Control of Paternally Expressed Imprinted UPWARD CURLY LEAF1, a Gene Encoding an F-Box Protein That Regulates CURLY LEAF Polycomb Protein, in the Arabidopsis Endosperm

PLoS One. 2015 Feb 17;10(2):e0117431. doi: 10.1371/journal.pone.0117431. eCollection 2015.

Abstract

Genomic imprinting, an epigenetic process in mammals and flowering plants, refers to the differential expression of alleles of the same genes in a parent-of-origin-specific manner. In Arabidopsis, imprinting occurs primarily in the endosperm, which nourishes the developing embryo. Recent high-throughput sequencing analyses revealed that more than 200 loci are imprinted in Arabidopsis; however, only a few of these imprinted genes and their imprinting mechanisms have been examined in detail. Whereas most imprinted loci characterized to date are maternally expressed imprinted genes (MEGs), PHERES1 (PHE1) and ADMETOS (ADM) are paternally expressed imprinted genes (PEGs). Here, we report that UPWARD CURLY LEAF1 (UCL1), a gene encoding an E3 ligase that degrades the CURLY LEAF (CLF) polycomb protein, is a PEG. After fertilization, paternally inherited UCL1 is expressed in the endosperm, but not in the embryo. The expression pattern of a β-glucuronidase (GUS) reporter gene driven by the UCL1 promoter suggests that the imprinting control region (ICR) of UCL1 is adjacent to a transposable element in the UCL1 5'-upstream region. Polycomb Repressive Complex 2 (PRC2) silences the maternal UCL1 allele in the central cell prior to fertilization and in the endosperm after fertilization. The UCL1 imprinting pattern was not affected in paternal PRC2 mutants. We found unexpectedly that the maternal UCL1 allele is reactivated in the endosperm of Arabidopsis lines with mutations in cytosine DNA METHYLTRANSFERASE 1 (MET1) or the DNA glycosylase DEMETER (DME), which antagonistically regulate CpG methylation of DNA. By contrast, maternal UCL1 silencing was not altered in mutants with defects in non-CpG methylation. Thus, silencing of the maternal UCL1 allele is regulated by both MET1 and DME as well as by PRC2, suggesting that divergent mechanisms for the regulation of PEGs evolved in Arabidopsis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Arabidopsis / genetics*
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics*
  • Base Sequence
  • DNA Methylation
  • Endosperm / metabolism*
  • F-Box Proteins / genetics*
  • Gene Expression Regulation, Plant*
  • Genomic Imprinting*
  • Polycomb-Group Proteins / metabolism*
  • Transgenes / genetics
  • Ubiquitin-Protein Ligases / genetics*

Substances

  • Arabidopsis Proteins
  • F-Box Proteins
  • Polycomb-Group Proteins
  • UPWARD CURLY LEAF1 protein, Arabidopsis
  • Ubiquitin-Protein Ligases

Grants and funding

This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2011-0022425 to JSL) and by the Brain Korea 21 Program (to GTP). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.