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Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis

Nature volume 514, pages 624–627 (2014)Cite this article

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Abstract

Zygotic genome activation in metazoans typically occurs several hours to a day after fertilization, and thus maternal RNAs and proteins drive early animal embryo development1. In plants, despite several molecular studies of post-fertilization transcriptional activation, the timing of zygotic genome activation remains a matter of debate. For example, two recent reports that used different hybrid ecotype combinations for RNA sequence profiling of early Arabidopsis embryo transcriptomes came to divergent conclusions. One identified paternal contributions that varied by gene, but with overall maternal dominance2, while the other found that the maternal and paternal genomes are transcriptionally equivalent3. Here we assess paternal gene activation functionally in an isogenic background, by performing a large-scale genetic analysis of 49 EMBRYO DEFECTIVE genes and testing the ability of wild-type paternal alleles to complement phenotypes conditioned by mutant maternal alleles. Our results demonstrate that wild-type paternal alleles for nine of these genes are completely functional 2 days after pollination, with the remaining 40 genes showing partial activity beginning at 2, 3 or 5 days after pollination. Using our functional assay, we also demonstrate that different hybrid combinations exhibit significant variation in paternal allele activation, reconciling the apparently contradictory results of previous transcriptional studies2,3. The variation in timing of gene function that we observe confirms that paternal genome activation does not occur in one early discrete step, provides large-scale functional evidence that maternal and paternal genomes make non-equivalent contributions to early plant embryogenesis, and uncovers an unexpectedly profound effect of hybrid genetic backgrounds on paternal gene activity.

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Figure 1: Paternal allele activation in early Arabidopsis embryogenesis varies between genes.
Figure 2: Delayed molecular and functional activity for GCT and CCT paternal alleles in early embryogenesis.
Figure 3: Gene activation kinetics differ between isogenic and hybrid embryos.

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Acknowledgements

This study was facilitated by the efforts of D. Meinke and collaborators in creating and maintaining the SeedGenes Project (http://www.seedgenes.org). Seeds were obtained from the Arabidopsis Biological Resource Center (http://abrc.osu.edu). We thank S. Poethig, in whose laboratory C.S.G. generated GCT and CCT GUS reporter constructs, K. Gallagher for reagents, C. Silva-Ortega for preliminary experiments, A. de Luna, D. Lepe-Soltero and C. Abreu-Goodger for suggestions on data analysis and presentation, R. Datla for suggesting Col/Tsu hybrid, D. Bergmann for advice, and L. Herrera-Estrella, D. Autran, C. Baroux, J.-P. Vielle-Calzada and D. Grimanelli for reading the manuscript. Research was supported by a CONACyT graduate fellowship to G.D.T.-D.L. (No. 300802), a CONACyT postdoctoral fellowship to M.G.-A., a CONACyT research grant (Ciencia Básica No. 152333) to C.S.G., and by CINVESTAV institutional funds.

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Authors and Affiliations

  1. Laboratorio Nacional de Genómica para la Biodiversidad (Langebio), Unidad de Genómica Avanzada, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), Irapuato, Guanajuato 36821, México,

    Gerardo Del Toro-De León, Marcelina García-Aguilar & C. Stewart Gillmor

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  1. Gerardo Del Toro-De León
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  2. Marcelina García-Aguilar
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  3. C. Stewart Gillmor
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Contributions

G.D.T.-D.L. performed phenotypic characterization of emb phenotypes and embryo complementation experiments with assistance from M.G.-A. and C.S.G.; C.S.G. made GUS reporter constructs; M.G.-A. performed GUS reporter experiments with assistance from G.D.T.-D.L.; G.D.T.-D.L., M.G.-A. and C.S.G. analysed data; G.D.T.-D.L. and C.S.G. wrote the paper.

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Correspondence to C. Stewart Gillmor.

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The authors declare no competing financial interests.

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This file contains Supplementary Tables 1-6 and Supplementary Dataset 1. (PDF 16077 kb)

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Del Toro-De León, G., García-Aguilar, M. & Gillmor, C. Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514, 624–627 (2014). https://doi.org/10.1038/nature13620

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