A model of triploid endosperm evolution driven by parent-offspring conflict

The parental investment in angiosperms comprises the endosperm, a nutrient reserve that is used during seed development. The endosperm contains genes from both parents. The most common endosperm form is the 3n Polygonum -type with more maternal genetic influence than paternal, i.e. with two maternal nuclei and one paternal nucleus. The evolutionary original state is thought to be a diploid endosperm with equal influence of the parents. We focus on the evolution of the triploid endosperm and show that a gene for triploid endosperm would have an initial advantage in a population of diploid endosperm type plants, and increase to fixation. We assume that endosperm amount is controlled by endosperm genes. Then a gene causing triploid endosperm will increase the influence of the mother plant on parental investment. The production of endosperm with two copies of the maternal genes will modify the inheritance of endosperm amount and cause an increased production of seeds.     

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.     

基因组印迹与种子发育

胚乳介导营养物质从母体到胚的转运过程,是开花植物中发生印迹的重要部位。胚乳的发育异常会导致胚的败育。在拟南芥中已鉴定到三个FIS (fertilization-independent seed) 基因,能制止无需受精即形成种子的发育过程,即FIS1/ MEDEA、FIS2和FIS3/FIE。其中MEDEA基因是胚乳发育的主要调控基因,在胚乳中被印迹。FWA基因也在胚乳中被印迹。系统阐述了植物基因组印迹的机理以及MEA和FWA印迹机制的研究进展,并介绍了印迹发生的亲本冲突学说、印迹的方式及其它已报道的印迹基因。     

DNA methylation causes predominant maternal controls of plant embryo growth

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.     

玉米籽粒性状的遗传效应分析

采用二倍体胚和三倍体胚乳种子遗传模型及其分析方法,以5个玉米自交系及其配制的F1,F2,BC1,BC2世代为材料,研究5个玉米种子性状的胚直接效应、胚乳直接效应、母体效应和细胞质效应。分析结果表明,除粒宽外,各性状的遗传同时由细胞质效应和胚、胚乳、母体基因效应所控制,百粒重主要受胚乳和母体效应的影响,粒长的遗传以母体效应为主,粒宽和粒厚以胚乳效应为主。各部位籽粒百粒重的胚乳直接加性效应与母体加性效应的协方差达到显著或极显著水平,其余性状的胚、胚乳直接效应与母体效应间的协方差均不显著,通过母体植株的遗传表现可以对这些性状进行有效的选择。S22 是改良百粒重的优良亲本。 Abstract：The embryo,endosperm and cytoplasm effects of seven seed traits were studied by genetic model for diploid embryo and triploid endosperm plant seeds using five inbreds and their F1, F2, BC1 and BC2 generations. The estimates of genetic variance components indicated that the inheritance of all other kernel traits was controlled by the four effects except kernel width. The 100?kernel weight was mainly controlled by endosperm and maternal effects , and kernel length was controlled by the maternal effects,while endosperm conrrolled kernel width and kernel thickness. Except the significant or highly significant covariances between the endosperm direct additive and maternal additive effects for 100－kernel weight,all other traits between the embryo or endosperm direct effect and the maternal were not significant. So,maize inbreds could be developed by direct selection based on maternal plants for these traits. S22 was the best inbred of the improvement for kernel weight in this study.     

Autonomous endosperm development in flowering plants: how to overcome the imprinting problem?

In the vast majority of sexually reproducing flowering plants, a ratio of 2 maternally derived genomes to 1 paternally derived genome (2m:1p) is essential for normal endosperm development, and therefore ultimately for seed development. Even in many pseudogamous apomicts, where the embryo develops without a paternal contribution, fertilisation of the endosperm to obtain the correct 2m:1p parental ratio is still necessary. How do autonomous apomicts, where both embryo and endosperm develop autonomously, circumvent this requirement? The background for the 2m:1p requirement is that the parental genomes are epigenetically different; in either genome, a set of genes is silenced in a sex-specific way by genomic imprinting. Removal of the imprints from the maternally derived endosperm genome leads to expression of normally maternally silenced genes, and effectively supplies the missing paternal genome. In Arabidopsis, we propose that a combination of the fie mutation and hypomethylation of the genome creates such a situation in the endosperm genome. As a result, in a fie mutant, hypomethylated ovule complete autonomous endosperm development takes place in the absence of fertilisation.     

