The evolution of imprinting in plants: beyond the seed

Abstract

Genomic imprinting results in the biased expression of alleles depending on if the allele was inherited from the mother or the father. Despite the prevalence of sexual reproduction across eukaryotes, imprinting is only found in placental mammals, flowering plants, and some insects, suggesting independent evolutionary origins. Numerous hypotheses have been proposed to explain the selective pressures that favour the innovation of imprinted gene expression and each differs in their experimental support and predictions. Due to the lack of investigation of imprinting in land plants, other than angiosperms with triploid endosperm, we do not know whether imprinting occurs in species lacking endosperm and with embryos developing on maternal plants. Here, we discuss the potential for uncovering additional examples of imprinting in land plants and how these observations may provide additional support for one or more existing imprinting hypotheses.

Exploring Breakthroughs in Three Traits Belonging to Seed Life

“…On the other hand, the number of PEGs was much lower than the number of MEGs in species as A. thaliana, maize, B. napus, sorghum and A. lyrata. The unbalanced MEGs and PEGs in plants agreed with the maternal-offspring co-adaptation theory, indicating that the maternal genes were more favored during natural selection [70]. In the present year, a work on the genomic imprinted genes of dicot B. napus endosperm provided 297 imprinted genes, including 283 MEGs and 14 PEGs.…”

“…In mammals, approximately 80% of the imprinted genes are clustered on chromosomes; but in plants, the majority of the imprinted genes are scattered on chromosomes. At present, and unlike in mammals, a wide debate exists regarding the conservation of the imprinted status in plants (for update see [70]). That is, in developing the seeds of higher plants, some genes show biased gene expression of the allele descended from a particular parent [71].…”

“…Given the interest in imprinting in higher plants, numerous updates have been published recently [69,70,80,[94][95][96]. By using: (i) the rapid development of modern technologies (e.g., CRISPR/Cas9, protein-DNA interactions by CUT&RUN, high-throughput transcriptome sequencing, and single-cell RNA sequencing, among others), together with yeast two-hybrid tests; and (ii) the F1 hybrid seeds derived from reciprocal crosses of plants with different ploidy levels to provide different dosages of the parental genomes, a direct genome-wide survey of imprinted genes at the transcription level has become possible.…”

Polycomb-mediated repression of paternal chromosomes maintains haploid dosage in diploid embryos of Marchantia

“…Why gene dosage control in Marchantia was achieved through imprinting might be explained by the fact that ancestor of bryophytes had separate sexes (Iwasaki et al, 2021) and embryos developed on mothers. It is thus likely that viviparity and its collateral maternal support of embryo development favored the evolution of imprinting as a way to impose maternal control, as proposed by a body of theoretical works (Carey et al, 2021; Haig, 2013; Haig & Wilczek, 2006; Montgomery & Berger, 2021; Shaw et al, 2011). Imprinting has not been discovered in viviparous non-therian animals, but only orthologous loci imprinted in mammals were investigated, thus a genome-wide search may yield new insights (Griffith, Brandley, Belov, & Thompson, 2016; Lawton et al, 2005; Renfree, Suzuki, & Kaneko-Ishino, 2013).…”

“…One of the two major land plant lineages, bryophytes, also evolved viviparity without extraembryonic tissues comparable with the endosperm of flowering plants. While it has been theorized that bryophytes may have imprinting, these predictions have not been tested experimentally [21][22][23][24][25] .…”