Cell-Fate Switch of Synergid to Egg Cell in Arabidopsis eostre Mutant Embryo Sacs Arises from Misexpression of the BEL1-Like Homeodomain Gene BLH1

Following fertilization in flowering plants (angiosperms), egg and sperm cells unite to form the zygote, which generates an entire new organism through a process called embryogenesis. In this review, we provide a comparative perspective on early zygotic embryogenesis in flowering plants by using the Poaceae maize and rice as monocot grass and crop models as well as Arabidopsis as a eudicot model of the Brassicaceae family. Beginning with the activation of the egg cell, we summarize and discuss the process of maternal-to-zygotic transition in plants, also taking recent work on parthenogenesis and haploid induction into consideration. Aspects like imprinting, which is mainly associated with endosperm development and somatic embryogenesis, are not considered. Controversial findings about the timing of zygotic genome activation as well as maternal versus paternal contribution to zygote and early embryo development are highlighted. The establishment of zygotic polarity, asymmetric division, and apical and basal cell lineages represents another chapter in which we also examine and compare the role of major signaling pathways, cell fate genes, and hormones in early embryogenesis. Except for the model Arabidopsis, little is known about embryo patterning and the establishment of the basic body plan in angiosperms. Using available in situ hybridization, RNA-sequencing, and marker data, we try to compare how and when stem cell niches are established. Finally, evolutionary aspects of plant embryo development are discussed. Expected final online publication date for the Annual Review of Plant Biology, Volume 72 is May 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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Recent advances in understanding female gametophyte development

F1000Research ◽

10.12688/f1000research.14508.1 ◽

2018 ◽

Vol 7 ◽

pp. 804 ◽

Cited By ~ 6

Author(s):

Debra J Skinner ◽

Venkatesan Sundaresan

Keyword(s):

Cell Fate ◽

Female Gametophyte ◽

Cell Communication ◽

Embryo Sac ◽

Cell Types ◽

Egg Cell ◽

Male Gametes ◽

Reproductive Unit ◽

Genetic Mechanisms ◽

Female Gametophyte Development

The haploid female gametophyte (embryo sac) is an essential reproductive unit of flowering plants, usually comprising four specialized cell types, including the female gametes (egg cell and central cell). The differentiation of these cells relies on spatial signals which pattern the gametophyte along a proximal-distal axis, but the molecular and genetic mechanisms by which cell identities are determined in the embryo sac have long been a mystery. Recent identification of key genes for cell fate specification and their relationship to hormonal signaling pathways that act on positional cues has provided new insights into these processes. A model for differentiation can be devised with egg cell fate as a default state of the female gametophyte and with other cell types specified by the action of spatially regulated factors. Cell-to-cell communication within the gametophyte is also important for maintaining cell identity as well as facilitating fertilization of the female gametes by the male gametes (sperm cells).

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Egg Cell Signaling by the Secreted Peptide ZmEAL1 Controls Antipodal Cell Fate

Developmental Cell ◽

10.1016/j.devcel.2012.05.018 ◽

2012 ◽

Vol 23 (1) ◽

pp. 219-225 ◽

Cited By ~ 32

Author(s):

Nadia Graciele Krohn ◽

Andreas Lausser ◽

Martina Juranić ◽

Thomas Dresselhaus

Keyword(s):

Cell Signaling ◽

Cell Fate ◽

Antipodal Cell ◽

Egg Cell

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Plant egg cell fate determination depends on its exact position in female gametophyte

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2017488118 ◽

2021 ◽

Vol 118 (8) ◽

pp. e2017488118 ◽

Cited By ~ 1

Author(s):

Yang Sun ◽

Xiu Wang ◽

Lin Pan ◽

Fei Xie ◽

Bo Dai ◽

...

