These peptides are highly expressed in the central cells and secreted to the apoplast and even to the intercellular space of the integuments Li et al.
It is possible that some protein factors required for the later endosperm development have been activated in advance in the central cell before fertilization. Three central cells-expressed cysteine-rich peptides, ESF1s, were identified to be required for the development of embryo suspensor Costa et al.
These ESF1s are also down-regulated in ccg ovules Li et al. It is still a mystery whether the numerous secreted peptides down-regulated in ccg have roles in cell-cell communication between the central cell and its neighbors or intercellular signaling between the fertilization products.
This type of regulation has been reported, for example, in maize the egg cell-expressed secreted peptide ZmEAL1 regulates the cell fate of the antipodal cells Krohn et al. In addition, one clue for the role of exosome signaling is the detection of expression of tetraspanin family members in the embryo sac Boavida et al.
However, the function of these tetraspanins in embryo sac is still unknown as the mutants exhibit no phenotype. Double fertilization entails fusion of sperm cells with the two dimorphic female gametes, the egg and the central cell. It is not known whether the central cell employs its own way to activate the sperm or takes advantage of the egg-secreted EC1. The putative receptor for gamete adhesion, GEX2, contains an extracellular domain and is required for the sperm fusion with both female gametes Mori et al.
This implies the presence of similar or the same ligand on the surface of egg and central cell. Live imaging studies showed a lagged sperm fusion with the central cell than the egg cell, indicating that differences between the two fusion events may exist Denninger et al. Study with the polyspermic tetraspore tes mutant has suggested that polyspermy block exists in egg, but not in central cell Scott et al. Other reports suggest that the egg cell can also fuse with two sperms to form triploid embryo with the central cell fuses with one sperm cell Grossniklaus, ; Mao et al.
Another distinction between the central cell and the egg cell is that plasma membrane fusion with sperm can trigger central cell mitotic division, suggesting signaling link between plasmogamy and activation of the nuclear division Aw et al. The evolutionary origin of the double fertilization that is characterized by the emergence of the central cell is still mysterious, since the double fertilization phenomenon was discovered in the late s.
Based on the diversity of embryo sac, different hypothesis were raised to explain the evolution of different ploidy of endosperms and the adaption significance, i. The developmental evolution of the embryo sac is tightly related to the endosperm genetics and the variation of endosperms will gives rise to phenotype variations that are subject to natural selection.
Among the extant flowering plants, seven types of endosperms exist. But our understanding on its evolutionary trajectory, adaption and even molecular modulation is still very limited. Genetic evidence in model plant Arabidopsis has now provided new clues on the central cell evolution. AGL80 loss-of-function mutant was recently found to be featured by the failed fusion with sperm cell and switch of marker genes to the accessory cells.
The study of AGL80 suggests a conserved mechanism of central cell determination in Brassicaceae by the EAR-motif mediated gene repression mechanism Zhang et al. This indicates multiple divergence of central cell specification during evolution and more primitive mechanisms are to be found. It would be interesting to investigate whether AGL80 homologs in other species are also involved in central cell specification or function even if EAR motif is not present.
Although the EAR motif is only conserved in Brassicaceae, whether other transcription repression mechanism executed by AGL80 homologs or other transcription factors in monocot and other taxa are still to be unveiled. From this study, it appears that the determination of central cell fate is not conserved as expected, instead it has originated more than one time. The evolutionary conservation of AGL80 in the central cell in the Brassicaceae family may reflect fast evolution of the central cell that is wired for postzygotic reproductive isolation.
The incompatibility of two species in the hybrid endosperm constitutes one of the major postzygotic isolation. In gymnosperms the non-flowering seed plants , like Cycads, Gnetales, and Gingko, the surrounding gametohpytic cells take the role of endosperm function to nourish the embryo.
The female gametophyte undergoes numerous rounds of mitosis to produce a coenocytic cell with approximately thousands of free nuclei Figure 2 ; Soma, At maturation, the egg-containing archegonia are structurally alike that of the moss Figure 2 , and the pollen grain contains two sperm cells at maturity and only one sperm cell would transmit the genome to the progeny.
It was suggested that the gametophytic cells surrounding the archegonia function analogously to the nourishing endosperm in angiosperms. These multicellular gametophytes store reserves before fertilization to support the embryogenesis after the egg cell fertilization. With the emergence of the central cell, the embryo-nourishing role shifts from the gametophyte to the fertilized central cell, the endosperm.
It confers the flowering plants several benefits and at the same time the fertilization process become more complex.
