Genomic Imprinting in Plants

CHAPTER ONE

Genomic Imprinting in Plants: What Makes the Functions of Paternal and Maternal Genes Different in Endosperm Formation? Takayuki Ohnishi*,1, Daisuke Sekine†, 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 1Corresponding author: e-mail address: [email protected], [email protected]

Contents 1.  Introduction2 2.  When Does Genomic Imprinting Occur? 4 2.1  Taxonomic Distribution of Genomic Imprinting 4 3.  Why Does Genomic Imprinting Occur? 6 3.1  Conflict Theory 6 3.2  Kinship Theory 7 4.  How Does Genomic Imprinting Occur? Mechanisms of Genomic Imprinting 7 4.1  DNA Methylation 7 4.2  Global DNA Demethylation in the Endosperm 11 4.3  H3K27me3-Dependent Imprinted Genes 13 4.4  Genomic Imprinting in the Plant Embryo 15 4.5  Interplay between DNA Methylation and Histone Modifications 15 5.  The Role of Genomic Imprinting in Plants: Function as a Reproductive Barrier 16 6.  Perspectives19 Acknowledgments20 References20

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 Advances in Genetics, Volume 86 ISSN 0065-2660 http://dx.doi.org/10.1016/B978-0-12-800222-3.00001-2

© 2014 Elsevier Inc. All rights reserved.

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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.

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

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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.)

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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).

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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

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may result in the replacement of one pattern of genomic imprinting by another that is better adapted to the survival of the species. Since the phylogenetic separation of monocots and eudicots, most imprinted genes have acquired a uniparental expression pattern. A few primitive and conserved genes that emerged before the divergence have been retained for certain selective advantages in every lineage (Figure 1.3). It is clear that imprinted genes have a great diversity of functions. As some imprinted genes are essential for normal development (Jiang & Kohler, 2012), they cannot lose their genomic imprinting status once complex gene expression patterns have evolved (Kaneko-Ishino, Kohda, & Ishino, 2003).

3.  WHY DOES GENOMIC IMPRINTING OCCUR? 3.1  Conflict Theory The evolutionary convergence of genomic imprinting in mammals and plants implies that imprinting affects inclusive fitness related to reproductive success. Under the conflict theory of genomic imprinting, the endosperm/ placenta, which acquires nutrient from the maternal sporophyte for nourishment of the embryo, is a participant in a conflict of interest among the mother, father, and offspring (Haig & Westoby, 1989). Against a background in which siblings from a single mother are destined to compete against each other, offspring of different fathers would strive to obtain a greater share of maternal resources with no regard to the interests of the mother. In contrast, the mother has an equal interest in all the offspring and strives to secure adequate nutrient for all sibs and for herself. Because of these conflicting interests, the paternal genome attempts to make its possessors larger, while the maternal genome attempts to make them smaller. Genomic imprinting has a predominant role in this process. It has been demonstrated in animals that imprinted genes have a role in brain function, and their effects are often manifested via actions on social behavior throughout an organism’s lifetime (Isles, Davies, & Wilkinson, 2006). Recently, it has been reported that the imprinted gene Meg1 of maize plays a significant role in the maternal nourishment of the embryo and promotes seed growth in a gene dosage-dependent manner (Costa et al., 2012). Thus, in contrast to the expectations of the conflict theory, the maternally expressed imprinted Meg1 gene enhances the growth of endosperm. The applicability of the conflict theory to plants still requires substantiation; certainly, it is known that most plant-imprinted genes have minimal roles in resource allocation. Current thinking holds that the action to optimize resource flow between

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generations is a part of the driving force to birth and/or to retention of uniparental gene expression patterns.

3.2  Kinship Theory Although the conflict theory provides a fascinating theoretical evolutionary strategy to explain the evolution of genomic imprinting, another explanation, “Kinship theory,” offers a more general, and possibly more logical, basis for the mechanisms of genomic imprinting (Trivers & Burt, 1999). Under kinship theory, parent of origin-specific (uniparental) gene expression evolved at a locus because the specific level of expression of a gene in one individual favors the reproductive success of that individual’s relatives compared to others who have different levels of expression at the locus. Thus, natural selection supports different levels of gene expression depending on the parent of origin of the allele in the previous generation. However, the majority of imprinted genes do not show a pattern of expression in which one allele is expressed and the other is suppressed; rather, an allele from one parent tends to show preferential expression at a higher level than the other parental allele (biased expression). In plants, it is necessary to distinguish preferential expression driven by imprinting from that caused by the unequal genetic background (i.e., two maternal genomes to one paternal genome in the endosperm).

