Download The plant genome`s methylation status and response to stress

The plant genome’s methylation status and response to stress:
implications for plant improvement
Lewis N Lukens and Shuhua Zhan
Plant improvement depends on generating phenotypic
variation and selecting for characteristics that are heritable.
Classical genetics and early molecular genetics studies on
single genes showed that differences in chromatin structure,
especially cytosine methylation, can contribute to heritable
phenotypic variation. Recent molecular genetic and genomic
studies have revealed a new importance of cytosine
methylation for gene regulation and have identified RNA
interference (RNAi)-related proteins that are necessary for
methylation. Methylation differences among plants can be
caused by cis- or trans-acting DNA polymorphisms or by
epigenetic phenomena. Although regulatory proteins might be
important in creating this variation, recent examples highlight
the central role of transposable elements and DNA repeats in
generating both genetic and epigenetic methylation
polymorphisms. The plant genome’s response to
environmental and genetic stress generates both novel genetic
and epigenetic methylation polymorphisms. Novel, stressinduced genotypes may contribute to phenotypic diversity
and plant improvement.
Addresses
Department of Plant Agriculture, University of Guelph, Guelph,
Ontario, Canada, N1G2W1
Corresponding author: Lukens, Lewis N ([email protected])
Current Opinion in Plant Biology 2007, 10:317–322
This review comes from a themed issue on
Physiology and metabolism
Edited by Clint Chapple and Malcolm M Campbell
Available online 30th April 2007
1369-5266/$ – see front matter
# 2007 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2007.04.012
Introduction
The genetic improvement of plants requires that individuals differ for traits and that these traits can be passed
on from one generation to the next. DNA methylation can
generate novel and heritable phenotypic variation by
influencing gene expression. DNA polymorphisms in
cis or trans elements that trigger cytosine methylation
can generate methylation polymorphisms. Alternatively,
identical alleles may take on different methylation states.
Environmental and genetic perturbations induce the
novel genetic and epigenetic changes that trigger methylation. This review describes recent papers that have
uncovered the regulatory control of cytosine methylation
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and the plasticity of cytosine methylation. It focuses on
studies that have linked methylation variation with trait
variation at the single gene and genome scales. Methylation polymorphisms are likely an important source of
novelty for crop improvement.
Cytosine methylation: RNAi targeting and
function
Cytosine methylation of DNA in plants occurs at CpG,
CpNpG (where N is any nucleotide), and asymmetric
CpHpH sites (where H is adenine [A], cytosine [C], or
thymine [T]). Several of the proteins that are necessary
for de novo and maintenance methylation at CpG,
CpNpG, and CpHpH sites are components of the RNAi
complex [1]. De novo methylation in Arabidopsis thaliana
involves the DOMAINS REARRANGED METHYLASE (DRM) methylases (DRM1 and DRM2) [2,3];
components of a short interfering RNA (siRNA) metabolizing pathway, including RNA-DEPENDENT RNA
POLYMERASE 2 (RDR2), DICER-LIKE3 (DCL3),
SILENCING DEFECTIVE4 (SDE4), and ARGONAUTE4 (AGO4) [4]; and the putative SNF2-containing
chromatin remodeling protein DRD1 [5,6]. CpG methylation is propagated by the DNA METHYLTRANSFERASE 1 (MET1), which methylates hemi-methylated
sites after DNA replication [7]. CpG maintenance methylation also can require HISTONE DEACETYLASE6
(HDA6) [8] and DNA METHYLATION 1 (DDM1), a
SWI2/SNF2-like chromatin remodeling enzyme that
is capable of modifying nucleosomes [9]. Unlike the
maintenance of CpG methylation, the maintenance of
non-CpG methylation requires active targeting of the
DNA following each replication cycle [10]. Maintenance
of CpNpG and asymmetric site methylation can require
AGO4, a potential component of the RNA-induced
silencing complex (RISC); the Su(var)3-9 homologue
4 (SUVH4) histone3 lysine 9 methyltransferase (also
known as ‘‘KRYPTONITE’’); and the DNA methyltransferases chromomethylase3 (CMT3), DRM1 and DRM2.
The bifunctional DNA glycosylase/lyase REPRESSOR
OF SILENCING1 (ROS1) actively removes DNA methylation by a base-excision repair mechanism [11,12].