The fertilization-dependent nutrients allocation to the endosperm saves energy as embryogenesis is not always a hundred percent successful. On the other hand, endosperm, containing the genome of both parents, takes a major part in the post-zygotic hybrid barrier Lafon-Placette et al. Figure 2. The development of Ginkgo archegonium. This is a schematic diagram of the major stages of female gametophyte development of Ginkgo and the mature female gametophyte of Cycads and Gnetales.
The schematic diagram was drawn according to Dhote, Gupta and Bijoy G www. The female gametogenesis of different gymnosperms is quite similar. The development of Ginkgo female gametophyte is described as a representative. In brief, it develops from the large functional megaspore, the remaining spore after meiosis. The nucleus of the megaspore divides mitotically to generate thousands of free nuclei within a cell with a large central vacuole.
Thereafter, the cellularization takes place in a centripetal fashion and finally the vacuole is obliterated. The cellularized gametophyte is usually called endosperm, because it undertakes the role of embryo-nourishing like the fertilization-generated endosperm in flowering plants.
Then the archegonium formation initiates. Two to four cells differentiate into the archegonial initials, which then divide periclinally to form an outer small primary neck initial and a large central cell. The primary neck initials divide vertically twice resulting in four neck cells. The central cell divide asymmetrically to generate the upper ventral canal cells which disappears quickly and a large egg cell. With the expansion of the egg cell, the neck cells are pushed outside and finally degenerate to form the opening for the sperm entry.
In Cycads and Gnetales, the ventral canal nucleus and the egg nucleus are within the same cell without cell wall separation. In Gnetales, a file of neck cells are formed thus generating a longer canal for sperm entry. The evolution of the endosperm in flowering plants has been discussed for years Berger, ; Friedman et al.
One scenario of the origin of the endosperm is a sexualized gametophytic cell and fertilization triggers the mitotic progression of the nourishing tissue.
This scenario is supported by the similar pattern between the endosperm development of angiosperms and the female gametophyte of gymnosperms. In addition, the fertilization-dependent endosperm development gives rise to the possibility of parental regulation. Another scenario of endosperm origination is that an altruistic embryo finally takes the role of embryo nourishing. At the present time, however, there is still no evidence to show the evolutionary origin of the central cell, as no transitional or primordial female gametophyte structure has been found.
Even in the most ancient flowering plant, Amborella, the four-cell-typed female gametophyte has already formed. Two recent studies suggested that the signaling component of cytokine, CKI1 in Arabidopsis regulate the central cell fate, and the orthologous CKI1 gene in Ginkgo, is expressed in archegonia and the precursor and surrounding tissues Yuan et al.
This study implies that at least some factors involved in female gametophyte development have been employed in the gymnosperm. Although no fertilization-based endosperm was generated in gymnosperms, some comparison has been made between gymnosperms Gnetales and angiosperms Friedman, In Gnetales, the binucleate sperm is carried by the pollen and released into the binucleate egg cell.
It was reported that in Gnetales, the egg cell contains two nuclei, the centrally placed one as the egg nucleus, another one is the ventral canal nucleus Figure 2. In Welwitschia , only the egg nucleus is fertilized since the second sperm nuclei does not enter the egg cell and degenerates Friedman, In Gnetum and Ephedra , the two sister nuclei of the egg cell fused with the two sister sperm nuclei, respectively Friedman, However, the coenocytic female gametophyte matures upon the pollen tube penetration and the simultaneous fertilization of the two haploid female nuclei determines the following fate of the fertilization products.
But this lack of egg differentiation is unique in Gnetales and Welwitschia Friedman, After fertilization, the conenocytic tissue undergoes cellularization and both fertilization products initiate embryogenesis and only one matures with the nourishment of the surrounding gametophytic tissues.
Despite the developmental similarities of the mitotic sister sperm nuclei within the same pollen and sister female gametophytic nuclei, no definitive homology of the double fertilization events between Gnetales and flowering plants has been drawn.
Another remaining mystery is the single fruitful fertilization at the expanse of waste of the other sperm. The emergence of two sperms likely have driven and provided the prerequisites for the origination of the second fertilization-competent cell and double fertilization.
In the absence of fossil record of species with central cell ancestor, the elucidation of the evolutionary ontogeny of this specialized cell is difficult. Genetic dissection and molecular evolution study of key genes especially that with conserved roles in central cell specification would be helpful, which benefit from the release of more and more whole genome sequences of different plant taxa. High through-put transcriptome sequencing of small amount of samples would also promote the unraveling of the genetic hierarchy and evolution of female gametophyte, although the functional study would be challenging due to the difficulty in genetic transformation of these species.
