantly smaller than the effect of RHT-B1a (33 cm or 34% increase) relative to RHT-B1b in the same field experiment. The RHT-B1b(E529K) mutation was also associated with length increases in coleoptiles, seedling shoots, and stem internodes relative to the RHT-B1b allele. We detected no significant differences in germination rate, seedling root length, tiller number, flag leaf size, spike length, or yield components. Using RNA-seq, we compared gene expression profiles of plants encoding RHT-B1b and RHT-B1b(E529K) in coleoptile, first leaf, and elongating peduncles. We detected limited overlap among tissues of the genes differentially regulated by the two genotypes, and more genes upregulated (77%) than downregulated (23%) in RHT-B1b(E529K) relative to RHT-B1b. These results suggest that the wheat DELLA protein affects the transcriptome in a tissue-specific manner and that the mutation mainly eliminates or reduces repression functions of the RHT-B1 protein. Our study identified distinct sets of potential DELLA direct or indirect target genes involved in cell wall and carbohydrate metabolisms, cell cycle/division, and hormone pathways. CONCLUSIONS: We identified the hypomorphic RHT-B1b(E529K) allele that confers an intermediate plant height and coleoptile elongation. This allele can be useful in rain-fed wheat breeding programs where the strong reduction in height and biomass associated with RHT-B1b has detrimental effects. Transcriptomic characterization of different tissues from the plants encoding RHT-B1b(E529K) and RHT-B1b provided valuable information for identifying DELLA downstream GA response genes in wheat. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1465-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-61964322018-10-30 Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b Mo, Youngjun Pearce, Stephen Dubcovsky, Jorge BMC Plant Biol Research Article BACKGROUND: As central regulators of the gibberellic acid (GA) signaling pathway in plants, DELLA proteins function as growth repressors and affect diverse biological processes. The wheat RHT-B1b and RHT-D1b semi-dwarfing alleles, which encode GA-insensitive DELLA proteins, have been widely adopted in modern wheat varieties to improve lodging tolerance and harvest index. However, the molecular mechanisms by which DELLA modulates these responses in wheat remain largely unknown. RESULTS: We identified a tall tetraploid wheat mutant line carrying an induced missense mutation (E529K) in the PFYRE motif of RHT-B1b that partially suppressed the semi-dwarf phenotype. The height-increasing effect of RHT-B1b(E529K) relative to RHT-B1b (19 cm or 21% increase) was significantly smaller than the effect of RHT-B1a (33 cm or 34% increase) relative to RHT-B1b in the same field experiment. The RHT-B1b(E529K) mutation was also associated with length increases in coleoptiles, seedling shoots, and stem internodes relative to the RHT-B1b allele. We detected no significant differences in germination rate, seedling root length, tiller number, flag leaf size, spike length, or yield components. Using RNA-seq, we compared gene expression profiles of plants encoding RHT-B1b and RHT-B1b(E529K) in coleoptile, first leaf, and elongating peduncles. We detected limited overlap among tissues of the genes differentially regulated by the two genotypes, and more genes upregulated (77%) than downregulated (23%) in RHT-B1b(E529K) relative to RHT-B1b. These results suggest that the wheat DELLA protein affects the transcriptome in a tissue-specific manner and that the mutation mainly eliminates or reduces repression functions of the RHT-B1 protein. Our study identified distinct sets of potential DELLA direct or indirect target genes involved in cell wall and carbohydrate metabolisms, cell cycle/division, and hormone pathways. CONCLUSIONS: We identified the hypomorphic RHT-B1b(E529K) allele that confers an intermediate plant height and coleoptile elongation. This allele can be useful in rain-fed wheat breeding programs where the strong reduction in height and biomass associated with RHT-B1b has detrimental effects. Transcriptomic characterization of different tissues from the plants encoding RHT-B1b(E529K) and RHT-B1b provided valuable information for identifying DELLA downstream GA response genes in wheat. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1465-4) contains supplementary material, which is available to authorized users. BioMed Central 2018-10-22 /pmc/articles/PMC6196432/ /pubmed/30348083 http://dx.doi.org/10.1186/s12870-018-1465-4 Text en © The Author(s). 2018 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
Mo, Youngjun
Pearce, Stephen
Dubcovsky, Jorge
Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b
title Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b
title_full Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b
title_fullStr Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b
title_full_unstemmed Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b
title_short Phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the C-terminal PFYRE motif of RHT-B1b
title_sort phenotypic and transcriptomic characterization of a wheat tall mutant carrying an induced mutation in the c-terminal pfyre motif of rht-b1b
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6196432/
https://www.ncbi.nlm.nih.gov/pubmed/30348083
http://dx.doi.org/10.1186/s12870-018-1465-4
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