Endosperm cellularization defines an important developmental transition for embryo development

The endosperm is a terminal seed tissue that is destined to support embryo development. In most angiosperms, the endosperm develops initially as a syncytium to facilitate rapid seed growth. The transition from the syncytial to the cellularized state occurs at a defined time point during seed development. Manipulating the timing of endosperm cellularization through interploidy crosses negatively impacts on embryo growth, suggesting that endosperm cellularization is a critical step during seed development. In this study, we show that failure of endosperm cellularization in fertilization independent seed 2 (fis2) and endosperm defective 1 (ede1) Arabidopsis mutants correlates with impaired embryo development. Restoration of endosperm cellularization in fis2 seeds by reducing expression of the MADS-box gene AGAMOUS-LIKE 62 (AGL62) promotes embryo development, strongly supporting an essential role of endosperm cellularization for viable seed formation. Endosperm cellularization failure in fis2 seeds correlates with increased hexose levels, suggesting that arrest of embryo development is a consequence of failed nutrient translocation to the developing embryo. Finally, we demonstrate that AGL62 is a direct target gene of FIS Polycomb group repressive complex 2 (PRC2), establishing the molecular basis for FIS PRC2-mediated endosperm cellularization.     

Endosperm development in the Araceae (Alismatales) and evolution of developmental modes in monocots

The Araceae, a basal-most family of Alismatales that basally diverged subsequent to Acorales in monocot phylogeny, are known to have diverse modes of endosperm development: nuclear, helobial, and cellular. However, the occurrence of nuclear and helobial endosperm development has long been debated. Here, we report a (re-)investigation of endosperm development in Lysichiton, Orontium, and Symplocarpus of the Orontioideae (a basal Araceae), in which nuclear endosperm development was recorded more than 100 years ago. The results show that all three genera exhibit a cellular, rather than nuclear, endosperm development and suggest that the helobial endosperm development reported as an “unmistakable record” from Ariopsis is likely cellular. Thus the Araceae are very likely characterized by cellular endosperm development alone. An extensive comparison with other monocots in light of phylogenetic relationships demonstrates that a plesiomorphic cellular endosperm development is restricted to the three basal monocot orders Acorales, Alismatales, and Petrosaviales, in which evolutionary changes from cellular to nuclear endosperm development occurred twice as major events, once within Alismatales and once as a synapomorphy of the eight remaining monocot orders, including Dioscoreales, Liliales, Asparagales, and Poales, and that helobial endosperm development, which is known for many monocot families, evolved as homoplasy throughout the monocots.     

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。     

Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals

Although maize endosperm undergoes programmed cell death during its development, it is not known whether this developmental feature is common to cereals or whether it arose inadvertently from the selection process that resulted in the enlarged endosperm of modern maize. Examination of wheat endosperm during its development revealed that this tissue undergoes a programmed cell death that shares features with the maize program but differs in some aspects of its execution. Cell death initiated and progressed stochastically in wheat endosperm in contrast to maize where cell death initiates within the upper central endosperm and expands outward. After a peak of ethylene production during early development, wheat endosperm DNA underwent internucleosomal fragmentation that was detectable from mid to late development. The developmental onset and progression of DNA degradation was regulated by the level of ethylene production and perception. These observations suggest that programmed cell death of the endosperm and regulation of this program by ethylene is not unique to maize but that differences in the execution of the program appear to exist among cereals.     

The Development of Embryo and Endosperm of Nelumbo nucifera Gaertn

The development of the embryo and endosperm of Nelumbo nucifera Gaertn can be summarized as follows: 1. Embryogenesis of N. nucifera belongs to Solanad type; the 1st mitotic division of the zygote takes place later than that of the primary endosperm nucleus. 2. The development of endosperm basically conforms to the Helobial endosperm. After fertilization, the primary endosperm nucleus divides first transversely. This division results in the formation of two cells. The wall of this division is a little oblique to the longitudinal axis of the embryo sac. In accordance with the character of the endospermic development, it can be divided into, three stages: (1) two-celled endosperm stage, (2) multicellular endosperm stage, and (3) the stage of the endospermic nutrition being absorbed and cells atrophy. The developments of the embryo and endosperm are well correlated. This relation is relatively stable. 3. The cotyledons of the mature embryo are comparatively developed, but the radicle is extremely reduced. 4. As the seed is ripening, a thin membrane remains outside the plumule, which is the remainder of the endosperm. Therefore, the seed of N. nucifera is exalbuminous.     