In plants, DNA methylation contributes to the transcriptional silencing of transposable elements or foreign DNA,
maintaining genome stability against non-homologous
recombination and controlling the transcription of a number of genes. Recent surveys of genome methylation and
gene expression have stressed the importance of methylation to gene regulation. Lippman et al. [13] hybridized
a methylated fraction of wild-type and ddm1 A. thaliana
Current Opinion in Plant Biology 2007, 10:317–322
318 Physiology and metabolism
genomic DNA to a tiling array representing a knob and
surrounding euchromatic sequence. Although the ddm1
mutation does not usually affect genic methylation, a
decrease in CpG DNA methylation in the ddm1 mutant
caused the activation of a small number of genes within
the knob. Hybridization of the methylated fraction of
DNA to a genome-wide tiling array suggested two regulatory roles for methylation. First, genes that have promoter-specific methylation have an unusually high level
of tissue-specific expression [14]. Consistent with
this finding, Jiao et al. [15] identified transposon-related
gene models in rice heterochromatic regions that were
more highly expressed in mature organs than in juvenile-stage organs. Second, surprisingly, genes that were
methylated within their coding sequences tended to be
highly expressed [14]. Tran et al. [16] also identified
regions of dense CpG methylation within scattered sites
throughout the genome that were preferentially associated
with genes. The importance of cytosine methylation to
genome structure has also been observed microscopically.
In interphase nuclei of A. thaliana, the structure of
euchromatic loops and heterochromatic chromocenters
varies among cells, and this structure is disrupted
in CpG-deficient genomes [17]. Cytosine methylation
could explain the tendency for gene neighbors to be
expressed and repressed together across growth conditions
(e.g. [18]).
DNA sequence polymorphisms targeted by
siRNA generate methylcytosine variation
Variation for cis-acting transposons and direct repeats can
cause one genotype to have methylation at loci that are
not methylated within a second genotype. RNAi components are required to maintain these differences. For
example, the A. thaliana Landsberg erecta (Ler) accession
is early flowering relative to the other accessions, in part
because the FLOWERING LOCUS C (FLC) transcription factor, which represses flowering, is expressed at low
levels in Ler. This low level of expression is due to the
insertion of a Mutator-like transposable element in the
first intron of the Ler FLC gene, and requires functional
siRNA metabolism [19]. Within the ddm1 mutant, an
upstream Vandal transposable element probably activates
a gene within a heterochromatic knob [13]. The Zea mays
Booster (B1) gene encodes a transcription factor that
activates the anthocyanin pathway and causes pigmentation throughout the plant. Some B1 alleles have seven
direct repeats of an 853-bp sequence located 100 kb
upstream of the B1-coding sequence whereas others do
not. The b-1 allele has a single copy of the sequence. The
direct repeats generate phenotypic diversity because
their methylation is associated with high levels of B1
expression and enhanced plant pigmentation. Low levels
of methylation are associated with high levels of B1
expression and the generation of purple plants [20]. A
RNA-dependent RNA polymerase (RDRP) is required
for the B1 repeats to influence gene expression [21].
Current Opinion in Plant Biology 2007, 10:317–322
Environmental and genetic stimuli can influence transposons and generate genetic diversity for cis-acting elements.
In Antirrhinum majus (snapdragon), nivea encodes a chalcone synthase and is necessary for flower pigmentation.
One line of A. majus is homozygous for the nivearecurrens:Tam3
allele. Within this allele, a Tam3 transposable element is
located near the nivea promoter. At high temperatures, the
element is stable and highly methylated, and the plants
have white or ivory flowers. At low temperatures, the
element excises at high frequency and has reduced methylation, and plants have flowers with red pigmentation
[22,23]. Imprecise excision of Tam3 also generates regulatory sequence novelty [24]. Additional environmental
stimuli induce transposable element activity [25,26].
The stress-induced amplification of a Tourist-like miniature
inverted-repeat transposable element (MITE) in the
temperate rice subspecies Oryza sativa japonica might
have contributed to its phenotypic diversity [27]. Crosses
between genetically distinct individuals can also influence
transposon activity. For example, allopolyploidization in a
number of species has been associated with transposable
element activity [28,29].
Trans-acting sequences can also generate genetic variation in cytosine methylation. For example, in the
A. thaliana accession WS, two phosphoribosylanthranilate
isomerase genes (PAI1 and PAI4) form an inverted repeat.
