LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation in early stages of cotton fiber cell development

Abstract BackgroundCotton fibers provide a powerful model for studying cell differentiation and elongation. Each cotton fiber is a singular and elongated cell derived from epidermal-layer cells of a cotton seed. Efforts to understand this dramatic developmental shift have been impeded by the difficulty of isolating fiber cells from epidermal cells.ResultsHere we employed laser-capture microdissection (LCM) to separate these cell types. RNA-seq analysis revealed transitional differences between the fiber and epidermal-layer cells at 0 or 2 days post anthesis. Specifically, down-regulation of putative cell cycle genes was coupled with upregulation of ribosome biosynthesis and translation-related genes, which may suggest their respective roles in fiber cell initiation and elongation. Indeed, the amount of fibers in cultured ovules was increased by cell cycle progression inhibitor, Roscovitine, and decreased by ribosome biosynthesis inhibitor, Rbin-1. Moreover, many phytohormone-related genes were upregulated in the ovules and down-regulated in the fibers, suggesting their spatial-temporal effects on fiber cell development. Key cell cycle regulators were predicted to be epialleles, and MYB-transcription factor related genes displayed expression divergence between fibers and ovules, implying their effects on fiber traits.ConclusionsWe revealed that fiber cell initiation is accompanied by cell cycle arrest coupled with active ribosome biosynthesis, spatial-temporal regulation of phytohormones and expression divergence between MYB transcription factor genes. These valuable genomic resources and molecular insights will help develop breeding and biotechnological tools to improve cotton fiber production.

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LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation

BMC Genomics ◽

10.1186/s12864-021-07579-1 ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Atsumi Ando ◽

Ryan C. Kirkbride ◽

Don C. Jones ◽

Jane Grimwood ◽

Z. Jeffrey Chen

Keyword(s):

Cell Cycle ◽

Cotton Fiber ◽

Epidermal Cells ◽

Fiber Cell ◽

Epidermal Layer ◽

Rna Seq ◽

Expression Bias ◽

Homoeolog Expression Bias ◽

Ribosome Biosynthesis ◽

Fiber Cell Initiation

Abstract Background Cotton fibers provide a powerful model for studying cell differentiation and elongation. Each cotton fiber is a singular and elongated cell derived from epidermal-layer cells of a cotton seed. Efforts to understand this dramatic developmental shift have been impeded by the difficulty of separation between fiber and epidermal cells. Results Here we employed laser-capture microdissection (LCM) to separate these cell types. RNA-seq analysis revealed transitional differences between fiber and epidermal-layer cells at 0 or 2 days post anthesis. Specifically, down-regulation of putative cell cycle genes was coupled with upregulation of ribosome biosynthesis and translation-related genes, which may suggest their respective roles in fiber cell initiation. Indeed, the amount of fibers in cultured ovules was increased by cell cycle progression inhibitor, Roscovitine, and decreased by ribosome biosynthesis inhibitor, Rbin-1. Moreover, subfunctionalization of homoeologs was pervasive in fiber and epidermal cells, with expression bias towards 10% more D than A homoeologs of cell cycle related genes and 40–50% more D than A homoeologs of ribosomal protein subunit genes. Key cell cycle regulators were predicted to be epialleles in allotetraploid cotton. MYB-transcription factor genes displayed expression divergence between fibers and ovules. Notably, many phytohormone-related genes were upregulated in ovules and down-regulated in fibers, suggesting spatial-temporal effects on fiber cell development. Conclusions Fiber cell initiation is accompanied by cell cycle arrest coupled with active ribosome biosynthesis, spatial-temporal regulation of phytohormones and MYB transcription factors, and homoeolog expression bias of cell cycle and ribosome biosynthesis genes. These valuable genomic resources and molecular insights will help develop breeding and biotechnological tools to improve cotton fiber production.

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Cytokinin inhibits cotton fiber initiation by disrupting PIN3a-mediated asymmetric accumulation of auxin in the ovule epidermis

Journal of Experimental Botany ◽

10.1093/jxb/erz162 ◽

2019 ◽

Vol 70 (12) ◽

pp. 3139-3151 ◽

Cited By ~ 7

Author(s):

Jianyan Zeng ◽

Mi Zhang ◽

Lei Hou ◽

Wenqin Bai ◽

Xingying Yan ◽

...

