Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton
Abstract Background The epidermis of cotton ovule produces fibers, the most important natural cellulose source for the global textile industry. However, the molecular mechanism of fiber cell growth is still poorly understood. Results Here, we develop an optimized protoplasting method, and integrate...
| Main Authors: | , , , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-03-01
|
| Series: | Genome Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13059-023-02886-0 |
| _version_ | 1797864560752852992 |
|---|---|
| author | Dehe Wang Xiao Hu Hanzhe Ye Yue Wang Qian Yang Xiaodong Liang Zilin Wang Yifan Zhou Miaomiao Wen Xueyan Yuan Xiaomin Zheng Wen Ye Boyu Guo Mayila Yusuyin Eugenia Russinova Yu Zhou Kun Wang |
| author_facet | Dehe Wang Xiao Hu Hanzhe Ye Yue Wang Qian Yang Xiaodong Liang Zilin Wang Yifan Zhou Miaomiao Wen Xueyan Yuan Xiaomin Zheng Wen Ye Boyu Guo Mayila Yusuyin Eugenia Russinova Yu Zhou Kun Wang |
| author_sort | Dehe Wang |
| collection | DOAJ |
| description | Abstract Background The epidermis of cotton ovule produces fibers, the most important natural cellulose source for the global textile industry. However, the molecular mechanism of fiber cell growth is still poorly understood. Results Here, we develop an optimized protoplasting method, and integrate single-cell RNA sequencing (scRNA-seq) and single-cell ATAC sequencing (scATAC-seq) to systematically characterize the cells of the outer integument of ovules from wild type and fuzzless/lintless (fl) cotton (Gossypium hirsutum). By jointly analyzing the scRNA-seq data from wildtype and fl, we identify five cell populations including the fiber cell type and construct the development trajectory for fiber lineage cells. Interestingly, by time-course diurnal transcriptomic analysis, we demonstrate that the primary growth of fiber cells is a highly regulated circadian rhythmic process. Moreover, we identify a small peptide GhRALF1 that circadian rhythmically controls fiber growth possibly through oscillating auxin signaling and proton pump activity in the plasma membrane. Combining with scATAC-seq, we further identify two cardinal cis-regulatory elements (CREs, TCP motif, and TCP-like motif) which are bound by the trans factors GhTCP14s to modulate the circadian rhythmic metabolism of mitochondria and protein translation through regulating approximately one third of genes that are highly expressed in fiber cells. Conclusions We uncover a fiber-specific circadian clock-controlled gene expression program in regulating fiber growth. This study unprecedentedly reveals a new route to improve fiber traits by engineering the circadian clock of fiber cells. |
| first_indexed | 2024-04-09T22:53:52Z |
| format | Article |
| id | doaj.art-69e6a04be8d346b3a5d6eb9014f46673 |
| institution | Directory Open Access Journal |
| issn | 1474-760X |
| language | English |
| last_indexed | 2024-04-09T22:53:52Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Genome Biology |
| spelling | doaj.art-69e6a04be8d346b3a5d6eb9014f466732023-03-22T11:22:16ZengBMCGenome Biology1474-760X2023-03-0124112810.1186/s13059-023-02886-0Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cottonDehe Wang0Xiao Hu1Hanzhe Ye2Yue Wang3Qian Yang4Xiaodong Liang5Zilin Wang6Yifan Zhou7Miaomiao Wen8Xueyan Yuan9Xiaomin Zheng10Wen Ye11Boyu Guo12Mayila Yusuyin13Eugenia Russinova14Yu Zhou15Kun Wang16State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityInstitute for Advanced Studies, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityMedical Research Institute, Frontier Science Center for Immunology and Metabolism, School of Medicine, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityResearch Institute of Economic Crops, Xinjiang Academy of Agricultural SciencesDepartment of Plant Biotechnology and Bioinformatics, Ghent UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityState Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan UniversityAbstract Background The epidermis of cotton ovule produces fibers, the most important natural cellulose source for the global textile industry. However, the molecular mechanism of fiber cell growth is still poorly understood. Results Here, we develop an optimized protoplasting method, and integrate single-cell RNA sequencing (scRNA-seq) and single-cell ATAC sequencing (scATAC-seq) to systematically characterize the cells of the outer integument of ovules from wild type and fuzzless/lintless (fl) cotton (Gossypium hirsutum). By jointly analyzing the scRNA-seq data from wildtype and fl, we identify five cell populations including the fiber cell type and construct the development trajectory for fiber lineage cells. Interestingly, by time-course diurnal transcriptomic analysis, we demonstrate that the primary growth of fiber cells is a highly regulated circadian rhythmic process. Moreover, we identify a small peptide GhRALF1 that circadian rhythmically controls fiber growth possibly through oscillating auxin signaling and proton pump activity in the plasma membrane. Combining with scATAC-seq, we further identify two cardinal cis-regulatory elements (CREs, TCP motif, and TCP-like motif) which are bound by the trans factors GhTCP14s to modulate the circadian rhythmic metabolism of mitochondria and protein translation through regulating approximately one third of genes that are highly expressed in fiber cells. Conclusions We uncover a fiber-specific circadian clock-controlled gene expression program in regulating fiber growth. This study unprecedentedly reveals a new route to improve fiber traits by engineering the circadian clock of fiber cells.https://doi.org/10.1186/s13059-023-02886-0scRNA-seqRhythmic regulationFiber developmentCotton |
| spellingShingle | Dehe Wang Xiao Hu Hanzhe Ye Yue Wang Qian Yang Xiaodong Liang Zilin Wang Yifan Zhou Miaomiao Wen Xueyan Yuan Xiaomin Zheng Wen Ye Boyu Guo Mayila Yusuyin Eugenia Russinova Yu Zhou Kun Wang Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton Genome Biology scRNA-seq Rhythmic regulation Fiber development Cotton |
| title | Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton |
| title_full | Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton |
| title_fullStr | Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton |
| title_full_unstemmed | Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton |
| title_short | Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton |
| title_sort | cell specific clock controlled gene expression program regulates rhythmic fiber cell growth in cotton |
| topic | scRNA-seq Rhythmic regulation Fiber development Cotton |
| url | https://doi.org/10.1186/s13059-023-02886-0 |
| work_keys_str_mv | AT dehewang cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT xiaohu cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT hanzheye cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT yuewang cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT qianyang cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT xiaodongliang cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT zilinwang cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT yifanzhou cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT miaomiaowen cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT xueyanyuan cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT xiaominzheng cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT wenye cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT boyuguo cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT mayilayusuyin cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT eugeniarussinova cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT yuzhou cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton AT kunwang cellspecificclockcontrolledgeneexpressionprogramregulatesrhythmicfibercellgrowthincotton |