The switch from vegetative to reproductive growth is marked by the termination of vegetative development and the adoption of floral identity by the shoot apical meristem (SAM). This process is called the floral transition. To elucidate the molecular determinants involved in this process, we performed genome-wide RNA expression profiling on maize (Zea mays) shoot apices at vegetative and early reproductive stages using massively parallel signature sequencing technology. Profiling revealed significant up-regulation of two maize MADS-box (ZMM) genes, ZMM4 and ZMM15, after the floral transition. ZMM4 and ZMM15 map to duplicated regions on chromosomes 1 and 5 and are linked to neighboring MADS-box genes ZMM24 and ZMM31, respectively. This gene order is syntenic with the vernalization1 locus responsible for floral induction in winter wheat (Triticum monococcum) and similar loci in other cereals. Analyses of temporal and spatial expression patterns indicated that the duplicated pairs ZMM4-ZMM24 and ZMM15-ZMM31 are coordinately activated after the floral transition in early developing inflorescences. More detailed analyses revealed ZMM4 expression initiates in leaf primordia of vegetative shoot apices and later increases within elongating meristems acquiring inflorescence identity. Expression analysis in late flowering mutants positioned all four genes downstream of the floral activators indeterminate1 (id1) and delayed flowering1 (dlf1). Overexpression of ZMM4 leads to early flowering in transgenic maize and suppresses the late flowering phenotype of both the id1 and dlf1 mutations. Our results suggest ZMM4 may play roles in both floral induction and inflorescence development.
Polycomb group (PcG) proteins play an important role in developmental and epigenetic regulation of gene expression in fruit fly (Drosophila melanogaster) and mammals. Recent evidence has shown that Arabidopsis homologs of PcG proteins are also important for the regulation of plant development. The objective of this study was to characterize the PcG homologs in maize (Zea mays). The 11 cloned PcG proteins from fruit fly and the Enhancer of zeste [E(z)], extra sex combs (esc), and Enhancer of Polycomb [E(Pc)] homologs from Arabidopsis were used as queries to perform TBLASTN searches against the public maize expressed sequence tag database and the Pioneer Hi-Bred database. Maize homologs were found for E(z), esc, and E(Pc), but not for Polycomb, pleiohomeotic, Posterior sex combs, Polycomblike, Additional sex combs, Sex combs on midleg, polyhometoic, or multi sex combs. Transcripts of the three maize Enhancer of zeste-like genes, Mez1, Mez2, and Mez3, were detected in all tissues tested, and the Mez2 transcript is alternatively spliced in a tissue-dependent pattern. Zea mays fertilization independent endosperm1 (ZmFie1) expression was limited to developing embryos and endosperms, whereas ZmFie2 expression was found throughout plant development. The conservation of E(z) and esc homologs across kingdoms indicates that these genes likely play a conserved role in repressing gene expression.Gene expression patterns in eukaryotes are regulated in response to developmental and environmental cues. Changes in the patterns of gene expression are often the result of specific transcriptional regulators. In many cases, patterns of gene expression must be stably maintained through mitotic cell divisions even though the transcriptional regulator that effected the change in expression is only present transiently. The Polycomb group (PcG) genes of fruit fly (Drosophila melanogaster) stabilize repressed chromatin states during development. Recently, homologs of PcG genes have also been shown to affect developmental gene regulation in other species.Simon (1995) defined a set of 13 PcG genes in fruit fly based on a common phenotype of homeotic transformation. The homeotic transformations caused by mutations in PcG genes are the result of a failure to maintain transcriptional repression of homeotic genes through development. Biochemical and genetic evidence indicates that the 13 PcG proteins operate in at least two distinct complexes (Franke et al., 1992; Strutt and Paro, 1997;Jones et al., 1998; Sewalt et al., 1998; van Lohuizen et al., 1998;Ng et al., 2000; Tie et al., 2001). One complex includes the PcG proteins E(Z) and ESC, as well as the histone deacetylase RPD3 and the histone-binding p55 proteins (Tie et al., 2001). The second complex includes Polycomb (PC), Posterior sex combs (PSC), Polyhomeotic (PH), Sex combs on Midleg (SCM), and additional uncharacterized proteins (Franke et al., 1992; Shao et al., 1999;Poux et al., 2001). PcG proteins have also been shown to repress expression of introduced (Pal-Bhadra et al., 1997, ...
Two maize genes with predicted translational similarity to the Arabidopsis FIE (Fertilization-Independent Endosperm) protein, a repressor of endosperm development in the absence of fertilization, were cloned and analyzed. Genomic sequences of fie1 and fie2 show significant homology within coding regions but none within introns or 5 upstream. The fie1 gene is expressed exclusively in the endosperm of developing kernels starting at ف 6 days after pollination. fie1 is an imprinted gene showing no detectable expression of the paternally derived fie1 allele during kernel development. Conversely, fie2 is expressed in the embryo sac before pollination. After pollination, its expression persists, predominantly in the embryo and at lower levels in the endosperm. The paternal fie2 allele is not expressed early in kernel development, but its transcription is activated at 5 days after pollination. fie2 is likely to be a functional ortholog of the Arabidopsis FIE gene, whereas fie1 has evolved a distinct function. The maize FIE2 and sorghum FIE proteins form a monophyletic group, sharing a closer relationship to each other than to the FIE1 protein, suggesting that maize fie genes originated from two different ancestral genomes.
Imprinting refers to the epigenetic regulation of gene expression that is dependent upon gene inheritance from the maternal or paternal parent. Previously, we have identified two maize homologs of the single Arabidopsis Polycomb Group gene FIE. Here, we report on the expression pattern of these genes in individual gametes before and after fertilization, and on the role of DNA methylation in determining the maternal expression of the Fie1 gene. We found that Fie1 is neither expressed in the sperm, egg cell nor central cell before fertilization. Activation of the Fie1 maternal allele occurs around two days after pollination (DAP) in the primary endosperm and peaks at 10-11 DAP coinciding with endosperm transition from mitotic division to endoreduplication. In contrast, Fie2 is expressed in the egg cell and more intensively in the central cell similar to Arabidopsis FIE, which strongly supports the hypothesis that it functions as a repressor of endosperm development before fertilization. Using MSRE-PCR and bisulfite sequencing, we could show that the methylated inactive state is the default status of Fie1 in most tissues. In the endosperm the paternal Fie1 allele remains methylated and silent, but the maternal allele appears hypomethylated and active, explaining mono-allelic expression of Fie1 in the endosperm. Taking together, these data demonstrate that the regulation of Fie1 imprinting in maize is different from Arabidopsis and that Fie1 is likely to have acquired important novel functions for endosperm development.
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