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Equal parental contribution to the transcriptome is not equal control of embryogenesis

Abstract

In animals, early embryogenesis is maternally controlled, whereas in plants, parents contribute equally to the proembryo transcriptome. Thus, the question remains whether equivalent parental contribution to the transcriptome of the early proembryo means equal control of early embryogenesis. Here, on the basis of cell-lineage-specific and allele-specific transcriptome analysis, we reveal that paternal and maternal genomes contribute equally to the transcriptomes of both the apical cell lineage and the basal cell lineage of early proembryos. However, a strong maternal effect on basal cell lineage development was found, indicating that equal parental contribution to the transcriptome is not necessarily coupled with equivalent parental control of proembryonic development. Parental contributions to embryogenesis therefore cannot be concluded solely on the basis of the ratio of paternal/maternal transcripts. Furthermore, we demonstrate that parent-of-origin genes display developmental-stage-dependent and cell-lineage-dependent allelic expression patterns. These findings will facilitate the investigation of specific parental roles in specific processes of early embryogenesis.

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Fig. 1: Parental contributions to the transcriptomes of ACLs and BCLs of early proembryos.
Fig. 2: Identification of parent-of-origin genes in the transcriptomes of ACLs and BCLs.
Fig. 3: Allele-specific expression analysis of parent-of-origin genes in zygotes, ACLs and BCLs of early proembryos.
Fig. 4: ACs and BCs inherit distinct allelic expression patterns of parent-of-origin genes from the zygote upon asymmetric cell division.
Fig. 5: Allelic expression patterns of parent-of-origin genes are dependent on developmental stage and cell lineage.
Fig. 6: Maternal effect on BCL development in early embryogenesis.
Fig. 7: GO and KEGG analysis of MEGs and PEGs identified in the BCL.

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Data availability

All RNA-seq data have been uploaded to the NCBI Gene Expression Omnibus (GEO) under accession no. GSE107700. Previously published RNA-seq data (GEO accession nos GSE120669, GSE121003 and GSE135422) were also used in the present study. The GO terms for each annotated gene and SNPs between the Col-0 and Ler genomes were downloaded from the TAIR (https://www.arabidopsis.org/). The pathway information for Arabidopsis genes was downloaded from the KEGG database (https://www.genome.jp/). Source data are provided with this paper.

Code availability

The in-house script for clean reads preparation is available from GitHub at https://github.com/frasergen-rna/FraserQC. Other details of the code for data analysis of the present study are available from the corresponding authors upon reasonable request.

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Acknowledgements

We thank W.-C. Yang (Institute of Genetics and Developmental Biology, CAS, China) and G. Drews (University of Utah, Salt Lake City, UT, USA) for their kind offer of DD45::GFP marker lines in the Ler and Col-0 backgrounds. This work was supported by the National Natural Science Foundation of China (grant nos 31770355 and 31970340) and the Fundamental Research Funds of the Central Universities (grant nos 2042020kf0198 and 2042020kf1074). We thank G. Yuan (Frasergen Bioinformatics Co., Ltd) for a suggestion regarding the data analysis.

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Authors and Affiliations

Authors

Contributions

P.Z. and M.-x.S. designed the experiments. P.Z., X.Z., Y.Z. and Y.R. performed the experiments. P.Z., X.Z. and M.-x.S. analysed the data. P.Z. and M.-x.S. wrote the manuscript. All authors discussed the results and agreed on the manuscript before submission.

Corresponding authors

Correspondence to Peng Zhao or Meng-xiang Sun.

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Competing interests

The authors declare no competing interests.

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Peer review information Nature Plants thanks Takashi Okamoto and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 RNA-seq data of the same cell type from reciprocal crosses between Col-0 and Ler are highly correlated.

The correlation coefficients among different samples are calculated according to the Pearson’s correlation coefficient method. AC, apical cell; BC, basal cell; 32E, embryo proper of the 32-cell emrbyo; 32S, suspensor of the 32-cell embryo. CAC, hybrid AC from the cross between Col-0 and Ler; LAC, hybrid AC from the cross between Ler and Col-0. Similar abbreviations are also used for CBC, LBC, C32E, L32E, C32S and L32S.

Extended Data Fig. 2 Detection of RNA contamination in each transcriptome.

Heat map displaying the results of tissue enrichment test of the transcriptomes of hybrid AC, BC, 32E and 32 S from the reciprocal crosses between Col-0 and Ler. EP, embryo proper; SUS, suspensor; MCE, micropylar endosperm; PEN, peripheral endosperm; CZE, chalazal endosperm; CZSC, chalazal seed coat; GSC, general seed coat.

