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Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton

Dehe Wang, Xiao Hu, Hanzhe Ye, Yue Wang, Qian Yang, Xiaodong Liang, Zilin Wang, Yifan Zhou, Miaomiao Wen, Xueyan Yuan, et al.
(2023) GENOME BIOLOGY. 24(1).
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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.
Keywords
Cotton, Fiber development, Rhythmic regulation, scRNA-seq, MYB TRANSCRIPTION FACTOR, CIRCADIAN CLOCK, STOMATAL LINEAGE, ELONGATION, INITIATION, DIFFERENTIATION, COMPLEXITY, PROFILES, PROTEINS, DYNAMICS

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MLA
Wang, Dehe, et al. “Cell-Specific Clock-Controlled Gene Expression Program Regulates Rhythmic Fiber Cell Growth in Cotton.” GENOME BIOLOGY, vol. 24, no. 1, 2023, doi:10.1186/s13059-023-02886-0.
APA
Wang, D., Hu, X., Ye, H., Wang, Y., Yang, Q., Liang, X., … Wang, K. (2023). Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton. GENOME BIOLOGY, 24(1). https://doi.org/10.1186/s13059-023-02886-0
Chicago author-date
Wang, Dehe, Xiao Hu, Hanzhe Ye, Yue Wang, Qian Yang, Xiaodong Liang, Zilin Wang, et al. 2023. “Cell-Specific Clock-Controlled Gene Expression Program Regulates Rhythmic Fiber Cell Growth in Cotton.” GENOME BIOLOGY 24 (1). https://doi.org/10.1186/s13059-023-02886-0.
Chicago author-date (all authors)
Wang, Dehe, 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, and Kun Wang. 2023. “Cell-Specific Clock-Controlled Gene Expression Program Regulates Rhythmic Fiber Cell Growth in Cotton.” GENOME BIOLOGY 24 (1). doi:10.1186/s13059-023-02886-0.
Vancouver
1.
Wang D, Hu X, Ye H, Wang Y, Yang Q, Liang X, et al. Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton. GENOME BIOLOGY. 2023;24(1).
IEEE
[1]
D. Wang et al., “Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton,” GENOME BIOLOGY, vol. 24, no. 1, 2023.
@article{01GW1ZGR9E0AE2SD94EHNRBWAJ,
  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.}},
  articleno    = {{49}},
  author       = {{Wang, Dehe and Hu, Xiao and Ye, Hanzhe and Wang, Yue and Yang, Qian and Liang, Xiaodong and Wang, Zilin and Zhou, Yifan and Wen, Miaomiao and Yuan, Xueyan and Zheng, Xiaomin and Ye, Wen and Guo, Boyu and Yusuyin, Mayila and Russinova, Eugenia and Zhou, Yu and Wang, Kun}},
  issn         = {{1474-760X}},
  journal      = {{GENOME BIOLOGY}},
  keywords     = {{Cotton,Fiber development,Rhythmic regulation,scRNA-seq,MYB TRANSCRIPTION FACTOR,CIRCADIAN CLOCK,STOMATAL LINEAGE,ELONGATION,INITIATION,DIFFERENTIATION,COMPLEXITY,PROFILES,PROTEINS,DYNAMICS}},
  language     = {{eng}},
  number       = {{1}},
  pages        = {{28}},
  title        = {{Cell-specific clock-controlled gene expression program regulates rhythmic fiber cell growth in cotton}},
  url          = {{http://doi.org/10.1186/s13059-023-02886-0}},
  volume       = {{24}},
  year         = {{2023}},
}
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