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1.  Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis 
The New phytologist  2010;186(1):46-53.
Summary
In manylants, including Arabidopsis, hybrids between species and subspecies encounter postfertilization barriers in which hybrid seed fail to develop, or else give rise to infertile progeny. In Arabidopsis, some of these barriers are sensitive to ploidy and to the epigenetic status of donor and recipient genomes. Recently, a role has been proposed for heterochromatin in reprogramming events that occur in reproductive cells, as well as in the embryo and endosperm after fertilization. 21 nt small interfering RNA (siRNA) from activated transposable elements accumulate in pollen, and are translocated from companion vegetative cells into the sperm, while in the maturing seed 24 nt siRNA are primarily maternal in origin. Thus maternal and paternal genomes likely contribute differing small RNA to the zygote and to the endosperm. As heterochromatic sequences also differ radically between, and within, species, small RNA sequences will diverge in hybrids. If transposable elements in the seed are not targeted by small RNA from the pollen, or vice versa, this could lead to hybrid seed failure, in a mechanism reminiscent of hybrid dysgenesis in Drosophila. Heterochromatin also plays a role in apomixis and nucleolar dominance, and may utilize a similar mechanism.
doi:10.1111/j.1469-8137.2010.03193.x
PMCID: PMC3756494  PMID: 20409176
allopolyploidy; dosage; hybrid lethality; siRNA; transposon
2.  Genome-Wide Transcript Profiling of Endosperm without Paternal Contribution Identifies Parent-of-Origin–Dependent Regulation of AGAMOUS-LIKE36 
PLoS Genetics  2011;7(2):e1001303.
Seed development in angiosperms is dependent on the interplay among different transcriptional programs operating in the embryo, the endosperm, and the maternally-derived seed coat. In angiosperms, the embryo and the endosperm are products of double fertilization during which the two pollen sperm cells fuse with the egg cell and the central cell of the female gametophyte. In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed. Here we have exploited cdka;1 fertilization as a novel tool for the identification of seed regulators and factors involved in parent-of-origin–specific regulation during seed development. We have generated genome-wide transcription profiles of cdka;1 fertilized seeds and identified approximately 600 genes that are downregulated in the absence of a paternal genome. Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented. Here, AGL36 was chosen for an in-depth study and shown to be imprinted. We demonstrate that AGL36 parent-of-origin–dependent expression is controlled by the activity of METHYLTRANSFERASE1 (MET1) maintenance DNA methyltransferase and DEMETER (DME) DNA glycosylase. Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.
Author Summary
Seeds of flowering plants consist of three different organisms that develop in parallel. In contrast to animals, a double fertilization event takes place in plants, producing two fertilization products, the embryo and the endosperm. Imprinting, the parent-of-origin–specific expression of genes, typically takes place in the mammalian placenta and in the plant endosperm. A prevailing hypothesis predicts that a parental tug-of-war on the allocation of available recourses to the developing progeny has led to the evolution of imprinting systems where genes expressed from the mother dampen growth whereas genes expressed from the father are growth enhancers. The number of imprinted genes identified in plants is low compared to mammals, and this precludes the elucidation of the epigenetic mechanisms responsible for this specialized expression system. Here, we have used genome-wide transcript profiling of endosperm without paternal contribution to identify seed regulators and, among these, imprinted genes. We identified a cluster of downregulated MADS-box transcription factors, including AGL36, that was subsequently shown to be imprinted by an epigenetic mechanism involving the DNA methylase MET1 and the glycosylase DME. In addition, the expression of the active AGL36 allele was dampened by the FIS Polycomb Repressive Complex, identifying a novel mode of regulation of imprinted genes.
doi:10.1371/journal.pgen.1001303
PMCID: PMC3040660  PMID: 21379330
3.  The Female Gametophyte 
The angiosperm female gametophyte is critical for plant reproduction. It contains the egg cell and central cell that become fertilized and give rise to the embryo and endosperm of the seed, respectively. Female gametophyte development begins early in ovule development with the formation of a diploid megaspore mother cell that undergoes meiosis. One resulting haploid megaspore then develops into the female gametophyte. Genetic and epigenetic processes mediate specification of megaspore mother cell identity and limit megaspore mother cell formation to a single cell per ovule. Auxin gradients influence female gametophyte polarity and a battery of transcription factors mediate female gametophyte cell specification and differentiation. The mature female gametophyte secretes peptides that guide the pollen tube to the embryo sac and contains protein complexes that prevent seed development before fertilization. Post-fertilization, the female gametophyte influences seed development through maternal-effect genes and by regulating parental contributions. Female gametophytes can form by an asexual process called gametophytic apomixis, which involves formation of a diploid female gametophyte and fertilization-independent development of the egg into the embryo. These functions collectively underscore the important role of the female gametophyte in seed and food production.
doi:10.1199/tab.0155
PMCID: PMC3268550  PMID: 22303279
4.  Rapid evolution in crop-weed hybrids under artificial selection for divergent life histories 
Evolutionary Applications  2008;2(2):172-186.