Extended Data Fig. 3 Expression profiles of MEGs and PEGs identified in apical and basal cell lineages.

a, b, Expression profiles of MEGs (a) and PEGs (b) identified from apical cell lineage in sperm cells, egg cells, zygotes, apical and basal cell lineages of early proembryos. c, d, Expression profiles of MEGs (c) and PEGs (d) identified from basal cell lineage in the sperm cells, egg cells, zygotes, apical and basal cell lineages of early proembryos. Color lines in each plot indicate the mean expression level of all the genes in each group. SP, sperm cell, EC, egg cell; Zy14, zygote at 14 h after pollination; Zy24, zygote at 24 h after pollination; MEGs, maternally expressed genes; PEGs, paternally expressed genes.

Extended Data Fig. 4 The expression levels of MEGs and PEGs in sperm cells, egg cells, zygotes, apical and basal cell lineages of early proembryos.

RT-qPCR was used to analyze relative expression levels of MEGs and PEGs in sperm cells, egg cells, zygotes, apical and basal cell lineages of early proembryos. The expression level of each gene in Zy14 is set as 1. Data represent meant ± standard error from three independent experiments.

Extended Data Fig. 5 Allele-specific expression analysis of parent-of-origin genes in apical and basal cell lineages of early proembryos.

a–k, Sanger sequencing chromatographs of PCR products at selected SNP sites showing allelic expression pattern of parent-of-origin genes. cDNA of apical and basal cell lineages of early proembryos from the reciprocal crosses between Arabidopsis Col-0 and Ler were prepared for RT-PCR and Sanger sequencing. Genomic DNA (gDNA) of Arabidopsis Col-0, Ler and F1 hybrids from the reciprocal crosses between Col-0 and Ler were used as the controls. The polymorphic nucleotide was underlined in each chromatogram. BEGs, biparentally expressed genes.

Extended Data Fig. 6 Morphological characteristics of Arabidopsis Col-0 and Ler egg cell.

a, Typical morphology of egg cells from Arabidopsis Col-0 and Ler. Scale bars, 10 μm. b, No significant differences in the length of egg cells from Arabidopsis Col-0 and Ler. Data represent the mean ± SD. (n = 54 for Col-0; 50 for Ler). Statistical analysis was performed using two-tailed Student’s t-tests; ns indicates no significant difference.

Source data

Extended Data Fig. 7 Morphological characteristics of apical cell of isogenic and hybrid 2-cell proembryos.

a, Statistics data for the length of apical cell from different Arabidopsis ecotypes. (C24, n = 97; Col-0, n = 156; Cvi, n = 121; Ler, n = 136; Ws, n = 134). b, Representative pictures of isogenic and hybrid 2-cell proembryos from the reciprocal crosses between Ler and Cvi. Scale bars, 20 μm. c, Statistics data for the length of hybrid apical cells from the reciprocal crosses between Ler and Cvi. (Ler, n = 136; Cvi, n = 121; Ler × Cvi, n = 151; Cvi × Ler, n = 125). Data for cell length are presented in Box-and-Whiskers plots. The bottom and top of each box represent 25th and 75th percentiles, respectively. The center line represents 50th percentile; and Whiskers in each box plot indicate the minimum and maximum value. Statistical analysis was performed using two-tailed Student’s t-tests; ** indicates P < 0.01; ns indicates no significant difference.

Source data

Supplementary information

Supplementary Information

Supplementary Tables 1–3.

Reporting Summary

Supplementary Data 1

Parental contributions to the expression of each gene in hybrid apical and basal cell lineages of early proembryos from reciprocal crosses between Col-0 and Ler. The number of Col-0 and Ler reads covering the SNPs of each gene in the transcriptome of apical and basal cell lineages of early proembryos was calculated. Each datum indicates the comprehensive results of three independent biological replicates. Statistical analysis was performed using binomial distribution two-sided tests, and the P values were adjusted using the false discovery rate method.

Supplementary Data 2

GO analysis of paternally and maternally expressed genes identified in apical and basal cell lineages of early proembryos.

Supplementary Data 3

KEGG analysis of paternally and maternally expressed genes identified in apical and basal cell lineages of early proembryos.

Supplementary Data 4

GO and KEGG analysis of MEGs detected in the basal cell lineage at both 1-cell and 32-cell embryo stages.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 5

Statistical source data.

Source Data Fig. 6

Statistical source data.

Source Data Extended Data Fig. 6

Statistical source data.

Source Data Extended Data Fig. 7

Statistical source data.

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Zhao, P., Zhou, X., Zheng, Y. et al. Equal parental contribution to the transcriptome is not equal control of embryogenesis. Nat. Plants 6, 1354–1364 (2020). https://doi.org/10.1038/s41477-020-00793-x

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