Transcription of this repeat generates a double-stranded
RNA (dsRNA) signal for cytosine methylation and causes
the methylation of the repeat itself and of two unlinked
PAI genes (PAI2 and PAI3) [30,31]. Within a segregating
population derived from two parents that differ for
nucleolus organizer region (NOR) cytosine methylation,
both cis and trans factors influence levels of NOR methylation [32]. Interestingly, in one cross, one of the two
NORs accounted for nearly all of the segregating NOR
methylation differences within the population [33]. Several proteins establish or maintain cytosine methylation
at particular sequences [5,12,34,35]. For example,
mutations in the Su(var)3-9 homologue 4 (SUVH4)/kryptonite H3K9 methyltransferase reduce methylation at
PAI2 and PAI3, but do not affect the methylation of
the inverted repeat [36]. Mutations in both SUVH4
and SUVH6 reduce the methylation of the inverted
repeat [37]. Allelic variation of these proteins could
potentially contribute to variation in methylcytosine patterns across different genotypes.
The influence of methylation on crop development has
been observed in species such as flax [38]. A small number
of studies suggest that crop genotypes that avoid cytosine
methylation might be agriculturally superior to those
genotypes that are sensitive to methylation. For example,
the yield of maize in central Iowa, United States, when
planted at low density has remained largely unchanged
since 1940, but the yield of maize when planted at high
density has steadily increased [39]. A study of a small
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Genome’s methylation status and response to stress Lukens and Zhan 319
number of loci found that high-density planting induced
methylation more within low-yielding inbred lines than
within high-yielding hybrid lines [40]. Guo et al. [41]
found that the proportion of genes that are additively
expressed is higher within a new density-tolerant maize
hybrid than within an old density-sensitive hybrid, consistent with the maintenance of parental transcriptional
programs.
Genetic variation for cytosine methylation:
epigenetic changes
Differences in DNA methylation within a single genotype can also contribute to heritable trait differences that
can be selected. In maize, alleles of B1 and the pericarp
color gene P1, another transcriptional regulator of the
flavonoid biosynthetic pathway, can have identical
sequences but different effects on gene expression and
pigment production. The B0 allele stably silences the B-I
allele and converts it to B0 . The tandem array of seven
repeats located 100 kb upstream of the B1 locus
(described above) is necessary both to enhance B1 expression (giving rise to the B-I allele) and to silence B1
expression (giving rise to the B0 allele) [20]. Alleles of
the P1 myb-like transcription factor gene are designated
by a two-letter suffix that denotes the presence or absence
of pigmentation in the kernal pericarp (similar to a seed
coat) and the cob. P-pr alleles generate plants with
patterned pericarps and red cobs and are derived from
a P-rr allele, which generates plants with red pericarps
and red cobs [42]. DNA methylation is increased in P-pr
plants relative to P-rr plants, and P-pr alleles were inherited as moderately stable Mendelian loci.
Trait differences that are caused by methylation are also
observed within natural populations. Cubas et al. [43]
found an epigenetic mutation within a naturally occurring
population of Linaria vulgaris (toadflax) that had originally
been described by Linnaeus. The mutant plants have
radial flowers whereas wildtype plants have bilaterally
symmetrical flowers. A methylated allele of the
TEOSINTE BRANCHED1, CYCLOIDEA and PCF
(TCP) transcription factor gene co-segregates with the
radial phenotype, and the mutant and wildtype have
only a single sequence polymorphism within about
1 kb of upstream sequence [43]. As described above, the
gene responsible for the epigenetic silencing of B, mediator
of paramutation1 (mop1), was recently cloned and shown to
be an RNA-dependent RNA polymerase. This result
strongly suggests that a siRNA-mediated transcriptional
gene silencing pathway, as well as transposons and other
non-coding repeats, acts to effect epigenetic changes
[21].
Epigenetic changes can occur at a high frequency in crop
plants and might generate phenotypic variation that is not
correlated with genetic variation. In a recent study, a
population of 49 Brassica napus rapeseed allopolyploids
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were re-synthesized by crossing two isogenic parents and
doubling the amphihaploid genomes of the S0 plants.
