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DNA methylation causes predominant maternal controls of plant embryo growth.

FitzGerald J, Luo M, Chaudhury A, Berger F - PLoS ONE (2008)

Bottom Line: Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth.Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase.We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.

View Article: PubMed Central - PubMed

Affiliation: Chromatin and reproduction Group, Temasek Life Sciences Laboratory, National University of Singapore, Department of Biological Sciences, Singapore, Singapore.

ABSTRACT
The parental conflict hypothesis predicts that the mother inhibits embryo growth counteracting growth enhancement by the father. In plants the DNA methyltransferase MET1 is a central regulator of parentally imprinted genes that affect seed growth. However the relation between the role of MET1 in imprinting and its control of seed size has remained unclear. Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth. We show that the loss of MET1 during male gametogenesis causes a reduction of seed size, presumably linked to silencing of the paternal allele of growth enhancers in the endosperm, which nurtures the embryo. However, we find no evidence for a similar role of MET1 during female gametogenesis. Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase. MET1 inhibits seed growth by restricting cell division and elongation in the maternal integuments that surround the seed. Our data demonstrate new controls of seed growth linked to the mode of reproduction typical of flowering plants. We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.

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Correlation between seed size and the inheritance of met1-3 associated to BASTA resistance.(A) BASTA resistance (Br) and sensitivity (Bs) are correlated with seed size in seeds from crosses between wild-type ovules and met1-3/+ pollen. Segregation of the BASTA marker remains 1∶1 (p = 0.4795 χ2), so although some seed lethality was observed (n = 11) it is not linked to met1-3. (B) Br and Bs are not correlated with seed size in seeds from crosses between met1-3/+ ovules and wild-type pollen.
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pone-0002298-g002: Correlation between seed size and the inheritance of met1-3 associated to BASTA resistance.(A) BASTA resistance (Br) and sensitivity (Bs) are correlated with seed size in seeds from crosses between wild-type ovules and met1-3/+ pollen. Segregation of the BASTA marker remains 1∶1 (p = 0.4795 χ2), so although some seed lethality was observed (n = 11) it is not linked to met1-3. (B) Br and Bs are not correlated with seed size in seeds from crosses between met1-3/+ ovules and wild-type pollen.

Mentions: To confirm the link between the small seeds and paternal inheritance of met1-3, seeds from wt×met1-3/+ crosses were visually sorted according to their size relative to a wild type control, and BASTA resistance associated to met1-3 was tested. Two populations of seeds were distinguished. All smallest seeds were resistant to BASTA (n = 323) while all largest seeds were sensitive to BASTA (n = 336). The 1∶1 proportion supported the predicted association of the paternal effect of met1-3 to gametogenesis (p = 0.6126 χ2). As we did not analyze the entire population we may have missed a complex genetic component regulating seed size. To ensure that abnormally small seeds or seed lethality were not missing from our bulked seed population, we analyzed all seeds from single crosses between wild-type mothers and pollen from met1-3/+ plants (Figure 2A, Table 2). In this analysis we also ensured that crosses with pollen from wt and met1-3/+ plants were performed on the same mother plant to allow an absolute size comparison. BASTA resistance correlated with the smallest seeds of the population (p<0.0001 ANOVA and Mann-Whitney) demonstrating that paternal inheritance of met1-3 causes seed size reduction as a result of the loss of MET1 activity during male gametogenesis. The loss of MET1 during male gametogenesis may allow paternal expression of imprinted growth inhibitors and cause a decrease of endosperm and seed size. Loss-of-function paternal effects are uncommon and until now have only been linked to defects in fertilization in Drosophila [18], [19], C.elegans [20] and Arabidopsis [3]. We thus conclude that met1-3 causes a paternal effect associated with defects after fertilization and thus representing a distinct class of paternal effect mutations.


DNA methylation causes predominant maternal controls of plant embryo growth.

