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The Plant Cell 18:781-784 (2006) © 2006 American Society of Plant Biologists
Genetic and Epigenetic Regulation of EmbryogenesisEmbryogenesis is a crucial period in the development of eukaryotes. In most plants, embryogenesis begins with an asymmetric cell division that gives rise to a polar embryo having a larger basal cell and a smaller apical cell. The embryo proper develops from the apical cell, and the basal cell develops into the suspensor, which is attached to the ovule and serves as a conduit for nutrient transfer to the developing embryo. The early stages of Arabidopsis embryo development have stereotyped cell divisions. Cotyledons then develop and serve to store nutrients for the seedling after germination. During late seed development, the seed desiccates and remains dormant until conditions are right for germination.
Cell division and differentiation during these events follow highly regulated patterns that are influenced by both genetic and epigenetic mechanisms. Mammalian genomes undergo genomic reprogramming during embryogenesis involving global changes in DNA methylation believed to play an important role in developmental regulation of gene expression. DNA methylation is often associated with transcriptionally inactive portions of the genome (heterochromatin), and during early embryogenesis, large portions of the genome undergo a demethylation and subsequent remethylation process that is thought to contribute to chromatin decondensation and transcriptional activation of genes essential for embryo development (Li, 2002 Two articles in this issue of The Plant Cell report on genetic and epigenetic aspects of the regulation of gene expression during embryogenesis. Xiao et al. (pages 805–814) show that DNA methylation performed by METHYLTRANSFERASE1 (MET1) influences gene expression during embryogenesis in Arabidopsis and is critical for normal development of the embryo and seed viability. In another article, Ding et al. (pages 815–830) show that the pentatricopeptide repeat (PPR) protein GLUTAMINE-RICH PROTEIN23 (GRP23) is a nuclear protein that interacts with RNA polymerase II and likely functions in regulating gene expression during early embryogenesis.
In mammals, cytosine methylation occurs mainly at CpG sites (a cytosine residue linked on its 3' side to the 5' side of a guanine residue) and is maintained by DNA methyltransferase1 (Dnmt1), which acts on hemimethylated DNA (double-stranded DNA methylated on only one strand, which occurs following DNA replication). During gametogenesis and embryogenesis, DNA methylation is lost (on both strands of double-stranded DNA) over a large portion of the genome and later in embryo development is reestablished by de novo methyltransferases Dnmt3a and Dnmt3b, which act on fully unmethylated DNA. Both maintenance and de novo methylation are essential in animals, as mutations in either the Dnmt1 or Dnmt3 gene are embryo lethal (Li et al., 1992  ; Okano et al., 1999). Imprinting, or the differential expression of gene alleles dependent on the parent of origin, depends on heritable DNA methylation patterns established during gametogenesis in animals, and imprinted genes are protected from demethylation in the global reprogramming during embryogenesis (Li, 2002). In plants, imprinting of certain genes occurs in the endosperm and affects endosperm development (reviewed in Gehring et al., 2004).
Arabidopsis contains at least three classes of DNA methyltransferase genes: MET1, which is a homolog of Dnmt1 and encodes the major CpG maintenance methyltransferase; CHROMOMETHYLASE3 (CMT3), which encodes a plant-specific DNA methyltransferase that acts mainly at CpNpG and CpNpN residues; and DOMAINS REARRANGED1 (DRM1) and DRM2, which share homology with Dnmt3 and are thought to function as the major de novo methyltransferases in plants (Cao and Jacobsen, 2002
Xiao et al. noticed that met1 mutant embryos resembled mutants having defects in establishing auxin gradients (described in Friml et al., 2003 ) in that the plane of cell divisions and apical-basal polarity appeared to be disrupted. Friml et al. (2003) used the auxin-responsive promoter DR5rev linked to green fluorescent protein (GFP) to show that establishing and maintaining auxin gradients is a critical process during early embryogenesis. Xiao et al. found that DR5:GFP transgene expression was evenly distributed in met1 mutant embryos, in contrast with the pattern indicative of an auxin gradient in the wild type, suggesting that DNA methylation may be important for setting up and/or maintaining auxin gradients in the developing embryo. They also examined the expression of PIN1, which encodes an auxin efflux carrier shown by Friml et al. (2003) to be responsible for establishing auxin gradients in early embryogenesis. PIN1 expression was found to be relatively evenly distributed throughout the developing embryo in met1 mutants, in contrast with the pattern observed in wild-type embryos, suggesting that DNA methylation may affect PIN1 expression. However, DNA methylation (as measured using DNA methylation–sensitive restriction endonucleases and DNA gel blot analysis) could not be detected in the coding, upstream, or downstream regions of PIN1 in DNA isolated from either met1 or wild-type seedlings, leading the authors to conclude that DNA methylation might affect PIN1 expression indirectly.
