Genomic imprinting and endosperm development in flowering plants

Genomic imprinting, the parent-of-origin-specific expression of genes, plays an important role in the seed development of flowering plants. As different sets of genes are imprinted and hence silenced in maternal and paternal gametophyte genomes, the contributions of the parental genomes to the offspring are not equal. Imbalance between paternally and maternally imprinted genes, for instance as a result of interploidy crosses, or in seeds in which imprinting has been manipulated, results in aberrant seed development. It is predominantly the endosperm, and not or to a far lesser extent the embryo, that is affected by such imbalance. Deviation from the normal 2m:1p ratio in the endosperm genome has a severe effect on endosperm development, and often leads to seed abortion. Molecular expression data for imprinted genes suggest that genomic imprinting takes place only in the endosperm of the developing seed. Although far from complete, a picture of how imprinting operates in flowering plants has begun to emerge. Imprinted genes on either the maternal or paternal side are marked and silenced in a process involving DNA methylation and chromatin condensation. In addition, on the maternal side, imprinted genes are most probably under control of the polycomb FIS genes.     

Evolutionary origins of the endosperm in flowering plants

The evolutionary origin of double fertilization and the resultant endosperm tissue in flowering plants remains a puzzle, despite over a century of research. The recent resurgence of approaches to evolutionary developmental biology combining comparative biology with phylogenetics provides new understanding of endosperm origins.     

Convergent evolution of genomic imprinting in plants and mammals

Parental genomic imprinting is characterized by the expression of a selected panel of genes from one of the two parental alleles. Recent evidence shows that DNA methylation and histone modifications are responsible for this parent-of-origin-dependent expression of imprinted genes. Because similar epigenetic marks have been recruited independently in plants and mammals, the only organisms in which imprinted gene loci have been identified so far, this phenomenon represents a case for convergent evolution. Here we discuss the emerging parallels in imprinting in both taxa. We also describe the significance of imprinting for reproduction and discuss potential models for its evolution.     

Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants

The sudden rise of angiosperms to ecological dominance was an "abominable mystery" to Charles Darwin, and understanding the underlying evolutionary driving force has remained a scientific challenge since then. The recognition of polyploidization as an important factor for plant speciation is likely to hold a key to this mystery and we will discuss possible mechanisms underlying this phenomenon. Polyploidization raises an immediate reproductive barrier in the endosperm, pointing towards an important but greatly underestimated role of the endosperm in preventing interploidy hybridizations. Parent-of-origin-specific gene expression is largely restricted to the endosperm, providing an explanation for the dosage sensitivity of the endosperm. Here, we review epigenetic mechanisms causing endosperm dosage sensitivity, their possible consequences for raising interploidy and interspecies hybridization barriers and their impact on flowering plant evolution. This article is part of a Special Issue entitled: Epigenetic Control.     

Genome demethylation and imprinting in the endosperm

Imprinting occurs in the endosperm of flowering plants. The endosperm, a product of central cell fertilization, is critical for embryo and seed development. Imprinting in the endosperm is mainly due to the inherited differences in gamete epigenetic composition. Studies have also shown that there are differences in genomic DNA methylation patterns between embryo and endosperm. Examining those differences, along with mutations in the DNA demethylase gene DEMETER, gives insight into the number of imprinted genes and how an antagonistic relationship between TE defense and gene regulation could evolutionarily affect imprinting establishment. Finally, studies demonstrate that DEMETER demethylase activity influences endosperm chromatin composition, and could possibly enhance DNA de novo methylation activity.     

Reproductive success,spontaneous embryo abortion,and genetic load in flowering plants

