Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis
Abstract Background Homoeologs are defined as homologous genes resulting from allopolyploidy. Bread wheat, Triticum aestivum, is an allohexaploid species with many homoeologs. Homoeolog expression bias, referring to the relative contribution of homoeologs to the transcriptome, is critical for determ...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-04-01
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| Series: | Genome Biology |
| Online Access: | https://doi.org/10.1186/s13059-023-02908-x |
| _version_ | 1797850028090327040 |
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| author | Lihua Zhang Chao He Yuting Lai Yating Wang Lu Kang Ankui Liu Caixia Lan Handong Su Yuwen Gao Zeqing Li Fang Yang Qiang Li Hailiang Mao Dijun Chen Wei Chen Kerstin Kaufmann Wenhao Yan |
| author_facet | Lihua Zhang Chao He Yuting Lai Yating Wang Lu Kang Ankui Liu Caixia Lan Handong Su Yuwen Gao Zeqing Li Fang Yang Qiang Li Hailiang Mao Dijun Chen Wei Chen Kerstin Kaufmann Wenhao Yan |
| author_sort | Lihua Zhang |
| collection | DOAJ |
| description | Abstract Background Homoeologs are defined as homologous genes resulting from allopolyploidy. Bread wheat, Triticum aestivum, is an allohexaploid species with many homoeologs. Homoeolog expression bias, referring to the relative contribution of homoeologs to the transcriptome, is critical for determining the traits that influence wheat growth and development. Asymmetric transcription of homoeologs has been so far investigated in a tissue or organ-specific manner, which could be misleading due to a mixture of cell types. Results Here, we perform single nuclei RNA sequencing and ATAC sequencing of wheat root to study the asymmetric gene transcription, reconstruct cell differentiation trajectories and cell-type-specific gene regulatory networks. We identify 22 cell types. We then reconstruct cell differentiation trajectories that suggest different origins between epidermis/cortex and endodermis, distinguishing bread wheat from Arabidopsis. We show that the ratio of asymmetrically transcribed triads varies greatly when analyzing at the single-cell level. Hub transcription factors determining cell type identity are also identified. In particular, we demonstrate that TaSPL14 participates in vasculature development by regulating the expression of BAM1. Combining single-cell transcription and chromatin accessibility data, we construct the pseudo-time regulatory network driving root hair differentiation. We find MYB3R4, REF6, HDG1, and GATAs as key regulators in this process. Conclusions Our findings reveal the transcriptional landscape of root organization and asymmetric gene transcription at single-cell resolution in polyploid wheat. |
| first_indexed | 2024-04-09T18:53:44Z |
| format | Article |
| id | doaj.art-4a11ff98ca84455eaed988c277cd0c69 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-09T18:53:44Z |
| publishDate | 2023-04-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-4a11ff98ca84455eaed988c277cd0c692023-04-09T11:17:43ZengBMCGenome Biology1474-760X2023-04-0124112510.1186/s13059-023-02908-xAsymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysisLihua Zhang0Chao He1Yuting Lai2Yating Wang3Lu Kang4Ankui Liu5Caixia Lan6Handong Su7Yuwen Gao8Zeqing Li9Fang Yang10Qiang Li11Hailiang Mao12Dijun Chen13Wei Chen14Kerstin Kaufmann15Wenhao Yan16National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityWuhan Igenebook Biotechnology Co., LtdNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityState Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing UniversityNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityDepartment for Plant Cell and Molecular Biology, Institute for Biology, Humboldt-Universität Zu BerlinNational Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural UniversityAbstract Background Homoeologs are defined as homologous genes resulting from allopolyploidy. Bread wheat, Triticum aestivum, is an allohexaploid species with many homoeologs. Homoeolog expression bias, referring to the relative contribution of homoeologs to the transcriptome, is critical for determining the traits that influence wheat growth and development. Asymmetric transcription of homoeologs has been so far investigated in a tissue or organ-specific manner, which could be misleading due to a mixture of cell types. Results Here, we perform single nuclei RNA sequencing and ATAC sequencing of wheat root to study the asymmetric gene transcription, reconstruct cell differentiation trajectories and cell-type-specific gene regulatory networks. We identify 22 cell types. We then reconstruct cell differentiation trajectories that suggest different origins between epidermis/cortex and endodermis, distinguishing bread wheat from Arabidopsis. We show that the ratio of asymmetrically transcribed triads varies greatly when analyzing at the single-cell level. Hub transcription factors determining cell type identity are also identified. In particular, we demonstrate that TaSPL14 participates in vasculature development by regulating the expression of BAM1. Combining single-cell transcription and chromatin accessibility data, we construct the pseudo-time regulatory network driving root hair differentiation. We find MYB3R4, REF6, HDG1, and GATAs as key regulators in this process. Conclusions Our findings reveal the transcriptional landscape of root organization and asymmetric gene transcription at single-cell resolution in polyploid wheat.https://doi.org/10.1186/s13059-023-02908-x |
| spellingShingle | Lihua Zhang Chao He Yuting Lai Yating Wang Lu Kang Ankui Liu Caixia Lan Handong Su Yuwen Gao Zeqing Li Fang Yang Qiang Li Hailiang Mao Dijun Chen Wei Chen Kerstin Kaufmann Wenhao Yan Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis Genome Biology |
| title | Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis |
| title_full | Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis |
| title_fullStr | Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis |
| title_full_unstemmed | Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis |
| title_short | Asymmetric gene expression and cell-type-specific regulatory networks in the root of bread wheat revealed by single-cell multiomics analysis |
| title_sort | asymmetric gene expression and cell type specific regulatory networks in the root of bread wheat revealed by single cell multiomics analysis |
| url | https://doi.org/10.1186/s13059-023-02908-x |
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