These plants were self-pollinated, and the frequency of
methylation and genomic differences were surveyed
among the S1. CpNpG methylation differences between
parental and S1 genomes were very rare. (CpNpG
changes occurred in only two of more than 14 000 comparisons between polyploid plants and the diploid
parents.) By contrast, over 500 comparisons identified
CpG methylation polymorphisms. The CpG methylation
status at some loci was targeted and changed at high
frequency, whereas CpG methylation at other loci never
changed [44]. Although methylation changes do not
occur at a high frequency in newly synthesized cotton
[45], Keyte et al. [46] examined cytosine methylation in
several Gossypium hirsutum (cotton) accessions. The
genetic diversity for cytosine methylation polymorphism
was greater than the diversity for DNA polymorphism
[46]. Similarly, there are numerous cytosine methylation
polymorphisms between different rice cultivars, and the
number of methylation differences is not correlated with
genetic distance [47]. Similar results were found using
A. thaliana accessions [48].
Meiotically heritable epialleles are inherited in a Mendelian fashion but revert at some frequency in subsequent
generations ([42,43]; C Pires, pers. comm.). In the context
of plant improvement, one desires to generate novel
variation in elite germplasm from which to select, but
the selected trait should be stably inherited thereafter.
Nonetheless, stable epigenetic events might be important in breeding. For example, maize geneticists had
isolated a series of P-rr alleles based on the red pericarp
and red cob phenotype [49]. Surprisingly, Cocciolone
et al. [50] found that the DNA sequence of many P-rr
alleles was identical to or only slightly different from that
of the P-wr (white pericarp/red cob) allele. The standard
P-rr allele is a single copy gene, but P-wr has six copies
[51]. As expected, the P-wr sequences that caused the
P-rr phenotype were consistently less methylated than
the P-wr sequence that caused the P-wr phenotype.
Additional evidence that epigenetic changes might be
important for selection comes from population studies.
Although there are a large number of methylation differences among cultivars, individuals from the same cultivar
or accession have remarkably stable methylation patterns
[47,48]. This pattern of diversity suggests that selection
has maintained fixed methylation patterns within the
different cultivars.
Environmental and genetic stimuli that induce methylation changes within a plant’s lifecycle could also create
novel epigenetic variation and affect the subsequent
generation. Because a plant’s reproductive cell lineage
is derived from somatic tissue late in development,
genomic changes that occur during a plant’s lifecycle
can be transmitted to its progeny. Several environmental
Current Opinion in Plant Biology 2007, 10:317–322
320 Physiology and metabolism
and genetic stimuli are known to alter methylation [52].
Steward et al. [53] identified a Z. mays transcript, ZmMI1,
that encodes part of the coding region of a putative
protein and part of a retrotransposon-like sequence.
ZmMI1 was transcribed and hypomethylated at both
CpG and CpNpG sites during a 4 8C chilling treatment.
Interestingly, the methylation was not reinitiated after
the plants were returned to warm growth conditions [53].
(By contrast, in tobacco cell culture, changes in heterochromatin CpNpG methylation occurred in response to
osmotic stress and were reversible [54].) Environmental
stimuli such as aluminum [55], heavy metals [56], and
water stress can also cause an increase or decrease in
cytosine methylation throughout the genome and at
specific loci [57]. Genetic stimuli such as the intra- or
inter-specific hybridization of plants also affect cytosine
methylation in maize, rice, and wheat [40,58,59]. Interestingly, Lauria et al. [60] found no CpG or CpNpG
methylated sites in the nuclear genome that differed
between F1 maize hybrid plants and their parents,
although a large number of genes were differentially
methylated in the endosperm. The use of HpaII, a
restriction enzyme that is sensitive to CpG and CpNpG
methylation, to survey cytosine methylation might help
to explain this result. Most of the non-parental methylation patterns detected in rice, for example, were due to
the loss of parental MspI fragments; MspI fails to cleave
methylated CpNpG sites.
recruit RNAi machinery and cause methylation differences. These, in turn, influence gene expression and
plant traits. Epigenetic differences that generate trait
diversity within the same genotype also involve methylation and also are associated with RNAi. Remarkably,
environmental and genetic factors stimulate both novel
epigenetic and genetic changes that alter methylation
patterns. Several crops have a very narrow germplasm but
are adapted to a wide range of growing conditions (e.g.
[64]). It is tempting to think that novel methylation
variation has helped and will continue to help in plant
breeding and diversification.
Acknowledgements
We thank Dr Orlene Guerra Peraza for his discussions about this article
and the Natural Sciences and Engineering Research Council of Canada
for research funding.
References and recommended reading
Papers of particular interest, published within the period of review,
have been highlighted as:
of special interest
of outstanding interest
1. Matzke MA, Birchler J: RNAi mediated pathways in the nucleus.
Nat Rev Genet 2005, 6:24-35.
This excellent review describes the involvement of RNAi-related processes in directing DNA methylation, heterochromatin formation and
DNA elimination. The review also discusses how RNAi silences unpaired
DNA regions during meiosis.
2.
