Endosperm cellularization defines an important developmental transition for embryo development

Frost

Proc. Natl. Acad. Sci. U.S.A.

et al. 2017

The DEMETER (DME) DNA glycosylase initiates active DNA demethylation via the base-excision repair pathway and is vital for reproduction in Arabidopsis thaliana. DME-mediated DNA demethylation is preferentially targeted to small, AT-rich, and nucleosome-depleted euchromatic transposable elements, influencing expression of adjacent genes and leading to imprinting in the endosperm. In the female gametophyte, DME expression and subsequent genome-wide DNA demethylation are confined to the companion cell of the egg, the central cell. Here, we show that, in the male gametophyte, DME expression is limited to the companion cell of sperm, the vegetative cell, and to a narrow window of time: immediately after separation of the companion cell lineage from the germline. We define transcriptional regulatory elements of DME using reporter genes, showing that a small region, which surprisingly lies within the DME gene, controls its expression in male and female companion cells. DME expression from this minimal promoter is sufficient to rescue seed abortion and the aberrant DNA methylome associated with the null dme-2 mutation. Within this minimal promoter, we found short, conserved enhancer sequences necessary for the transcriptional activities of DME and combined predicted binding motifs with published transcription factor binding coordinates to produce a list of candidate upstream pathway members in the genetic circuitry controlling DNA demethylation in gamete companion cells. These data show how DNA demethylation is regulated to facilitate endosperm gene imprinting and potential transgenerational epigenetic regulation, without subjecting the germline to potentially deleterious transposable element demethylation.S exual reproduction is characterized by fertilization of an egg by a sperm cell, generating the embryo. Uniquely in angiosperms, a second sperm cell fertilizes the companion cell of the egg, the central cell, to generate the endosperm, which supports development of the embryo. During reproduction in angiosperm Arabidopsis thaliana, the DEMETER (DME) DNA glycosylase exhibits a striking expression pattern. Within the ovule, the female gametophyte is generated by mitosis of the haploid megaspore, forming a mature gametophyte of seven cells. During this process, the egg and central cell lineages are separated, and, at this point, DME expression and DNA demethylation is initiated solely in the central cell (1, 2). DME expression is switched off after fertilization (2). This precise pattern of expression initiated in the central cell, and not in the egg cell, is responsible for hypomethylation specifically in the maternal endosperm genome and not in the maternal embryo genome (3). DME expression in the central cell is essential for plant reproduction and genomic imprinting, whereby its absence results in loss of genomic imprinting, aberrant endosperm development, and early seed abortion (2, 4, 5).In the male gametophyte, indirect evidence suggests that DME is expressed during development of the mature three-cell pollen gra...

Section: Dme Is Expressed Specifically In the Companion Cell Of The Malementioning

confidence: 99%

Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells in Arabidopsis thaliana

Frost

Proc. Natl. Acad. Sci. U.S.A.

et al. 2017

“…S17), implicating a differential transcriptional regulation between embryo and endosperm. It was previously reported that TFs of MADS function in seed and endosperm development (Kang et al, 2008;Sreenivasulu et al, 2008;Bemer et al, 2010;Le et al, 2010;Agarwal et al, 2011;Hehenberger et al, 2012). AGL62, a MADS protein of Arabidopsis, is the direct target of FIS Polycomb group repressive complex2 (PRC2), establishing the molecular basis for FIS PRC2-mediated endosperm cellularization (Hehenberger et al, 2012).…”

Section: Differential Regulatory Mechanisms In Embryo and Endospermmentioning

confidence: 99%

The Differential Transcription Network between Embryo and Endosperm in the Early Developing Maize Seed