Summary Reproductive success is divided into two phases: preemergent (the number of viable seeds that enter the ambient environment) and postemergent (the percentage of progeny that survive to reproduce). We studied preemergent reproductive success (PERS) in flowering plants by measuring the fruit/flower (Fr/Fl) ratio and the seed/ovule (S/O) ratio in a number of species of outcrossing and inbreeding plants, where PERS=the product of (Fr/Fl) and (S/O). In order to determine the influence of the ambient environment (including resource availability) we studied pairs of outcrossing and inbreeding species occurring in the same habitat. Among outcrossing species PERS averaged about 22%, whereas in inbreeding species the average was approximately 90%. The progeny/zygote (P/Z) ratio was studied in hand-pollinated populations in Epilobium angustifolium (a strongly outcrossing species) from populations in Oregon and Utah, by direct observation of embryogenesis at twoday intervals throughout the course of seed development. The P/Z ratio in both populations averaged near 30%, and the developing embryos showed a surprising array of abnormalities that resulted in embryo death. During early development >95% of the ovules had normally developing globular embryos, but beginning with differentiation (cotyledon formation) about 70% of the original globular embryos aborted during the course of embryogenesis and seed development. The clustering of developmental lethals during peroids of major differentiation events parallels the animal model of development. We found little evidence that PERS was limited by the ambient environment (including resource availability), pollination, or factors associated with the inbreeding habit. Instead, PERS was found to be inextricably linked to outcrossing plants, whose breeding systems promote genetic variability. The high incidence of developmental lethals in E. angustifolium and the resulting low P/Z ratio (ca. 30%) is attributed to genetic load (any lethal mutation or allelic combination) possibly working in combination with developmental selection (interovarian competition among genetically diverse embryos). Examples of maternally controlled, fixed patterns of ovule abortion with respect to position or number are discussed. However, we found no need to employ female choice as a hypothesis to explain our results for the extensive, seemingly random patterns of embryo abortion in E. angustifolium and other outcrossing species. A more parsimonious, mechanistic explanation based on genetic load-developmental selection is sufficient to account for the differential survivorship of embryos. Likewise, the traditional concept of a positive growth regulator feedback system based on the number of surviving ovules in an ovary can account for subsequent fruit survivorship.     

Modularity of the angiosperm female gametophyte and its bearing on the early evolution of endosperm in flowering plants

The monosporic seven-celled/eight-nucleate Polygonum-type female gametophyte has long served as a focal point for discussion of the origin and subsequent evolution of the angiosperm female gametophyte. In Polygonum-type female gametophytes, two haploid female nuclei are incorporated into the central cell, and fusion of a sperm cell with the binucleate central cell produces a triploid endosperm with a complement of two maternal and one paternal genomes, characteristic of most angiosperms. We document the development of a four-celled/four-nucleate female gametophyte in Nuphar polysepala (Engelm.) and infer its presence in many other ancient lineages of angiosperms. The central cell of the female gametophyte in these taxa contains only one haploid nucleus; thus endosperm is diploid and has a ratio of one maternal to one paternal genome. Based on comparisons among flowering plants, we conclude that the angiosperm female gametophyte is constructed of modular developmental subunits. Each module is characterized by a common developmental pattern: (1) positioning of a single nucleus within a cytoplasmic domain (pole) of the female gametophyte; (2) two free-nuclear mitoses to yield four nuclei within that domain; and (3) partitioning of three uninucleate cells adjacent to the pole such that the fourth nucleus is confined to the central region of the female gametophyte (central cell). Within the basal angiosperm lineages Nymphaeales and Illiciales, female gametophytes are characterized by a single developmental module that produces a four-celled/four-nucleate structure with a haploid uninucleate central cell. A second pattern, typical of Amborella and the overwhelming majority of eumagnoliids, monocots, and eudicots, involves the early establishment of two developmental modules that produce a seven-celled/eight-nucleate female gametophyte with two haploid nuclei in the central cell. Comparative analysis of ontogenetic sequences suggests that the seven-celled female gametophyte (two modules) evolved by duplication and ectopic expression of an ancestral Nuphar-like developmental module within the chalazal domain of the female gametophyte. These analyses indicate that the first angiosperm female gametophytes were composed of a single developmental module, which upon double fertilization yielded a diploid endosperm. Early in angiosperm history this basic module was duplicated, and resulted in a seven-celled/eight-nucleate female gametophyte, which yielded a triploid endosperm with the characteristic 2:1 maternal to paternal genome ratio.     

Genetic conflicts in genomic imprinting

The expression pattern of genes in mammals and plants can depend upon the parent from which the gene was inherited, evidence for a mechanism of parent-specific genomic imprinting. Kinship considerations are likely to be important in the natural selection of many such genes, because coefficients of relatedness will usually differ between maternally and paternally derived genes. Three classes of gene are likely to be involved in genomic imprinting: the imprinted genes themselves, trans-acting genes in the parents, which affect the application of the imprint, and trnas-acting genes in the offspring, which recognize and affect the expression of the imprint. We show that coefficients of relatedness will typically differ among these three classes, thus engendering conflicts of interest between Imprinter genes, imprinted genes, and imprint-recognition genes, with probable consequences for the evolution of the imprinting machinery.     

Chromatin mechanisms in genomic imprinting

Mammalian imprinted genes are clustered in chromosomal domains. Their mono-allelic, parent-of-origin-specific expression is regulated by imprinting control regions (ICRs), which are essential sequence elements marked by DNA methylation on one of the two parental alleles. These methylation “imprints” are established during gametogenesis and, after fertilization, are somatically maintained throughout development. Nonhistone proteins and histone modifications contribute to this epigenetic process. The way ICRs mediate imprinted gene expression differs between domains. At some domains, for instance, ICRs produce long noncoding RNAs that mediate chromatin silencing. Lysine methylation on histone H3 is involved in this developmental process and is particularly important for imprinting in the placenta and brain. Together, the newly discovered chromatin mechanisms provide further clues for addressing imprinting-related pathologies in humans.     

Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants

Parental conflicts can lead to antagonistic coevolution of the sexes and of parental genomes. Within a population, the resulting antagonistic effects should balance, but crosses between populations can reveal conflict. Parental conflict is less intense in self-pollinating plants than in outcrossers because outcrossing plants are pollinated by multiple pollen donors unrelated to the seed parent, while a self-pollinating plant is primarily pollinated by one individual (itself). Therefore, in crosses between plants with differing mating systems, outcrossing parents are expected to "overpower" selfing parents. We call this the weak inbreeder/strong outbreeder (WISO) hypothesis. Prezygotically, such overpowering can alter pollination success, and we argue that our hypothesis explains a common pattern of unilateral incompatibility, in which pollen from self-incompatible populations fertilizes ovules of self-compatible individuals but the reciprocal cross fails. A postzygotic manifestation of overpowering is aberrant seed development due to parent-of-origin effects such as genomic imprinting. We evaluate evidence for the WISO hypothesis by reviewing published accounts of crosses between plants of different mating systems. Many, but not all, of such reports support our hypothesis. Since parental conflicts can perturb fertilization and development, such conflicts may strengthen reproductive barriers between populations, contributing to speciation.     

Genomic imprinting in plants

Genomic imprinting attracted particular attention in the 1980’s following the discovery that the parental origin of genetic information is essential for normal development of eutherians,1,2 for review see.3 The term imprinting was first introduced in the 1960s to describe the elimination of the paternal chromosomes during spermatogenesis in the Sciarid fly.4?6Today the term genomic imprinting mainly refers to parent?of?origin specific effects distinguishing each parental genome which can be regarded as memories, or “imprints”.7,8 Breaking the rules of Mendel, genomic imprinting is an epigenetic phenomenon per se. Epigenetics is currently defined as the study of mitotically or meiotically heritable changes in gene expression without any change in DNA sequence9,10 and it is intimately linked to the study of inheritance of chromatin states.11 Gene imprinting currently refers to differential expression of autosomal genes according to their parent of origin.12The phenomenon of genomic imprinting explains several cases of parent?specific human disorders.13 To date over 80 imprinted genes have been described in mammals14 and their parent?of?origin specific expression can correlate with changes in DNA methylation patterns, antisense noncoding RNAs and chromatin folding.3 Epigenetic imprints can either activate or silence the “imprinted” allele, and hence imprinting can be associated with either an expressed or silenced allele.15 In mammals, the number of paternally expressed imprinted genes is almost equivalent to the number of maternally expressed genes and the imprinted status can differs according to tissue, developmental stage and species. It is then crucial for our understanding to clearly indicate the status of imprinting (i.e., paternally or maternally expressed) and the context (e.g., species, developmental stage, tissue).     

Association of endosperm reduction with parental imprinting in maize

Among 38 reciprocal translocations between the maize B chromosome and the proximal region of the long arm of chromosome 10 were six interchanges associated with reduced endosperm development. These six have breakpoints that are the most proximal of the set and constitute a graded series with those broken nearer the centromere which have the most abnormal phenotypes. The group of six defines three major regions that produce the endosperm effects. The remaining 32 translocations reduce kernel size very slightly, suggesting the presence of a fourth region distal to all break-points.-The affected class of kernels lacks a paternally derived representative of that segment of 10L translocated to the B centromeric element (B(10) chromosome; 10 10 B(10)). An accompanying class of kernel in which the paternal B(10) chromosome is duplicated in the endosperm (10 10 10(B) B(10) B(10)) is normal. Kernels of the same endosperm constitution synthesized by introducing both 10 and B(10) maternally, however, are defective, resembling 10 10 10(B). Maternal B(10)'s are therefore unable to compensate for the absence of a paternal B(10). Clearly expression of the 10L genes involved supports normal endosperm growth only following pollen transmission.     

Chromatin regulators of genomic imprinting

Genomic imprinting is an epigenetic phenomenon in which genes are expressed monoallelically in a parent-of-origin-specific manner. Each chromosome is imprinted with its parental identity. Here we will discuss the nature of this imprinting mark. DNA methylation has a well-established central role in imprinting, and the details of DNA methylation dynamics and the mechanisms that target it to imprinted loci are areas of active investigation. However, there is increasing evidence that DNA methylation is not solely responsible for imprinted expression. At the same time, there is growing appreciation for the contributions of post-translational histone modifications to the regulation of imprinting. The integration of our understanding of these two mechanisms is an important goal for the future of the imprinting field. This article is part of a Special Issue entitled: Chromatin and epigenetic regulation of animal development.     