4.  HOW DOES GENOMIC IMPRINTING OCCUR? MECHANISMS OF GENOMIC IMPRINTING 4.1  DNA Methylation The epigenetic control of imprinted genes by DNA methylation contributes to a parent of origin-specific expression pattern in both mammals and flowering plants. In mammals, many imprinted genes are clustered in specific chromosomal regions.The level of DNA methylation of an imprinting control region (ICR) determines imprinted gene expression within the cluster. Although similar imprinted gene clusters have been suggested to occur in maize (Zhang et al., 2011), the existence of ICRs remains uncertain in plants (Ikeda, 2012). Epigenetic modifications, such as DNA methylation patterns, can be constitutively different in female and male germ cells before fertilization so that maternal and paternal chromosomes are functionally different. Mammals and plants also differ in the control of DNA methylation. In mammals, the epigenetic modifications that produce parent of originspecific gene expression are established by de novo DNA methylation after

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erasure of “imprints” of the previous generation. This DNA methylation modification is termed “bidirectional control” of genomic imprinting during sexual reproduction. By contrast, plant imprinting is not required for de novo DNA methylation (Cao & Jacobsen, 2002). Instead, many imprinted genes are controlled by allele-specific activation through DNA demethylase activity before fertilization, as in Arabidopsis (Gehring, Bubb, & Henikoff, 2009; Hsieh et al., 2011; Kinoshita et al., 2004). In plants, DNA can be methylated in three sequence contexts, namely, CG, CHG, and CHH (where H = A,T, or C).The regulation of DNA methylation is, to some extent, independent for the different sequence contexts (Law & Jacobsen, 2010). For CG sites, DNA methyltransferase (MET1) maintains the epigenetic state during DNA replication; this pattern has been shown to be indispensable for the expression of some imprinted genes in Arabidopsis (Jullien, Kinoshita, Ohad, & Berger, 2006; Kinoshita et al., 2004). CHG sites are methylated by CHROMOMETHYLASE3 (CMT3) depending on the chromatin state of dimethylation of lysine 9 of H3 (H3K9me2) (Feng, Cokus, et al., 2010; Law & Jacobsen, 2010; Zemach, McDaniel, Silva, & Zilberman, 2010). Methylation of CHH sites is mainly controlled by the RNA interference machinery, and is referred to as the RNA-dependent DNA methylation pathway (Saze, Tsugane, Kanno, & Nishimura, 2012). Controlling mechanisms involving PIWI-interacting (pi) RNA and small interfering (si) RNA have also been identified as important to genomic imprinting in mammals and plants, respectively (Vu et al., 2013; Watanabe et al., 2011). The active DNA demethylation of silent genes is a necessary step in many biological processes.The mechanisms of active DNA demethylation in mammals have been elucidated recently (Franchini, Schmitz, & Petersen-Mahrt, 2012; Ooi & Bestor, 2008), while in Arabidopsis, genetic studies have shown that the DNA glycosylase genes DEMETER (DME) and REPRESSOR OF SILENCING1 (ROS1) participate in the DNA demethylation of imprinted genes and silenced transgenes (Choi et al., 2002; Gong et al., 2002). DME and ROS1 proteins contain conserved DNA glycosylase and Fe–S cluster binding domains; they contain extra domains that are not conserved in any other organisms (Mok et al., 2010). ROS1 was first identified as a repressor of transcriptional gene silencing (Gong et al., 2002). In the ros1 mutant, the level of DNA methylation is increased in genomic regions, including transposons, suggesting that ROS1 is involved in the removal of DNA methylation in those regions (Zhu, Kapoor, Sridhar, Agius, & Zhu, 2007). In vitro experiments have shown that the Arabidopsis proteins