Nowadays, we have a more comprehensive understanding of the cell specification and intercellular signaling of central cell in molecular and evolutionary aspects. The active involvement of central cell in diverse aspect of fertilization points to an emerging importance of this non-heritable female gamete.
Experimental evidence is still limited for the full understanding of this mysterious cell. Although with the studies in the past two decades, the identification of the key components and their functional connectivity remains the major hurdle in understanding of central cell function and evolution.
The central cell is enriched in secreted peptides, but most of them have yet to be functionally characterized as the conventional T-DNA and gene knock-down approaches are powerless in these highly redundant and sequence-diverged gene families. In addition, the relaxation of the gene silencing machinery activates the transposable elements and a large number of genes that would make the reverse genetic study laborious.
Both authors contributed to the article and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Armenta-Medina, A. Epigenetic control of cell specification during female gametogenesis. Plant Reprod. Ashapkin, V. Epigenetic regulation of plant gametophyte development. Aw, S. Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis.
Development , — Baroux, C. Epigenetic regulation and reprogramming during gamete formation in plants. Evolutionary origins of the endosperm in flowering plants. Genome Biol. Google Scholar. Bemer, M. Plant Physiol. Plant Cell 20, — Berger, F. Endosperm: the crossroad of seed development. Plant Biol. Boavida, L.
Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo- and heterodimers when expressed in yeast. Cai, Q. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science , — Chen, Y. The central cell plays a critical role in pollen tube guidance in Arabidopsis.
Plant Cell 19, — Cheng, C. Cytokinin-dependent specification of the functional megaspore in the Arabidopsis female gametophyte. Plant J. Chevalier, E. Cell-cell communication and signalling pathways within the ovule: from its inception to fertilization.
New Phytol. Christensen, C. Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 14, — Megagametogenesis in Arabidopsis wild type and the Gf mutant. Costa, L. Central cell-derived peptides regulate early embryo patterning in flowering plants.
Deng, Y. Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22, — Denninger, P. Male-female communication triggers calcium signatures during fertilization in Arabidopsis. El-Kasmi, F. Erbasol Serbes, I. Further mitosis of the microspore produces two nuclei: the generative nucleus and the tube nucleus.
Upon maturity, the male gametophyte pollen is released from the male cones and is carried by the wind to land on female cones. The female cone also has a central axis on which bracts known as megasporophylls are present.
In the female cone, megaspore mother cells are present in the megasporangium. The megaspore mother cell divides by meiosis to produce four haploid megaspores. One of the megaspores divides to form the multicellular female gametophyte, while the others divide to form the rest of the structure.
The female gametophyte is contained within a structure called the archegonium. Upon landing on the female cone, the tube cell of the pollen forms the pollen tube, through which the generative cell migrates towards the female gametophyte through the micropyle.
It takes approximately one year for the pollen tube to grow and migrate towards the female gametophyte. The male gametophyte containing the generative cell splits into two sperm nuclei, one of which fuses with the egg, while the other degenerates. After fertilization of the egg, the diploid zygote is formed, which divides by mitosis to form the embryo. The scales of the cones are closed during development of the seed. The seed is covered by a seed coat, which is derived from the female sporophyte.
Seed development takes another one to two years. Once the seed is ready to be dispersed, the bracts of the female cones open to allow the dispersal of seed; no fruit formation takes place because gymnosperm seeds have no covering. Double fertilization is a key event in the lifecycle of angiosperms, but is completely absent in gymnosperms.
The male and female gametophyte structures are present on separate male and female cones in gymnosperms, whereas in angiosperms, they are a part of the flower.
Lastly, wind plays an important role in pollination in gymnosperms because pollen is blown by the wind to land on the female cones. Although many angiosperms are also wind-pollinated, animal pollination is more common. The flower contains the reproductive structures of a plant. All complete flowers contain four whorls: the calyx, corolla, androecium, and gynoecium. The stamens are made up of anthers, in which pollen grains are produced, and a supportive strand called the filament.
The pollen contains two cells— a generative cell and a tube cell—and is covered by two layers called the intine and the exine. The carpels, which are the female reproductive structures, consist of the stigma, style, and ovary.
The female gametophyte is formed from mitotic divisions of the megaspore, forming an eight-nuclei ovule sac. This is covered by a layer known as the integument.
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