When species hybridize, offspring typically exhibit reduced fitness and maladapted phenotypes. This situation has biosafety implications regarding the unintended spread of novel transgenes, and risk assessments of crop-wild hybrids often assume that poorly adapted hybrid progeny will not evolve adaptive phenotypes. We explored the evolutionary potential of early generation hybrids using nontransgenic wild and cultivated radish (Raphanus raphanistrum, Raphanus sativus) as a model system. We imposed four generations of selection for two weedy traits – early flowering or large size – and measured responses in a common garden in Michigan, USA. Under selection for early flowering, hybrids evolved to flower as early as wild lineages, which changed little. These early-flowering hybrids also recovered wild-type pollen fertility, suggesting a genetic correlation that could accelerate the loss of crop traits when a short life cycle is advantageous. Under selection for large size at reproduction, hybrids evolved longer leaves faster than wild lineages, a potentially advantageous phenotype under longer growing seasons. Although early generation hybrid offspring have reduced fitness, our findings provide novel support for rapid adaptation in crop-wild hybrid populations. Biosafety risk assessment programs should consider the possibility of rapid evolution of weedy traits from early generations of seemingly unfit crop-wild hybrids.
doi:10.1111/j.1752-4571.2008.00051.x
PMCID: PMC3352370
artificial selection; contemporary evolution; correlated evolution; crop-to-wild gene flow; extreme phenotypes; flowering phenology; introgression; plant size
5.  Loss of LORELEI function in the pistil delays initiation but does not affect embryo development in Arabidopsis thaliana 
Plant Signaling & Behavior  2010;5(11):1487-1490.
Double fertilization, uniquely observed in plants, requires successful sperm cell delivery by the pollen tube to the female gametophyte, followed by migration, recognition and fusion of the two sperm cells with two female gametic cells. The female gametophyte not only regulates these steps but also controls the subsequent initiation of seed development. Previously, we reported that loss of LORELEI, which encodes a putative glycosylphosphatidylinositol (GPI)-anchored protein, in the female reproductive tissues causes a delay in initiation of seed development. From these studies, however, it was unclear if embryos derived from fertilization of lre-5 gametophytes continued to lag behind wild-type during seed development. Additionally, it was not determined if the delay in initiation of seed development had any lingering effects during seed germination. Finally, it was not known if loss of LORELEI function affects seedling development given that LORELEI is expressed in eight-day-old seedlings. Here, we showed that despite a delay in initiation, lre-5/lre-5 embryos recover, becoming equivalent to the developing wild-type embryos beginning at 72 hours after pollination. Additionally, lre-5/lre-5 seed germination, and seedling and root development are indistinguishable from wild-type indicating that loss of LORELEI is tolerated, at least under standard growth conditions, in vegetative tissues.
doi:10.4161/psb.5.11.13598
PMCID: PMC3115263  PMID: 21051955
LORELEI; glycosylphosphatidylinositol (GPI)-anchored protein; embryogenesis; DD45; seed germination; primary and lateral root growth; seedling development
6.  PHYSIOLOGY AND BIO – CHEMISTRY OF GERMINATION OF DIFFERENT TYPES OF SEEDS – IV – EFFECT OF CERTAIN CHEMICALS ON GROWTH ANDDEVELOPMENT OF CUCUMBER, MUNGO, PADDY, RADDISH AND TOMATO PLANTS 
Ancient Science of Life  1984;3(4):238-244.
The effect of 100 ppm solution of each of kinetin, adenine, uracil and thymine on the vegetative and reproductive growth of Cucumis sativus, phaseolus mungo, Oryza sativus, Raphanus sativus and Lycopersicum esculentum plants were studied. The rate of vegetative growth was found to be more in the Cucumis sativus, Raphanus sativus and Lycopersicum esculentum plants treated with all the chemicals mentioned above over that of the controls. Phaseolus mungo and Oryza sativa plants shows almost the same growth rate with that of the control plants. So far the reproductive phase is concerned, measured as the size of fruit and number of fruit and seed, Cucumis sativus plants produced about same number of fruits in all the treatments but fruit size varied greatly along with the number of seeds in kinetin and adenine treated plants.
PMCID: PMC3331565  PMID: 22557413
7.  A Statistical Model for Estimating Maternal-Zygotic Interactions and Parent-of-Origin Effects of QTLs for Seed Development 
PLoS ONE  2008;3(9):e3131.
Proper development of a seed requires coordinated exchanges of signals among the three components that develop side by side in the seed. One of these is the maternal integument that encloses the other two zygotic components, i.e., the diploid embryo and its nurturing annex, the triploid endosperm. Although the formation of the embryo and endosperm contains the contributions of both maternal and paternal parents, maternally and paternally derived alleles may be expressed differently, leading to a so-called parent-of-origin or imprinting effect. Currently, the nature of how genes from the maternal and zygotic genomes interact to affect seed development remains largely unknown. Here, we present a novel statistical model for estimating the main and interaction effects of quantitative trait loci (QTLs) that are derived from different genomes and further testing the imprinting effects of these QTLs on seed development. The experimental design used is based on reciprocal backcrosses toward both parents, so that the inheritance of parent-specific alleles could be traced. The computing model and algorithm were implemented with the maximum likelihood approach. The new strategy presented was applied to study the mode of inheritance for QTLs that control endoreduplication traits in maize endosperm. Monte Carlo simulation studies were performed to investigate the statistical properties of the new model with the data simulated under different imprinting degrees. The false positive rate of imprinting QTL discovery by the model was examined by analyzing the simulated data that contain no imprinting QTL. The reciprocal design and a series of analytical and testing strategies proposed provide a standard procedure for genomic mapping of QTLs involved in the genetic control of complex seed development traits in flowering plants.