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DME and ROS1 possess both DNA glycosylase and apyrimidinic (AP) lyase activities (Gehring et al., 2006; Morales-Ruiz et al., 2006) and are referred to as bifunctional enzymes. Both DME and ROS1 contain conserved domains similar to those of the helix–hairpin–helix DNA glycosylase domain superfamily, some of which are known to be mismatch DNA repair enzymes (Choi et al., 2002; Gong et al., 2002; Kapoor et al., 2005). It is likely that the DNA base excision repair machinery is involved in the locus-specific DNA demethylation of imprinted genes and other loci. The first step of base excision repair is the removal of a base by a DNA glycosylase; this is followed by the cleavage of the abasic site by an AP lyase (Figure 1.4). DNA-strand cleavage 3′ to the AP site results in the formation

Figure 1.4  A model for DNA demethylation in plants.  A specific target is recognized possibly by siRNA, and DNA demethylation occurs following recruitment of an unknown DNA demethylation complex. In the base excision repair steps, 5-methylcytosine is excised to cytosine; this step is probably accompanied by a change in chromatin structure. It is believed that chromatin remodeling factors and histone modification proteins convert the chromatin to an active transcription state. During the base excision repair process, a bifunctional DNA glycosylase, DME or ROS1, removes a base via its DNA glycosylase activity and cuts off the abasic site using its AP lyase activity. Then, a DNA polymerase and a DNA ligase are predicted to play roles in later steps of the base excision repair DNA demethylation process. (See the color plate.)

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of β-elimination products. The subsequent cleavage of the phosphodiester linkage on the 5′ side yields δ-elimination products. DME and ROS1 can catalyze both β- and δ-elimination. Further, DME and ROS1 accept all methylation contexts observed in plants (CG, CHG, and CHH). DME and ROS1 have also been reported to remove G/T mismatches in vitro (Gehring et al., 2006; Morales-Ruiz et al., 2006), although they show a higher activity on 5-methylcytosine than on G/T mismatches. Overall, these analyses demonstrate that bifunctional DNA glycosylases are involved in DNA demethylation in plants. Other enzymes that participate in the base excision repair machinery have also been identified through genetic analyses in Arabidopsis. After 5-methylcytosine removal, the Arabidopsis DNA glycosylase/lyase incises the DNA backbone, and part of the product has a single-nucleotide gap flanked by 3′- and 5′-phosphate termini. Therefore, a DNA polymerase and a DNA ligase are predicted to play a role in later steps of the base excision repair-based DNA demethylation process (Andreuzza et al., 2010).The zinc finger 3′ DNA phosphoesterase removes the blocking 3′ phosphate, allowing subsequent DNA polymerization and ligation steps needed to complete the repair reactions (Martinez-Macias et al., 2012). DNA methylation-dependent plant-imprinted gene expression is preferentially regulated in Arabidopsis endosperm by cytosine demethylation of the maternal genome mediated by the DNA glycosylase DME (Choi et al., 2002; Gehring et al., 2009; Gehring et al., 2006; Hsieh et al., 2009). Plant studies investigating imprinted gene expression through the use of transgenic constructs revealed that the cis element for controlling the imprinted gene expression pattern is most likely located near the imprinted loci (Choi et al., 2002; Gutierrez-Marcos et al., 2006; Kinoshita et al., 2004; Luo, Bilodeau, Dennis, Peacock, & Chaudhury, 2000; Makarevich, Villar, Erilova, & Kohler, 2008). In Arabidopsis, methylated DNA sequences have been found in the promoter regions of the maternally expressed imprinted genes MEDEA (MEA), FERTILIZATION-INDEPENDENT SEED2 (FIS2), and FWA, and in the 3′-tandem repeats of the paternally expressed imprinted gene PHERES1 (PHE1). The methylated sequences included in the control of imprinted FWA, PHE1 gene expression contains transposon insertions or repeat sequence. The relationship between genomic imprinting and transposon insertion is of interest because in mammals the paternally expressed imprinted gene PEG10 shows similarity to the sushiichi retrotransposon. PEG10 is present in eutherian mammals but not in nonmammalian vertebrates that have not evolved a placenta or genomic imprinting (Suzuki et al., 2007).

