The Zygotic Transition Is Initiated in Unicellular Plant Zygotes with Asymmetric Activation of Parental Genomes

The zygotic transition, from a fertilized egg to an embryo, is central to animal and plant reproduction. Animal embryos depend upon maternally provided factors until zygotic genome activation (ZGA). In plants, the timing and parental genome contributions to ZGA are unresolved. Here, we use the flowe...

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Published in:Developmental cell Vol. 43; no. 3; pp. 349 - 358.e4
Main Authors: Anderson, Sarah N., Johnson, Cameron S., Chesnut, Joshua, Jones, Daniel S., Khanday, Imtiyaz, Woodhouse, Margaret, Li, Chenxin, Conrad, Liza J., Russell, Scott D., Sundaresan, Venkatesan
Format: Journal Article
Language:English
Published: United States Elsevier Inc 06-11-2017
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Abstract The zygotic transition, from a fertilized egg to an embryo, is central to animal and plant reproduction. Animal embryos depend upon maternally provided factors until zygotic genome activation (ZGA). In plants, the timing and parental genome contributions to ZGA are unresolved. Here, we use the flowering plant Oryza sativa (rice) to characterize transcriptomes of time-staged isogenic and hybrid zygotes following fertilization. Large-scale transcriptomic changes were observed in unicellular zygotes, including upregulation of S-phase genes, a characteristic of ZGA. The parental contributions to ZGA were highly asymmetric. Zygotic transcription was primarily from the maternal genome and included genes for basic cellular processes. Transcription of the paternal genome was highly restricted but unexpectedly included genes encoding putative pluripotency factors expressed at the onset of ZGA. Thus, distinct transcriptional activities are exhibited by the parental genomes during the initiation of embryogenesis, which presumptively derive from divergent pre-zygotic transcriptional states established in the gametes. [Display omitted] •Zygotic genome activation in plants initiates soon after fertilization•Genes for S phase are primarily expressed from the maternal genome•Putative embryogenic transcription factors are expressed before the S-phase genes•Paternal genome expression includes expression of putative pluripotency factors The transition from maternal to zygotic gene expression is critical to multicellular organism development. Anderson et al. elucidate timing and parental genome contribution to zygotic genome activation (ZGA) in rice. ZGA occurs in the unicellular zygote, with unequal parental contribution where most genes are expressed primarily from the maternal genome.
AbstractList The zygotic transition, from a fertilized egg to an embryo, is central to animal and plant reproduction. Animal embryos depend upon maternally provided factors until zygotic genome activation (ZGA). In plants, the timing and parental genome contributions to ZGA are unresolved. Here, we use the flowering plant Oryza sativa (rice) to characterize transcriptomes of time-staged isogenic and hybrid zygotes following fertilization. Large-scale transcriptomic changes were observed in unicellular zygotes, including upregulation of S-phase genes, a characteristic of ZGA. The parental contributions to ZGA were highly asymmetric. Zygotic transcription was primarily from the maternal genome and included genes for basic cellular processes. Transcription of the paternal genome was highly restricted but unexpectedly included genes encoding putative pluripotency factors expressed at the onset of ZGA. Thus, distinct transcriptional activities are exhibited by the parental genomes during the initiation of embryogenesis, which presumptively derive from divergent pre-zygotic transcriptional states established in the gametes. [Display omitted] •Zygotic genome activation in plants initiates soon after fertilization•Genes for S phase are primarily expressed from the maternal genome•Putative embryogenic transcription factors are expressed before the S-phase genes•Paternal genome expression includes expression of putative pluripotency factors The transition from maternal to zygotic gene expression is critical to multicellular organism development. Anderson et al. elucidate timing and parental genome contribution to zygotic genome activation (ZGA) in rice. ZGA occurs in the unicellular zygote, with unequal parental contribution where most genes are expressed primarily from the maternal genome.
The zygotic transition, from a fertilized egg to an embryo, is central to animal and plant reproduction. Animal embryos depend upon maternally provided factors until zygotic genome activation (ZGA). In plants, the timing and parental genome contributions to ZGA are unresolved. Here, we use the flowering plant Oryza sativa (rice) to characterize transcriptomes of time-staged isogenic and hybrid zygotes following fertilization. Large-scale transcriptomic changes were observed in unicellular zygotes, including upregulation of S-phase genes, a characteristic of ZGA. The parental contributions to ZGA were highly asymmetric. Zygotic transcription was primarily from the maternal genome and included genes for basic cellular processes. Transcription of the paternal genome was highly restricted but unexpectedly included genes encoding putative pluripotency factors expressed at the onset of ZGA. Thus, distinct transcriptional activities are exhibited by the parental genomes during the initiation of embryogenesis, which presumptively derive from divergent pre-zygotic transcriptional states established in the gametes.
Author Johnson, Cameron S.
Jones, Daniel S.
Conrad, Liza J.
Chesnut, Joshua
Woodhouse, Margaret
Li, Chenxin
Sundaresan, Venkatesan
Anderson, Sarah N.
Khanday, Imtiyaz
Russell, Scott D.
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  fullname: Johnson, Cameron S.
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  organization: Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA
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  surname: Jones
  fullname: Jones, Daniel S.
  organization: Department of Microbiology and Plant Biology, University of Oklahoma, Norman, OK 73019, USA
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  givenname: Imtiyaz
  surname: Khanday
  fullname: Khanday, Imtiyaz
  organization: Department of Plant Biology, University of California, Davis, CA 95616, USA
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  fullname: Woodhouse, Margaret
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  surname: Li
  fullname: Li, Chenxin
  organization: Department of Plant Biology, University of California, Davis, CA 95616, USA
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  givenname: Liza J.
  surname: Conrad
  fullname: Conrad, Liza J.
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  givenname: Scott D.
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  givenname: Venkatesan
  surname: Sundaresan
  fullname: Sundaresan, Venkatesan
  email: sundar@ucdavis.edu
  organization: Department of Plant Biology, University of California, Davis, CA 95616, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29112853$$D View this record in MEDLINE/PubMed
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Issue 3
Keywords genome activation
plant development
maternal to zygotic transition
fertilization
plant reproduction
Language English
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Snippet The zygotic transition, from a fertilized egg to an embryo, is central to animal and plant reproduction. Animal embryos depend upon maternally provided factors...
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SubjectTerms Arabidopsis - genetics
fertilization
Gene Expression Regulation, Plant - genetics
Genes, Plant - genetics
genome activation
Genome, Plant - genetics
maternal to zygotic transition
plant development
plant reproduction
Seeds
Transcriptional Activation - genetics
Transcriptome - genetics
Title The Zygotic Transition Is Initiated in Unicellular Plant Zygotes with Asymmetric Activation of Parental Genomes
URI https://dx.doi.org/10.1016/j.devcel.2017.10.005
https://www.ncbi.nlm.nih.gov/pubmed/29112853
https://search.proquest.com/docview/1961856447
Volume 43
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