Cao X, Jacobsen SE: Role of the Arabidopsis DRM
methyltransferases in de novo DNA methylation and gene
silencing. Curr Biol 2002, 12:1138-1144.
3.
Cao X, Aufsatz W, Zilberman D, Mette MF, Huang M, Matzke M,
Jacobsen S: Role of DRM and CMT3 methyltransferases in
RNA directed DNA methylation. Curr Biol 2003, 13:2212-2217.
4.
Chan SW, Zilberman D, Xie Z, Johansen L, Carrington J,
Jacobsen S: RNA silencing genes control de novo DNA
methylation. Science 2004, 303:1336.
5.
Kanno T, Mette M, Kreil D, Aufstaz W, Matzke M, Matzke A:
Involvement of a putative SNF2 chromatin remodeling protein
DRD1 in RNA-directed DNA methylation. Curr Biol 2004,
14:801-805.
Mechanistically, genetic or environmental stimuli might
influence chromatin by producing or removing epigenetic
‘marks’ that guide RNA-mediated DNA methylation.
After the mark has been modified, the methylation status
is faithfully replicated. Genetic analyses of the RNAi
pathway suggest that sequences do have epigenetic
marks that target them for methylation. Genomic regions
that are hypomethylated within the A. thaliana ddm1 or
met1 mutants remain hypomethylated when introduced
into a wild-type background [61,62]. Similarly, a FWA
transgene is methylated in wild-type DRM1 DRM2 A.
thaliana. By contrast, the transgene is not methylated in a
drm1 drm2 double mutant, and the construct remains
unmethylated when crossed into a wild-type plant [4].
Perhaps genetic or environmental stimuli influence such
an epigenetic mark. Recently, it was shown that treatment of plants with flagellin or UV-B light caused heritable increases in the frequency of homologous
recombination — it would be fascinating to see if methylation changes contribute to this change [63].
6.
Kanno T, Aufsatz W, Jaligot E, Mette MF, Matzke M, Matzke A: A
SNF2-like protein facilitates dynamic control of DNA
methylation. EMBO Rep 2005, 6:649-655.
This report describes an interesting dual role for the chromatin remodeling protein DRD1. DRD1 is required for de novo methylation and also
facilitates a loss of CG methylation when a RNA silencing signal is
withdrawn by segregation.
7.
Chan SW, Henderson I, Jacobsen SE: Gardening the genome:
DNA methylation in Arabidopsis thaliana. Nat Rev Genet 2005,
6:351-360.
8.
Probst AV, Fagard M, Proux F, Mourrain P, Boutet S, Earley K,
Lawrence R, Pikaard C, Murfett J, Furner I et al.: Arabidopsis
histone deacetylase HDA6 is required for maintenance of
transcriptional gene silencing and determines nuclear
organization of rDNA repeats. Plant Cell 2004, 16:1021-1034.
Conclusions
9.
Plant improvement depends on generating novel genetic
diversity and upon selecting that diversity to obtain
improved heritable types. Methylation differences contribute to natural heritable variation. DNA sequence
polymorphisms, such as the presence or absence of transposable elements and repeats in cis with a target gene,
Brzeski J, Jerzmanowski A: Deficient in DNA methylation 1
(DDM1) defines a novel family of chromatin-remodeling
factors. J Biol Chem 2003, 278:823-828.
10. Cao X, Jacobsen SE: Locus specific control of asymmetric and
CpNpG methylation by the DRM and CMT3 methyltransferase
genes. Proc Natl Acad Sci USA 2002, 99:16491-16498.
Current Opinion in Plant Biology 2007, 10:317–322
11. Gong Z, Morales-Ruiz T, Ariza R, Roldan-Arjona T, David L,
Zhu JK: Ros1, a repressor of transcriptional gene silencing in
www.sciencedirect.com
Genome’s methylation status and response to stress Lukens and Zhan 321
Arabidopsis, encodes a DNA glycosylase/lyase. Cell 2002,
111:803-814.
12. Kapoor A, Agius F, Zhu JK: Preventing transcriptional gene
silencing by active DNA demethylation. FEBS Lett 2005,
579:5889-5898.
This paper reviews the evidence that the A. thaliana glycosylase/lyase
ROS1 causes DNA demethylation. Both genetic and molecular studies
suggest that DNA is actively demethylated through a ROS1-mediated
base excision repair mechanism. The authors suggest that ROS1 activity
might help explain why siRNAs differ in their ability to cause transcriptional gene silencing.