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One well-known example of a cis element that confers an imprinted expression in plants is the short interspersed nuclear element (SINE)-related tandem repeat structure located in the 5′-region of FWA (Chan, Zhang, Bernatavichute, & Jacobsen, 2006; Chan et al., 2004; Kinoshita et al., 2007; Lippman et al., 2004). The DNA methylation level for the tandem repeats is strongly correlated with the transcriptional state of FWA (Kinoshita et al., 2007; Soppe et al., 2000). When the level of DNA methylation at the locus is low, transcription starts within this repeat region, and the FWA protein then causes delayed flowering (Ikeda, Kobayashi, Yamaguchi, Abe, & Araki, 2007; Soppe et al., 2000). A transgene driven by the SINE-related tandem repeats and with a GFP reporter showed a similar pattern of uniparental expression as that of the endogenous FWA gene (Kinoshita et al., 2007). Induced hypermethylation of the normally hypomethylated allele of FWA, using an RNA-directed de novo DNA methylation strategy, showed that the DNA methylation of the SINE-related tandem repeats determine the expression level of the FWA gene. An analysis of the evolution of this SINE-related tandem repeat, the region corresponding to this cis element for imprinting in Arabidopsis species, suggested that this sequence, without a tandem repeat structure, is responsible for the imprinted pattern of FWA expression in Arabidopsis halleri (Fujimoto et al., 2008). Thus, in A. halleri at least, the tandem repeat structure, but not the SINE-related sequence, is dispensable for imprinting.

4.2  Global DNA Demethylation in the Endosperm Two independent analyses of genomewide DNA methylation profiles in Arabidopsis endosperm revealed that global DNA demethylation occurs in the endosperm; by contrast, the embryo maintains relatively high levels of DNA methylation (Gehring et al., 2009; Hsieh et al., 2009). Mutation of DME restores the CG methylation levels in the endosperm to a level equivalent to that of other tissues, suggesting that DME is involved in genomewide CG demethylation (Hsieh et al., 2009). Transposable elements are extensively demethylated in the endosperm (Gehring et al., 2009). Therefore, for genes that neighbor hypomethylated transposon insertions, maternally derived allele would also be hypomethylated and would show altered gene expression in the central cell and endosperm; however, the paternally derived allele would retain a higher level of DNA methylation. As a consequence, the parental alleles show differential DNA methylation levels that would then influence gene expression patterns in the endosperm. Indeed, some imprinted genes in Arabidopsis are regulated by active DNA

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methylation in the central cell before fertilization (Gehring et al., 2009; Hsieh et al., 2009; Wolff et al., 2011). The DNA methylation landscape of rice endosperm is similar to that of Arabidopsis in that it is largely demethylated. However, rice endosperm DNA is hypomethylated in all sequence contexts (Zemach, Kim, et al., 2010). Non-CG methylation is reduced evenly across the genome, whereas CG hypomethylation is localized (Zemach, Kim, et al., 2010). In rice, a null mutation for the ROS1a gene that encodes a putative cytosine DNA demethylase, a homolog of DME, causes failure of early stage endosperm development when it is inherited maternally. This finding indicates that DNA demethylation plays important roles in female gametophytic generation (Ono et al., 2012). Genes preferentially expressed in the endosperm, including those coding for major storage proteins and starch synthesizing enzymes, are frequently hypomethylated in the endosperm. This effect is demonstrated by a large number of endosperm-specific expressed genes that are regulated by DNA methylation (Zemach, Kim, et al., 2010). It should be noted that the population of transposable elements is relatively higher in cereals than in Arabidopsis. Genomewide analyses in plant endosperm show that endosperm demethylation is accompanied by both non-CG hypermethylation of small interfering RNA-targeted sequences and CHH hypermethylation of embryo transposable elements (Hsieh et al., 2009). This demonstrates that the extensive reconfiguration of the endosperm methylation landscape likely reinforces transposon silencing in the embryo through the siRNAs from the endosperm. It has been suggested that DNA hypomethylation in Arabidopsis endosperm prevents transposable element activation in the embryo (Hsieh et al., 2009).This hypothesis is consistent with an abundance of transposable element-derived small RNAs in the endosperm (Mosher et al., 2009). In Arabidopsis pollen, transposable elements are unexpectedly reactivated in the vegetative cell of the male gametophyte and can undergo transposition (Slotkin et al., 2009). However, vegetative cells accompany the sperm cells but do not provide DNA to the fertilized zygote. The siRNAs from transposable elements are transcribed and processed in the vegetative cell and can induce targeted silencing in gametes.Transposable element activation in response to global DNA demethylation in the nurse cells of gametes is widely recognized as a strategy for silencing of transposable elements in the germ cells via mobile small RNAs. This phenomenon of RNAdirected DNA methylation may hold the key to another type of imprinted gene control in angiosperms (Mosher et al., 2011; Rodrigues et al., 2013; Vu et al., 2013).

