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.

Cheol Woong Jeong,Yang Do Choi,Tzung-Fu Hsieh,Hyein Yun,Guen Tae Park,Yeonhee Choi,Jong Seob Lee

doi:10.1371/journal.pone.0117431

Cheol Woong Jeong, Yang Do Choi + Show 5 more

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https://doi.org/10.1371/journal.pone.0117431

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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.

Highlights

Arabidopsis seeds contain three tissues that have distinct parental genome contributions, namely 1) the diploid embryo, which is the diploid fertilization product of the maternal and paternal genomes, 2) the triploid endosperm, which is the fertilization product of the diploid maternal and haploid paternal genomes, and 3) the seed coat, which is of diploid maternal origin [1,2]
While the Col-0 and En-2 ecotypes contained the two ATLINE1_1 transposable elements (TEs), Ler, RLD, and C24 possess only the short ATLINE1_1 TE, which is closer to the UPWARD CURLY LEAF1 (UCL1) coding region (Fig. 2A)
All transgenic plants showed bi-allelic expression of the GUS transgenes (Figs. 3 and S4). These results clearly demonstrate that the imprinting control region (ICR) that underlies the maternal repression of UCL1 is located in the 50-upstream region of this gene, between 2.7 kb and 2.0 kb from the translation start site, but that the cis-element(s) responsible for default bi-allelic expression of UCL1 is contained in the 1.0-kb upstream sequence

Summary

Introduction

Arabidopsis seeds contain three tissues that have distinct parental genome contributions, namely 1) the diploid embryo, which is the diploid fertilization product of the maternal and paternal genomes, 2) the triploid endosperm, which is the fertilization product of the diploid maternal and haploid paternal genomes, and 3) the seed coat, which is of diploid maternal origin [1,2]. Imprinted genes are predominantly expressed from either the maternal or paternal allele. Several theories have been proposed to explain the evolution of imprinting, the most popular of which is that imprinting arose due to parental conflict over resource allocation to the embryo [7,8,9]. Another theory for the evolution of imprinting is that it is required to limit the gene dosage of key genes during early development [10,11]. The genomic imbalance between maternal and paternal dosages affects seed and embryo development in both plants and mammals. An increase in paternal dosage leads to an increase in placental or endosperm growth, whereas an increase in maternal dosage has the opposite effect [12,13]

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