Keyword(s):

Cell Fate ◽

Sperm Cell ◽

Female Gametophyte ◽

Imaging System ◽

Egg Cell ◽

Cell Identity ◽

Auxin Level ◽

Egg Apparatus

Plant fertilization involves both an egg cell, which fuses with a sperm cell, and synergid cells, which guide pollen tubes for sperm cell delivery. Therefore, egg and synergid cell functional specifications are prerequisites for successful fertilization. However, how the egg and synergid cells, referred to as the “egg apparatus,” derived from one mother cell develop into distinct cell types remains an unanswered question. In this report, we show that the final position of the nuclei in female gametophyte determines the cell fate of the egg apparatus. We established a live imaging system to visualize the dynamics of nuclear positioning and cell identity establishment in the female gametophyte. We observed that free nuclei should migrate to a specific position before egg apparatus specialization. Artificial changing in the nuclear position on disturbance of the actin cytoskeleton, either in vitro or in vivo, could reset the cell fate of the egg apparatus. We also found that nuclei of the same origin moved to different positions and then showed different cell identities, whereas nuclei of different origins moved to the same position showed the same cell identity, indicating that the final positions of the nuclei, rather than specific nucleus lineage, play critical roles in the egg apparatus specification. Furthermore, the active auxin level was higher in the egg cell than in synergid cells. Auxin transport inhibitor could decrease the auxin level in egg cells and impair egg cell identity, suggesting that directional and accurate auxin distribution likely acts as a positional cue for egg apparatus specialization.

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Embryo development in Carica papaya Linn

10.1101/2021.03.11.434975 ◽

2021 ◽

Author(s):

Miguel Acevedo-Benavides ◽

Pablo Bolaños-Villegas

Keyword(s):

Cell Fate ◽

Female Gametophyte ◽

Carica Papaya ◽

Genetic Regulation ◽

Draft Genome ◽

Embryo Sac ◽

Egg Cell ◽

Parental Line ◽

Before And After ◽

Autonomous Development

ABSTRACTPapaya (Carica papaya Linn.) is a tropical plant whose draft genome has been sequenced. Papaya produces large fruits rich in vitamins A and C and is an important cash crop in developing countries. Nonetheless, little is known about how the female gametophyte develops, how it is fertilized and how it develops into a mature seed containing an embryo and an endosperm. The Papaya female gametophyte displays a Polygonum-type architecture consisting of two synergid cells, an egg cell, a central cell, and three antipodal cells. Reports are available of the presumed existence of varieties in which cross fertilization is bypassed and autonomous development of embryos occurs (e.g., apomixis). In this study, we analyzed the development of female gametophytes in a commercial Hawaiian parental line and in the presumed apomictic Costa Rican line L1. Samples were collected before and after anthesis to compare the overall structure, size and transcriptional patterns of several genes that may be involved in egg and endosperm cell fate and proliferation. These genes were the putative papaya homologs of ARGONAUTE9 (AGO9), MEDEA (MEA), RETINOBLASTOMA RELATED-1 (RBR1), and SLOW WALKER-1 (SWA1). Our results suggest that its feasible to identify the contour of structural features of Polygonum-type development, and that in bagged female flowers of line L1 we might have observed autonomous development of embryo-like structures. Possible downregulation of papaya homologs for AGO9, MEA, RBR1 and SWA1 was observed in embryo sacs from line L1 before and after anthesis, which may suggest a tentative link between suspected apomixis and transcriptional downregulation of genes for RNA-directed DNA methylation, histone remodelers, and rRNA processing. Most notably, the large size of the papaya embryo sac suggests that it could be a cytological alternative to Arabidopsis thaliana for study. Significant variation in embryo sac size was observed between the varieties under study, suggesting wide differences in the genetic regulation of anatomical features.

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Transcriptional repression specifies the central cell for double fertilization

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1909465117 ◽

2020 ◽

Vol 117 (11) ◽

pp. 6231-6236 ◽

Cited By ~ 1

Author(s):

Meng-Xia Zhang ◽

Shan-Shan Zhu ◽

Yong-Chao Xu ◽

Ya-Long Guo ◽

Wei-Cai Yang ◽

...

Keyword(s):

Cell Fate ◽

Transcriptional Repression ◽

Female Gametophyte ◽

Embryo Sac ◽

Central Cell ◽

Egg Cell ◽

Accessory Cell ◽

Double Fertilization ◽

Genetic Rescue ◽

Key Innovation

Double fertilization is a key innovation for the evolutionary success of angiosperms by which the two fertilized female gametes, the egg cell and central cell, generate the embryo and endosperm, respectively. The female gametophyte (embryo sac) enclosed in the sporophyte is derived from a one-celled haploid cell lineage. It undergoes successive events of mitotic divisions, cellularization, and cell specification to give rise to the mature embryo sac, which contains the two female gametes accompanied by two types of accessory cells, namely synergids and antipodals. How the cell fate of the central cell is specified has long been equivocal and is further complicated by the structural diversity of female gametophyte across plant taxa. Here, MADS-box protein AGL80 was verified as a transcriptional repressor that directly suppresses the expression of accessory cell-specific genes to specify the central cell. Further genetic rescue and phylogenetic assay of the AGL80 orthologs revealed a possible conserved mechanism in the Brassicaceae family. Results from this study provide insight into the molecular determination of the second female gamete cell in Brassicaceae.

