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

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Main Authors: Atsumi Ando, Ryan C. Kirkbride, Don C. Jones, Jane Grimwood, Z. Jeffrey Chen
Format: Article
Language:English
Published: BMC 2021-04-01
Series:BMC Genomics
Online Access:https://doi.org/10.1186/s12864-021-07579-1
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spelling doaj-66b42c68d1ea425e8b2ba7f1e3fe1cad2021-05-02T11:23:15ZengBMCBMC Genomics1471-21642021-04-0122111610.1186/s12864-021-07579-1LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiationAtsumi Ando0Ryan C. Kirkbride1Don C. Jones2Jane Grimwood3Z. Jeffrey Chen4Department of Molecular Biosciences, and Center for Computational Biology and Bioinformatics, The University of Texas at AustinDepartment of Molecular Biosciences, and Center for Computational Biology and Bioinformatics, The University of Texas at AustinAgriculture and Environmental Research, Cotton IncorporatedHudsonAlpha Institute for BiotechnologyDepartment of Molecular Biosciences, and Center for Computational Biology and Bioinformatics, The University of Texas at AustinAbstract 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.https://doi.org/10.1186/s12864-021-07579-1
collection DOAJ
language English
format Article
sources DOAJ
author Atsumi Ando
Ryan C. Kirkbride
Don C. Jones
Jane Grimwood
Z. Jeffrey Chen
spellingShingle Atsumi Ando
Ryan C. Kirkbride
Don C. Jones
Jane Grimwood
Z. Jeffrey Chen
LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
BMC Genomics
author_facet Atsumi Ando
Ryan C. Kirkbride
Don C. Jones
Jane Grimwood
Z. Jeffrey Chen
author_sort Atsumi Ando
title LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
title_short LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
title_full LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
title_fullStr LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
title_full_unstemmed LCM and RNA-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
title_sort lcm and rna-seq analyses revealed roles of cell cycle and translational regulation and homoeolog expression bias in cotton fiber cell initiation
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2021-04-01
description 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.
url https://doi.org/10.1186/s12864-021-07579-1
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