Regulation and Flexibility of Genomic Imprinting during Seed Development

Abstract

Genomic imprinting results in monoallelic gene expression in a parent-of-origin-dependent manner. It is achieved by the differential epigenetic marking of parental alleles. Over the past decade, studies in the model systems Arabidopsis thaliana and maize (Zea mays) have shown a strong correlation between silent or active states with epigenetic marks, such as DNA methylation and histone modifications, but the nature of the primary imprint has not been clearly established for all imprinted genes. Phenotypes and expression patterns of imprinted genes have fueled the perception that genomic imprinting is specific to the endosperm, a seed tissue that does not contribute to the next generation. However, several lines of evidence suggest a potential role for imprinting in the embryo, raising questions as to how imprints are erased and reset from one generation to the next. Imprinting regulation in flowering plants shows striking similarities, but also some important differences, compared with the mechanisms of imprinting described in mammals. For example, some imprinted genes are involved in seed growth and viability in plants, which is similar in mammals, where imprinted gene regulation is essential for embryonic development. However, it seems to be more flexible in plants, as imprinting requirements can be bypassed to allow the development of clonal offspring in apomicts.

A Role for CHH Methylation in the Parent-of-Origin Effect on Altered Circadian Rhythms and Biomass Heterosis inArabidopsisIntraspecific Hybrids

“…This model of the parent-of-origin effect on circadian rhythms and growth vigor is consistent with the parental conflict theory for imprinting in mammals and flowering plants, which predicts that the maternal genome provides factors that inhibit growth whereas the paternal genome carries the factors that promote growth (Moore and Haig, 1991;Ferguson-Smith, 2011;Raissig et al, 2011;Haig, 2013). This parental conflict theory could apply to the maternal effect of the clock function on growth vigor during the early stages of embryo development in hybrids and sexually reproducing organisms.…”

“…Parent-of-origin effects are often associated with paternal and maternal inheritance of DNA methylation patterns (Huh et al, 2008;Ferguson-Smith, 2011;Raissig et al, 2011), and methylation levels in promoter regions correlate with gene expression levels (Zilberman et al, 2007). To test this, we examined the methylation levels of CG, CHG, and CHH (where H = A, T, or C) sites in the CCA1 promoter region using the bisulfite sequencing method (Gruntman et al, 2008).…”

Seed evolution: parental conflicts in a multi-generational household

“…One extreme case of differential allelic expression is imprinting, where only one of the parental alleles is expressed. The maize R gene was the first imprinted locus to be discovered (49) and today several imprinted genes are known in flowering plants and mammals (reviewed in [50][51][52]. The evolutionary origins of imprinting are not well understood, but a theory proposed by David Haig and Mark Westoby (the parental-conflict theory of the evolution of genomic imprinting) offers a popular (but sometimes misinterpreted) explanation for some types of imprinting (39,53).…”

“…In addition to DNA methylation, imprinting in both plants and animals is also regulated by histone methylation (50,52,79,80). The Polycomb Repressive Complex 2 (PRC2) catalyzes trimethylation of histone H3 at lysine 27 (H3K27me3), a repressive mark associated with gene silencing.…”

Genetic Imprinting in Maize

“…ZmFie1 and ZmFie2 are maize orthologs of the Arabidopsis FIE gene, (Gutierrez-Marcos et al, 2006;Raissig et al, 2011). ZmFie1 is imprinted in the endosperm, which shows maternal expression, and Figure 1 Fertilization events in the angiosperms Note: Flowering plants undergo double fertilization and triple fusion; Two sperm are produced from a single meiotic division during micro-sporogenesis; One fertilizes the egg cell to produce the diploid embryo; The other fertilizes the diploid central cell to produce a triploid endosperm paternal expression is completely absent throughout seed development, which is repressed by DNA methylation of CpG island Gutierrez-Marcos et al, 2006;Huan and Springer;.…”