Keyword(s):

Cotton Fiber ◽

Plasma Membranes ◽

Antagonistic Effect ◽

Fiber Cell ◽

In Planta ◽

Polar Localization ◽

Fiber Cells ◽

Fiber Initiation ◽

Fiber Cell Initiation

AbstractAuxin-dependent cell expansion is crucial for initiation of fiber cells in cotton (Gossypium hirsutum), which ultimately determines fiber yield and quality. However, the regulation of this process is far from being well understood. In this study, we demonstrate an antagonistic effect between cytokinin (CK) and auxin on cotton fiber initiation. In vitro and in planta experiments indicate that enhanced CK levels can reduce auxin accumulation in the ovule integument, which may account for the defects in the fiberless mutant xu142fl. In turn, supplementation with auxin can recover fiber growth of CK-treated ovules and mutant ovules. We further found that GhPIN3a is a key auxin transporter for fiber-cell initiation and is polarly localized to the plasma membranes of non-fiber cells, but not to those of fiber cells. This polar localization allows auxin to be transported within the ovule integument while specifically accumulating in fiber cells. We show that CKs antagonize the promotive effect of auxin on fiber cell initiation by undermining asymmetric accumulation of auxin in the ovule epidermis through down-regulation of GhPIN3a and disturbance of the polar localization of the protein.

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The Transcription Factor B-Myb Is Maintained in an Inhibited State in Target Cells through Its Interaction with the Nuclear Corepressors N-CoR and SMRT

Molecular and Cellular Biology ◽

10.1128/mcb.22.11.3663-3673.2002 ◽

2002 ◽

Vol 22 (11) ◽

pp. 3663-3673 ◽

Cited By ~ 27

Author(s):

Xiaolin Li ◽

Donald P. McDonnell

Keyword(s):

Cell Cycle ◽

Transcription Factor ◽

Transcriptional Activity ◽

Cyclin A ◽

Myb Transcription Factor ◽

Target Cells ◽

Expression Of Genes ◽

Phosphorylation Event ◽

Cycle Regulation ◽

Nuclear Corepressors

ABSTRACT The B-Myb transcription factor has been implicated in coordinating the expression of genes involved in cell cycle regulation. Although it is expressed in a ubiquitous manner, its transcriptional activity is repressed until the G1-S phase of the cell cycle by an unknown mechanism. In this study we used biochemical and cell-based assays to demonstrate that the nuclear receptor corepressors N-CoR and SMRT interact with B-Myb. The significance of these B-Myb-corepressor interactions was confirmed by the finding that B-Myb mutants, which were unable to bind N-CoR, exhibited constitutive transcriptional activity. It has been shown previously that phosphorylation of B-Myb by cdk2/cyclin A enhances its transcriptional activity. We have now determined that phosphorylation by cdk2/cyclin A blocks the interaction between B-Myb and N-CoR and that mutation of the corepressor binding site within B-Myb bypasses the requirement for this phosphorylation event. Cumulatively, these findings suggest that the nuclear corepressors N-CoR and SMRT serve a previously unappreciated role as regulators of B-Myb transcriptional activity.

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GhJAZ2 negatively regulates cotton fiber initiation by interacting with the R2R3-MYB transcription factor GhMYB25-like

The Plant Journal ◽

10.1111/tpj.13273 ◽

2016 ◽

Vol 88 (6) ◽

pp. 921-935 ◽

Cited By ~ 52

Author(s):

Haiyan Hu ◽

Xin He ◽

Lili Tu ◽

Longfu Zhu ◽

Sitao Zhu ◽

...

Keyword(s):

Transcription Factor ◽

Cotton Fiber ◽

Myb Transcription Factor ◽

Fiber Initiation ◽

R2r3 Myb

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Positive and negative regulation of c-Myb by cyclin D1, cyclin-dependent kinases, and p27 Kip1

Blood ◽

10.1182/blood-2004-08-3342 ◽

2005 ◽

Vol 105 (10) ◽

pp. 3855-3861 ◽

Cited By ~ 26

Author(s):

Wanli Lei ◽

Fan Liu ◽

Scott A. Ness

Keyword(s):

Cell Cycle ◽

Transcription Factor ◽

Cyclin D1 ◽

Target Genes ◽

Cell Types ◽

Myb Transcription Factor ◽

Human T Cells ◽

Transforming Activity ◽

Differentiation And Proliferation ◽

P27 Kip1

AbstractThe c-Myb transcription factor controls differentiation and proliferation in hematopoietic and other cell types and has latent transforming activity, but little is known about its regulation during the cell cycle. Here, c-Myb was identified as part of a protein complex from human T cells containing the cyclin-dependent kinase (CDK) CDK6. Assays using model reporter constructs as well as endogenous target genes showed that the activity of c-Myb was inhibited by cyclin D1 plus CDK4 or CDK6 but stimulated by expression of the CDK inhibitors p16 Ink4a, p21 Cip1, or p27 Kip1. Mapping experiments identified a highly conserved region in c-Myb which, when transferred to the related A-Myb transcription factor, also rendered it responsive to CDKs and p27. The results suggest that c-Myb activity is directly regulated by cyclin D1 and CDKs and imply that c-Myb activity is regulated during the cell cycle in hematopoietic cells.

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