Duplicated <i>fie</i> Genes in Maize

Danilevskaya, Olga N.; Hermon, Pedro; Hantke, Sabine; Muszynski, Michael G.; Kollipara, K. P.; Ananiev, E. V.

doi:10.1105/tpc.006759

Cited by 169 publications

(67 citation statements)

References 61 publications

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“…S5). These results showed that the imprinted expression of certain endosperm genes depends on developmental stages, with some of them being imprinted only in early stages, consistent with previous reports for Fie1, Fie2, and Meg1 genes (20,28).…”

Section: Resultssupporting

confidence: 81%

Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm

Zhang

Zhao

Xie

et al. 2011

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

169

228

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Although genetic imprinting was discovered in maize 40 years ago, its exact extent in the triploid endosperm remains unknown. Here, we have analyzed global patterns of allelic gene expression in developing maize endosperms from reciprocal crosses between inbreds B73 and Mo17. We have defined an imprinted gene as one in which the relative expression of the maternal and paternal alleles differ at least fivefold in both hybrids of the reciprocal crosses. We found that at least 179 genes (1.6% of protein-coding genes) expressed in the endosperm are imprinted, with 68 of them showing maternal preferential expression and 111 paternal preferential expression. Additionally, 38 long noncoding RNAs were imprinted. The latter are transcribed in either sense or antisense orientation from intronic regions of normal protein-coding genes or from intergenic regions. Imprinted genes show a clear pattern of clustering around the genome, with a number of imprinted genes being adjacent to each other. Analysis of allele-specific methylation patterns of imprinted loci in the hybrid endosperm identified 21 differentially methylated regions (DMRs) of several hundred base pairs in length, corresponding to both imprinted genes and noncoding transcripts. All DMRs identified are uniformly hypomethylated in maternal alleles and hypermethylated in paternal alleles, regardless of the imprinting direction of their corresponding loci. Our study indicates highly extensive and complex regulation of genetic imprinting in maize endosperm, a mechanism that can potentially function in the balancing of the gene dosage of this triploid tissue.

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Section: Resultssupporting

confidence: 81%

Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm

Zhang

Zhao

Xie

et al. 2011

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

169

228

View full text Add to dashboard Cite

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“…Only genes identified in maize and for which expression data have been reported were selected, for, while a more comprehensive list of sequences could have been made using sequences with homology to Arabidopsis endosperm-expressed genes, the striking level of neo-and subfunctionalization that has occurred during evolution of the gramineae (Springer et al 2002;Danilevskaya et al 2003;Gutiérrez-Marcos et al 2006) suggests that this would introduce an unacceptable level of error into our data. Semiquantitative RT-PCR (25, 30 and/or 35 cycles) was carried out for each gene using extracted RNA samples from at least two biological replicates for each time point.…”

Section: Resultsmentioning

confidence: 99%

Balance between maternal and paternal alleles sets the timing of resource accumulation in the maize endosperm

Dickinson

2009

Proc. R. Soc. B.

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Key aspects of seed development in flowering plants are held to be under epigenetic control and to have evolved as a result of conflict between the interests of the male and female gametes (kinship theory). Attempts to identify the genes involved have focused on imprinted sequences, although imprinting is only one mechanism by which male or female parental alleles may be exclusively expressed immediately post-fertilization. We have studied the expression of a subset of endosperm gene classes immediately following interploidy crosses in maize and show that departure from the normal 2 : 1 ratio between female and male genomes exerts a dramatic effect on the timing of expression of some, but not all, genes investigated. Paternal genomic excess prolongs the expression of early genes and delays accumulation of reserves, while maternal genomic excess foreshortens the expression period of early genes and dramatically brings forward endosperm maturation. Our data point to a striking interdependence between the phases of endosperm development, and are consonant with previous work from maize showing progression from cell proliferation to endoreduplication is regulated by the balance between maternal and paternal genomes, and from Arabidopsis suggesting that this 'phasing' is regulated by maternally expressed imprinted genes. Our findings are discussed in context of the kinship theory.

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“…For example, there are two Esc homologs in maize and rice. Zm FIE1 is exclusively expressed in developing endosperm and shows maternal-specific expression; Zm FIE2 is expressed throughout the plant (Danilevskaya et al, 2003). Similar to the maize Esc homologs, Os FIE1 is imprinted, with the maternal allele specifically expressed in endosperm, and Os FIE2 is expressed in a wide range of tissues (Luo et al, 2009).…”

Section: Introductionmentioning

confidence: 97%

“…It has been reported that the common ancestor of the grass family underwent genome duplication 50 to 70 million years ago (Wang et al, 2005;Messing and Bennetzen, 2008), which may have resulted in the duplication of Esc in rice. Like Zm FIE1 (Danilevskaya et al, 2003), Os FIE1 might have evolved an endosperm-specific expression pattern and inherited the imprinting feature; epigenetic marks, such as DNA methylation, may play an important role during this evolution process. FIE1 is an endosperm-specific expressing gene, which is silenced in other tissues via epigenetic repressive modifications.…”

Section: Methylation Is Essential For Normal Endosperm-specific Exprementioning

confidence: 99%

Identification and Characterization of an Epi-Allele of FIE1 Reveals a Regulatory Linkage between Two Epigenetic Marks in Rice

et al. 2012

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DNA methylation and histone H3 Lys 9 dimethylation (H3K9me2) are important epigenetic repression marks for silencing transposons in heterochromatin and for regulating gene expression. However, the mechanistic relationship to other repressive marks, such as histone H3 Lys 27 trimethylation (H3K27me3) is unclear. FERTILIZATION-INDEPENDENT ENDOSPERM1 (FIE1) encodes an Esc-like core component of the Polycomb repressive complex 2, which is involved in H3K27me3-mediated gene repression. Here, we identify a gain-of-function epi-allele (Epi-df) of rice (Oryza sativa) FIE1; this allele causes a dwarf stature and various floral defects that are inherited in a dominant fashion. We found that Epi-df has no changes in nucleotide sequence but is hypomethylated in the 59 region of FIE1 and has reduced H3K9me2 and increased H3K4me3. In Epi-df, FIE1 was ectopically expressed and its imprinting was disrupted. FIE1 interacted with rice Enhancer of Zeste homologs, consistent with its role in H3K27me3 repression. Ectopic expression of FIE1 in Epi-df resulted in alteration of H3K27me3 levels in hundreds of genes. In summary, this work identifies an epi-allele involved in H3K27me3-mediated gene repression that itself is highly regulated by DNA methylation and histone H3K9me2, thereby shedding light on the link between DNA methylation and histone methylation, the two important epigenetic marks regulating rice development.

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Duplicated fie Genes in Maize

Cited by 169 publications

References 61 publications

Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm

Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm

Balance between maternal and paternal alleles sets the timing of resource accumulation in the maize endosperm

Identification and Characterization of an Epi-Allele of FIE1 Reveals a Regulatory Linkage between Two Epigenetic Marks in Rice

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