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Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos

Abstract

In animals, maternal gene products deposited into eggs regulate embryonic development before activation of the zygotic genome1. In plants, an analogous period of prolonged maternal control over embryogenesis is thought to occur based on some gene-expression studies2,3,4,5,6. However, other gene-expression studies and genetic analyses show that some transcripts must derive from the early zygotic genome7,8,9,10,11,12,13,14, implying that the prevailing model does not fully explain the nature of zygotic genome activation in plants. To determine the maternal, paternal and zygotic contributions to the early embryonic transcriptome, we sequenced the transcripts of hybrid embryos from crosses between two polymorphic inbred lines of Arabidopsis thaliana and used single-nucleotide polymorphisms diagnostic of each parental line to quantify parental contributions. Although some transcripts seemed to be either inherited from primarily one parent or transcribed from imprinted loci, the vast majority of transcripts were produced in near-equal amounts from both maternal and paternal alleles, even during the initial stages of embryogenesis. Results of reporter experiments and analyses of transcripts from genes that are not expressed in sperm and egg indicate early and widespread zygotic transcription. Thus, in contrast to early animal embryogenesis, early plant embryogenesis is mostly under zygotic control.

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Figure 1: Maternal and paternal genomes contribute equally to the early embryonic transcriptome.
Figure 2: Maternally and paternally inherited transgenes are transcribed in the initial stages of embryogenesis.
Figure 3: Dozens of transcripts are preferentially inherited or preferentially expressed.

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Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

Raw and processed RNA-seq data sets have been deposited into NCBI GEO (http://www.ncbi.nlm.nih.gov/geo/) under accession number GSE33713.

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Acknowledgements

We thank J. Ecker and the 1001 Genomes Project for generating the list of Cvi-0 SNPs; the J. Harada and R. Goldberg laboratories for making the Arabidopsis seed development LCM microarray data sets publicly available; I. Moore for the transactivation vectors; J. Long for the UBI3 promoter fragment; the Whitehead Genome Technology Core for sequencing; and D. Meinke for providing a curated list of preglobular zygotic-recessive mutants before publication. This work used the W. M. Keck Biological Imaging Facility at the Whitehead Institute and was supported by NIH grant GM067031 (D.P.B.) and NIH Postdoctoral Fellowship GM084656 (M.D.N). D.P.B. is an Investigator of the Howard Hughes Medical Institute.

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Authors

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M.D.N. designed and performed the experiments. M.D.N. and D.P.B. interpreted the results and wrote the manuscript.

Corresponding author

Correspondence to David P. Bartel.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-3 with legends and Supplementary Tables 1-5. It includes RNA-Seq statistics, independent validation of parental enrichments, analyses of potential contamination by seed-coat mRNA in our datasets and the dataset of ref. 2, percentile ranks of RNA polymerase II transcript levels, a list of the oligonucleotides used in this study and maternal-to-paternal ratios for transcripts that correspond to preglobular zygotic-recessive genes. (PDF 571 kb)

Supplementary Data

This file contains Supplementary Data files 1-3, which comprise: 1. RNA-Seq results for all genes that have at least one overlapping read in at least one stage. Includes numbers of reads overlapping genes, numbers of reads overlapping SNPs within each gene, presence/absence in egg/sperm datasets, RPM percentile ranks, maternal-to-paternal ratios and changes in transcript levels between 1-cell/2-cell and 8-cell embryos; 2. RNA-Seq values and functional annotations for genes with transcripts enriched for Col-0 or Cvi-0 isoforms. It includes the total number of reads overlapping SNPs contained within each gene, the corresponding Col-0/Cvi-0 ratios and TAIR10 functional annotations and 3. RNA-Seq values and functional annotations for genes with transcripts maternally or paternally enriched. It includes the total number of reads overlapping SNPs contained within each gene, the corresponding maternal-to-paternal ratios, mean-centered transcript levels and TAIR10 functional annotations. (ZIP 17471 kb)

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Nodine, M., Bartel, D. Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482, 94–97 (2012). https://doi.org/10.1038/nature10756

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