Some genes in mammals and flowering plants are subject to parental imprinting, a process by which differential epigenetic marks are imposed on male and female gametes so that one set of alleles is silenced on chromosomes contributed by the mother while another is silenced on paternal chromosomes. Therefore, each genome contributes a different set of active alleles to the offspring, which develop abnormally if the parental genome balance is disturbed. In Arabidopsis, seeds inheriting extra maternal genomes show distinctive phenotypes such as low weight and inhibition of mitosis in the endosperm, while extra paternal genomes result in reciprocal phenotypes such as high weight and endosperm overproliferation. DNA methylation is known to be an essential component of the parental imprinting mechanism in mammals, but there is less evidence for this in plants. For the present study, seed development was examined in crosses using a transgenic Arabidopsis line with reduced DNA methylation. Crosses between hypomethylated and wild-type diploid plants produced similar seed phenotypes to crosses between plants with normal methylation but different ploidies. This is consistent with a model in which hypomethylation of one parental genome prevents silencing of alleles that would normally be active only when inherited from the other parent - thus phenocopying the effects of extra genomes. These results suggest an important role for methylation in parent-of-origin effects, and by inference parental imprinting, in plants. The phenotype of biparentally hypomethylated seeds is less extreme than the reciprocal phenotypes of uniparentally hypomethylated seeds. The observation that development is less severely affected if gametes of both sexes (rather than just one) are ‘neutralized’ with respect to parent-of-origin effects supports the hypothesis that parental imprinting is not necessary to regulate development.

Bartolomei
M. S.
,
Tilghman
S. M.
(
1997
)
Genomic imprinting in mammals.
Annu. Rev. Genet
31
,
493
525
Blomstedt
C. K.
,
Knox
R. B.
,
Singh
M. B.
(
1996
)
Generative cells of Lilium longiflorum possess translatable mRNA and functional protein synthesis machinery.
Plant Mol. Biol
31
,
1083
1086
Brannan
C. I.
,
Bartolomei
M. S.
(
1999
)
Mechanisms of genomic imprinting.
Curr. Opin. Genet. Dev
9
,
164
170
Braselton
J. P.
,
Wilkinson
M. J.
,
Clulow
S. A.
(
1996
)
Feulgen staining of intact plant tissues for confocal microscopy.
Biotech. Histochem
71
,
84
87
Edwards
K.
,
Johnstone
C.
,
Thompson
C.
(
1991
)
A simple and rapid method for the preparation of plant genomic DNA for PCR analysis.
Nucl. Acids Res
19
,
1349
–.
Finnegan
E. J.
,
Peacock
W. J.
,
Dennis
E. S.
(
1996
)
Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development.
Proc. Natl. Acad. Sci. USA
93
,
8449
8454
Haig
D.
,
Westoby
M.
(
1989
)
Parent-specific gene expression and the triploid endosperm.
Am. Nat
134
,
147
155
Jaenisch
R.
(
1997
)
DNA methylation and imprinting: why bother?.
Trends Genet
13
,
323
329
Jeddeloh
J. A.
,
Stokes
T. L.
,
Richards
E. J.
(
1999
)
Maintenance of genomic methylation requires a SWI2/SNF2-like protein.
Nat. Genet
22
,
94
97
Kakutani
T.
,
Jeddeloh
J. A.
,
Richards
E. J.
(
1995
)
Characterization of an Arabidopsis thaliana DNA hypomethylation mutant.
Nucl. Acids Res
23
,
130
137
Kakutani
T.
,
Jeddeloh
J. A.
,
Flowers
S. K.
,
Munakata
K.
,
Richards
E. J.
(
1996
)
Developmental abnormalities and epimutations associated with DNA hypomethylation mutants.
Proc. Natl. Acad. Sci. USA
93
,
12406
12411
Kermicle
J. L.
(
1970
)
Dependence of the R -mottled aleurone phenotype in maize on mode of sexual transmission.
Genetics
66
,
69
85
Kinoshita
T.
,
Yadegari
R.
,
Harada
J. J.
,
Goldberg
R. B.
,
Fischer
R. L.
(
1999
)
Imprinting of the MEDEA Polycomb gene in the Arabidopsis endosperm.
Plant Cell
11
,
1945
1952
Li
E.
,
Bestor
T. H.
,
Jaenisch
R.
(
1992
)
Targeted mutation of the DNA methyltransferase gene results in embryonic lethality.
Cell
69
,
915
926
Li
E.
,
Beard
C.
,
Jaenisch
R.
(
1993
)
Role for DNA methylation in genomic imprinting.
Nature
366
,
362
365
Lin
B.-Y.
(
1984
)
Ploidy barrier to endosperm development in maize.
Genetics
107
,
103
115
Lopes
M. A.
,
Larkins
B. A.
(
1993
)
Endosperm origin, development, and function.
Plant Cell
5
,
1383
1399
Lund
G.
,
Ciceri
P.
,
Viotti
A.
(
1995
)
Maternal-specific hypomethylation and expression of specific alleles of zein genes in the endosperm of Zea mays L.
Plant J
8
,
571
581
McClelland
M.
,
Nelson
M.
,
Raschke
E.
(
1994
)
Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases.
Nucleic Acids Res
22
,
3640
3659
McCormick
S.
(
1993
)
Male gametophyte development.
Plant Cell
5
,
1265
1275
Mertineit
C.
,
Yoder
J. A.
,
Taketo
T.
,
Laird
D. W.
,
Trasler
J. M.
,
Bestor
T. H.
(
1998
)
Sex-specific exons control DNA methyltransferase in mammalian germ cells.
Development
125
,
889
897
Moore
T.
,
Haig
D.
(
1991
)
Genomic imprinting in mammalian development: a parental tug of war.
Trends Genet
7
,
45
49
Neumann
B.
,
Barlow
D. P.
(
1996
)
Multiple roles for DNA methylation in gametic imprinting.
Curr. Opin. Genet. Dev
6
,
159
163
Paul
W.
,
Hodge
R.
,
Smartt
S.
,
Draper
J.
,
Scott
R.
(
1992
)
The isolation and characterisation of the tapetum-specific Arabidopsis thaliana A9 gene.
Plant Mol. Biol
19
,
611
622
Sarkar
K. R.
,
Coe
E. H.
Jr
(
1966
)
A genetic analysis of the origin of maternal haploids in maize.
Genetics
54
,
453
464
Southern
E. M.
(
1975
)
Detection of specific sequences among DNA fragments separated by gel electrophoresis.
J. Mol. Biol
98
,
503
517
Tilghman
S. M.
(
1999
)
The sins of the fathers and mothers: genomic imprinting in mammalian development.
Cell
96
,
185
193
Vielle-Calzada
J.-P.
,
Thomas
J.
,
Spillane
C.
,
Coluccio
A.
,
Hoeppner
M. A.
,
Grossniklaus
U.
(
1999
)
Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity.
Genes Dev
13
,
2971
2982
Vongs
A.
,
Kakutani
T.
,
Martienssen
R. A.
,
Richards
E. J.
(
1993
)
Arabidopsis thaliana DNA methylation mutants.
Science
260
,
1926
1928
This content is only available via PDF.