Endosperm differentiation in barley wild-type and sex mutants

The cereal endosperm is a storage organ consisting of the central starchy endosperm surrounded by the aleurone layer. In barley, endosperm development is subdivisible into four main stages, i.e. the syncytial (I), the cellularization (II), the differentiation (III) and the maturation stage (IV). During stage I, a multinucleate syncytium is formed, which in stage II develops into the undifferentiated cellular endosperm. During stage III the cells of the endosperm differentiate into two types of aleurone cells (peripheral and modified) and three different starchy endosperm cell types (irregular, prismatic and subaleurone). To elucidate the ontogenetic relationship between the endosperm tissues, the phenotypes of sex (shrunken endosperm mutants expressing xenia) mutant endosperms were studied. These mutants can be classified into two groups, i.e. those in which development is arrested at one of the four wild-type stages described above, and those with abnormal development with new organizational patterns in the endosperm or with novel cell types. Based on these studies, it is suggested that the two endosperm halves represent cell lines derived from the two daughter nuclei of the primary endosperm nucleus, and that the prismatic starchy endosperm cells arise from a peripheral endosperm meristematic activity during stage III. Finally, a model for the main molecular events underlying the morphogenetic processes is discussed.     

Positional cues specify and maintain aleurone cell fate in maize endosperm development

A genetic analysis of maize aleurone development was conducted. Cell lineage was examined by simultaneously marking cells with C1 for anthocyanin pigmentation in the aleurone and wx1 for amylose synthesis in the starchy endosperm. The aleurone and starchy endosperm share a common lineage throughout development indicating that positional cues specify aleurone fate. Mutants in dek1 block aleurone formation at an early stage and cause peripheral endosperm cells to develop as starchy endosperm. Revertant sectors of a transposon-induced dek1 allele showed that peripheral endosperm cells remain competent to differentiate as aleurone cells until late in development. Ds-induced chromosome breakage was used to generate Dek1 loss-of-function sectors. Events occurring until late development caused aleurone cells to switch fate to starchy endosperm indicating that cell fate is not fixed. Thus, positional cues are required to specify and maintain aleurone fate and Dek1 function is required to respond to these cues. An analysis of additional mutants that disrupt aleurone differentiation suggests a hierarchy of gene functions to specify aleurone cell fate and then control aleurone differentiation. These mutants disrupt aleurone differentiation in reproducible patterns suggesting a relationship to endosperm pattern formation.     

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.     

Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis

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.     

The ethylene biosynthetic and perception machinery is differentially expressed during endosperm and embryo development in maize

The maize endosperm undergoes programmed cell death late in its development so that, with the exception of the aleurone layer, the tissue is dead by the time the kernel matures. Although ethylene is known to regulate the onset of endosperm cell death, the temporal and spatial control of the ethylene biosynthetic and perception machinery during maize endosperm development has not been examined. In this study, we report the isolation of the maize gene families for ACC synthase, ACC oxidase, the ethylene receptor, and EIN2 and EIL, which act downstream of the receptor. We show that ACC oxidase is expressed primarily in the endosperm, and only at low levels in the developing embryo late in its development. ACC synthase is expressed throughout endosperm development but, in contrast to ACC oxidase, it is transiently expressed to a significantly higher level in the developing embryo at a time that corresponds with the onset of endosperm cell death. Only two ethylene receptor gene families were identified in maize, in contrast to the five types previously identified in Arabidopsis. Members of both ethylene receptor families were expressed to substantially higher levels in the developing embryo than in the endosperm, as were members of the EIN2 and EIL gene families. These results suggest that the endosperm and embryo both contribute to the synthesis of ethylene, and they provide a basis for understanding why the developing endosperm is especially sensitive to ethylene-induced cell death while the embryo is protected.Electronic Supplementary Material Supplementary material is available in the online version of this article at Communicated by G. Jürgens     

