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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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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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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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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DOI: https://doi.org/10.1038/nature13620
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