DNA Methylation Causes Predominant Maternal Controls of Plant Embryo Growth

Abstract

The parental conflict hypothesis predicts that the mother inhibits embryo growth counteracting growth enhancement by the father. In plants the DNA methyltransferase MET1 is a central regulator of parentally imprinted genes that affect seed growth. However the relation between the role of MET1 in imprinting and its control of seed size has remained unclear. Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth. We show that the loss of MET1 during male gametogenesis causes a reduction of seed size, presumably linked to silencing of the paternal allele of growth enhancers in the endosperm, which nurtures the embryo. However, we find no evidence for a similar role of MET1 during female gametogenesis. Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase. MET1 inhibits seed growth by restricting cell division and elongation in the maternal integuments that surround the seed. Our data demonstrate new controls of seed growth linked to the mode of reproduction typical of flowering plants. We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.

Combinatorial Networks Regulating Seed Development and Seed Filling

“…Seeds derived from crosses between wild-type pollen and ovules from MET1 antisense plants (MET1a/s) display increased seed size (Adams et al, 2000;Luo et al, 2000), owing to the loss of MET1 activity in the female gametes, the integuments, or both (Berger & Chaudhury, 2009). Similar results were obtained from crosses between wild-type pollen and homozygous met1/met1 ovules, resulting in the formation of larger seeds, which is due to ovules with more cells and autonomous elongation (FitzGerald et al, 2008). Therefore, MET1 was proposed to play a role in inhibiting ovule proliferation and elongation and the effect of MET1 on seed size results mainly from the maternal controls (Berger & Chaudhury, 2009).…”

“…MET1-mediated DNA methylation is involved in the epigenetic control of seed size. During male gametogenesis, endosperm growth in met1 mutants was inhibited and smaller seeds were produced (Luo et al, 2000;Garcia et al, 2005;Xiao et al, 2006;FitzGerald et al, 2008). This is probably due to the ectopic expression of imprinted paternal alleles of loci such as FIS2 and FWA.…”

Integration of epigenetic and genetic controls of seed size by cytokinin in Arabidopsis

“…Seeds that inherit a paternal copy of the loss of function allele met1 show a phenotype similar to that caused by excess of maternal genome dosage (13,15). To monitor CKX2 expression in small seeds produced by DNA demethylation of the paternal genome we designed the following experiment.…”

“…An excess of the paternal genome dosage has opposite effects. The reduction of seed size caused by increased maternal genome dosage is phenocopied by fertilization of WT ovules with pollen from mutants in DNA METHYLTRANSFERASE 1 (MET1), which maintains CG methylation (13)(14)(15). DNA methylation controls the activity of the maternally expressed imprinted genes MEDEA (MEA) and FERTILIZATION INDEPENDENT SEED 2 (FIS2), which both encode subunits of the POLYCOMB GROUP REPRESSIVE COMPLEX2 (PRC2) (16,17).…”

Seed evolution: parental conflicts in a multi-generational household

“…One explanation is that the release of repressive methylation marks from paternally silenced genes originates extra transcription of otherwise maternal-specific genes, originating a maternal excess phenotype. The reciprocal cross of a hypomethylated met1 seed parent with normal pollen mimics the phenotype of a paternal excess cross (40,62,63), although this appears to rather be caused by a sporophytic effect in the cell proliferation in the seed integuments, and not by a gametophytic effect (64). The maintenance of MET1 CpG methylation in the gametophytic phase has been shown to be essential for the inheritance of epigenetic marks (65).…”