Rice caryopsis development Ⅱ: Dynamic changes in the endosperm

The rice endosperm plays crucial roles in nourishing the embryo during embryogenesis and seed germination. Although previous studies have provided the general information about rice endosperm, a systematic investigation throughout the entire endosperm developmental process is still lacking. In this study, we examined in detail rice endosperm development on a daily basis throughout the 30‐day period of post‐fertilization development. We observed that coenocytic nuclear division occurred in the first 2 days after pollination (DAP), cellularization occurred between 3 and 5 DAP, differentiation of the aleurone and starchy endosperm occurred between 6 and 9 DAP, and accumulation of storage products occurred concurrently with the aleurone/starchy endosperm differentiation from 6 DAP onwards and was accomplished by 21 DAP. Changes in cytoplasmic membrane permeability, possibly caused by programmed cell death, were observed in the central region of the starchy endosperm at 8 DAP, and expanded to the whole starchy endosperm at 21 DAP when the aleurone is the only living component in the endosperm. Further, we observed that a distinct multi‐layered dorsal aleurone formed near the dorsal vascular bundle, while the single‐ or occasionally two‐cell layered aleurone was located in the lateral and ventral positions of endosperm. Our results provide in detail the dynamic changes in mitotic divisions, cellularization, cell differentiation, storage product accumulation, and programmed cell death that occur during rice endosperm development.     

Degree of pectin methyl esterification in endosperm cell walls is involved in embryo bending in Arabidopsis thaliana

The endosperm is a transitory structure involved in proper embryo elongation. The cell walls of mature seed endosperm are generally composed of a uniform distribution of cellulose, unesterified homogalacturonans, and arabinans. Recent studies suggest that changes in cell wall properties during endosperm development could be related to embryo growth. The degree of methyl esterification of homogalacturonans may be involved in this endosperm tissue remodelling. The relevance of the degree of homogalacturonan methyl esterification during seed development was determined by immunohistochemical analyses using a panel of probes with specificity for homogalaturonans with different degrees of methyl esterification. Low-esterified and un-esterified homogalacturonans were abundant in endosperm cells during embryo bending and were also detected in mature embryos. BIDXII (BDX) could be involved in seed development, because bdx-1 mutants had misshapen embryos. The methyl esterification pattern described for WT seeds was different during bdx-1 seed development; un-esterified homogalacturonans were scarcely present in the cell walls of endosperm in bending embryos and mature seeds. Our results suggested that the degree of methyl esterification of homogalacturonans in the endosperm cell wall may be involved in proper embryo development.     

水稻淀粉胚乳程序性细胞死亡中的去核化

对水稻品种中籼8836淀粉胚乳细胞的去核化发育阶段的细胞超微结构变化和同期籽粒灌浆速率及相关酶活性的动态进行了观察和分析。开花受精后约在第3天胚乳完成细胞化,花后第5天少数淀粉胚乳细胞启动去核发育过程。核消亡是淀粉胚乳细胞程序性细胞死亡(PCD)的第一步。同一籽粒淀粉胚乳细胞的去核进程是不同步的。花后第13天所有淀粉胚乳细胞都已完成去核过程。在去核过程中,胚乳核的形态变化特征既有动植物PCD的共性又有其特殊性。伴随核降解过程,一部分线粒体解体,表明去核化与线粒体解体有一定联系。在去核化发育阶段,与PCD有关的酶类,如超氧化物歧化酶(SOD)、过氧化氢酶(CAT)活性非常高;与淀粉合成有关的酶类,如ADPG焦磷酸化酶、可溶性淀粉合成酶(SSS酶)、淀粉分支酶(或Q酶)也表现出很高的活性。去核化发育阶段籽粒灌浆速率最高,籽粒增重亦最快。淀粉胚乳细胞去核之后,细胞并未立即死亡,这些无核的细胞仍维持正常有序的代谢活动,继续进行淀粉和贮藏蛋白的合成与积累,但上述酶类的活性明显降低,灌浆速率也明显趋缓。淀粉胚乳细胞最终被贮藏物质充满时成为死细胞,完成其程序性死亡过程。Evan‘s blue染色鉴定表明淀粉胚乳细胞死亡不同步,细胞死亡在淀粉胚乳组织中是随机发生的。     