The authors analyzed gene expression of three other genes that play important roles in specification of cell identity during embryogenesis: YODA (YDA), which encodes a mitogen-activated protein kinase kinase kinase involved in specifying embryo and suspensor cell identity (Lukowitz et al., 2004
The reduction in WOX gene expression was perhaps surprising, as DNA methylation typically is associated with gene silencing, and hypomethylation in the mutant therefore would be expected to result in enhanced gene expression. It has been shown that DNA methylation enhances transcription of mouse insulin growth factor2, apparently by blocking the binding of repressors to a specific intragenic region (Murrell et al., 2001 The work of Xiao et al. shows that DNA methylation is critical for embryogenesis in Arabidopsis and is involved in regulating gene expression affecting both auxin responsiveness and embryo cell identity.
Eukaryotic transcription of protein coding sequences into mRNA is performed by RNA polymerase II. The core of this enzyme supercomplex is essentially the same for the many thousands of genes that are transcribed, and specificity for the regulation of gene expression lies within the multitude of interacting factors and subunits that influence formation and binding of the complex to gene promoter regions (Holstege et al., 1998 ). Screening of embryo-defective (emb) and seed coat mutants in Arabidopsis has identified  750 genes that are required for normal seed development (McElver et al., 2001; Tzafrir et al., 2003, 2004). Among an initial set of 250 EMB genes, 5% were predicted to be transcription factors (Tzafrir et al., 2004). The function of most of these genes remains unknown.
Yang et al. isolated an emb mutant from a collection of enhancer trap mutants that carry an Ac/Ds transposable element linked to the ß-glucuronidase reporter gene (see Springer et al., 1995
PPR proteins constitute one the largest protein families in plants, with >400 members in Arabidopsis. Evidence is emerging that a number of plant PPR proteins are RNA binding proteins involved in posttranscriptional processes, such as mRNA processing, often in mitochondria and chloroplasts (Lurin et al., 2004
Ding et al. show that GRP23 is a nuclear PPR protein that interacts physically with subunit III of RNA polymerase II via its C-terminal WQQ domain in experiments with both yeast and plant cells. The gene is expressed at a relatively high level in gametophytes (particularly pollen grains) and young embryos and at low levels in endosperm tissue and in actively dividing cells in meristems of vegetative tissues. GRP23 therefore exhibits clear differences relative to other known PPR proteins, which mostly have been characterized as putative RNA binding proteins expressed at low levels in all tissues and predicted to be targeted to organelles (e.g., Small and Peeters, 2000 Structural sequence features of the gene suggest that GRP23 is a novel type of basic domain leucine zipper (bZIP) protein, as it has a bZIP domain unrelated to known bZIP proteins in Arabidopsis. bZIP domains are known to be involved in protein–protein interactions, forming homodimers or heterodimers via the zipper portion of the domain, and to bind DNA in a sequence-specific manner via the basic part of the domain. PPR motifs are also predicted to be sequence-specific RNA or DNA binding domains, and Ding et al. hypothesize that GRP23 may bind directly to DNA cis-regulatory elements through the basic region of the bZIP domain or through the PPR motifs. The interaction of the WQQ domain with RNA polymerase III, together with gene expression patterns and mutant phenotypes, suggest that GRP23 may recruit RNA polymerase II to control the expression of genes essential during early embryogenesis. It will be important to determine the downstream targets of transcriptional control by GRP23, the function of the bZIP domain and PPR motif, and the possibility of direct sequence-specific binding to DNA.