doi:10.1371/journal.pone.0003131
PMCID: PMC2519836  PMID: 18769549
8.  Paternal effects in Arabidopsis indicate that offspring can influence their own size 
The existence of genetic variation in offspring size in plants and animals is puzzling because offspring size is often strongly associated with fitness and expected to be under stabilizing selection. An explanation for variation in seed size is conflict between parents and between parents and offspring. However, for this hypothesis to be true, it must be shown that the offspring genotype can affect its own size. The existence of paternal effects would support this hypothesis, but these have rarely been shown. Using a diallel cross among four natural accessions of Arabidopsis thaliana we show that maternal, paternal and positional effects jointly influence seed size, number and the frequency of seed abortion. We found that seed abortion (%) depends on the combination of maternal and paternal genotypes, suggesting the existence of mate choice or epistatic incompatibility among accessions of A. thaliana. In addition, since paternal genotype explains approximately 10 per cent of the variation in seed size, we propose that A. thaliana's offspring must influence the amount of resources allocated to themselves. Identification of paternal effects in Arabidopsis should facilitate dissection of the genetic mechanisms involved in paternal effects.
doi:10.1098/rspb.2010.0572
PMCID: PMC2981992  PMID: 20444721
seed number; seed size; trade-off; natural variation; selective seed abortion; intraspecific incompatibility
9.  Pollen flow and effects of population structure on selfing rates and female and male reproductive success in fragmented Magnolia stellata populations 
BMC Ecology  2013;13:10.
Background
Fragmentation of plant populations may affect mating patterns and female and male reproductive success. To improve understanding of fragmentation effects on plant reproduction, we investigated the pollen flow patterns in six adjacent local populations of Magnolia stellata, an insect-pollinated, threatened tree species in Japan, and assessed effects of maternal plant (genet) size, local genet density, population size and neighboring population size on female reproductive success (seed production rates), and effects of mating distance, paternal genet size, population size and separation of populations on male reproductive success.
Results
The seed production rate, i.e. the proportion of ovules that successfully turned into seeds, varied between 1.0 and 6.5%, and increased with increasing population size and neighboring population size, and with decreasing maternal genet size and local genet density. The selfing rate varied between 3.6 and 28.9%, and increased with increasing maternal genet size and with declining local genet density. Male reproductive success increased with increasing paternal genet size, and decreased with increasing mating distance and separation of population. Pollen flow between the populations was low (6.1%) and highly leptocurtic.
Conclusions
Our results indicate that habitat fragmentation, separation and reduced size of populations, affected mating patterns and reproductive success of M. stellata. Local competition for pollinators and plant display size were likely to alter the reproductive success.
doi:10.1186/1472-6785-13-10
PMCID: PMC3670206  PMID: 23517612
Conservation; Fragmentation; Gene flow; Geitonogamy; Insect pollination; Landscape; Magnoliaceae; Paternity analysis; Pollen dispersal; Seed production
10.  Endosperm triploidy has a selective advantage during ongoing parental conflict by imprinting. 
The endosperm of the flowering plant mediates the supply of maternal resources for embryogenesis. An endosperm formed in sexual reproduction between diploid parents is typically triploid, with a 2 : 1 ratio of maternal genetic material (denoted as 2m : 1p). Variation from this ratio affects endosperm size, indicating parent-specific expression of genes involved in endosperm growth and development. The presence of paternally or maternally imprinted genes can be explained by parental conflict over the transfer of nutrients from maternal to offspring tissue. Genomic imprinting can, for example, provide the male parent of an embryo in a mixed-paternity seed pod, with an opportunity for expressing its preference for a disproportionate allocation of resources to its embryo. It has been argued that a diploid 1m : 1p endosperm was ancestral and the 2m : 1p endosperm evolved after parental conflict, to improve maternal control over seed provisioning. We present a population genetic model, which instead places the origin of triploidy early in the parental conflict over resource allocation. We find that there is an advantage to having a triploid endosperm as the parental conflict continues. This advantage can help to explain why the 2m : 1p endosperm prevails among flowering plants.
doi:10.1098/rspb.2004.2783
PMCID: PMC1691787  PMID: 15306295
11.  Effects of pollination timing on seed paternity and seed mass in Silene latifolia (Caryophyllaceae) 
Annals of Botany  2009;104(4):767-773.
Background and Aims
Competition among genetically different pollen donors within one recipient flower may play an important role in plant populations, increasing offspring genetic diversity and vigour. However, under field conditions stochastic pollen arrival times may result in disproportionate fertilization success of the first-arriving pollen, even to the detriment of the recipient plant's and offspring fitness. It is therefore critical to evaluate the relative importance of arrival times of pollen from different donors in determining siring success.