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Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis

PLoS Biology ◽

10.1371/journal.pbio.3001123 ◽

2021 ◽

Vol 19 (3) ◽

pp. e3001123

Author(s):

Daichi Susaki ◽

Takamasa Suzuki ◽

Daisuke Maruyama ◽

Minako Ueda ◽

Tetsuya Higashiyama ◽

...

Keyword(s):

Gene Expression ◽

Cell Fate ◽

Female Gametophyte ◽

Nuclear Division ◽

Cell Plate ◽

Egg Cell ◽

Specific Gene ◽

Cell Plate Formation ◽

Plate Formation ◽

Female Gametophyte Development

The female gametophytes of angiosperms contain cells with distinct functions, such as those that enable reproduction via pollen tube attraction and fertilization. Although the female gametophyte undergoes unique developmental processes, such as several rounds of nuclear division without cell plate formation and final cellularization, it remains unknown when and how the cell fate is determined during development. Here, we visualized the living dynamics of female gametophyte development and performed transcriptome analysis of individual cell types to assess the cell fate specifications in Arabidopsis thaliana. We recorded time lapses of the nuclear dynamics and cell plate formation from the 1-nucleate stage to the 7-cell stage after cellularization using an in vitro ovule culture system. The movies showed that the nuclear division occurred along the micropylar–chalazal (distal–proximal) axis. During cellularization, the polar nuclei migrated while associating with the forming edge of the cell plate, and then, migrated toward each other to fuse linearly. We also tracked the gene expression dynamics and identified that the expression of MYB98pro::GFP–MYB98, a synergid-specific marker, was initiated just after cellularization in the synergid, egg, and central cells and was then restricted to the synergid cells. This indicated that cell fates are determined immediately after cellularization. Transcriptome analysis of the female gametophyte cells of the wild-type and myb98 mutant revealed that the myb98 synergid cells had egg cell–like gene expression profiles. Although in myb98, egg cell–specific gene expression was properly initiated in the egg cells only after cellularization, but subsequently expressed ectopically in one of the 2 synergid cells. These results, together with the various initiation timings of the egg cell–specific genes, suggest complex regulation of the individual gametophyte cells, such as cellularization-triggered fate initiation, MYB98-dependent fate maintenance, cell morphogenesis, and organelle positioning. Our system of live-cell imaging and cell type–specific gene expression analysis provides insights into the dynamics and mechanisms of cell fate specifications in the development of female gametophytes in plants.

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Dynamics of the cell fate specifications during female gametophyte development in Arabidopsis

10.1101/2020.04.07.023028 ◽

2020 ◽

Cited By ~ 3

Author(s):

Daichi Susaki ◽

Takamasa Suzuki ◽

Daisuke Maruyama ◽

Minako Ueda ◽

Tetsuya Higashiyama ◽

...

Keyword(s):

