Regulation of Seed Size by Hypomethylation of Maternal and Paternal Genomes

Abstract

DNA methylation is an epigenetic modification of cytosine that is important for silencing gene transcription and transposons, gene imprinting, development, and seed viability. DNA METHYLTRANSFERASE1 (MET1) is the primary maintenance DNA methyltransferase in Arabidopsis (Arabidopsis thaliana). Reciprocal crosses between antisense MET1 transgenic and wild-type plants show that DNA hypomethylation has a parent-of-origin effect on seed size. However, due to the dominant nature of the antisense MET1 transgene, the parent with a hypomethylated genome, its gametophyte, and both the maternal and paternal genomes of the F 1 seed become hypomethylated. Thus, the distinct role played by hypomethylation at each generation is not known. To address this issue, we examined F 1 seed from reciprocal crosses using a loss-of-function recessive null allele, met1-6. Crosses between wild-type and homozygous met1-6 parents show that hypomethylated maternal and paternal genomes result in significantly larger and smaller F 1 seeds, respectively. Our analysis of crosses between wild-type and heterozygous MET1/ met1-6 parents revealed that hypomethylation in the female or male gametophytic generation was sufficient to influence F 1 seed size. A recessive mutation in another gene that dramatically reduces DNA methylation, DECREASE IN DNA METHYLATION1, also causes parent-of-origin effects on F 1 seed size. By contrast, recessive mutations in genes that regulate a smaller subset of DNA methylation (CHROMOMETHYLASE3 and DOMAINS REARRANGED METHYLTRANSFERASES1 and 2) had little effect on seed size. Collectively, these results show that maternal and paternal genomes play distinct roles in the regulation of seed size in Arabidopsis.

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

“…Notably, siRNAs and RdDM pathways may also regulate other traits, such as seed size. For example, seed size was dramatically increased when the maternal siRNAs were reduced (Lu et al, 2012) or when the demethylation lines were the maternal parent in the genetic crosses (Adams et al, 2000;Xiao et al, 2006). In addition, biomass accumulation is affected by other factors, such as quantitative trait loci, that regulate metabolism during the early stages of seedling development (Lisec et al, 2009;Meyer et al, 2012).…”

Networks controlling seed size in Arabidopsis

“…When 268 crossing MET1::RNAi pistils with wild-type pollen, the 269 result is production of enlarged F1 seeds. Meanwhile, 270 reciprocal crosses generated smaller F1 seeds, as expected 271 from the presence of hypomethylated paternal genome 272 (Adams et al 2000;Luo et al 2000;Xiao et al 2006). 273 Thus, the methylation status of both the maternal and 274 paternal genome directly influences seed size.…”

“…This 264 leads to specific DNA hypomethylation of the maternally 265 inherited genome. Previous studies showed that altering 266 DNA methylation in a parental-specific manner via MET1 267 resulted in variation in seed size (Xiao et al 2006). When 268 crossing MET1::RNAi pistils with wild-type pollen, the 269 result is production of enlarged F1 seeds.…”

Hypomethylated Pollen Bypasses the Interploidy Hybridization Barrier inArabidopsis

“…Hypomethylated pollen derived from the met1 mutant causes precocious endosperm cellularization and decreased seed size (Xiao et al, 2006), which may be a consequence of suppressed activity of paternally expressed imprinted genes (Hsieh et al, 2011). Deregulated expression of the paternally expressed imprinted gene ADM was shown to be causally responsible for triploid seed abortion (Kradolfer et al, 2013b); therefore, we raised and tested the hypothesis that paternal CG hypomethylation bypasses the interploidy hybridization barrier by suppressing deregulated imprinted genes.…”