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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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Analysis of cdka;1 microarray profiles.(A) Venn diagram representing overlap of genes expressed in globular stage seeds of Arabidopsis Ws-0 plants (red) and genes expressed in 3 DAP seeds from Ler plants pollinated with Col cdka;1 pollen (green). As high as 67.8% of the cdka;1 set and 90,7% of the GH set genes were found in the overlap. Gene numbers refer to the reference set of genes (see material and methods). GH: Goldberg & Harada laboratories (http://www.seedgenenetwork.net). (B) Boxplot showing the reduced relative expression of known maternally imprinted (blue background) and paternally imprinted (pink background) genes in the Ler x cdka;1 versus Ler x Col seeds. Calculations are based on values taken from three independent biological replicas. (C) GO functional classification of microarray expression data. Deregulated genes identified in the microarray experiment were functionally classified regarding their molecular function using the GO Slim classification system (http://www.arabidopsis.org/tools/bulk/go/). The total number of unique GO-term:locus assignments for each group is indicated (n). The functional classifications of all genes present on the microarray (On microarray) and all genes having a present call (All expressed) have been included for comparison. The cut-off for deregulation is ≤0.8 for the downregulated group, and ≥1.5 and ≥1.2 for the upregulated groups.
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pgen-1001303-g001: Analysis of cdka;1 microarray profiles.(A) Venn diagram representing overlap of genes expressed in globular stage seeds of Arabidopsis Ws-0 plants (red) and genes expressed in 3 DAP seeds from Ler plants pollinated with Col cdka;1 pollen (green). As high as 67.8% of the cdka;1 set and 90,7% of the GH set genes were found in the overlap. Gene numbers refer to the reference set of genes (see material and methods). GH: Goldberg & Harada laboratories (http://www.seedgenenetwork.net). (B) Boxplot showing the reduced relative expression of known maternally imprinted (blue background) and paternally imprinted (pink background) genes in the Ler x cdka;1 versus Ler x Col seeds. Calculations are based on values taken from three independent biological replicas. (C) GO functional classification of microarray expression data. Deregulated genes identified in the microarray experiment were functionally classified regarding their molecular function using the GO Slim classification system (http://www.arabidopsis.org/tools/bulk/go/). The total number of unique GO-term:locus assignments for each group is indicated (n). The functional classifications of all genes present on the microarray (On microarray) and all genes having a present call (All expressed) have been included for comparison. The cut-off for deregulation is ≤0.8 for the downregulated group, and ≥1.5 and ≥1.2 for the upregulated groups.

Mentions: When we compared the transcriptional profiles of Ler x cdka;1 versus Ler x Col seeds 3 DAP, we detected 17223 nuclear genes that were expressed in all biological replicates of both mutant (cdka;1 set) and wild-type (WT set) seed profiles. Our result is in good agreement with a set of genes identified by Goldberg & Harada laboratories (GH) in globular stage seeds of Arabidopsis Ws-0 plants as 68% of our genes were also identified by GH, and our gene set included >90% of the GH globular seed gene set (Figure 1A; http://seedgenenetwork.net, [44]).


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)

Analysis of cdka;1 microarray profiles.(A) Venn diagram representing overlap of genes expressed in globular stage seeds of Arabidopsis Ws-0 plants (red) and genes expressed in 3 DAP seeds from Ler plants pollinated with Col cdka;1 pollen (green). As high as 67.8% of the cdka;1 set and 90,7% of the GH set genes were found in the overlap. Gene numbers refer to the reference set of genes (see material and methods). GH: Goldberg & Harada laboratories (http://www.seedgenenetwork.net). (B) Boxplot showing the reduced relative expression of known maternally imprinted (blue background) and paternally imprinted (pink background) genes in the Ler x cdka;1 versus Ler x Col seeds. Calculations are based on values taken from three independent biological replicas. (C) GO functional classification of microarray expression data. Deregulated genes identified in the microarray experiment were functionally classified regarding their molecular function using the GO Slim classification system (http://www.arabidopsis.org/tools/bulk/go/). The total number of unique GO-term:locus assignments for each group is indicated (n). The functional classifications of all genes present on the microarray (On microarray) and all genes having a present call (All expressed) have been included for comparison. The cut-off for deregulation is ≤0.8 for the downregulated group, and ≥1.5 and ≥1.2 for the upregulated groups.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3040660&req=5

pgen-1001303-g001: Analysis of cdka;1 microarray profiles.(A) Venn diagram representing overlap of genes expressed in globular stage seeds of Arabidopsis Ws-0 plants (red) and genes expressed in 3 DAP seeds from Ler plants pollinated with Col cdka;1 pollen (green). As high as 67.8% of the cdka;1 set and 90,7% of the GH set genes were found in the overlap. Gene numbers refer to the reference set of genes (see material and methods). GH: Goldberg & Harada laboratories (http://www.seedgenenetwork.net). (B) Boxplot showing the reduced relative expression of known maternally imprinted (blue background) and paternally imprinted (pink background) genes in the Ler x cdka;1 versus Ler x Col seeds. Calculations are based on values taken from three independent biological replicas. (C) GO functional classification of microarray expression data. Deregulated genes identified in the microarray experiment were functionally classified regarding their molecular function using the GO Slim classification system (http://www.arabidopsis.org/tools/bulk/go/). The total number of unique GO-term:locus assignments for each group is indicated (n). The functional classifications of all genes present on the microarray (On microarray) and all genes having a present call (All expressed) have been included for comparison. The cut-off for deregulation is ≤0.8 for the downregulated group, and ≥1.5 and ≥1.2 for the upregulated groups.
Mentions: When we compared the transcriptional profiles of Ler x cdka;1 versus Ler x Col seeds 3 DAP, we detected 17223 nuclear genes that were expressed in all biological replicates of both mutant (cdka;1 set) and wild-type (WT set) seed profiles. Our result is in good agreement with a set of genes identified by Goldberg & Harada laboratories (GH) in globular stage seeds of Arabidopsis Ws-0 plants as 68% of our genes were also identified by GH, and our gene set included >90% of the GH globular seed gene set (Figure 1A; http://seedgenenetwork.net, [44]).

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