title: Timing of Tissue-specific Cell Division Requires a Differential Onset of Zygotic Transcription during Metazoan Embryogenesis.
abstract: Metazoan development demands not only precise cell fate differentiation but also accurate timing of cell division to ensure proper development. How cell divisions are temporally coordinated during development is poorly understood. Caenorhabditis elegans embryogenesis provides an excellent opportunity to study this coordination due to its invariant development and widespread division asynchronies. One of the most pronounced asynchronies is a significant delay of cell division in two endoderm progenitor cells, Ea and Ep, hereafter referred to as E2, relative to its cousins that mainly develop into mesoderm organs and tissues. To unravel the genetic control over the endoderm-specific E2 division timing, a total of 822 essential and conserved genes were knocked down using RNAi followed by quantification of cell cycle lengths using in toto imaging of C. elegans embryogenesis and automated lineage. Intriguingly, knockdown of numerous genes encoding the components of general transcription pathway or its regulatory factors leads to a significant reduction in the E2 cell cycle length but an increase in cell cycle length of the remaining cells, indicating a differential requirement of transcription for division timing between the two. Analysis of lineage-specific RNA-seq data demonstrates an earlier onset of transcription in endoderm than in other germ layers, the timing of which coincides with the birth of E2, supporting the notion that the endoderm-specific delay in E2 division timing demands robust zygotic transcription. The reduction in E2 cell cycle length is frequently associated with cell migration defect and gastrulation failure. The results suggest that a tissue-specific transcriptional activation is required to coordinate fate differentiation, division timing, and cell migration to ensure proper development.
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Ming-Kin
authors.initials: MK
authors.lastname: Wong
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Daogang
authors.initials: D
authors.lastname: Guan
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Kaoru Hon Chun
authors.initials: KHC
authors.lastname: Ng
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Vincy Wing Sze
authors.initials: VWS
authors.lastname: Ho
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Xiaomeng
authors.initials: X
authors.lastname: An
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Runsheng
authors.initials: R
authors.lastname: Li
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China.
authors.forename: Xiaoliang
authors.initials: X
authors.lastname: Ren
authors.affiliation: Department of Biology, Hong Kong Baptist University, Hong Kong Baptist University, Hong Kong, China; State Key Laboratory of Environmental and Biological Analysis, Hong Kong Baptist University, Hong Kong, China. Electronic address: zyzhao@hkbu.edu.hk.
authors.forename: Zhongying
authors.initials: Z
authors.lastname: Zhao
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D017173:Caenorhabditis elegans / Q000166:cytology / Q000196:embryology / Q000235:genetics*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics; D002453:Cell Cycle / Q000235:genetics; D002454:Cell Differentiation / Q000235:genetics; D002455:Cell Division / Q000235:genetics; D019070:Cell Lineage / Q000235:genetics; D002465:Cell Movement / Q000235:genetics; D004625:Embryo, Nonmammalian / Q000166:cytology / Q000196:embryology / Q000378:metabolism*; D047108:Embryonic Development / Q000235:genetics; D004707:Endoderm / Q000166:cytology / Q000196:embryology / Q000378:metabolism; D020869:Gene Expression Profiling / Q000379:methods*; D018507:Gene Expression Regulation, Developmental; D008648:Mesoderm / Q000166:cytology / Q000196:embryology / Q000378:metabolism; D009928:Organ Specificity / Q000235:genetics*; D034622:RNA Interference; D013997:Time Factors
chemical_list: D029742:Caenorhabditis elegans Proteins
keywords: Caenorhabditis elegans (C. elegans); cell cycle; cell cycle length; cell differentiation; embryo; embryogenesis; endoderm; transcription