Bentolila, S., Alfonso, A.A., and Hanson, M.R. (2002). A pentatricopeptide repeat-containing gene restores fertility to cytoplasmic male-sterile plants. Proc. Natl. Acad. Sci. USA 99, 10887–10892. Cao, S., and Jacobsen, S.E. (2002). Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr. Biol. 12, 1138–1144.[CrossRef][ISI][Medline] Cao, X., Aufsatz, W., Zilberman, D., Mette, M.F., Huang, M.S., Matzke, M., and Jacobsen, S.E. (2003). Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr. Biol. 13, 2212–2217.[CrossRef][ISI][Medline] Ding, Y.-H., Liu, N.-Y., Tang, Z.-S., Liu, J., and Yang, W.-C. (2006). Arabidopsis GLUTAMINE-RICH PROTEIN23 is essential for early embryogenesis and encodes a novel nuclear PPR motif protein that interacts with RNA polymerase II subunit III. Plant Cell 18, 815–830. Friml, J., Vieten, A., Sauer, M., Weijers, D., Schwarz, H., Hamann, T., Offringa, R., and Jurgens, G. (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153.[CrossRef][Medline] Gehring, M., Choi, Y., and Fischer, R.L. (2004). Imprinting and seed development. Plant Cell 16 (suppl.), S203–S213. Haecker, A., Gross-Hardt, R., Geiges, B., Sarkar, A., Breuninger, H., Herrmann, M., and Laux, T. (2004). Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131, 657–668. Holstege, F.C.P., Jenning, E.G., Wyrick, J.J., Lee, T.I., Hengartner, C.J., Green, M.R., Golub, T.R., Lander, E.S., and Young, R.A. (1998). Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95, 717–728.[CrossRef][ISI][Medline] Li, E. (2002). Chromatin modification and epigenetic reprogramming in mammalian development. Nat. Rev. Genet. 3, 662–673.[CrossRef][ISI][Medline] Li, E., Bestor, T.H., and Jaenisch, R. (1992). Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915–926.[CrossRef][ISI][Medline] Lukowitz, W., Roeder, A., Parmenter, D., and Somerville, C. (2004). A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116, 109–119.[CrossRef][ISI][Medline] Lurin, C., et al. (2004). Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16, 2089–2103. McElver, J., et al. (2001). Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics 159, 1751–1763. Murrell, A., Heeson, S., Bowden, L., Constância, M., Dean, W., Kelsey, G., and Reik, W. (2001). An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep. 2, 1101–1106.[CrossRef][ISI][Medline] Okano, M., Bell, D.W., Haber, D.A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247–257.[CrossRef][ISI][Medline] Small, I.D., and Peeters, N. (2000). The PPR motif: A TPR-related motif prevalent in plant organellar proteins. Trends Biochem. Sci. 2, 46–47. Springer, P.S., McCombie, W.R., Sundaresan, V., and Martienssen, R.A. (1995). Gene trap tagging of PROLIFERA, an essential MCM2-3-5–like gene in Arabidopsis. Science 268, 877–880. Sundaresan, V., Springer, P.S., Volpe, T., Haward, S., Jones, J.D.G., Dean, C., Ma, H., and Martienssen, R.A. (1995). Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 9, 1797–1810. Tzafrir, I., Dickerman, A., Brazhnik, O., Nguyen, Q., McElver, J., Frye, C., Patton, D., and Meinke, D. (2003). The Arabidopsis SeedGenes project. Nucleic Acids Res. 31, 90–93. Tzafrir, I., Pena-Muralla, R., Dickerman, A., Berg, M., Rogers, R., Hutchens, S., Sweeney, T.C., McElver, J., Aux, G., Patton, D., and Meinke, D. (2004). Identification of genes required for embryo development in Arabidopsis. Plant Physiol. 135, 1206–1220. Wang, Z., et al. (2006). Cytoplasmic male sterility of rice with Boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell 18, 676–687. Xiao, W., Custard, K.D., Brown, R.C., Lemmon, B.E., Harada, J.J., Goldberg, R.B., and Fischer, R.L. (2006). DNA methylation is critical for Arabidopsis embryogenesis and seed viability. Plant Cell 18, 805–814. Related articles in Plant Cell:
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