Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination

Abstract The walnut (Juglans regia) is an important oilseed tree species characterized by its extensive distribution, high oil yield, and nutrient-dense kernels, which provide substantial economic benefits. However, the rising incidence of late-spring frosts, exacerbated by global climate change, ha...

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Main Authors: Kai Zhao, Xiaofan Wu, Bo Liang, Shuang Gao, Jieyan Yang, Yan Bai, Yaru Wang, Xin Tian, Fang Wang, Xiuqing Yang
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-025-11272-y
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author Kai Zhao
Xiaofan Wu
Bo Liang
Shuang Gao
Jieyan Yang
Yan Bai
Yaru Wang
Xin Tian
Fang Wang
Xiuqing Yang
author_facet Kai Zhao
Xiaofan Wu
Bo Liang
Shuang Gao
Jieyan Yang
Yan Bai
Yaru Wang
Xin Tian
Fang Wang
Xiuqing Yang
author_sort Kai Zhao
collection DOAJ
description Abstract The walnut (Juglans regia) is an important oilseed tree species characterized by its extensive distribution, high oil yield, and nutrient-dense kernels, which provide substantial economic benefits. However, the rising incidence of late-spring frosts, exacerbated by global climate change, has adversely affected walnut yields. A comprehensive understanding of the regulatory mechanisms involved in bud dormancy, germination, and development is essential for developing strategies to mitigate the effects of late-spring frosts and for breeding frost-resistant cultivars. This study focused on W13, a protogynous walnut variety with early germination of dormant buds in spring, employing a combination of transcriptomic and hormone metabolomic analyses. Our results emphasized four key biological processes—cellular response to ethylene stimulus, phenylpropanoid metabolic process, ethylene-activated signaling pathway, and monooxygenase activity—along with several relevant pathways, including plant hormone signal transduction, flavone and flavonol biosynthesis, biosynthesis of secondary metabolites, and MAPK signaling pathway, all crucial for walnut bud germination. Additionally, bud germination is closely associated with alterations in various hormone signaling pathways, including abscisic acid, auxin, cytokinin, ethylene, gibberellins, jasmonic acid, and salicylic acid. By assessing hormone levels and gene expression at different developmental stages, we pinpointed potential regulatory genes and critical hormones associated with bud germination. Furthermore, through weighted correlation network analysis, we constructed a co-expression network, identifying gene modules specifically expressed during dormancy, germination, budding, and leafing phases. The hub genes within these modules are likely pivotal in regulating walnut bud germination. Our analysis also revealed that genes from various transcription factor families are central within the co-expression network, indicating their significant roles in the bud germination process. Correlation network analysis of hormone and gene further illuminated the mechanisms through which genes and hormones jointly influence walnut bud germination. These findings establish a crucial molecular basis for a more comprehensive understanding of the mechanisms governing germination and development in dormant walnut buds.
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spelling doaj-art-bde3dff2ce3a42088a8f5b3c80a7f02f2025-02-02T12:10:12ZengBMCBMC Genomics1471-21642025-01-0126112010.1186/s12864-025-11272-yIntegrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germinationKai Zhao0Xiaofan Wu1Bo Liang2Shuang Gao3Jieyan Yang4Yan Bai5Yaru Wang6Xin Tian7Fang Wang8Xiuqing Yang9College of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityResearch Institute of Pomology, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityCollege of Forestry, Shanxi Agricultural UniversityAbstract The walnut (Juglans regia) is an important oilseed tree species characterized by its extensive distribution, high oil yield, and nutrient-dense kernels, which provide substantial economic benefits. However, the rising incidence of late-spring frosts, exacerbated by global climate change, has adversely affected walnut yields. A comprehensive understanding of the regulatory mechanisms involved in bud dormancy, germination, and development is essential for developing strategies to mitigate the effects of late-spring frosts and for breeding frost-resistant cultivars. This study focused on W13, a protogynous walnut variety with early germination of dormant buds in spring, employing a combination of transcriptomic and hormone metabolomic analyses. Our results emphasized four key biological processes—cellular response to ethylene stimulus, phenylpropanoid metabolic process, ethylene-activated signaling pathway, and monooxygenase activity—along with several relevant pathways, including plant hormone signal transduction, flavone and flavonol biosynthesis, biosynthesis of secondary metabolites, and MAPK signaling pathway, all crucial for walnut bud germination. Additionally, bud germination is closely associated with alterations in various hormone signaling pathways, including abscisic acid, auxin, cytokinin, ethylene, gibberellins, jasmonic acid, and salicylic acid. By assessing hormone levels and gene expression at different developmental stages, we pinpointed potential regulatory genes and critical hormones associated with bud germination. Furthermore, through weighted correlation network analysis, we constructed a co-expression network, identifying gene modules specifically expressed during dormancy, germination, budding, and leafing phases. The hub genes within these modules are likely pivotal in regulating walnut bud germination. Our analysis also revealed that genes from various transcription factor families are central within the co-expression network, indicating their significant roles in the bud germination process. Correlation network analysis of hormone and gene further illuminated the mechanisms through which genes and hormones jointly influence walnut bud germination. These findings establish a crucial molecular basis for a more comprehensive understanding of the mechanisms governing germination and development in dormant walnut buds.https://doi.org/10.1186/s12864-025-11272-yWalnutBud germinationTranscriptomeHormone
spellingShingle Kai Zhao
Xiaofan Wu
Bo Liang
Shuang Gao
Jieyan Yang
Yan Bai
Yaru Wang
Xin Tian
Fang Wang
Xiuqing Yang
Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
BMC Genomics
Walnut
Bud germination
Transcriptome
Hormone
title Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
title_full Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
title_fullStr Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
title_full_unstemmed Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
title_short Integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
title_sort integrated analysis of the transcriptome and hormone metabolome elucidates the regulatory mechanisms governing walnut bud germination
topic Walnut
Bud germination
Transcriptome
Hormone
url https://doi.org/10.1186/s12864-025-11272-y
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