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Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana.

Wolff P, Jiang H, Wang G, Santos-González J, Köhler C - Elife (2015)

Bottom Line: While many imprinted genes have been identified in plants, the functional roles of most of them are unknown.In this study, we systematically examine the functional requirement of paternally expressed imprinted genes (PEGs) during seed development in Arabidopsis thaliana.Our work reveals that a subset of PEGs maintains functional roles in the inbreeding plant Arabidopsis that become evident upon deregulated expression.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and Zurich-Basel Plant Science Center, Swiss Federal Institute of Technology, Zurich, Switzerland.

ABSTRACT
Genomic imprinting is an epigenetic phenomenon causing parent-of-origin specific differential expression of maternally and paternally inherited alleles. While many imprinted genes have been identified in plants, the functional roles of most of them are unknown. In this study, we systematically examine the functional requirement of paternally expressed imprinted genes (PEGs) during seed development in Arabidopsis thaliana. While none of the 15 analyzed peg mutants has qualitative or quantitative abnormalities of seed development, we identify three PEGs that establish postzygotic hybridization barriers in the endosperm, revealing that PEGs have a major role as speciation genes in plants. Our work reveals that a subset of PEGs maintains functional roles in the inbreeding plant Arabidopsis that become evident upon deregulated expression.

No MeSH data available.


Related in: MedlinePlus

Additional ruthenium red staining of seeds.Ruthenium red staining of sections of additional seeds derived from crosses of Col plants pollinated with Col and osd1 at 4 DAP and 6 DAP. A minimum of 100 seeds was analyzed for each cross. Scale bar, 0.1 mm.DOI:http://dx.doi.org/10.7554/eLife.10074.017
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fig4s1: Additional ruthenium red staining of seeds.Ruthenium red staining of sections of additional seeds derived from crosses of Col plants pollinated with Col and osd1 at 4 DAP and 6 DAP. A minimum of 100 seeds was analyzed for each cross. Scale bar, 0.1 mm.DOI:http://dx.doi.org/10.7554/eLife.10074.017

Mentions: To test the hypothesis that endosperm cellularization failure in triploid seeds is a consequence of disturbed pectin degradation pathways, we analyzed expression of 173 genes acting in pectin degrading pathways (pectate lyases (GO:0030570), pectin methylesterases (GO:0030599) and polygalacturonases (GO:0004650)). Of those, 33 genes were upregulated in triploid seeds (Figure 4A). In contrast, expression of pectin biosynthesis genes (Atmodjo et al., 2013) was not negatively affected in triploid seeds (Figure 4B), suggesting that pectin degradation rather than pectin biosynthesis is disturbed in triploid seeds. Most of the 33 pectin degradation genes remained repressed until the heart stage of embryo development in wild-type seeds (Figure 4C) and became expressed at the cotyledon stage of embryo development, concomitantly with endosperm degradation (Figure 4C). In concordance with restored endosperm cellularization in triploid peg mutants, expression of 27 out of 33 pectin degradation genes that were upregulated in triploid seeds was normalized in at least one of the peg mutants (Figure 4D). Pectins are polymerized and methylesterified in the golgi and secreted into the cell wall as highly methylesterified forms. Subsequently, they can be modified by pectinases such as pectin methylesterases that catalyse the demethylesterification of homogalacturonans releasing acidic pectins, which can be visualized by ruthenium red binding (Downie et al., 1998; Micheli, 2001). Before endosperm cellularization, the ruthenium red signal was similar between diploid and triploid seeds (Figure 4E; Figure 4—figure supplement 1), suggesting that there were no major differences in pectin synthesis and degradation between diploid and triploid seeds. At 6 DAP the wild-type endosperm was largely cellularized and only a weak ruthenium red signal could be detected (Figure 4E; Figure 4—figure supplement 1), in agreement with pectin being deposited in the cell wall in a highly methylesterified form that is less intensively stained by ruthenium red (Micheli, 2001). Consistent with the expression of genes encoding for pectin degrading enzymes in 6 DAP triploid seeds (Figure 4D), the ruthenium red signal in the uncellularized endosperm at 6 DAP seeds was substantially weaker compared to the signal in 4DAP seeds (Figure 4E; Figure 4—figure supplement 1).10.7554/eLife.10074.016Figure 4.Analysis of pectin biosynthesis and degradation genes in diploid and triploid seeds.


Paternally expressed imprinted genes establish postzygotic hybridization barriers in Arabidopsis thaliana.

Wolff P, Jiang H, Wang G, Santos-González J, Köhler C - Elife (2015)

Additional ruthenium red staining of seeds.Ruthenium red staining of sections of additional seeds derived from crosses of Col plants pollinated with Col and osd1 at 4 DAP and 6 DAP. A minimum of 100 seeds was analyzed for each cross. Scale bar, 0.1 mm.DOI:http://dx.doi.org/10.7554/eLife.10074.017
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4589659&req=5

fig4s1: Additional ruthenium red staining of seeds.Ruthenium red staining of sections of additional seeds derived from crosses of Col plants pollinated with Col and osd1 at 4 DAP and 6 DAP. A minimum of 100 seeds was analyzed for each cross. Scale bar, 0.1 mm.DOI:http://dx.doi.org/10.7554/eLife.10074.017
Mentions: To test the hypothesis that endosperm cellularization failure in triploid seeds is a consequence of disturbed pectin degradation pathways, we analyzed expression of 173 genes acting in pectin degrading pathways (pectate lyases (GO:0030570), pectin methylesterases (GO:0030599) and polygalacturonases (GO:0004650)). Of those, 33 genes were upregulated in triploid seeds (Figure 4A). In contrast, expression of pectin biosynthesis genes (Atmodjo et al., 2013) was not negatively affected in triploid seeds (Figure 4B), suggesting that pectin degradation rather than pectin biosynthesis is disturbed in triploid seeds. Most of the 33 pectin degradation genes remained repressed until the heart stage of embryo development in wild-type seeds (Figure 4C) and became expressed at the cotyledon stage of embryo development, concomitantly with endosperm degradation (Figure 4C). In concordance with restored endosperm cellularization in triploid peg mutants, expression of 27 out of 33 pectin degradation genes that were upregulated in triploid seeds was normalized in at least one of the peg mutants (Figure 4D). Pectins are polymerized and methylesterified in the golgi and secreted into the cell wall as highly methylesterified forms. Subsequently, they can be modified by pectinases such as pectin methylesterases that catalyse the demethylesterification of homogalacturonans releasing acidic pectins, which can be visualized by ruthenium red binding (Downie et al., 1998; Micheli, 2001). Before endosperm cellularization, the ruthenium red signal was similar between diploid and triploid seeds (Figure 4E; Figure 4—figure supplement 1), suggesting that there were no major differences in pectin synthesis and degradation between diploid and triploid seeds. At 6 DAP the wild-type endosperm was largely cellularized and only a weak ruthenium red signal could be detected (Figure 4E; Figure 4—figure supplement 1), in agreement with pectin being deposited in the cell wall in a highly methylesterified form that is less intensively stained by ruthenium red (Micheli, 2001). Consistent with the expression of genes encoding for pectin degrading enzymes in 6 DAP triploid seeds (Figure 4D), the ruthenium red signal in the uncellularized endosperm at 6 DAP seeds was substantially weaker compared to the signal in 4DAP seeds (Figure 4E; Figure 4—figure supplement 1).10.7554/eLife.10074.016Figure 4.Analysis of pectin biosynthesis and degradation genes in diploid and triploid seeds.

Bottom Line: While many imprinted genes have been identified in plants, the functional roles of most of them are unknown.In this study, we systematically examine the functional requirement of paternally expressed imprinted genes (PEGs) during seed development in Arabidopsis thaliana.Our work reveals that a subset of PEGs maintains functional roles in the inbreeding plant Arabidopsis that become evident upon deregulated expression.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology and Zurich-Basel Plant Science Center, Swiss Federal Institute of Technology, Zurich, Switzerland.

ABSTRACT
Genomic imprinting is an epigenetic phenomenon causing parent-of-origin specific differential expression of maternally and paternally inherited alleles. While many imprinted genes have been identified in plants, the functional roles of most of them are unknown. In this study, we systematically examine the functional requirement of paternally expressed imprinted genes (PEGs) during seed development in Arabidopsis thaliana. While none of the 15 analyzed peg mutants has qualitative or quantitative abnormalities of seed development, we identify three PEGs that establish postzygotic hybridization barriers in the endosperm, revealing that PEGs have a major role as speciation genes in plants. Our work reveals that a subset of PEGs maintains functional roles in the inbreeding plant Arabidopsis that become evident upon deregulated expression.

No MeSH data available.


Related in: MedlinePlus