Chapter One

Genomic Imprinting in Plants

What Makes the Functions of Paternal and Maternal Genes Different in Endosperm Formation?

Takayuki Ohnishi?,1, Daisuke Sekine† and Tetsu Kinoshita?,1     ?Kihara Institute for Biological Research, Yokohama City University, Kanagawa, Japan     †Division of Life Sciences, Graduate School of Natural Science and Technology, Kanazawa University, Ishikawa, Japan
1 Corresponding author: e-mail address: ohnishi@yokohama-cu.ac.jp, tkinoshi@yokohama-cu.ac.jp 

Abstract

Genomic imprinting refers to the unequal expression of maternal and paternal alleles according to the parent of origin. This phenomenon is regulated by epigenetic controls and has been reported in placental mammals and flowering plants. Although conserved characteristics can be identified across a wide variety of taxa, it is believed that genomic imprinting evolved independently in animal and plant lineages. Plant genomic imprinting occurs most obviously in the endosperm, a terminally differentiated embryo-nourishing tissue that is required for seed development. Recent studies have demonstrated a close relationship between genomic imprinting and the development of elaborate defense mechanisms against parasitic elements during plant sexual reproduction. In this chapter, we provide an introductory description of genomic imprinting in plants, and focus on recent advances in our understanding of its role in endosperm development, the frontline of maternal and paternal epigenomes.

Keywords

DNA methylation; Endosperm; Epigenetics; Plant genomic imprinting; Polycomb repressive complex 2(PRC2); Sexual reproduction; Transposable elements (transposons)

1. Introduction

Genomic imprinting results in two alleles at the same locus being functionally nonequivalent and is caused by different epigenetic modifications depending on whether the allele is inherited from the mother or the father. The phenotypic differences between heterozygotes are referred to as parent-of-origin effects. The term genomic imprinting was first used to describe the elimination of paternal chromosomes during spermatogenesis in sciarid flies (Crouse, 1960; Goday & Esteban, 2001; Stern, 1958). The term was later applied to both mammals (McGrath & Solter, 1984; Surani, Barton, & Norris, 1984) and flowering plants (Kermicle, 1970; Kermicle & Alleman, 1990; Kinoshita, Yadegari, Harada, Goldberg, & Fischer, 1999; Vielle-Calzada et al., 1999). These early studies focused on functional differences between parental genomes. In mammals, gynogenetic or androgenetic mice, which contain only a maternally or paternally derived chromosome set, respectively, show contrasting developmental outcomes; gynogenones characteristically have a poorly developed placenta and thin membrane layers surrounding the embryo (extraembryonic membranes), but produce a reasonably well-developed embryo proper; however, androgenones are characterized by retarded embryos that are enveloped by well-developed placenta and extraembryonic membranes (McGrath & Solter, 1984; Surani et al., 1984). In higher plants, the parent-of-origin gene dosage effects can enhance or repress seed development. Such effects are particularly evident following interploidy crosses. Reproductive barriers can prevent intercrosses between different groups within a species, reducing gene flow between the groups and promoting speciation. The evolution of a reproductive barrier is important for the establishment or fixing of a new species. In angiosperms, it has been estimated that about 15–30% of speciation events within genera are accompanied by polyploidy formation (Mayrose et al., 2011; Wood et al., 2009). An increased dosage of maternal chromosomes enhances endosperm development, while a paternal genome excess results in repressed endosperm development. This suggests that maternally and paternally derived chromosomes are unable to complement one another to play the same roles in development. In both mammals and flowering plants, the phenotypic characteristics produced by the unequal functions of parental chromosomes have much in common. First, both the placenta and endosperm, which are essential to support embryo development, are very sensitive to parent-of-origin effects on gene expression. Second, maternal and paternal parent-of-origin effects generate a similar directional phenotypic change in the target tissue in both animals and plants, namely, the maternal effect enhances development, while the paternal effects represses development (Figure 1.1). The endosperm is the product of double fertilization (Figure 1.2). During double fertilization, one of the sperm cells fertilizes the haploid egg cell to give rise to the diploid embryo. The other sperm cell fuses with the diploid central cell to form the triploid endosperm, the tissue that will surround the embryo after fertilization. The endosperm is a triploid tissue composed of two maternal sets of chromosomes and one paternal set. Therefore, although the endosperm contains both maternally and paternally derived chromosomes, its genetic composition is totally different from that of the mammalian placenta.
Figure 1.1 Parent-of-origin effects generate a similar directional phenotypic change. Schematic illustration highlighting the phenotypic characteristics produced by the parent-of-origin effect to the placenta in mammals and to the endosperm in plants. (See the color plate.)
Figure 1.2 Double fertilization in angiosperms. Angiosperm seeds are produced by a double fertilization event. During double fertilization, one of the sperm cells fertilizes the haploid egg cell to give rise to the diploid embryo. The other sperm cell fuses with the diploid central cell to form the triploid endosperm, the tissue that will surround and nourish the embryo after fertilization. A seed coat derived from maternal tissues develops from the integuments of the ovule after fertilization. (See the color plate.) The plant endosperm nourishes and supports both embryo development and the subsequent growth of the seedling. The endosperm is responsive to problems in interspecific compatibility and in ploidy level differences (Haig & Westoby, 1991). If endosperm development fails, then embryo development will also eventually get arrested (Hehenberger, Kradolfer, & Kohler, 2012). Abnormal development of the endosperm in response to hybridization causes an effective reproductive barrier in angiosperms. The production of endosperm by double fertilization is a specific characteristic of angiosperms and does not occur in other land plant groups; consequently, plant genomic imprinting has only been observed in angiosperms.

