Imprinting in plants as a mechanism to generate seed phenotypic diversity

Abstract

Normal plant development requires epigenetic regulation to enforce changes in developmental fate. Genomic imprinting is a type of epigenetic regulation in which identical alleles of genes are expressed in a parent-of-origin dependent manner. Deep sequencing of transcriptomes has identified hundreds of imprinted genes with scarce evidence for the developmental importance of individual imprinted loci. Imprinting is regulated through global DNA demethylation in the central cell prior to fertilization and directed repression of individual loci with the Polycomb Repressive Complex 2 (PRC2). There is significant evidence for transposable elements and repeat sequences near genes acting as cis-elements to determine imprinting status of a gene, implying that imprinted gene expression patterns may evolve randomly and at high frequency. Detailed genetic analysis of a few imprinted loci suggests an imprinted pattern of gene expression is often dispensable for seed development. Few genes show conserved imprinted expression within or between plant species. These data are not fully explained by current models for the evolution of imprinting in plant seeds. We suggest that imprinting may have evolved to provide a mechanism for rapid neofunctionalization of genes during seed development to increase phenotypic diversity of seeds.

Keywords: Arabidopsis endosperm; DNA methylation; epigenetics; genomics; histone modification; imprinting; maize endosperm; seed development.

FIGURE 1

Comparison of seed development in maize and Arabidopsis thaliana. The endosperm proliferates initially as a multi-nucleate syncytium, while the globular embryo develops. Endosperm cellularization precedes embryo transition. Endosperm cells expand and accumulate storage molecules once cellularization is complete. In maize, the endosperm is persistent and undergoes programmed cell death starting around 18 days after pollination (DAP). The Arabidopsis embryo consumes most of the endosperm prior to seed maturation. Endosperm (endo) nuclei are indicated in red. The embryo (em) is in green.

FIGURE 2

Comparison of Mendelian genetic inheritance and imprinted inheritance. (A) The a1 locus shows Mendelian inheritance in self-pollinations of A1/a1 individuals. Full purple color kernels are dominant over yellow kernels and the progeny segregate in a 3:1 ratio. (B) The R^r allele shows imprinted inheritance. Self-pollination of R^r/r yields three kernel color types in a 2:1:1 ratio of purple to mottled to yellow kernels. Purple kernels inherited the R^r allele from the megagametophyte. Mottled kernels are heterozygous individuals that inherited the R^r allele from the pollen. Kernel counts are given for the ears shown in the upper panels.