Methods
Hand pollinations and genetic markers were used to investigate experimentally the effect of pollination timing on seed paternity, seed mass and stigmatic wilting in the the dioecious plant Silene latifolia. In this species, high prevalence of multiply-sired fruits in natural populations suggests that competition among different donors may often take place (at fertilization or during seed development); however, the role of variation due to pollen arrival times is not known.
Key Results
First-arriving pollen sired significantly more seeds than later-arriving pollen. This advantage was expressed already before the first pollen tubes could reach the ovary. Simultaneously with pollen tube growth, the stigmatic papillae wilted visibly. Individual seeds were heavier in fruits where one donor sired most seeds than in fruits where both donors had more even paternity shares.
Conclusions
In field populations of S. latifolia, fruits are often multiply-sired. Because later-arriving pollen had decreased chances of fertilizing the ovules, this implies that open-pollinated flowers often benefit from pollen carry-over or pollinator visits within short time intervals, which may contribute to increase offspring genetic diversity and fitness.
doi:10.1093/aob/mcp154
PMCID: PMC2729624  PMID: 19567418
Reproduction; reproductive success; pollen; siring success; microsatellite DNA; paternity; pollen tube growth; seed mass; Silene alba; stigma wilting
12.  The impact of plant and flower age on mating patterns 
Annals of Botany  2009;105(1):7-22.
Background
Over a season, plant condition, amount of ongoing reproduction and biotic and abiotic environmental factors vary. As flowers age, flower condition and amount of pollen donated and received also vary. These internal and external changes are significant for fitness if they result in changes in reproduction and mating.
Scope
Literature from several fields was reviewed to provide a picture of the changes that occur in plants and flowers that can affect mating over a season. As flowers age, both the entire flower and individual floral whorls show changes in appearance and function. Over a season, changes in mating often appear as alteration in seed production vs. pollen donation. In several species, older, unpollinated flowers are more likely to self. If flowers are receiving pollen, staying open longer may increase the number of mates. In wild radish, for which there is considerable information on seed paternity, older flowers produce fewer seeds and appear to discriminate less among pollen donors. Pollen donor performance can also be linked to maternal plant age. Different pollinators and mates are available across the season. Also in wild radish, maternal plants appear to exert the most control over paternity when they are of intermediate age.
Conclusions
Although much is known about the characters of plants and flowers that can change over a season, there is less information on the effects of age on mating. Several studies document changes in self-pollination over time, but very few, other than those on wild radish, consider more subtle aspects of differential success of pollen donors over time.
doi:10.1093/aob/mcp260
PMCID: PMC2794063  PMID: 19875519
Mating patterns; plant age; flower age; wild radish; Raphanus
13.  Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis 
Sexual Plant Reproduction  2009;22(4):277-289.
Arabidopsis APETALA2 (AP2) controls seed mass maternally, with ap2 mutants producing larger seeds than wild type. Here, we show that AP2 influences development of the three major seed compartments: embryo, endosperm, and seed coat. AP2 appears to have a significant effect on endosperm development. ap2 mutant seeds undergo an extended period of rapid endosperm growth early in development relative to wild type. This early expanded growth period in ap2 seeds is associated with delayed endosperm cellularization and overgrowth of the endosperm central vacuole. The subsequent period of moderate endosperm growth is also extended in ap2 seeds largely due to persistent cell divisions at the endosperm periphery. The effect of AP2 on endosperm development is mediated by different mechanisms than parent-of-origin effects on seed size observed in interploidy crosses. Seed coat development is affected; integument cells of ap2 mutants are more elongated than wild type. We conclude that endosperm overgrowth and/or integument cell elongation create a larger postfertilization embryo sac into which the ap2 embryo can grow. Morphological development of the embryo is initially delayed in ap2 compared with wild-type seeds, but ap2 embryos become larger than wild type after the bent-cotyledon stage of development. ap2 embryos are able to fill the enlarged postfertilization embryo sac, because they undergo extended periods of cell proliferation and seed filling. We discuss potential mechanisms by which maternally acting AP2 influences development of the zygotic embryo and endosperm to repress seed size.
doi:10.1007/s00497-009-0116-1
PMCID: PMC2796121  PMID: 20033449
AP2; Maternal control; Seed development; Seed mass
14.  Genetic subtraction profiling identifies genes essential for Arabidopsis reproduction and reveals interaction between the female gametophyte and the maternal sporophyte 
Genome Biology  2007;8(10):R204.
Genetic subtraction and expression profiling of wild-type Arabidopsis and a sporophytic mutant lacking an embryo sac identified 1,260 genes expressed in the embryo sac; a total of 527 genes were identified for their expression in ovules of mutants lacking an embryo sac.
Background
The embryo sac contains the haploid maternal cell types necessary for double fertilization and subsequent seed development in plants. Large-scale identification of genes expressed in the embryo sac remains cumbersome because of its inherent microscopic and inaccessible nature. We used genetic subtraction and comparative profiling by microarray between the Arabidopsis thaliana wild-type and a sporophytic mutant lacking an embryo sac in order to identify embryo sac expressed genes in this model organism. The influences of the embryo sac on the surrounding sporophytic tissues were previously thought to be negligible or nonexistent; we investigated the extent of these interactions by transcriptome analysis.
