Maternal Epigenetic Pathways Control Parental Contributions to Arabidopsis Early Embryogenesis

Abstract

Defining the contributions and interactions of paternal and maternal genomes during embryo development is critical to understand the fundamental processes involved in hybrid vigor, hybrid sterility, and reproductive isolation. To determine the parental contributions and their regulation during Arabidopsis embryogenesis, we combined deep-sequencing-based RNA profiling and genetic analyses. At the 2-4 cell stage there is a strong, genome-wide dominance of maternal transcripts, although transcripts are contributed by both parental genomes. At the globular stage the relative paternal contribution is higher, largely due to a gradual activation of the paternal genome. We identified two antagonistic maternal pathways that control these parental contributions. Paternal alleles are initially downregulated by the chromatin siRNA pathway, linked to DNA and histone methylation, whereas transcriptional activation requires maternal activity of the histone chaperone complex CAF1. Our results define maternal epigenetic pathways controlling the parental contributions in plant embryos, which are distinct from those regulating genomic imprinting.

Arabidopsis LORELEI, a Maternally Expressed Imprinted Gene, Promotes Early Seed Development

“…Additionally, monoallelic expression of LRE expression after fertilization in the developing seed is earlier than reported for other MEGs (Jahnke and Scholten, 2009;Ngo et al, 2012;Nodine and Bartel, 2012;Raissig et al, 2013). Because the patrigenic allele of LRE remains silent in various stages of seed development after 24 HAP Gehring et al, 2011;Hsieh et al, 2011;Nodine and Bartel, 2012;Raissig et al, 2013), our observations also cannot be explained by delayed paternal genome activation (Autran et al, 2011;Del Toro-De León et al, 2014;García-Aguilar and Gillmor, 2015). Based on these observations, we conclude that LRE expression is imprinted in both zygote and endosperm.…”

“…Loss of SUVH4 histone methyltransferase KRYPTONITE (KYP) function in the female gametophyte led to increased and earlier expression of the patrigenic alleles of RPS5a, AGP18, PROLIFERA, and GRP23 in the seeds of crosses between kyp mutant pistils and wild-type pollen (Autran et al, 2011). In other instances, maternal histone methylation activity is required for continued repression of the silent patrigenic allele of two MEGs after fertilization (Raissig et al, 2013).…”

Genomic Imprinting Was Evolutionarily Conserved during Wheat Polyploidization

“…In plants, imprinting primarily occurs in the endosperm; however, recent studies have shown that a portion of genes are also imprinted in the embryo of Arabidopsis thaliana (Raissig et al, 2013), rice (Oryza sativa) (Luo et al, 2011), and maize (Zea mays) (Meng et al, 2017). This uniparental transcription pattern indicates that, to some extent, parental genomes might not contribute equally to the filial genome, at least for some specific loci, if not at the genome-wide level (Vielle-Calzada et al, 2000;Grimanelli et al, 2005;Autran et al, 2011).…”

Imprinting meets genomics: new insights and new challenges

“…In contrast to animal models and a previous plant investigation, which described the embryo as predominantly controlled by the maternal genome [33], Nodine and Bartel found that maternally and paternally inherited genomes contribute largely equally to the early embryonic transcriptome. Apart from this interesting result, they also found a little over a hundred genes that exhibited parent of origin effects in at least one of the three stages investigated.…”