Hybridization alters maternal and paternal genome contributions to early plant embryogenesis

Abstract

After fertilization, zygotic genome activation (ZGA) results in a transcriptionally competent embryo. Hybrid transcriptome experiments in Arabidopsis have concluded that the maternal and paternal genomes make equal contributions to zygotes and embryos, yet embryo defective (emb) mutants in the Columbia (Col) ecotype display early maternal effects. Here we show that hybridization of Col with Landsberg erecta (Ler) or Cape Verde Islands (Cvi) ecotypes decreases maternal effects of emb mutants. Reanalysis of Col/Ler and Col/Cvi transcriptomes confirmed equal parental contributions in Col/Cvi early embryos. By contrast, thousands of genes in Col/Ler zygotes and 1-cell embryos were biallelic in one cross and monoallelic in the reciprocal cross, with analysis of intron reads pointing to active transcription as responsible for this parent-of-origin bias. Our analysis shows that, contrary to previous conclusions, the maternal and paternal genomes in Col/Ler zygotes are activated in an asymmetric manner. The decrease in maternal effects in hybrid embryos compared to isogenic Col plus differences in genome activation between Col/Cvi and Col/Ler suggest that neither of these hybrids accurately reflects general trends of parent-of-origin regulation in Arabidopsis embryogenesis.

Paternal DNA methylation is remodeled to maternal levels in rice zygote

“…15a, b ), indicating an increased paternal contribution to gene expression in GE, as observation in Arabidopsis 12 , 13 , 15 , which was consistent with the reestablishment of the parental allelic-specific DNA methylome in GE. It is shown that increased paternal allele contributions from embryo genes by the globular stage have functional significance in Arabidopsis embryogenesis 13 , 15 . Analysis of monoallelic gene expression in the reciprocal hybrid GEs identified 102 PEGs and 350 MEGs (Supplementary Fig.…”

“…Several genes such as GAMETE EXPRESSED PROTEIN1 (GEX1), RALF-like secreted peptide RALF3, and Arabinogalactan protein 7 (AGP7) were shown to function in male gametophyte development and during early embryogenesis 13,[41][42][43] . Recent results showed that gex1 mutants condition both maternal and paternal effects in early embryogenesis 13 , providing genetic evidence that paternal GEX1 transcripts have a function in early embryos. Nearly all (26/28) of the PEGs showed a low expression in the egg cells (Fig.…”

“…However, a reanalysis of the published data 6 , 7 showed that, on a gene-by-gene basis, the Arabidopsis hybrid (Col/Ler) zygotes do not show equal parental transcriptome contributions; thousands of genes in hybrid zygotes are represented by transcripts from either the maternal or paternal allele, but not both 13 . There is also genetic evidence that maternal alleles of most embryo genes make a more important contribution functional to early embryogenesis than paternal alleles, and that hybridization itself can affect parental genome contributions to early embryogenesis 13 , 15 . In rice, analysis of allele-specific transcriptome in the zygote revealed that transcription of the zygotic genome is mainly from the maternal alleles, which results in a maternally dominated transcriptome 9 .…”

“…However, parental contribution to the zygotic transcriptome in plants is under debate 5,11 . Studies in Arabidopsis revealed that maternal transcripts dominate the transcriptomes of embryos at the 2-4 cell and globular stages 12,13 , whereas other results indicated that maternal and paternal genomes contribute equally to the transcriptome of early embryos, even at the 1-2 cell stage or elongated zygotes 6,7,14 . However, a reanalysis of the published data 6,7 showed that, on a gene-by-gene basis, the Arabidopsis hybrid (Col/Ler) zygotes do not show equal parental transcriptome contributions; thousands of genes in hybrid zygotes are represented by transcripts from either the maternal or paternal allele, but not both 13 .…”

“…Studies in Arabidopsis revealed that maternal transcripts dominate the transcriptomes of embryos at the 2-4 cell and globular stages 12,13 , whereas other results indicated that maternal and paternal genomes contribute equally to the transcriptome of early embryos, even at the 1-2 cell stage or elongated zygotes 6,7,14 . However, a reanalysis of the published data 6,7 showed that, on a gene-by-gene basis, the Arabidopsis hybrid (Col/Ler) zygotes do not show equal parental transcriptome contributions; thousands of genes in hybrid zygotes are represented by transcripts from either the maternal or paternal allele, but not both 13 . There is also genetic evidence that maternal alleles of most embryo genes make a more important contribution functional to early embryogenesis than paternal alleles, and that hybridization itself can affect parental genome contributions to early embryogenesis 13,15 .…”