Chen

Shu

et al. 2013

Plant Physiology

Transcriptome analysis of early-developing maize (Zea mays) seed was conducted using Illumina sequencing. We mapped 11,074,508 and 11,495,788 paired-end reads from endosperm and embryo, respectively, at 9 d after pollination to define gene structure and alternative splicing events as well as transcriptional regulators of gene expression to quantify transcript abundance in both embryo and endosperm. We identified a large number of novel transcribed regions that did not fall within maize annotated regions, and many of the novel transcribed regions were tissue-specifically expressed. We found that 50.7% (8,556 of 16,878) of multiexonic genes were alternatively spliced, and some transcript isoforms were specifically expressed either in endosperm or in embryo. In addition, a total of 46 trans-splicing events, with nine intrachromosomal events and 37 interchromosomal events, were found in our data set. Many metabolic activities were specifically assigned to endosperm and embryo, such as starch biosynthesis in endosperm and lipid biosynthesis in embryo. Finally, a number of transcription factors and imprinting genes were found to be specifically expressed in embryo or endosperm. This data set will aid in understanding how embryo/endosperm development in maize is differentially regulated.Maize (Zea mays) seeds are one of the most important crop materials that provide resources for food, feed, biofuel, and raw material for processing. Maize seed development initiates from double fertilization, in which two of the pollen sperms fuse with an egg cell and a central cell to produce embryo and endosperm, respectively (Randolph, 1936;Chaudhury et al., 2001). The main function of endosperm is to provide nutrient for the developing embryo and germinating embryo.After fertilization, the zygote undergoes an asymmetric division into a small apical cell and a large basal cell, giving rise to the embryo proper and the suspensor, respectively. The radial symmetry of the proembryo is shifted to a bilateral symmetry at the transition stage, which is characterized by protoderm formation. The shoot apical meristem and the root apical meristem can be distinguished at the onset of the coleoptile stage, and then the position of the future coleoptile is marked by a small protuberance. The mature embryo is composed of the embryo axis, which is formed by the plumule with five or six short internodes, and leaf primordia and primary root surrounded by the coleoptile and the coleorhiza, respectively, and the scutellum (Randolph, 1936;Abbe and Stein, 1954;Diboll, 1968;Lammeren, 1986;Vernoud et al., 2005).Maize endosperm follows the nucleus-type endosperm development, where the fertilized central cell undergoes several rounds of synchronous division in the absence of cell wall formation and cytokinesis to produce a syncytium (Lopes and Larkins, 1993;Olsen, 2004). Cellularization allows the formation of the internuclear radial microtubule systems and open-ended alveolation from the periphery of the endosperm toward the central vacuole (Olsen et al., ...

“…Interestingly, a recent work in Arabidopsis revealed a failure of endosperm cellularization correlated with increased hexose content in the seed (Hehenberger et al, 2012), suggesting that a low hexose level is required for endosperm cellularization. Indeed, compared with 5-DAA cotton seed, Glc and Fru content significantly declined in 10-DAA filial tissues (Supplemental Fig.…”

Section: Ghcwin1 Is Involved In Endosperm Nuclear Division But Not Inmentioning

confidence: 99%

New Insights into Roles of Cell Wall Invertase in Early Seed Development Revealed by Comprehensive Spatial and Temporal Expression Patterns of GhCWIN1 in Cotton

Wang

Ruan

2012

Plant Physiology

Despite substantial evidence on the essential roles of cell wall invertase (CWIN) in seed filling, it remains largely unknown how CWIN exerts its regulation early in seed development, a critical stage that sets yield potential. To fill this knowledge gap, we systematically examined the spatial and temporal expression patterns of a major CWIN gene, GhCWIN1, in cotton (Gossypium hirsutum) seeds from prefertilization to prestorage phase. GhCWIN1 messenger RNA was abundant at the innermost seed coat cell layer at 5 d after anthesis but became undetectable at 10 d after anthesis, at the onset of its differentiation into transfer cells characterized by wall ingrowths, suggesting that CWIN may negatively regulate transfer cell differentiation. Within the filial tissues, GhCWIN1 transcript was detected in endosperm cells undergoing nuclear division but not in those cells at the cellularization stage, with similar results observed in Arabidopsis (Arabidopsis thaliana) endosperm for CWIN, AtCWIN4. These findings indicate a function of CWIN in nuclear division but not cell wall biosynthesis in endosperm, contrasting to the role proposed for sucrose synthase (Sus). Further analyses revealed a preferential expression pattern of GhCWIN1 and AtCWIN4 in the provascular region of the torpedo embryos in cotton and Arabidopsis seed, respectively, indicating a role of CWIN in vascular initiation. Together, these novel findings provide insights into the roles of CWIN in regulating early seed development spatially and temporally. By comparing with previous studies on Sus expression and in conjunction with the expression of other related genes, we propose models of CWIN-and Sus-mediated regulation of early seed development.