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4.3  H3K27me3-Dependent Imprinted Genes In addition to DNA methylation, histone modifications can also influence parent-of-origin gene expression. Trimethylation of lysine 27 on histone H3 (H3K27me3) is responsible for allele-specific repression of genomic imprinting through the activity of the PRC2 complex, which catalyzes the H3K27me3. PRC2 component proteins are conserved and are important regulators of cell fate phase transitions and of cell identity (Schuettengruber & Cavalli, 2009). In Arabidopsis, Polycomb group (PcG) genes belonging to the Fertilization-Independent Seed (FIS) class were first identified in mutant plants that showed spontaneous initiation of endosperm development and eventual seed abortion; these genes regulate early aspects of endosperm development such as cellularization. During early endosperm development, the primary endosperm nucleus initiates several rounds of synchronous division in the absence of cell wall synthesis and cytokinesis to form a syncytium. This period of synchronous nuclear division is followed by cellularization in which peripheral nuclei simultaneously synthesize cell walls. Endosperm cell divisions then continue in a centripetal direction

Figure 1.5  Endosperm development.  After fertilization, the primary endosperm nucleus initiates several rounds of synchronous division in the absence of cell wall synthesis and cytokinesis to form a syncytium. This period of synchronous nuclear division is followed by cellularization in which peripheral nuclei simultaneously synthesize cell walls. Endosperm cell divisions then continue in a centripetal direction. (A) Histological analysis of endosperm development in seeds from self-fed plants in Oryza sativa cv. Nipponbare at 1–3 days after pollination. (This figure has been reproduced from a previously published work. Ishikawa et al., 2011.) (B) Illustration of early endosperm development in rice. (See the color plate.)

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(Figure 1.5) (Berger, 2003; Brown, Lemmon, Nguyen, & Olsen, 1999). AGAMOUS-LIKE 62 (AGL62) plays a role as a suppressor of cellularization in endosperm development (Kang, Steffen, Portereiko, Lloyd, & Drews, 2008). AGL62 expression is negatively controlled by FIS class PRC2. Loss of FIS class PRC2 function causes AGL62 overexpression and failure of endosperm cellularization (Wolff et al., 2011); the timing of endosperm cellularization is also likely to be regulated indirectly through FIS class PRC2. Although a plant species has a number of homologous genes for FIS class PRC2 components, for example, MEA, FIS2, FIE, and MSI1, some of these genes have been found to be imprinted and repressed in vegetative tissues in all surveyed plant species. In Arabidopsis, MEA and FIS2 are imprinted; the FIS class PRC2 is activated in the central cell of the female gametophyte before fertilization and in the endosperm after fertilization through DME-mediated removal of DNA methylation (Hennig & Derkacheva, 2009). FIS class PRC2 also regulates the repression of the paternal alleles of some maternally expressed genes. It remains unclear how FIS class PRC2 discriminates maternally and paternally inherited alleles at imprinted loci. In a similar fashion as in mammals (Beisel & Paro, 2011), it is possible that long intergenic noncoding RNAs (lincRNAs) participate in the recruitment of the PcG complex. During vernalization (the acquisition of the ability to flower following exposure to the prolonged cold conditions), lincRNAs orchestrate the repression of specific genomic regions.The lincRNA COLDAIR transcripts are bound by PcG complexes, and COLDAIR remains coupled with the FLC locus long enough to recruit a vernalization-specific PcG complex that initiates a change in the chromatin that provides stable FLC repression (Heo & Sung, 2011). Rice and maize have two homologous genes for FIE1; one gene shows a biallelic expression pattern, and the other gene is imprinted. In rice, the imprinted OsFIE1 gene is expressed at a level of only about 4% of that of the nonimprinted OsFIE2 gene in the endosperm (Nallamilli et al., 2013). Mutation of OsFIE1 by insertion of T-DNA does not result in an abnormal phenotype (Luo, Platten, Chaudhury, Peacock, & Dennis, 2009), while the knockdown of both OsFIE1 and OsFIE2 causes autonomous endosperm development (Li et al., 2014). Rice FIE genes are involved in the regulation of fertilization-independent endosperm development, and may share redundant functions between OsFIE1 and OsFIE2 during early endosperm development. The biological significance of the imprinting of some FIS class PRC2 components remains uncertain. Local gene duplication seems to be one of the driving forces for the formation of imprinted genes (Dickinson, Costal, & Gutierrez-Marcos, 2012;Yoshida & Kawabe, 2013).