Gene Expression ◽

Cell Fate ◽

Female Gametophyte ◽

Nuclear Division ◽

Cell Plate ◽

Egg Cell ◽

Specific Gene ◽

Cell Plate Formation ◽

Plate Formation ◽

Female Gametophyte Development

ABSTRACTThe female gametophytes of angiosperms contain cells with distinct functions, such as those that enable reproduction via pollen tube attraction and fertilization. Although the female gametophyte undergoes unique developmental processes, such as several rounds of nuclear division without cell plate formation, and the final cellularization, it remains unknown when and how the cell fate is determined during their development. Here, we visualized the living dynamics of female gametophyte development and performed transcriptome analysis of its individual cell types, to assess the cell fate specifications in Arabidopsis thaliana. We recorded time lapses of the nuclear dynamics and cell plate formation from the one-nucleate stage to the seven-cell stage after cellularization, using the in vitro ovule culture system. The movies showed that the nuclear division occurred along the micropylar–chalazal axis. During cellularization, the polar nuclei migrated while associating with forming edge of the cell plate. Then, each polar nucleus migrated to fuse linearly towards each other. We also tracked the gene expression dynamics and identified that the expression of the MYB98pro∷GFP, a synergid-specific marker, was initiated before cellularization, and then restricted to the synergid cells after cellularization. This indicated that cell fates are determined immediately after cellularization. Transcriptome analysis of the female gametophyte cells of the wild type and myb98 mutant, revealed that the myb98 synergid cells had the egg cell-like gene expression profile. Although in the myb98, the egg cell-specific gene expressions were properly initiated only in the egg cells after cellularization, but subsequently expressed ectopically in one of the two synergid cells. These results, together with the various initiation timings of the egg cell-specific genes suggest the complex regulation of the individual gametophyte cells, such as cellularization-triggered fate initiation, MYB98-dependent fate maintenance, cell morphogenesis, and organelle positioning. Our system of live-cell imaging and cell-type-specific gene expression analysis provides insights into the dynamics and mechanisms of cell fate specifications in the development of female gametophytes in plants.

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Immunogold and immunoblot studies on a cell surface protein found in primary mesenchyme cells and in the cortical secretory vesicles of the sea urchin egg

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100128444 ◽

1987 ◽

Vol 45 ◽

pp. 832-833

Author(s):

G.L. Decker ◽

M.C. Valdizan

Keyword(s):

Cell Surface ◽

Sea Urchin ◽

Surface Protein ◽

Egg Cell ◽

Secretory Vesicles ◽

Cell Surface Protein ◽

Surface Complexes ◽

Mesenchyme Cells ◽

Lowicryl K4m ◽

Primary Mesenchyme Cells

A monoclonal antibody designated MAb 1223 has been used to show that primary mesenchyme cells of the sea urchin embryo express a 130-kDa cell surface protein that may be directly involved in Ca2+ uptake required for growth of skeletal spicules. Other studies from this laboratory have shown that the 1223 antigen, although in relatively low abundance, is also expressed on the cell surfaces of unfertilized eggs and on the majority of blastomeres formed prior to differentiation of the primary mesenchyme cells.We have studied the distribution of 1223 antigen in S. purpuratus eggs and embryos and in isolated egg cell surface complexes that contain the cortical secretory vesicles. Specimens were fixed in 1.0% paraformaldehyde and 1.0% glutaraldehyde and embedded in Lowicryl K4M as previously reported. Colloidal gold (8nm diameter) was prepared by the method of Mulpfordt.

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Centrosome Aurora A gradient ensures single polarity axis in C. elegans embryos

Biochemical Society Transactions ◽

10.1042/bst20200298 ◽

2020 ◽

Vol 48 (3) ◽

pp. 1243-1253 ◽

Cited By ~ 1

Author(s):

Sukriti Kapoor ◽

Sachin Kotak

Keyword(s):

Symmetry Breaking ◽

Cell Fate ◽

Cell Cortex ◽

Axis Formation ◽

Aurora A Kinase ◽

Aurora A ◽

C Elegans ◽

Cell Embryo ◽

Polarity Establishment

Cellular asymmetries are vital for generating cell fate diversity during development and in stem cells. In the newly fertilized Caenorhabditis elegans embryo, centrosomes are responsible for polarity establishment, i.e. anterior–posterior body axis formation. The signal for polarity originates from the centrosomes and is transmitted to the cell cortex, where it disassembles the actomyosin network. This event leads to symmetry breaking and the establishment of distinct domains of evolutionarily conserved PAR proteins. However, the identity of an essential component that localizes to the centrosomes and promotes symmetry breaking was unknown. Recent work has uncovered that the loss of Aurora A kinase (AIR-1 in C. elegans and hereafter referred to as Aurora A) in the one-cell embryo disrupts stereotypical actomyosin-based cortical flows that occur at the time of polarity establishment. This misregulation of actomyosin flow dynamics results in the occurrence of two polarity axes. Notably, the role of Aurora A in ensuring a single polarity axis is independent of its well-established function in centrosome maturation. The mechanism by which Aurora A directs symmetry breaking is likely through direct regulation of Rho-dependent contractility. In this mini-review, we will discuss the unconventional role of Aurora A kinase in polarity establishment in C. elegans embryos and propose a refined model of centrosome-dependent symmetry breaking.

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