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Genome-wide transcript profiling of endosperm without paternal contribution identifies parent-of-origin-dependent regulation of AGAMOUS-LIKE36.

Shirzadi R, Andersen ED, Bjerkan KN, Gloeckle BM, Heese M, Ungru A, Winge P, Koncz C, Aalen RB, Schnittger A, Grini PE - PLoS Genet. (2011)

Bottom Line: In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed.Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented.Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biosciences (IMBV), University of Oslo, Oslo, Norway.

ABSTRACT
Seed development in angiosperms is dependent on the interplay among different transcriptional programs operating in the embryo, the endosperm, and the maternally-derived seed coat. In angiosperms, the embryo and the endosperm are products of double fertilization during which the two pollen sperm cells fuse with the egg cell and the central cell of the female gametophyte. In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed. Here we have exploited cdka;1 fertilization as a novel tool for the identification of seed regulators and factors involved in parent-of-origin-specific regulation during seed development. We have generated genome-wide transcription profiles of cdka;1 fertilized seeds and identified approximately 600 genes that are downregulated in the absence of a paternal genome. Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented. Here, AGL36 was chosen for an in-depth study and shown to be imprinted. We demonstrate that AGL36 parent-of-origin-dependent expression is controlled by the activity of METHYLTRANSFERASE1 (MET1) maintenance DNA methyltransferase and DEMETER (DME) DNA glycosylase. Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.

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A model for the imprinted expression of AGL36.Paternal silencing of AGL36 is maintained by the action of MET1 in the male germline prior to fertilization (1). The maternal copy of AGL36 is repressed after fertilization, either directly or indirectly, by the maternally expressed FIS-complex (2) (only MEA is indicated in the figure). DME is expressed only in the central cell and activates the maternal allele of MEA and AGL36 (3 & 4). The autoregulatory repression of maternal MEA upon paternal MEA is indicated (5). Solid lines indicate direct regulation. Dashed lines indicate possible indirect regulation.
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pgen-1001303-g008: A model for the imprinted expression of AGL36.Paternal silencing of AGL36 is maintained by the action of MET1 in the male germline prior to fertilization (1). The maternal copy of AGL36 is repressed after fertilization, either directly or indirectly, by the maternally expressed FIS-complex (2) (only MEA is indicated in the figure). DME is expressed only in the central cell and activates the maternal allele of MEA and AGL36 (3 & 4). The autoregulatory repression of maternal MEA upon paternal MEA is indicated (5). Solid lines indicate direct regulation. Dashed lines indicate possible indirect regulation.

Mentions: In our study, we have shown that AGL36 is only maternally expressed. Our current model suggests that the paternal allele is silenced by the action of MET1 and the maternal allele activated by DME (Figure 8). In addition, we have also shown that PRC2FIS regulates the expression of the maternal AGL36 allele at the transition between proliferation and cellularization (Figure 8).


Genome-wide transcript profiling of endosperm without paternal contribution identifies parent-of-origin-dependent regulation of AGAMOUS-LIKE36.

Shirzadi R, Andersen ED, Bjerkan KN, Gloeckle BM, Heese M, Ungru A, Winge P, Koncz C, Aalen RB, Schnittger A, Grini PE - PLoS Genet. (2011)

A model for the imprinted expression of AGL36.Paternal silencing of AGL36 is maintained by the action of MET1 in the male germline prior to fertilization (1). The maternal copy of AGL36 is repressed after fertilization, either directly or indirectly, by the maternally expressed FIS-complex (2) (only MEA is indicated in the figure). DME is expressed only in the central cell and activates the maternal allele of MEA and AGL36 (3 & 4). The autoregulatory repression of maternal MEA upon paternal MEA is indicated (5). Solid lines indicate direct regulation. Dashed lines indicate possible indirect regulation.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3040660&req=5

pgen-1001303-g008: A model for the imprinted expression of AGL36.Paternal silencing of AGL36 is maintained by the action of MET1 in the male germline prior to fertilization (1). The maternal copy of AGL36 is repressed after fertilization, either directly or indirectly, by the maternally expressed FIS-complex (2) (only MEA is indicated in the figure). DME is expressed only in the central cell and activates the maternal allele of MEA and AGL36 (3 & 4). The autoregulatory repression of maternal MEA upon paternal MEA is indicated (5). Solid lines indicate direct regulation. Dashed lines indicate possible indirect regulation.
Mentions: In our study, we have shown that AGL36 is only maternally expressed. Our current model suggests that the paternal allele is silenced by the action of MET1 and the maternal allele activated by DME (Figure 8). In addition, we have also shown that PRC2FIS regulates the expression of the maternal AGL36 allele at the transition between proliferation and cellularization (Figure 8).

Bottom Line: In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed.Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented.Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Biosciences (IMBV), University of Oslo, Oslo, Norway.

ABSTRACT
Seed development in angiosperms is dependent on the interplay among different transcriptional programs operating in the embryo, the endosperm, and the maternally-derived seed coat. In angiosperms, the embryo and the endosperm are products of double fertilization during which the two pollen sperm cells fuse with the egg cell and the central cell of the female gametophyte. In Arabidopsis, analyses of mutants in the cell-cycle regulator CYCLIN DEPENDENT KINASE A;1 (CKDA;1) have revealed the importance of a paternal genome for the effective development of the endosperm and ultimately the seed. Here we have exploited cdka;1 fertilization as a novel tool for the identification of seed regulators and factors involved in parent-of-origin-specific regulation during seed development. We have generated genome-wide transcription profiles of cdka;1 fertilized seeds and identified approximately 600 genes that are downregulated in the absence of a paternal genome. Among those, AGAMOUS-LIKE (AGL) genes encoding Type-I MADS-box transcription factors were significantly overrepresented. Here, AGL36 was chosen for an in-depth study and shown to be imprinted. We demonstrate that AGL36 parent-of-origin-dependent expression is controlled by the activity of METHYLTRANSFERASE1 (MET1) maintenance DNA methyltransferase and DEMETER (DME) DNA glycosylase. Interestingly, our data also show that the active maternal allele of AGL36 is regulated throughout endosperm development by components of the FIS Polycomb Repressive Complex 2 (PRC2), revealing a new type of dual epigenetic regulation in seeds.

Show MeSH
Related in: MedlinePlus