2. When Does Genomic Imprinting Occur?

2.1. Taxonomic Distribution of Genomic Imprinting

In mammals, evidence of genomic imprinting has been found in a wide range of both eutherian and marsupial species. These two mammalian groups diverged about 160 million years ago (Ma) (Luo, Yuan, Meng, & Ji, 2011). Comprehensive comparative genomic studies have shown that some imprinted regions are conserved in both groups, indicating that genomic imprinting likely evolved in an ancestral species of the two lineages (Renfree, Suzuki, & Kaneko-Ishino, 2013). No imprinted genes have been found in monotremes, birds, and reptiles (Figure 1.3) (Renfree, Hore, Shaw, Graves, & Pask, 2009).
Figure 1.3 The occurrence of genomic imprinting in animals and plants. The timing of genomic imprinting acquisition and of the divergence of animals and plants. The vertical axes represent the time line from 400 Ma to the present. The colored boxes represent the evolution of the groups with and without genomic imprinting. In animals, genomic imprinting is widespread in eutherian and marsupial mammals, although it is not observed in monotremes or in birds. In plants, genomic imprinting occurs in eudicots (Arabidopsis) and monocots (rice, maize). Currently, there is no information whether the phenomenon also occurs in basal angiosperms and in gymnosperms. (See the color plate.) Recent studies in plants using genomewide detection of differential gene expression patterns in parental alleles have provided new insights into the evolution of plant genomic imprinting. Roughly 150 Ma, flowering plants diverged to form the two dominant extant lineages, monocots, and eudicots (Hedges, Dudley, & Kumar, 2006). Comparison of the genes showing an imprinted expression pattern in Oryza sativa (rice), a monocot species, with those in the model eudicots Arabidopsis thaliana (Arabidopsis), revealed a low degree of overlap between monocots and eudicots, suggesting that genomic imprinting has evolved independently in the two plant clades (Luo, Taylor, et al., 2011). Further analyses and filtering of transcriptome databases have identified some genes that are imprinted in both monocots and eudicots (Kohler, Wolff, & Spillane, 2012). It is possible that genomic imprinting arose at many different time points in plant evolution as an adaptation to various selection pressures in different environments. Possibly, natural selection may result in the replacement of one pattern of genomic imprinting by another that is better adapted to the survival of the...