The<i>Polycomb</i>-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene<i>PHERES1</i>

In developing progeny of mammals the two parental genomes are differentially expressed according to imprinting marks, and embryos with only a uniparental genetic contribution die [1][2][3] . Gene expression that is dependent on the parent of origin has also been observed in the offspring of flowering plants, and mutations in the imprinting machinery lead to embryonic lethality, primarily affecting the development of the endosperm-a structure in the seed that nourishes the embryo, analogous to the function of the mammalian placenta 4 . Here we have generated Arabidopsis thaliana seeds in which the endosperm is of uniparental, that is, maternal, origin. We demonstrate that imprinting in developing seeds can be bypassed and viable albeit smaller seedlings can develop from seeds lacking a paternal contribution to the endosperm. Bypassing is only possible if the mother is mutant for any of the FIS-class genes, which encode Polycomb group chromatinmodifying factors. Thus, these data provide functional evidence that the action of the FIS complex balances the contribution of the paternal genome. As flowering plants have evolved a special reproduction system with a parallel fusion of two female with two male gametes, our findings support the hypothesis that only with the evolution of double fertilization did the action of the FIS genes become a requirement for seed development. Furthermore, our data argue for a gametophytic origin of endosperm in flowering plants, thereby supporting a hypothesis raised in 1900 by Eduard Strasburger.Flowering plants (angiosperms) have evolved to be one of the predominant life forms on earth with more than 250,000 extant species. An important feature, and probably one of the main reasons for this evolutionary success, is the development of an embryo along with a second fertilization product, the endosperm. The endosperm is usually triploid because a homo-diploid female central cell fuses with one of the male gametes. The exact genome dosage of typically two maternal and one paternal genomes seems to be crucial for endosperm development. Raising the maternal contribution in the endosperm has been found to result in smaller seeds comprising fewer endosperm cells and smaller embryos. In contrast, increasing the paternal input results in larger seeds [5][6][7] . These results have been interpreted in light of the parental conflict theory (kinship theory) according to which mothers and fathers have a different interest in allocation of resources to their offspring 8,9 . Hence, it has been proposed that paternal genes promote seed growth, whereas maternal genes rather reduce growth; or, conversely, that in the maternal genome growth promoting factors are inactivated.Indeed, flowering plants have been found to imprint certain genes during endosperm development, which is similar to the situation observed for the placenta of mammals [10][11][12][13][14] . Interestingly, the imprinting machinery seems to regulate itself [15][16][17] . Imprinting involves the recognition of methylated DNA and histone...

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“…3). Consistent with previous findings, PHE1 expression is strongly upregulated in mea mutants 26 . This effect is more pronounced at 4 d.a.p.…”

Section: Letterssupporting

confidence: 81%

Bypassing genomic imprinting allows seed development

Nowack

Shirzadi

Dißmeyer

et al. 2007

Nature

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“…Loss-of-function mutations of FIS genes cause autonomous onset of cell division in the central cell in the absence of fertilization [14,15]. The FIS complex also includes the WD40 protein MULTICOPY SUPPRESSOR OF IRA 1 (MSI1) [16,17]. Unexpectedly, when compared to the fis mutants, msi mutants show additional autonomous division in the egg cell that leads to a non-viable parthenogenetic embryo [18 ].…”

Section: Control Of Cell Cycle Progression Before and After Fertilizamentioning

confidence: 99%

“…Small-scale microarray analyses using combinations of fis mutants have to date discovered two genes that are repressed by the FIS-complex, and these genes encode the MADS-box protein PHERES1 (PHE1) and the SKP1-like protein MEIDOS [16]. What functions these proteins have in seed development and growth is not known, but PHE1 has been shown to be expressed exclusively from the paternal genome after fertilization [42 ].…”

Section: Coordination Of Maternal and Zygotic Cues During Seed Develomentioning

confidence: 99%

Endosperm: an integrator of seed growth and development

Berger

Grini

Schnittger

2006

Current Opinion in Plant Biology

167

107

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“…Because the previously identified imprinted genes are mostly MEGs, there is no previous report on parental differential methylation for PEGs. Silencing of the maternal allele of a PEG gene (PHE1) in Arabidopsis is reported to require demethylation of the maternal allele and depends on the PRC2 complex (43)(44)(45). All eight PEGs having DMRs are also maternally hypomethylated, suggesting that there could be an additional mechanism for the regulation of PEGs.…”

Section: Dna Methylation Is Involved In the Regulation Of A Small Framentioning

confidence: 99%

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.

166

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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ThePolycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box genePHERES1

Cited by 399 publications

References 39 publications

Bypassing genomic imprinting allows seed development

Bypassing genomic imprinting allows seed development

Endosperm: an integrator of seed growth and development

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

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