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Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach

Reproductive growth is a bioenergetic process with high energy consumption. Pollination induces female flower longevity in spinach by accelerating sepal retention and development. Cellular bioenergetics involved in cellular growth is at the foundation of all developmental activities. By contrast, ho...

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Autores principales: Ma, Xiaokai, Fatima, Mahpara, Li, Jing, Zhou, Ping, Zaynab, Madiha, Ming, Ray
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795224/
https://www.ncbi.nlm.nih.gov/pubmed/36589106
http://dx.doi.org/10.3389/fpls.2022.1010149
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author Ma, Xiaokai
Fatima, Mahpara
Li, Jing
Zhou, Ping
Zaynab, Madiha
Ming, Ray
author_facet Ma, Xiaokai
Fatima, Mahpara
Li, Jing
Zhou, Ping
Zaynab, Madiha
Ming, Ray
author_sort Ma, Xiaokai
collection PubMed
description Reproductive growth is a bioenergetic process with high energy consumption. Pollination induces female flower longevity in spinach by accelerating sepal retention and development. Cellular bioenergetics involved in cellular growth is at the foundation of all developmental activities. By contrast, how pollination alter the sepal cells bioenergetics to support energy requirement and anabolic biomass accumulation for development is less well understood. To investigate pollination-induced energy-associated pathway changes in sepal tissues after pollination, we utilized RNA-sequencing to identify transcripts that were differentially expressed between unpollinated (UNP) and pollinated flower sepals at 12, 48, and 96HAP. In total, over 6756 non-redundant DEGs were identified followed by pairwise comparisons (i.e. UNP vs 12HAP, UNP vs 48HAP, and UNP vs 96HAP). KEGG enrichment showed that the central carbon metabolic pathway was significantly activated after pollination and governed by pivotal energy-associated regulation pathways such as glycolysis, the citric acid cycle, oxidative phosphorylation, photosynthesis, and pentose phosphate pathways. Co-expression networks confirmed the synergistically regulation interactions among these pathways. Gene expression changes in these pathways were not observed after fertilization at 12HAP, but started after fertilization at 48HAP, and significant changes in gene expression occurred at 96HAP when there is considerable sepal development. These results were also supported by qPCR validation. Our results suggest that multiple energy-associated pathways may play a pivotal regulatory role in post-pollination sepal longevity for developing the seed coat, and proposed an energy pathway model regulating sepal retention in spinach.
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spelling pubmed-97952242022-12-29 Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach Ma, Xiaokai Fatima, Mahpara Li, Jing Zhou, Ping Zaynab, Madiha Ming, Ray Front Plant Sci Plant Science Reproductive growth is a bioenergetic process with high energy consumption. Pollination induces female flower longevity in spinach by accelerating sepal retention and development. Cellular bioenergetics involved in cellular growth is at the foundation of all developmental activities. By contrast, how pollination alter the sepal cells bioenergetics to support energy requirement and anabolic biomass accumulation for development is less well understood. To investigate pollination-induced energy-associated pathway changes in sepal tissues after pollination, we utilized RNA-sequencing to identify transcripts that were differentially expressed between unpollinated (UNP) and pollinated flower sepals at 12, 48, and 96HAP. In total, over 6756 non-redundant DEGs were identified followed by pairwise comparisons (i.e. UNP vs 12HAP, UNP vs 48HAP, and UNP vs 96HAP). KEGG enrichment showed that the central carbon metabolic pathway was significantly activated after pollination and governed by pivotal energy-associated regulation pathways such as glycolysis, the citric acid cycle, oxidative phosphorylation, photosynthesis, and pentose phosphate pathways. Co-expression networks confirmed the synergistically regulation interactions among these pathways. Gene expression changes in these pathways were not observed after fertilization at 12HAP, but started after fertilization at 48HAP, and significant changes in gene expression occurred at 96HAP when there is considerable sepal development. These results were also supported by qPCR validation. Our results suggest that multiple energy-associated pathways may play a pivotal regulatory role in post-pollination sepal longevity for developing the seed coat, and proposed an energy pathway model regulating sepal retention in spinach. Frontiers Media S.A. 2022-12-14 /pmc/articles/PMC9795224/ /pubmed/36589106 http://dx.doi.org/10.3389/fpls.2022.1010149 Text en Copyright © 2022 Ma, Fatima, Li, Zhou, Zaynab and Ming https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Ma, Xiaokai
Fatima, Mahpara
Li, Jing
Zhou, Ping
Zaynab, Madiha
Ming, Ray
Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
title Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
title_full Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
title_fullStr Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
title_full_unstemmed Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
title_short Post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
title_sort post-pollination sepal longevity of female flower co-regulated by energy-associated multiple pathways in dioecious spinach
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9795224/
https://www.ncbi.nlm.nih.gov/pubmed/36589106
http://dx.doi.org/10.3389/fpls.2022.1010149
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