A statistical model for estimating maternal-zygotic interactions and parent-of-origin effects of QTLs for seed development

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.     

The occurrence of phenotypically complementary apomixis-recombinants in crosses between sexual and apomictic dandelions (<Emphasis Type="Italic">Taraxacum officinale</Emphasis>)

Apomictic seed development in dandelion ( Taraxacum officinale) involves (1) restitutional meiosis (diplospory), (2) egg cell parthenogenesis, and (3) autonomous endosperm development. The question is whether these elements of apomixis are controlled by one single gene or by several independent genes. Five triploid non-apomictic hybrids, obtained in diploid sexual × triploid apomict crosses were characterized using cyto-embryological and genetic methods. Nomarski-differential interference contrast microscopy and the transmission of microsatellite markers and ploidy levels indicated that the hybrids combined elements of the apomictic and the sexual developmental pathway. Hybrids form two complementary groups with respect to the presence or absence of parthenogenesis and autonomous endosperm development. The occurrence of complementary apomixis-recombinants suggests that parthenogenesis and autonomous endosperm development in Taraxacum are regulated independently by different genes. This study also indicates that early embryo development is independent of endosperm formation, but that endosperm is essential for later embryo growth.     

Kin selection and conflict in seed maturation

There are four genetically distinct components in the developing seeds of flowering plants: maternal sporophyte, gametophyte, endosperm, and embryo. Each component can potentially influence the quantity or quality of nutrients provided to the embryo of its seed, thereby reducing the amount available to embryos in other seeds of that plant. The theory of kin selection predicts that each component will be selected to favor its own embryo over the other embryos to the extent that it is more closely related to its own. Under this criterion, an embryo should be selected to try to acquire more nutrients than the endosperm should be selected to provide, the endosperm should try to supply more than the gametophyte should, and the gametophyte more than the parent sporophyte. Evidence for this conflict of interests is found in the higher frequency of endopolyploidy, nutrient-absorbing haustoria, and food storage tissues in the embryo and endosperm than in the gametophyte of maternal tissues.This theory also suggests how the gametophyte, which is the nurse tissue of gymnosperm seeds, was displaced from this role in the flowering plants by an endosperm initiated by a secondary fertilization. “Neoteny” in the pro-angiosperms created conditions in which (1) an endosperm initiated by double fertilization would be more closely related to the embryo than is the gametophyte and (2) the endosperm would be formed early enough to be of significant aid to the embryo.If this theory is correct it (1) requires a different approach to the study of seed morphology and physiology, (2) increases the plausibility of arguments that flowering plants are a polyphyletic group, (3) provides evidence that parents cannot always control the outcome of conflict with their offspring, and (4) forges a conceptual link in our understanding of the evolution of social interactions in plants and animals.     

植物胚乳发育的表观遗传学调控

被子植物的种子发育从双受精开始, 产生二倍体的胚和三倍体的胚乳。在种子发育和萌发过程中, 胚乳向胚组织提供营养物质, 因此胚乳对胚和种子的正常生长发育至关重要。开花植物发生基因组印迹的主要器官是胚乳。印迹基因的表达受表观遗传学机制的调控, 包括DNA甲基化和组蛋白H3K27甲基化修饰以及依赖于PolIV的siRNAs (p4-siRNAs)调控。基因组印迹的表观遗传学调控对胚乳的正常发育和种子育性具有不可或缺的重要作用。最新研究显示, 胚乳的整个基因组DNA甲基化水平降低, 而且去甲基化作用可能源于雌配子体的中央细胞。该文综述了种子发育的表观遗传学调控机制, 包括基因组印迹机制以及胚乳基因组DNA甲基化变化研究的最新进展。     