13. Lippman Z, Gendel A, Black M, Vaughn M, Dedhia N,
McCombie R, Lavine K, Mittal V, May B, Kasschau K et al.: Role of
transposable elements in heterochromatin and epigenetic
control. Nature 2004, 430:471-477.
14. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan S, Chen H,
Henderson I, Shinn P, Pellegrini M, Jacobsen S, Ecker J: Genomewide high resolution mapping and functional analysis of DNA
methylation in Arabidopsis. Cell 2006, 126:1189-1201.
The authors fractionated methylated and unmethylated A. thaliana DNA
by methylcytosine immunoprecipitation and generated a comprehensive
DNA methylation map of the plant genome by hybridizing to a wholegenome tiling array. As expected, heterochromatic, siRNA producing,
and repetitive sequences were heavily methylated. Surprisingly, cytosine
methylation was found in genes that were highly transcribed. Cytosine
methylation was rare in promoters and favored genes that have tissuespecific expression. The expression levels of large number of genes
changed in methyltransferase mutant backgrounds.
15. Jiao Y, Jia P, Wang X, Su N, Yu S, Zhang D, Ma L, Feng Q, Jin Z,
Li L et al.: A tiling microarray expression analysis of rice
chromosome 4 suggests a chromosome-level regulation of
transcription. Plant Cell 2005, 17:1641-1657.
16. Tran RK, Henikoff J, Zilberman D, Ditt R, Jacobsen S, Henikoff S:
DNA methylation profiling identifies CpG methylation clusters
in Arabidopsis genes. Curr Biol 2005, 15:154-159.
17. Fransz P, Soppe W, Shubert I: Heterochromatin in interphase
nuclei of Arabidopsis thaliana. Chromosome Res 2003,
11:227-240.
18. Zhan S, Horrocks J, Lukens L: Islands of co-expressed
neighbouring genes in Arabidopsis thaliana suggest higherorder chromosome domains. Plant J 2006, 45:347-357.
19. Liu J, He Y, Amasino R, Chen X: siRNAs targeting an intronic
transposon in the regulation of natural flowering behavior in
Arabidopsis. Genes Dev 2004, 18:2873-2878.
20. Stam M, Belele C, Dorweiler J, Chandler VL: Differential
chromatin structure within a tandem array of 100 kb upstream
of the maize b1 locus is associated with paramutation.
Genes Dev 2002, 16:1906-1918.
21. Alleman M, Sidorenko L, McGinnis K, Seshadri V, Dorweiler JE,
White J, Sikkink K, Chandler VL: An RNA dependent RNA
polymerase is required for paramutation in maize. Nature 2006,
442:295-298.
Paramutation results in the heritable silencing of one allele by another.
This work demonstrates that paramutation of the B-I allele in maize by B0
depends on a RDRP. The RDRP is most similar to RDR2 of A. thaliana,
which is involved in siRNA-mediated transcriptional silencing.
22. Hashida SN, Kitamura K, Mikami T, Kishima Y: Temperature shift
co-ordinately changes the activity and methylation state of
transposon Tam3 in Antirrhinum majus. Plant Physiol 2003,
132:1207-1216.
23. Hashida SN, Uchiyama U, Martin C, Kishima Y, Sano Y, Mikami T:
The temperature dependent change in methylation of the
Antirrhinum transposon TAM3 is controlled by the activity of
its transposase. Plant Cell 2006, 18:104-118.
24. Almeida J, Carpenter R, Robbins TP, Martin C, Coen ES: Genetic
interactions underlying flower color patterns in Antirrhinum
majus. Genes Dev 1989, 3:1758-1767.
25. Walbot V: Reactivation of Mutator transposable elements of
maize by ultraviolet light. Mol Gen Genet 1992, 234:353-360.
26. Grandbastien MA, Audeon C, Bonnivard E, Casacuberta JM,
Chalhoub B, Costa AP, Le Q, Melayah D, Petit M, Poncet C et al.:
www.sciencedirect.com
Stress activation and genomic impact of Tnt1
retrotransposons in Solanaceae. Cytogenet Genome Res 2005,
110:229-241.
27. Jiang N, Bao Z, Zhang X, Hirochika H, Eddy S, McCouch S,
Wessler S: An active DNA transposon family in rice.
Nature 2003, 421:163-167.
28. Liu B, Wendel J: Non-Mendelian phenomena in allopolyploid
genome evolution. Curr Genomics 2002, 3:489-505.
29. Lukens L, Quijada P, Udall J, