Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides

Aegilops speltoides, the closest ancestor of the wheat B subgenome, has been well studied genomically. However, the epigenetic landscape of Ae. speltoides and the effects of epigenetics on its growth and development remain poorly understood. Here, we present a comprehensive multi-omics atlas of leav...

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Main Authors: Lingfeng Miao, Zhe Chen, Lifeng Gao, Jizeng Jia, Weilong Guo, Guangyao Zhao
Format: Article
Language:English
Published: KeAi Communications Co., Ltd. 2025-02-01
Series:Crop Journal
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Online Access:http://www.sciencedirect.com/science/article/pii/S2214514124001946
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author Lingfeng Miao
Zhe Chen
Lifeng Gao
Jizeng Jia
Weilong Guo
Guangyao Zhao
author_facet Lingfeng Miao
Zhe Chen
Lifeng Gao
Jizeng Jia
Weilong Guo
Guangyao Zhao
author_sort Lingfeng Miao
collection DOAJ
description Aegilops speltoides, the closest ancestor of the wheat B subgenome, has been well studied genomically. However, the epigenetic landscape of Ae. speltoides and the effects of epigenetics on its growth and development remain poorly understood. Here, we present a comprehensive multi-omics atlas of leaves and roots in Ae. speltoides, encompassing transcriptome, DNA methylation, histone modifications, and small RNA profiling. Divergent DNA methylation levels were detected between leaves and roots, and were associated with differences in accumulated 24-nt siRNAs. DNA methylation changes in promoters and gene bodies showed strong connections with altered expression between leaves and roots. Transcriptional regulatory networks (TRN) reconstructed between leaves and roots were driven by tissue-specific TF families. DNA methylation and histone modification act together as switches that shape root and leaf morphogenesis by modulating the binding of tissue-specific TFs to their target genes. The TRNs in leaves and roots reshaped during wheat polyploidization were associated with alterations in epigenetic modifications. Collectively, these results not only shed light on the critical contribution of epigenetic regulation in the morphogenesis of leaves and roots in Ae. speltoides but also provide new insights for future investigations into the complex interplay of genetic and epigenetic factors in the developmental biology of common wheat.
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issn 2214-5141
language English
publishDate 2025-02-01
publisher KeAi Communications Co., Ltd.
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series Crop Journal
spelling doaj-art-528059ee1538490ea5e3fcca60cb0dba2025-08-20T03:02:06ZengKeAi Communications Co., Ltd.Crop Journal2214-51412025-02-0113129229810.1016/j.cj.2024.09.015Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoidesLingfeng Miao0Zhe Chen1Lifeng Gao2Jizeng Jia3Weilong Guo4Guangyao Zhao5Key Laboratory of Crop Gene Resources and Breeding, the National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; Frontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis and Utilization, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, ChinaFrontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis and Utilization, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, ChinaKey Laboratory of Crop Gene Resources and Breeding, the National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaKey Laboratory of Crop Gene Resources and Breeding, the National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaFrontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis and Utilization, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China; Corresponding authors.Key Laboratory of Crop Gene Resources and Breeding, the National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China; Corresponding authors.Aegilops speltoides, the closest ancestor of the wheat B subgenome, has been well studied genomically. However, the epigenetic landscape of Ae. speltoides and the effects of epigenetics on its growth and development remain poorly understood. Here, we present a comprehensive multi-omics atlas of leaves and roots in Ae. speltoides, encompassing transcriptome, DNA methylation, histone modifications, and small RNA profiling. Divergent DNA methylation levels were detected between leaves and roots, and were associated with differences in accumulated 24-nt siRNAs. DNA methylation changes in promoters and gene bodies showed strong connections with altered expression between leaves and roots. Transcriptional regulatory networks (TRN) reconstructed between leaves and roots were driven by tissue-specific TF families. DNA methylation and histone modification act together as switches that shape root and leaf morphogenesis by modulating the binding of tissue-specific TFs to their target genes. The TRNs in leaves and roots reshaped during wheat polyploidization were associated with alterations in epigenetic modifications. Collectively, these results not only shed light on the critical contribution of epigenetic regulation in the morphogenesis of leaves and roots in Ae. speltoides but also provide new insights for future investigations into the complex interplay of genetic and epigenetic factors in the developmental biology of common wheat.http://www.sciencedirect.com/science/article/pii/S2214514124001946Aegilops speltoidesDNA methylationHistone modificationTranscriptional regulatory network
spellingShingle Lingfeng Miao
Zhe Chen
Lifeng Gao
Jizeng Jia
Weilong Guo
Guangyao Zhao
Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides
Crop Journal
Aegilops speltoides
DNA methylation
Histone modification
Transcriptional regulatory network
title Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides
title_full Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides
title_fullStr Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides
title_full_unstemmed Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides
title_short Integrated multi-omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in Aegilops speltoides
title_sort integrated multi omics reveals contrasting epigenetic patterns in leaf and root morphogenesis in aegilops speltoides
topic Aegilops speltoides
DNA methylation
Histone modification
Transcriptional regulatory network
url http://www.sciencedirect.com/science/article/pii/S2214514124001946
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