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4.4  Genomic Imprinting in the Plant Embryo Embryonic imprinting in mammals is actively reprogrammed to produce allele-specific expression patterns that vary between sexes (Feng, Jacobsen, & Reik, 2010). Plant reproduction differs from that of mammals in many respects. In plants, development of the germline lineage initiates very late from sporophytic cells that undergo meiosis to form spores that subsequently give rise to the gametophytes. Little is known about the machinery for erasure and resetting of epigenetic marks in the plant embryo. Although the endosperm is generally viewed as the sole site of imprinting in plants, the maize mee1 gene has been shown to be maternally expressed in both early embryos and endosperm (Jahnke & Scholten, 2009). This maternal specific expression pattern is determined by the status of DNA methylation at the proximal promoter region of the MEE1 gene. In addition to MEE1, a genomewide analysis for imprinted loci in rice identified 262 candidate-imprinted loci in endosperm and three in embryos (Luo, Taylor, et al., 2011). Similar studies in maize (Waters et al., 2011) and Arabidopsis (Gehring, Missirian, & Henikoff, 2011) have also detected the presence of a small number of potentially imprinted genes in embryos. The number of imprinted genes in plant embryos is clearly very much smaller compared to that of the endosperm.The striking asymmetry in the number of imprinted genes in the endosperm and that in the embryo suggests that genomic imprinting in the embryo may have arisen as a by-product transmitted from surrounding tissue. Overall, relatively little is known about its biological significance. A recent study on imprinted embryo-expressed genes showed that some of these are regulated by PRC2 rather than by DNA methylation (Raissig, Bemer, Baroux, & Grossniklaus, 2013).

4.5  Interplay between DNA Methylation and Histone Modifications The regions around genes that have been silenced by DNA methylation or repressive histone modifications are predicted to form facultative heterochromatin, which impairs access by either the transcriptional machinery or by the DNA demethylation machinery.Therefore, in order for transcription to occur, it is necessary to open the chromatin structure. One possible means of achieving this is through the DNA base excision repair machinery, which has a role in altering the chromatin structure (Hajkova et al., 2008). Structural chromatin changes and histone replacement are known to be regulated through mechanisms that control the repair of damaged and mismatched

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DNA bases (Groth, Rocha, Verreault, & Almouzni, 2007). The interplay of the DNA methylation and histone modifications is another aspect that needs to be addressed. It has been reported in both Neurospora and Arabidopsis that histone methylation on H3 Lys9 affects DNA methylation (Jackson, Lindroth, Cao, & Jacobsen, 2002;Tamaru et al., 2003). In addition, recent studies have demonstrated a role for H2B monoubiquitination in DNA methylation (Sridhar et al. 2007), and revealed that histone acetyl transferase IDM1 is also involved in active DNA demethylation (Qian et al., 2012). IDM1 is a histone H3 acetyl transferase that is capable of recognizing methylated DNA through its Metal-Binding Domain (MBD) and recognizing unmethylated histone H3K4 through its Plant Homeo finger Domain (PHD) to create acetylated H3K18 and H3K23 marks. These multiple epigenetic marks may be recognized by DNA demethylation enzymes. Thus, it will be interesting to determine whether the chromatin state affects the DNA demethylation process or whether DNA demethylation affects the chromatin state. The imprinted FWA gene provides a model system for understanding the series of steps in DNA demethylation and transcription activation. The FWA gene is specifically activated in the central cell before fertilization; DME DNA glycosylase mediates DNA demethylation in the central cell (Kinoshita et al., 2004). Through the use of a genetic screen for mutations that impair FWA gene expression in the central cell and by analyzing early endosperm lineage, the SSRP1 gene has been shown to have a role in FWA expression. SSRP1 is a component of the Facilitate to Chromatin Transcription/Transaction histone chaperone, which shows evolutionary conservation from yeast to humans (Ikeda et al., 2011). Interestingly, the ssrp1 mutation not only has impaired activation of the FWA gene but it also has hypermethylation of the 5′ SINE-related tandem repeats.These observations suggest that the DME DNA demethylase cannot initiate the base excision repair pathway for DNA demethylation or access the chromatin of the target region without SSRP1. In addition to SSRP1, Histone H1 also contributes to imprinted gene expression in the endosperm (Rea et al., 2012).