Results
We identified 1,260 genes as embryo sac expressed by analyzing both our dataset and a recently reported dataset, obtained by a similar approach, using three statistical procedures. Spatial expression of nine genes (for instance a central cell expressed trithorax-like gene, an egg cell expressed gene encoding a kinase, and a synergid expressed gene encoding a permease) validated our approach. We analyzed mutants in five of the newly identified genes that exhibited developmental anomalies during reproductive development. A total of 527 genes were identified for their expression in ovules of mutants lacking an embryo sac, at levels that were twofold higher than in the wild type.
Conclusion
Identification of embryo sac expressed genes establishes a basis for the functional dissection of embryo sac development and function. Sporophytic gain of expression in mutants lacking an embryo sac suggests that a substantial portion of the sporophytic transcriptome involved in carpel and ovule development is, unexpectedly, under the indirect influence of the embryo sac.
doi:10.1186/gb-2007-8-10-r204
PMCID: PMC2246279  PMID: 17915010
15.  Unrestricted quality of seeds in European broad-leaved tree species growing at the cold boundary of their distribution 
Annals of Botany  2011;109(2):473-480.
Background and Aims
The low-temperature range limit of tree species may be determined by their ability to produce and disperse viable seeds. Biological processes such as flowering, pollen transfer, pollen tube growth, fertilization, embryogenesis and seed maturation are expected to be affected by cold temperatures. The aim of this study was to assess the quality of seeds of nine broad-leaved tree species close to their elevational limit.
Methods
We studied nine, mostly widely distributed, European broad-leaved tree species in the genera Acer, Fagus, Fraxinus, Ilex, Laburnum, Quercus, Sorbus and Tilia. For each species, seeds were collected from stands close to optimal growth conditions (low elevation) and from marginal stands (highest elevation), replicated in two regions in the Swiss Alps. Measurements included seed weight, seed size, storage tissue quality, seed viability and germination success.
Key Results
All species examined produced a lot of viable seeds at their current high-elevation range limit during a summer ranked ‘normal’ by long-term temperature records. Low- and high-elevation seed sources showed hardly any trait differences. The concentration of non-structural carbohydrates tended to be higher at high elevation. Additionally, in one species, Sorbus aucuparia, all measured traits showed significantly higher seed quality in high-elevation seed sources.
Conclusions
For the broad-leaved tree taxa studied, the results are not in agreement with the hypothesis of reduced quality of seeds in trees at their high-elevation range limits. Under the current climatic conditions, seed quality does not constitute a serious constraint in the reproduction of these broad-leaved tree species at their high-elevation limit.
doi:10.1093/aob/mcr299
PMCID: PMC3268544  PMID: 22156401
Rosaceae; Fagaceae; Aceraceae; Oleaceae; Tiliaceae; Aquifoliaceae; Fabaceae; seed morphology; elevation; germination; carbohydrates; Alps
16.  Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development 
PLoS Genetics  2013;9(1):e1003163.
Seed development in flowering plants is initiated after a double fertilization event with two sperm cells fertilizing two female gametes, the egg cell and the central cell, leading to the formation of embryo and endosperm, respectively. In most species the endosperm is a polyploid tissue inheriting two maternal genomes and one paternal genome. As a consequence of this particular genomic configuration the endosperm is a dosage sensitive tissue, and changes in the ratio of maternal to paternal contributions strongly impact on endosperm development. The FERTILIZATION INDEPENDENT SEED (FIS) Polycomb Repressive Complex 2 (PRC2) is essential for endosperm development; however, the underlying forces that led to the evolution of the FIS-PRC2 remained unknown. Here, we show that the functional requirement of the FIS-PRC2 can be bypassed by increasing the ratio of maternal to paternal genomes in the endosperm, suggesting that the main functional requirement of the FIS-PRC2 is to balance parental genome contributions and to reduce genetic conflict. We furthermore reveal that the AGAMOUS LIKE (AGL) gene AGL62 acts as a dosage-sensitive seed size regulator and that reduced expression of AGL62 might be responsible for reduced size of seeds with increased maternal genome dosage.
Author Summary
Flowering plants reproduce by forming seeds that contain an embryo surrounded by a nourishing endosperm tissue that, similar to the mammalian placenta, supports embryo growth. Normal endosperm development requires the FERTILIZATION INDEPENDENT SEED (FIS) Polycomb Repressive Complex2 (PRC2). In most flowering plants the endosperm is a polyploid tissue containing two maternal and one paternal genome copies. As a consequence of this particular genomic configuration the endosperm is a dosage sensitive tissue, and changes in the ratio of maternal and paternal genome copies have drastic effects on endosperm development. Here we investigated the consequences of increased maternal genome dosage on endosperm and seed development. We found that increased maternal genome dosage alleviates the need for the FIS-PRC2 in the endosperm. While in fis mutant seeds with normal maternal genome dosage the endosperm fails to cellularize and embryos arrest, in fis mutant seeds with increased maternal genome dosage the endosperm cellularizes and viable embryos develop. Our study suggests a functional role of the FIS-PRC2 in balancing parental genome dosage in the endosperm. We propose that the FIS-PRC2 evolved to reduce genetic conflict that arose as a consequence of unbalanced genome contributions in the endosperm.
doi:10.1371/journal.pgen.1003163
PMCID: PMC3542072  PMID: 23326241
17.  DNA Methylation Causes Predominant Maternal Controls of Plant Embryo Growth 
PLoS ONE  2008;3(5):e2298.
The parental conflict hypothesis predicts that the mother inhibits embryo growth counteracting growth enhancement by the father. In plants the DNA methyltransferase MET1 is a central regulator of parentally imprinted genes that affect seed growth. However the relation between the role of MET1 in imprinting and its control of seed size has remained unclear. Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth. We show that the loss of MET1 during male gametogenesis causes a reduction of seed size, presumably linked to silencing of the paternal allele of growth enhancers in the endosperm, which nurtures the embryo. However, we find no evidence for a similar role of MET1 during female gametogenesis. Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase. MET1 inhibits seed growth by restricting cell division and elongation in the maternal integuments that surround the seed. Our data demonstrate new controls of seed growth linked to the mode of reproduction typical of flowering plants. We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.
doi:10.1371/journal.pone.0002298
PMCID: PMC2390113  PMID: 18509545
18.  Imprinting in the endosperm: a possible role in preventing wide hybridization. 
Reproductive isolation is considered to play a key part in evolution, and plants and animals have developed a range of strategies that minimize gene flow between species. In plants, these strategies involve either pre-zygotic barriers, such as differences in floral structure and pollen-stigma recognition, or post-zygotic barriers, which are less well understood and affect aspects of seed development ranging from fertilization to maturation. In most angiosperms, a double fertilization event gives rise to a zygote and the endosperm: a triploid tissue with an unequal parental genomic contribution, which, like the placenta of mammals, provides reserves to the developing embryo. Interestingly, many aspects of endosperm development, again like the placenta, are regulated by a range of epigenetic mechanisms that are globally termed imprinting. Imprinted genes are characterized by their uniparental expression, the other parental allele being silenced. Normal development of the endosperm thus requires a highly specific balance of gene expression, from either the maternal or paternal genomes. Any alteration of this balance resulting from changes in allelic copy number, sequence or epigenetic imprints can cause endosperm failure and eventual seed abortion. In its widest sense, the endosperm thus serves as an accurate 'sensor' of compatibility between parents. A first step in understanding this important, yet complex system must clearly be the isolation and characterization of as wide a range as possible of imprinted genes.
doi:10.1098/rstb.2003.1292
PMCID: PMC1693205  PMID: 12831476
19.  Seed dimorphism, nutrients and salinity differentially affect seed traits of the desert halophyte Suaeda aralocaspica via multiple maternal effects 
BMC Plant Biology  2012;12:170.
Background
Maternal effects may influence a range of seed traits simultaneously and are likely to be context-dependent. Disentangling the interactions of plant phenotype and growth environment on various seed traits is important for understanding regeneration and establishment of species in natural environments. Here, we used the seed-dimorphic plant Suaeda aralocaspica to test the hypothesis that seed traits are regulated by multiple maternal effects.
Results
Plants grown from brown seeds had a higher brown:black seed ratio than plants from black seeds, and germination percentage of brown seeds was higher than that of black seeds under all conditions tested. However, the coefficient of variation (CV) for size of black seeds was higher than that of brown seeds. Seeds had the smallest CV at low nutrient and high salinity for plants from brown seeds and at low nutrient and low salinity for plants from black seeds. Low levels of nutrients increased size and germinability of black seeds but did not change the seed morph ratio or size and germinability of brown seeds. High levels of salinity decreased seed size but did not change the seed morph ratio. Seeds from high-salinity maternal plants had a higher germination percentage regardless of level of germination salinity.
Conclusions
Our study supports the multiple maternal effects hypothesis. Seed dimorphism, nutrient and salinity interacted in determining a range of seed traits of S. aralocaspica via bet-hedging and anticipatory maternal effects. This study highlights the importance of examining different maternal factors and various offspring traits in studies that estimate maternal effects on regeneration.
doi:10.1186/1471-2229-12-170
PMCID: PMC3515402  PMID: 23006315
Bet-hedging; Germination; Seed heteromorphism; Seed morph ratio; Seed size
20.  Requirement of proline synthesis during Arabidopsis reproductive development 
BMC Plant Biology  2012;12:191.
Background
Gamete and embryo development are crucial for successful reproduction and seed set in plants, which is often the determining factor for crop yield. Proline accumulation was largely viewed as a specific reaction to overcome stress conditions, while recent studies suggested important functions of proline metabolism also in reproductive development. Both the level of free proline and proline metabolism were proposed to influence the transition to flowering, as well as pollen and embryo development.
Results
In this study, we performed a detailed analysis of the contribution of individual proline biosynthetic enzymes to vegetative development and reproductive success in Arabidopsis. In contrast to previous reports, we found that pyrroline-5-carboxylate (P5C) synthetase 2 (P5CS2) is not essential for sexual reproduction although p5cs2 mutant plants were retarded in vegetative development and displayed reduced fertility under long-day conditions. Single mutant plants devoid of P5CS1 did not show any developmental defects. Simultaneous absence of both P5CS isoforms resulted in pollen sterility, while fertile egg cells could still be produced. Expression of P5C reductase (P5CR) was indispensable for embryo development but surprisingly not needed for pollen or egg cell fertility. The latter observation could be explained by an extreme stability of P5CR activity, which had a half-life time of greater than 3 weeks in vitro. Expression of P5CR-GFP under the control of the endogenous P5CR promoter was able to restore growth of homozygous p5cr mutant embryos. The analysis of P5CR-GFP-fluorescence in planta supported an exclusively cytoplasmatic localisation of P5CR.
Conclusions
Our results demonstrate that potential alternative pathways for proline synthesis or inter-generation transfer of proline are not sufficient to overcome a defect in proline biosynthesis from glutamate during pollen development. Proline biosynthesis through P5CS2 and P5CR is limiting for vegetative and reproductive development in Arabidopsis, whereas disruption of P5CS1 alone does not affect development of non-stressed plants.
doi:10.1186/1471-2229-12-191
PMCID: PMC3493334  PMID: 23062072
Proline metabolism; Gamete and embryo development; Enzyme stability; Subcellular localisation
21.  The Arabidopsis general transcription factor TFIIB1 (AtTFIIB1) is required for pollen tube growth and endosperm development 
Journal of Experimental Botany  2013;64(8):2205-2218.
Pollen tube growth and endosperm development are important for fertilization and seed formation. The genetic mechanism of the processes remains poorly understood. This study reports the functional characterization of AtTFIIB1 in pollen tube growth and endosperm development. AtTFIIB1 shares 86% and 44% similarity with AtTFIIB2 and AtTFIIB3/AtpBRP2, respectively. It is expressed in many tissues including vegetative nuclei and generative cells of pollen grains and pollen tubes, endosperm, and embryos. It is thus different from AtTFIIB2, whose expression is not found in the endosperm and vegetative nucleus of mature pollen, and AtTFIIB3/AtpBRP2, which is expressed mostly in male gametophytes and weakly in seeds. Mutations in AtTFIIB1 caused a drastic retardation of pollen tube growth and endosperm development, as well as impaired pollen tube guidance and reception, leading to disruption of fertilization and seed development. Expression of AtTFIIB2 driven by the AtTFIIB1 promoter could restore the defective pollen tube growth, guidance, and reception completely, but only partially recovered the seed development in attfiib1, whilst expression of AtTFIIB3/AtpBRP2 driven by the AtTFIIB1 promoter could rescue only the defective attfiib1 seeds. All these results suggest that AtTFIIB1 plays important roles in pollen tube growth, guidance, and reception as well as endosperm development and is partially functionally different from AtTFIIB2 and AtTFIIB3/AtpBRP2.
doi:10.1093/jxb/ert078
PMCID: PMC3654413  PMID: 23547107
Arabidopsis; AtTFIIB1; endosperm; fertilization; pollen; transcription factor.
22.  One tissue, two fates: different roles of megagametophyte cells during Scots pine embryogenesis 
Journal of Experimental Botany  2009;60(4):1375-1386.
In the Scots pine (Pinus sylvestris L.) seed, embryos grow and develop within the corrosion cavity of the megagametophyte, a maternally derived haploid tissue, which houses the majority of the storage reserves of the seed. In the present study, histochemical methods and quantification of the expression levels of the programmed cell death (PCD) and DNA repair processes related genes (MCA, TAT-D, RAD51, KU80, and LIG) were used to investigate the physiological events occurring in the megagametophyte tissue during embryo development. It was found that the megagametophyte was viable from the early phases of embryo development until the early germination of mature seeds. However, the megagametophyte cells in the narrow embryo surrounding region (ESR) were destroyed by cell death with morphologically necrotic features. Their cell wall, plasma membrane, and nuclear envelope broke down with the release of cell debris and nucleic acids into the corrosion cavity. The occurrence of necrotic-like cell death in gymnosperm embryogenesis provides a favourable model for the study of developmental cell death with necrotic-like morphology and suggests that the mechanism underlying necrotic cell death is evolutionary conserved.
doi:10.1093/jxb/erp020
PMCID: PMC2657542  PMID: 19246593
Conifer; developmental cell death; embryogenesis; megagametophyte; necrotic cell death; seed development
23.  Imprinting of the Polycomb Group Gene MEDEA Serves as a Ploidy Sensor in Arabidopsis 
PLoS Genetics  2009;5(9):e1000663.
Balanced maternal and paternal genome contributions are a requirement for successful seed development. Unbalanced contributions often cause seed abortion, a phenomenon that has been termed “triploid block.” Misregulation of imprinted regulatory genes has been proposed to be the underlying cause for abnormalities in growth and structure of the endosperm in seeds with deviating parental contributions. We identified a mutant forming unreduced pollen that enabled us to investigate direct effects of unbalanced parental genome contributions on seed development and to reveal the underlying molecular mechanism of dosage sensitivity. We provide evidence that parent-of-origin–specific expression of the Polycomb group (PcG) gene MEDEA is causally responsible for seed developmental aberrations in Arabidopsis seeds with increased paternal genome contributions. We propose that imprinted expression of PcG genes is an evolutionary conserved mechanism to balance parental genome contributions in embryo nourishing tissues.
Author Summary
Crosses between plants of different ploidy often fail because seed development does not proceed normally and non-viable seeds are produced. It is assumed that abnormalities in growth and structure of the endosperm (the nutritional tissue of the seed) are the cause of triploid seed failure, consistent with the proposed role of the endosperm in reproductive isolation and angiosperm speciation. In many species, the ratio of maternal to paternal genomes in the endosperm is important for normal seed development, giving rise to the hypothesis that parent-of-origin–specific gene expression (imprinting) of regulatory genes in the endosperm is the underlying cause for developmental failure in seeds with deviating parental contributions. We tested this hypothesis using the jason mutant that forms unreduced male gametes and triploid seeds with increased paternal genome dosage. Based on the results of our study, we propose that imprinting of the FIS component MEDEA serves as a dosage sensor for increasing paternal genome contributions, establishing the molecular basis for dosage sensitivity. Our study provides strong evidence supporting the hypothesis that misbalanced expression of imprinted genes is the cause of seed development defects after interploidy crosses and demonstrates that MEDEA imprinting is a major origin of developmental defects caused by increased paternal genome contributions.
doi:10.1371/journal.pgen.1000663
PMCID: PMC2738949  PMID: 19779546
24.  Environmental Maternal Effects Mediate the Resistance of Maritime Pine to Biotic Stress 
PLoS ONE  2013;8(7):e70148.
The resistance to abiotic stress is increasingly recognised as being impacted by maternal effects, given that environmental conditions experienced by parent (mother) trees affect stress tolerance in offspring. We hypothesised that abiotic environmental maternal effects may also mediate the resistance of trees to biotic stress. The influence of maternal environment and maternal genotype and the interaction of these two factors on early resistance of Pinus pinaster half-sibs to the Fusarium circinatum pathogen was studied using 10 mother genotypes clonally replicated in two contrasting environments. Necrosis length of infected seedlings was 16% shorter in seedlings grown from favourable maternal environment seeds than in seedlings grown from unfavourable maternal environment seeds. Damage caused by F. circinatum was mediated by maternal environment and maternal genotype, but not by seed mass. Mechanisms unrelated to seed provisioning, perhaps of epigenetic nature, were probably involved in the transgenerational plasticity of P. pinaster, mediating its resistance to biotic stress. Our findings suggest that the transgenerational resistance of pines due to an abiotic stress may interact with the defensive response of pines to a biotic stress.
doi:10.1371/journal.pone.0070148
PMCID: PMC3724826  PMID: 23922944
25.  Parental Genome Dosage Imbalance Deregulates Imprinting in Arabidopsis 
PLoS Genetics  2010;6(3):e1000885.
In mammals and in plants, parental genome dosage imbalance deregulates embryo growth and might be involved in reproductive isolation between emerging new species. Increased dosage of maternal genomes represses growth while an increased dosage of paternal genomes has the opposite effect. These observations led to the discovery of imprinted genes, which are expressed by a single parental allele. It was further proposed in the frame of the parental conflict theory that parental genome imbalances are directly mirrored by antagonistic regulations of imprinted genes encoding maternal growth inhibitors and paternal growth enhancers. However these hypotheses were never tested directly. Here, we investigated the effect of parental genome imbalance on the expression of Arabidopsis imprinted genes FERTILIZATION INDEPENDENT SEED2 (FIS2) and FLOWERING WAGENINGEN (FWA) controlled by DNA methylation, and MEDEA (MEA) and PHERES1 (PHE1) controlled by histone methylation. Genome dosage imbalance deregulated the expression of FIS2 and PHE1 in an antagonistic manner. In addition increased dosage of inactive alleles caused a loss of imprinting of FIS2 and MEA. Although FIS2 controls histone methylation, which represses MEA and PHE1 expression, the changes of PHE1 and MEA expression could not be fully accounted for by the corresponding fluctuations of FIS2 expression. Our results show that parental genome dosage imbalance deregulates imprinting using mechanisms, which are independent from known regulators of imprinting. The complexity of the network of regulations between expressed and silenced alleles of imprinted genes activated in response to parental dosage imbalance does not support simple models derived from the parental conflict hypothesis.
Author Summary
In mammals and plants, imprinted genes are expressed preferentially by the copy inherited from either the mother or the father. In plants genome dosage is easily manipulated using tetraploid plants that contain twice the genome dosage of the natural diploid plants. The increased maternal dosage reduces seed size while increased paternal dosage has the opposite effect. It was further proposed that parental genomic imbalances are directly mirrored by antagonistic regulations of imprinted genes encoding maternal growth inhibitors and paternal growth enhancers. However these hypotheses were never tested directly. We measured the expression of imprinted genes and their regulators, in crosses between diploid and tetraploid Arabidopsis plants. Surprisingly, parental dosage imbalance affected each imprinted gene in a different manner and the imprinted status was also affected. Our results point to a relationship between imprinting and dosage imbalance that is more complex than predicted.
doi:10.1371/journal.pgen.1000885
PMCID: PMC2841625  PMID: 20333248

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