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Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids

BACKGROUND: Heterosis, or hybrid vigor, refers to the phenotypic superiority of an F(1) hybrid relative to its parents in terms of growth rate, biomass production, grain yield, and stress tolerance. Light is an energy source and main environmental cue with marked impacts on heterosis in plants. Rese...

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Autores principales: Zhan, Weimin, Guo, Guanghui, Cui, Lianhua, Rashid, Muhammad Abdul Rehman, Jiang, Liangliang, Sun, Guanghua, Yang, Jianping, Zhang, Yanpei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9847186/
https://www.ncbi.nlm.nih.gov/pubmed/36653749
http://dx.doi.org/10.1186/s12870-023-04059-4
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author Zhan, Weimin
Guo, Guanghui
Cui, Lianhua
Rashid, Muhammad Abdul Rehman
Jiang, Liangliang
Sun, Guanghua
Yang, Jianping
Zhang, Yanpei
author_facet Zhan, Weimin
Guo, Guanghui
Cui, Lianhua
Rashid, Muhammad Abdul Rehman
Jiang, Liangliang
Sun, Guanghua
Yang, Jianping
Zhang, Yanpei
author_sort Zhan, Weimin
collection PubMed
description BACKGROUND: Heterosis, or hybrid vigor, refers to the phenotypic superiority of an F(1) hybrid relative to its parents in terms of growth rate, biomass production, grain yield, and stress tolerance. Light is an energy source and main environmental cue with marked impacts on heterosis in plants. Research into the production applications and mechanism of heterosis has been conducted for over a century and a half, but little is known about the effect of light on plant heterosis. RESULTS: In this study, an integrated transcriptome and metabolome analysis was performed using maize (Zea mays L.) inbred parents, B73 and Mo17, and their hybrids, B73 × Mo17 (BM) and Mo17 × B73 (MB), grown in darkness or under far-red, red, or blue light. Most differentially expressed genes (73.72–92.50%) and differentially accumulated metabolites (84.74–94.32%) exhibited non-additive effects in BM and MB hybrids. Gene Ontology analysis revealed that differential genes and metabolites were involved in glutathione transfer, carbohydrate transport, terpenoid biosynthesis, and photosynthesis. The darkness, far-red, red, and blue light treatments were all associated with phenylpropanoid–flavonoid biosynthesis by Weighted Gene Co-expression Network Analysis and Kyoto Encyclopedia of Genes and Genomes enrichment analysis. Five genes and seven metabolites related to phenylpropanoid–flavonoid biosynthesis pathway were identified as potential contributors to the interactions between maize heterosis and light conditions. Consistent with the strong mid-parent heterosis observed for metabolites, significant increases in both fresh and dry weights were found in the MB and BM hybrids compared with their inbred parents. Unexpectedly, increasing light intensity resulted in higher biomass heterosis in MB, but lower biomass heterosis in BM. CONCLUSIONS: The transcriptomic and metabolomic results provide unique insights into the effects of light quality on gene expression patterns and genotype–environment interactions, and have implications for gene mining of heterotic loci to improve maize production. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04059-4.
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spelling pubmed-98471862023-01-19 Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids Zhan, Weimin Guo, Guanghui Cui, Lianhua Rashid, Muhammad Abdul Rehman Jiang, Liangliang Sun, Guanghua Yang, Jianping Zhang, Yanpei BMC Plant Biol Research BACKGROUND: Heterosis, or hybrid vigor, refers to the phenotypic superiority of an F(1) hybrid relative to its parents in terms of growth rate, biomass production, grain yield, and stress tolerance. Light is an energy source and main environmental cue with marked impacts on heterosis in plants. Research into the production applications and mechanism of heterosis has been conducted for over a century and a half, but little is known about the effect of light on plant heterosis. RESULTS: In this study, an integrated transcriptome and metabolome analysis was performed using maize (Zea mays L.) inbred parents, B73 and Mo17, and their hybrids, B73 × Mo17 (BM) and Mo17 × B73 (MB), grown in darkness or under far-red, red, or blue light. Most differentially expressed genes (73.72–92.50%) and differentially accumulated metabolites (84.74–94.32%) exhibited non-additive effects in BM and MB hybrids. Gene Ontology analysis revealed that differential genes and metabolites were involved in glutathione transfer, carbohydrate transport, terpenoid biosynthesis, and photosynthesis. The darkness, far-red, red, and blue light treatments were all associated with phenylpropanoid–flavonoid biosynthesis by Weighted Gene Co-expression Network Analysis and Kyoto Encyclopedia of Genes and Genomes enrichment analysis. Five genes and seven metabolites related to phenylpropanoid–flavonoid biosynthesis pathway were identified as potential contributors to the interactions between maize heterosis and light conditions. Consistent with the strong mid-parent heterosis observed for metabolites, significant increases in both fresh and dry weights were found in the MB and BM hybrids compared with their inbred parents. Unexpectedly, increasing light intensity resulted in higher biomass heterosis in MB, but lower biomass heterosis in BM. CONCLUSIONS: The transcriptomic and metabolomic results provide unique insights into the effects of light quality on gene expression patterns and genotype–environment interactions, and have implications for gene mining of heterotic loci to improve maize production. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04059-4. BioMed Central 2023-01-18 /pmc/articles/PMC9847186/ /pubmed/36653749 http://dx.doi.org/10.1186/s12870-023-04059-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhan, Weimin
Guo, Guanghui
Cui, Lianhua
Rashid, Muhammad Abdul Rehman
Jiang, Liangliang
Sun, Guanghua
Yang, Jianping
Zhang, Yanpei
Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
title Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
title_full Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
title_fullStr Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
title_full_unstemmed Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
title_short Combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
title_sort combined transcriptome and metabolome analysis reveals the effects of light quality on maize hybrids
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9847186/
https://www.ncbi.nlm.nih.gov/pubmed/36653749
http://dx.doi.org/10.1186/s12870-023-04059-4
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