Arabidopsis haiku mutants reveal new controls of seed size by endosperm

In flowering plants, maternal seed integument encloses the embryo and the endosperm, which are both derived from double fertilization. Although the development of these three components must be coordinated, we have limited knowledge of mechanisms involved in such coordination. The endosperm may play a central role in these mechanisms as epigenetic modifications of endosperm development, via imbalance of dosage between maternal and paternal genomes, affecting both the embryo and the integument. To identify targets of such epigenetic controls, we designed a genetic screen in Arabidopsis for mutants that phenocopy the effects of dosage imbalance in the endosperm. The two mutants haiku 1 and haiku 2 produce seed of reduced size that resemble seed with maternal excess in the maternal/paternal dosage. Homozygous haiku seed develop into plants indistinguishable from wild type. Each mutation is sporophytic recessive, and double-mutant analysis suggests that both mutations affect the same genetic pathway. The endosperm of haiku mutants shows a premature arrest of increase in size that causes precocious cellularization of the syncytial endosperm. Reduction of seed size in haiku results from coordinated reduction of endosperm size, embryo proliferation, and cell elongation of the maternally derived integument. We present further evidence for a control of integument development mediated by endosperm-derived signals.     

Ploidy barrier to endosperm development in maize

Maize kernels inheriting the indeterminate gametophyte mutant (ig) on the female side had endosperms that ranged in ploidy level from diploid (2x) to nonaploid (9x). In crosses with diploid males, only kernels of the triploid endosperm class developed normally. Kernels of the tetraploid endosperm class were half-sized but with well-developed embryos that regularly germinated. Kernels of endosperm composition other than triploid or tetraploid were abortive.-Endosperm ploidy level resulting from mating ig/ig x tetraploid Ig similarly was variable. Most endosperms started to degenerate soon after pollination and remained in an arrested state. Hexaploid endosperm was exceptional; it developed normally during the sequence of stages studied and accounted for plump kernels on mature ears. Since such kernels have diploid maternal tissues (pericarp) but triploid embryos, the present finding favors the view that endosperm failure or success in such circumstances is governed by conditions within the endosperm itself.-Whereas tetraploid endosperm consisting of three maternal genomes and one paternal genome is slightly reduced in size but supports viable seed development, that endosperm having two maternal and two paternal chromosome sets was highly defective and conditioned abortion. Thus, development of maize endosperm evidently is affected by the parental source of its sets of chromosomes.     

籼稻糙米厚度的发育遗传研究

应用包括３套遗传体系基因效应的数量性状发育遗传模型,分析了１２个籼稻亲本在４个不同稻米发育时期的糙米厚性状。结果表明,三倍体胚乳、二倍体母体植株基因的加性和显性效应以及细胞质效应均可以明显影响各个稻米发育时期的糙米厚度,其中灌浆始期以二倍体母体植株效应为主,灌浆中后期以三倍体胚乳效应为主,成熟期则以细胞质效应为主。在４个不同发育时期中,控制糙米厚的基因加性效应和显性效应交替为主。胚乳显性方差和母体     

Embryo and endosperm development is disrupted in the female gametophytic capulet mutants of Arabidopsis

The female gametophyte of higher plants gives rise, by double fertilization, to the diploid embryo and triploid endosperm, which develop in concert to produce the mature seed. What roles gametophytic maternal factors play in this process is not clear. The female-gametophytic effects on embryo and endosperm development in the Arabidopsis mea, fis, and fie mutants appear to be due to gametic imprinting that can be suppressed by METHYL TRANSFERASE1 antisense (MET1 a/s) transgene expression or by mutation of the DECREASE IN DNA METHYLATION1 (DDM1) gene. Here we describe two novel gametophytic maternal-effect mutants, capulet1 (cap1) and capulet2 (cap2). In the cap1 mutant, both embryo and endosperm development are arrested at early stages. In the cap2 mutant, endosperm development is blocked at very early stages, whereas embryos can develop to the early heart stage. The cap mutant phenotypes were not rescued by wild-type pollen nor by pollen from tetraploid plants. Furthermore, removal of silencing barriers from the paternal genome by MET1 a/s transgene expression or by the ddm1 mutation also failed to restore seed development in the cap mutants. Neither cap1 nor cap2 displayed autonomous seed development, in contrast to mea, fis, and fie mutants. In addition, cap2 was epistatic to fis1 in both autonomous endosperm and sexual development. Finally, both cap1 and cap2 mutant endosperms, like wild-type endosperms, expressed the paternally inactive endosperm-specific FIS2 promoter GUS fusion transgene only when the transgene was introduced via the embryo sac, indicating that imprinting was not affected. Our results suggest that the CAP genes represent novel maternal functions supplied by the female gametophyte that are required for embryo and endosperm development.     

Pseudogamous Apomixis in Maize and Sorghum in Diploid-Tetraploid Crosses

Apomictic seed development is a complex process including formation of unreduced embryo sac, parthenogenetic embryo development from the egg cell, and endosperm formation either autonomously, or due to fertilization of polar nuclei by the sperm (under pseudogamous form of apomixis). In the latter case, an obstacle to the normal endosperm development is disturbance of maternal (m) -to-paternal (p) genomic ratio 2m: 1p that occurs in the cases of pollination of unreduced embryo sac with haploid sperms. Usage of tetraploid pollinators can overcome this problem because in such crosses maternal-to-paternal genomic ratio is 4m: 2p that provides formation of kernels with plump endosperm. Using tetraploid lines as pollen parents we observed formation of plump kernels on the ears and panicles of diploid maize and sorghum accessions. These kernels had hybrid endosperm and diploid maternaltype embryo or hybrid embryo with different ploidy level (2n, 3n, 4n). The frequencies of plump kernels on the ear ranged from 0.2-0.3% to 5.7-6.2% counting from the number of ovaries. Maternal-type plants were found in two maize lines, their frequency varying from 10.7 to 37.5% of the progeny plants. In CMS-lines of sorghum pollinated with tetraploid sorghum accessions, the frequency of plump kernels ranged from 0.6 to 14.0% counting from the number of ovaries; the frequency of maternal-type plants varied from 33.0 up to 96.1%. The hybrid nature of endosperm of the kernels that gave rise to maternal-type plants has been proved by marker gene expression and by SDS-electrophoresis of endosperm proteins. These data testify to variable modes of seed formation under diploid × tetraploid crosses in maize and sorghum both by amphi- and by apomixis. Therefore, usage of tetraploid pollinators might be a promising approach for isolation of apomixis in maize and sorghum accessions.     

The dynamic gene expression from different genetic systems for protein and lysine contents of indica rice

The dynamic expression of genes for protein and lysine contents of rice grain under different environments was carried out with time-dependent measures by using the developmental genetic models for quantitative traits of triploid endosperm in cereal crops. The results showed that the genetic effects, especially genotype × environment (GE) interaction effects from the genes expression of different genetic systems including triploid endosperm, cytoplasm and diploid maternal plant were important for the performance of both nutrient quality traits at all developmental times/stages of rice grain. The conditional genetic variance analysis found that the activation of quantitative genes especially from endosperm and maternal plant genetic systems for protein and lysine contents was gradually carried through the developmental process of rice grain. The net genetic effects showed that the new expression of quantitative genes for protein and lysine contents was more active at late filling stage (15–21 days after flowering) and maturity stage (22–28 days) of rice grain. Also the sequential expression of cytoplasmic genes cannot be ignorable for the development of nutrient quality traits. The phenomena that some genes could continuously express for several developmental stages or the genes expression could be interrupted among developmental stages of rice grain was detected especially for net endosperm additive main effects or maternal additive main effects. The differences of genetic relationships from different genetic systems were found for protein and lysine contents among developmental times of rice grain.     

Increased Maternal Genome Dosage Bypasses the Requirement of the FIS Polycomb Repressive Complex 2 in Arabidopsis Seed Development

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.