5.  THE ROLE OF GENOMIC IMPRINTING IN PLANTS: FUNCTION AS A REPRODUCTIVE BARRIER In interploidy crosses, the phenotypes of the hybrid seed are indicative of the antagonistic functions of the maternal and paternal genomes on endosperm growth. Failure of crosses between species sometimes resembles that observed in interploidy crosses within species. Abnormal

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seed development in interspecies crosses is also caused by parent-of-origin effects depending on the direction of the cross (Bushell, Spielman, & Scott, 2003; Gutierrez-Marcos, Pennington, Costa, & Dickinson, 2003; Johnston, Dennijs, Peloquin, & Hanneman, 1980; Kohler & Kradolfer, 2011). Various genetic mechanisms contribute to the functional differences between male and female genomes, such as an incompatibility between maternally derived tissue and endosperm, and uniparental (cytoplasmic) inheritance of organelles such as mitochondria and plastids. These mechanisms are exemplified through examination of crosses between closely related Arabidopsis species. Arabidopsis arenosa has an estimated genome size of 203 Mbp and a haploid chromosome number of 8, whereas A. thaliana has a genome size of 157 Mbp and a haploid chromosome number of 5 (Figure 1.6) (Johnston et al., 2005). The establishment of a reproductive barrier in this interspecies cross may be initiated by a combination of different intrinsic cues, namely, differences in DNA sequences and differences in ploidy levels. Rice species have the same chromosome number (2n = 24) and similar genome sizes (∼430 Mbp) (Ammiraju et al., 2006). In interspecies crosses in rice, the timing of cellularization, which may be controlled by the PcG complex, depends on which parental species are used for the cross; the rates of nuclear divisions in the hybrid endosperm are not affected in this manner (Ishikawa et al., 2011). Studies of hybrid endosperm in Arabidopsis and rice have shown extensive disruption of gene expression, including deregulation of imprinting of PHE1, MEA, and OsMADS87 (Ishikawa et al., 2011;

Figure 1.6  Interspecific crosses in Arabidopsis and rice species.  In the genus Arabidopsis, interspecific crosses usually involve differences in both chromosome number and genome size. A. thaliana has a genome of 157 Mbp and a haploid chromosome number of 5, whereas A. arenosa has an estimated genome size of 203 Mbp and a haploid chromosome number of 8. By contrast, Oryza species have the same chromosome number (2n = 24) and similar genome sizes (∼430 Mbp).

