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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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Maternal effects of met1/met1 on ovule integument.(A) Wild-type ovule at the mature stage shows four or five cell layers of integuments (int) surrounding the central cell (cc). (B) A similar confocal section of a met1/met1 ovule. (C) Fruits from met1-3/met1-3 plants elongate in absence of fertilization (10 Days After Emasculation, (DAE)) in comparison to wild-type fruits. (D) Wild-type ovule with collapsed central cell at 8 DAE. (E) Seed-like structure in elongated fruits from met1-3/met1-3 plants at 8 DAE. Scale bars represent 20 µm (A, B, D and E) and 1.5 mm (C).
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pone-0002298-g003: Maternal effects of met1/met1 on ovule integument.(A) Wild-type ovule at the mature stage shows four or five cell layers of integuments (int) surrounding the central cell (cc). (B) A similar confocal section of a met1/met1 ovule. (C) Fruits from met1-3/met1-3 plants elongate in absence of fertilization (10 Days After Emasculation, (DAE)) in comparison to wild-type fruits. (D) Wild-type ovule with collapsed central cell at 8 DAE. (E) Seed-like structure in elongated fruits from met1-3/met1-3 plants at 8 DAE. Scale bars represent 20 µm (A, B, D and E) and 1.5 mm (C).

Mentions: The maternal inheritance of the dominant MET1a/s construct caused a dramatic increase of seed size [7]. Similarly, seeds from crosses between ovules from met1-6 [15] or met1-3 homozygous crossed to wild type pollen are much larger than seeds produced from met1/+ heterozygous mothers crossed to wild type pollen (Figures S1, C and D, see the supplemental data available with this article online). The range of phenotypes suggested that seed size and development were influenced by MET1 dosage in the maternal sporophyte. All seeds were affected, indicating that defects could originate from the maternal tissues responsible for supplying maternal nutrients to the seed or the maternal seed integuments. Deregulation of cell proliferation and cell elongation of integuments influences seed size [1], [21], [22]. We thus investigated whether MET1 controls integuments development. We observed that met1-3/met1-3 integuments contain 50% more cells than in the wild type (Figures 3A and 3B and Table 3). We thus conclude that MET1 represses cell proliferation in the integuments. In addition, we observed that in the absence of fertilization, the fruits of met1-3/met1-3 plants elongated (Figure 3C and Table 3), resulting in production of seed-like structures devoid of embryo and endosperm (Figure 3, D and E and Table 3). Similar observations were made with MET1a/s plants (Table 3 and Figure S3, see the supplemental data available with this article online). The autonomous seed-like structures are devoid of endosperm or embryo and develop only from ovules that are deficient of MET1 in the sporophytic integuments but not from ovules from met1/+ plants, 50% of which are deficient of MET1 in the female gametophyte. We conclude that autonomous growth of seed-like structures did not originate from the loss of MET1 activity in the central cell or the egg cell. Rather, MET1 thus controls seed size maternally through its action on cell proliferation and elongation in the seed integuments. Double fertilization causes enhanced cell division followed by elongation in the wild type [1]. Our results thus suggest that double-fertilization releases MET1-inhibited controls. Hence we show that mechanisms acting in the integuments in addition to the endosperm [23] and the embryo [3], [24] prevent seed development in absence of fertilization.


DNA methylation causes predominant maternal controls of plant embryo growth.

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

Maternal effects of met1/met1 on ovule integument.(A) Wild-type ovule at the mature stage shows four or five cell layers of integuments (int) surrounding the central cell (cc). (B) A similar confocal section of a met1/met1 ovule. (C) Fruits from met1-3/met1-3 plants elongate in absence of fertilization (10 Days After Emasculation, (DAE)) in comparison to wild-type fruits. (D) Wild-type ovule with collapsed central cell at 8 DAE. (E) Seed-like structure in elongated fruits from met1-3/met1-3 plants at 8 DAE. Scale bars represent 20 µm (A, B, D and E) and 1.5 mm (C).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2390113&req=5

pone-0002298-g003: Maternal effects of met1/met1 on ovule integument.(A) Wild-type ovule at the mature stage shows four or five cell layers of integuments (int) surrounding the central cell (cc). (B) A similar confocal section of a met1/met1 ovule. (C) Fruits from met1-3/met1-3 plants elongate in absence of fertilization (10 Days After Emasculation, (DAE)) in comparison to wild-type fruits. (D) Wild-type ovule with collapsed central cell at 8 DAE. (E) Seed-like structure in elongated fruits from met1-3/met1-3 plants at 8 DAE. Scale bars represent 20 µm (A, B, D and E) and 1.5 mm (C).
Mentions: The maternal inheritance of the dominant MET1a/s construct caused a dramatic increase of seed size [7]. Similarly, seeds from crosses between ovules from met1-6 [15] or met1-3 homozygous crossed to wild type pollen are much larger than seeds produced from met1/+ heterozygous mothers crossed to wild type pollen (Figures S1, C and D, see the supplemental data available with this article online). The range of phenotypes suggested that seed size and development were influenced by MET1 dosage in the maternal sporophyte. All seeds were affected, indicating that defects could originate from the maternal tissues responsible for supplying maternal nutrients to the seed or the maternal seed integuments. Deregulation of cell proliferation and cell elongation of integuments influences seed size [1], [21], [22]. We thus investigated whether MET1 controls integuments development. We observed that met1-3/met1-3 integuments contain 50% more cells than in the wild type (Figures 3A and 3B and Table 3). We thus conclude that MET1 represses cell proliferation in the integuments. In addition, we observed that in the absence of fertilization, the fruits of met1-3/met1-3 plants elongated (Figure 3C and Table 3), resulting in production of seed-like structures devoid of embryo and endosperm (Figure 3, D and E and Table 3). Similar observations were made with MET1a/s plants (Table 3 and Figure S3, see the supplemental data available with this article online). The autonomous seed-like structures are devoid of endosperm or embryo and develop only from ovules that are deficient of MET1 in the sporophytic integuments but not from ovules from met1/+ plants, 50% of which are deficient of MET1 in the female gametophyte. We conclude that autonomous growth of seed-like structures did not originate from the loss of MET1 activity in the central cell or the egg cell. Rather, MET1 thus controls seed size maternally through its action on cell proliferation and elongation in the seed integuments. Double fertilization causes enhanced cell division followed by elongation in the wild type [1]. Our results thus suggest that double-fertilization releases MET1-inhibited controls. Hence we show that mechanisms acting in the integuments in addition to the endosperm [23] and the embryo [3], [24] prevent seed development in absence of fertilization.

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
Related in: MedlinePlus