FitzGerald J, Luo M, Chaudhury A, Berger F - PLoS ONE (2008)

Correlation between seed size and the inheritance of met1-3 associated to BASTA resistance.(A) BASTA resistance (Br) and sensitivity (Bs) are correlated with seed size in seeds from crosses between wild-type ovules and met1-3/+ pollen. Segregation of the BASTA marker remains 1∶1 (p = 0.4795 χ2), so although some seed lethality was observed (n = 11) it is not linked to met1-3. (B) Br and Bs are not correlated with seed size in seeds from crosses between met1-3/+ ovules and wild-type pollen.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2390113&req=5

pone-0002298-g002: Correlation between seed size and the inheritance of met1-3 associated to BASTA resistance.(A) BASTA resistance (Br) and sensitivity (Bs) are correlated with seed size in seeds from crosses between wild-type ovules and met1-3/+ pollen. Segregation of the BASTA marker remains 1∶1 (p = 0.4795 χ2), so although some seed lethality was observed (n = 11) it is not linked to met1-3. (B) Br and Bs are not correlated with seed size in seeds from crosses between met1-3/+ ovules and wild-type pollen.
Mentions: To confirm the link between the small seeds and paternal inheritance of met1-3, seeds from wt×met1-3/+ crosses were visually sorted according to their size relative to a wild type control, and BASTA resistance associated to met1-3 was tested. Two populations of seeds were distinguished. All smallest seeds were resistant to BASTA (n = 323) while all largest seeds were sensitive to BASTA (n = 336). The 1∶1 proportion supported the predicted association of the paternal effect of met1-3 to gametogenesis (p = 0.6126 χ2). As we did not analyze the entire population we may have missed a complex genetic component regulating seed size. To ensure that abnormally small seeds or seed lethality were not missing from our bulked seed population, we analyzed all seeds from single crosses between wild-type mothers and pollen from met1-3/+ plants (Figure 2A, Table 2). In this analysis we also ensured that crosses with pollen from wt and met1-3/+ plants were performed on the same mother plant to allow an absolute size comparison. BASTA resistance correlated with the smallest seeds of the population (p<0.0001 ANOVA and Mann-Whitney) demonstrating that paternal inheritance of met1-3 causes seed size reduction as a result of the loss of MET1 activity during male gametogenesis. The loss of MET1 during male gametogenesis may allow paternal expression of imprinted growth inhibitors and cause a decrease of endosperm and seed size. Loss-of-function paternal effects are uncommon and until now have only been linked to defects in fertilization in Drosophila [18], [19], C.elegans [20] and Arabidopsis [3]. We thus conclude that met1-3 causes a paternal effect associated with defects after fertilization and thus representing a distinct class of paternal effect mutations.

Bottom Line: Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth.Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase.We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.

View Article: PubMed Central - PubMed

Affiliation: Chromatin and reproduction Group, Temasek Life Sciences Laboratory, National University of Singapore, Department of Biological Sciences, Singapore, Singapore.

ABSTRACT
The parental conflict hypothesis predicts that the mother inhibits embryo growth counteracting growth enhancement by the father. In plants the DNA methyltransferase MET1 is a central regulator of parentally imprinted genes that affect seed growth. However the relation between the role of MET1 in imprinting and its control of seed size has remained unclear. Here we combine cytological, genetic and statistical analyses to study the effect of MET1 on seed growth. We show that the loss of MET1 during male gametogenesis causes a reduction of seed size, presumably linked to silencing of the paternal allele of growth enhancers in the endosperm, which nurtures the embryo. However, we find no evidence for a similar role of MET1 during female gametogenesis. Rather, the reduction of MET1 dosage in the maternal somatic tissues causes seed size increase. MET1 inhibits seed growth by restricting cell division and elongation in the maternal integuments that surround the seed. Our data demonstrate new controls of seed growth linked to the mode of reproduction typical of flowering plants. We conclude that the regulation of embryo growth by MET1 results from a combination of predominant maternal controls, and that DNA methylation maintained by MET1 does not orchestrate a parental conflict.

Show MeSH