The Developments of Embryo and Endosperm of Zizyphus jujuba Mill

The development of the embryo of Zizyphus jujuba Mill. conforms to the Asterad type. The transverse division of the zygote results in the formation of the terminal and basal cells. The basal cell of the two-celled proembryo divides transversely first and contributes to the suspensor and a minor part of the embryo proper in further development. The terminal cell first divides vertically and the divisions in various ways contribute to almost all parts of the embryo proper. The endosperm development is of the nuclear type. Three stages may be divided as follows: the free nuclear stage, the wall formation stage and the stage in which the disorganization of the endosperm cells takes place rapidly. The developments of the embryo and endosperm are well correlated. Thus the morphological development of the embryo may be used as an indicator to tell the development stage of the endosperm. The adequate stage for endosperm culture is in the wall formation stage.     

Invertase Activity in Normal and Mutant Maize Endosperms during Development

A bound invertase and two soluble invertases are found in the developing endosperm of maize (Zea mays L.). The two soluble invertases can be separated on diethylaminoethyl-cellulose and Sephadex columns and distinguished by their kinetic constants. One soluble invertase, invertase I, is present from the 10- to 28-day stages of endosperm development with maximal activity per normal endosperm at the 12-day stage. In two endosperm mutant lines, shrunken-1 and shrunken-2, there is a second increase in invertase I activity later in development which could be a secondary effect caused by the abnormal metabolism in these lines. Another soluble invertase, invertase II, is present in the embryo upon germination and is also found in the very young developing endosperm (6-day stage). The third form of invertase, bound invertase, is present in the endosperm by the 6-day stage, and its activity remains approximately constant during development.     

水稻淀粉胚乳程序性细胞死亡中的去核化

对水稻品种中籼8836淀粉胚乳细胞的去核化发育阶段的细胞超微结构变化和同期籽粒灌浆速率及相关酶活性的动态进行了观察和分析。开花受精后约在第3天胚乳完成细胞化,花后第5天少数淀粉胚乳细胞启动去核发育过程。核消亡是淀粉胚乳细胞程序性细胞死亡(PCD)的第一步。同一籽粒淀粉胚乳细胞的去核进程是不同步的。花后第13天所有淀粉胚乳细胞都已完成去核过程。在去核过程中,胚乳核的形态变化特征既有动植物PCD的共性又有其特殊性。伴随核降解过程,一部分线粒体解体,表明去核化与线粒体解体有一定联系。在去核化发育阶段,与PCD有关的酶类,如超氧化物歧化酶(SOD)过氧化氢酶(CAT)活性非常高;与淀粉合成有关的酶类,如ADPG焦磷酸化酶、可溶性淀粉合成酶(SSS酶)、淀粉分支酶(或Q酶)也表现出很高的活性。去核化发育阶段籽粒灌浆速率最高,籽粒增重亦最快。淀粉胚乳细胞去核之后,细胞并未立即死亡,这些无核的细胞仍维持正常有序的代谢活动,继续进行淀粉和贮藏蛋白的合成与积累,但上述酶类的活性明显降低,灌浆速率也明显趋缓。淀粉胚乳细胞最终被贮藏物质充满时成为死细胞,完成其程序性死亡过程。Evan’s blue染色鉴定表明淀粉胚乳细胞死亡不同步,细胞死亡在淀粉胚乳组织中是随机发生的。