Selective abortion and the evolution of genomic imprinting

Mothers can determine which genotypes of offspring they will produce through selective abortion or selective implantation. This process can, at some loci, favour matching between maternal and offspring genotype whereas at other loci mismatching may be favoured (e.g. MHC, HLA). Genomic imprinting generally renders gene expression monoallelic and could thus be adaptive at loci where matching or mismatching is beneficial. This hypothesis, however, remains unexplored despite evidence that loci known to play a role in genetic compatibility may be imprinted. We develop a simple model demonstrating that, when matching is beneficial, imprinting with maternal expression is adaptive because the incompatible paternal allele is not detected, protecting offspring from selective abortion. Conversely, when mismatching is beneficial, imprinting with paternal expression is adaptive because the maternal genotype is more able to identify the presence of a foreign allele in offspring. Thus, imprinting may act as a genomic ‘cloaking device’ during critical periods in development when selective abortion is possible.     

Gene interactions in the evolution of genomic imprinting

Numerous evolutionary theories have been developed to explain the epigenetic phenomenon of genomic imprinting. Here, we explore a subset of theories wherein non-additive genetic interactions can favour imprinting. In the simplest genic interaction—the case of underdominance—imprinting can be favoured to hide effectively low-fitness heterozygous genotypes; however, as there is no asymmetry between maternally and paternally inherited alleles in this model, other means of enforcing monoallelic expression may be more plausible evolutionary outcomes than genomic imprinting. By contrast, more successful interaction models of imprinting rely on an asymmetry between the maternally and paternally inherited alleles at a locus that favours the silencing of one allele as a means of coordinating the expression of high-fitness allelic combinations. For example, with interactions between autosomal loci, imprinting functionally preserves high-fitness genotypes that were favoured by selection in the previous generation. In this scenario, once a focal locus becomes imprinted, selection at interacting loci favours a matching imprint. Uniparental transmission generates similar asymmetries for sex chromosomes and cytoplasmic factors interacting with autosomal loci, with selection favouring the expression of either maternal or paternally derived autosomal alleles depending on the pattern of transmission of the uniparentally inherited factor. In a final class of models, asymmetries arise when genes expressed in offspring interact with genes expressed in one of its parents. Under such a scenario, a locus evolves to have imprinted expression in offspring to coordinate the interaction with its parent''s genome. We illustrate these models and explore key links and differences using a unified framework.     

Self-incompatibility in flowering plants

Self-pollination in some groups of plants is prevented by a sophisticated biochemical signalling system. The molecule active in the female emerges as a highly charged glycoprotein, but the identity of the male determinant remains unknown. Studies of both the molecular biology and the physiology of the interaction suggest that the female polypeptide belongs to a family of glycoproteins which may play an additional, and more general, role in pollination. Pollen compatibility is controlled by one of two genetic systems and new information indicates a mechanism by which they may have arisen, together with the different stigma types with which they are correlated.     

Embryology in Trithuria submersa (Hydatellaceae) and relationships between embryo, endosperm, and perisperm in early-diverging flowering plants

? Premise of the study: Despite their highly reduced morphology, Hydatellaceae bear the unmistakable embryological signature of Nymphaeales, including a starch-rich maternal perisperm and a minute biparental endosperm and embryo. The co-occurrence of perisperm and endosperm in Nymphaeales and other lineages of flowering plants, and their respective functions during the course of seed development and embryo germination, remain enigmatic. ? Methods: Development of the embryo, endosperm, and perisperm was examined histologically from fertilization through germination in flowers and fruits of Trithuria submersa. ? Key results: The embryo of T. submersa initiates two cotyledons prior to seed maturity/dormancy, and their tips remain in contact with the endosperm throughout germination. The endosperm persists as a single layer of cells and serves as the interface between the embryo and the perisperm. The perisperm contains carbohydrates and proteins, and functions as the main storage tissue. The endosperm accumulates proteins and aleurone grains and functions as a transfer cell layer. ? Conclusions: In Nymphaeales, the multiple roles of a more typical endosperm have been separated into two different tissues and genetic entities: a maternal perisperm (nutrient acquisition, storage, mobilization) and a minute biparental endosperm (nutrient transfer to the embryo). The presence of perisperms among several other ancient lineages of angiosperms suggests a modest degree of developmental and functional lability for the nutrient storage tissue (perisperm or endosperm) within seeds during the early evolution of flowering plants. Finally, we examine the evolutionary developmental hypothesis that, contrary to longstanding assumptions, an embryo-nourishing perisperm along with a minute endosperm may represent the plesiomorphic condition for flowering plants.