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Josefsson, Dilkes, & Comai, 2006; Walia et al., 2009). In hybrid endosperm, the expression patterns of the imprinted MEA and PHE1 genes are disrupted (Josefsson et al., 2006). The two genes usually show uniparental gene expression patterns in crosses between A. thaliana ecotypes. However, in interspecific crosses, the two genes are released from imprinted regulation and show a biallelic gene expression pattern. Moreover, a maternal phe1 mutation partially restores fertility in the interspecies (Josefsson et al., 2006), suggesting that the endosperm overgrowth phenotype in interspecies crosses is probably involved in the de-repression of maternal PHE1 gene expression.The hybrid seeds produced in interspecies crosses of Oryza species exhibit similar phenotypes as those of Arabidopsis species (Ishikawa et al., 2011). In the cross between female Oryza sativa and male Oryza longistaminata, the hybrid seeds are aborted due to endosperm overgrowth with arrested embryo development. In the hybrid endosperm, the disruption of imprinted gene expression patterns is found; expression from the paternal allele has been demonstrated in OsMADS87, a gene that normally shows maternally specific expression pattern (Ishikawa et al., 2011). OsMADS87 is a homolog of the Arabidopsis PHE1 gene. However, the paternally derived allele is also expressed in interspecific crosses. Therefore, it has been suggested that the misregulation of imprinted genes might act as a postzygotic isolation mechanism in Arabidopsis and Oryza species (Ishikawa et al., 2011; Josefsson et al., 2006; Kinoshita, 2007). Genomic imprinting is likely to play a key role in the generation of a reproductive barrier between plant species. In rice interploidy crosses, the maternal genome excess induces precocious cellularization with reduced mitotic activity; by contrast, a paternal genome excess prolongs the syncytial stage with increased mitotic activity (Sekine et al., 2013). These effects are similar to those reported for interploidy crosses in the eudicot Arabidopsis (Scott, Spielman, Bailey, & Dickinson, 1998). Therefore, maternal and paternal genome excess can have the opposite effects on endosperm development in monocot rice and eudicot Arabidopsis. This similarity suggests either that the molecular mechanisms of the hybridization barriers are conserved with regard to interploidy crosses, or that convergent evolution of parent-of-origin effects has occurred in rice and Arabidopsis species. Endosperm development is sensitive to the balance of parental genome dosage. In the interploidy cross between female diploid Arabidopsis (2n) and male tetraploid Arabidopsis (4n) (paternal genome excess), the hybrid endosperm shows overgrowth (Dilkes et al., 2008; Scott et al., 1998). An altered pattern of the expression of MEA and FIS2 genes occurs in interploidy

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crosses generating a paternal excess, although changes in expression patterns differ between crosscombinations (Erilova et al., 2009; Jullien & Berger, 2010; Kradolfer, Wolff, Jiang, Siretskiy, & Kohler, 2013). For example, in the A. Landsberg erecta (Ler) accession, the level of MEA expression decreases in interploidy crosses; by contrast, expression increases in the Columbia (Col) accession. Further, the imprinted pattern of MEA expression is present in interploidy crosses using Ler accession plants but breaks down for the Col accession plants. Although there are differences between A. thaliana accessions in interploidy crosses, deregulation of FIS class PRC2 targeted genes, such as PHE1 and AGL62, seems to be a common phenomenon that is probably responsible for the abnormal endosperm development in these crosses (Erilova et al., 2009; Kradolfer et al., 2013). In Arabidopsis endosperm, the paternally derived ADMETOS (ADM) gene is expressed; increased expression of this gene causes endosperm failure in triploid seeds with a paternal genome excess (Kradolfer et al., 2013). To date, however, orthologs of ADM have only been identified in Brassicaceae species that are closely related to Arabidopsis (Kradolfer et al., 2013). In rice interploidy crosses, endosperm overgrowth occurs where a paternal excess is generated, and is also correlated with deregulation of the pattern of imprinted gene expression of OsMADS87 gene (Sekine et al., 2013). Imprinted genes can act as a dosage-sensitive regulator and disturbed balance of these regulators may cause endosperm abnormality in response to interploidy crosses. Syncytial endosperm development is thought to have evolved independently in monocots and eudicots (Floyd, Lerner, & Friedman, 1999; Friedman & Floyd, 2001; Geeta, 2003).Therefore, although Arabidopsis and rice may share many similarities in interploidy hybridization barriers in the endosperm, the underlying molecular mechanisms are unlikely to be conserved in these species.

6.  PERSPECTIVES Genomic imprinting in plants was first reported for the maize R locus (Kermicle, 1970; Kermicle & Alleman, 1990); subsequently, additional imprinted genes have been identified at the molecular level in the model plant Arabidopsis. High-throughput genomewide transcriptome screening to identify imprinted genes has recently revealed a large number of candidate imprinted genes in other plant species, and considerable progress has been made in our understanding of such imprinted genes. However, relatively little is known about the molecular machinery of imprinting, and the little that is known is derived mainly from studies using Arabidopsis. Whether

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and to what extent plant genomic imprinting is conserved between species remains to be investigated. The clear influence of genomic imprinting on cereal seed development has obvious implications for agricultural traits, and, in future, plant-imprinted genes may be considered as a valuable tool for conferring superior crop characteristics.

ACKNOWLEDGMENTS This work was supported by a Grant-in-Aid for JSPS Fellows (recipient; T.O.).

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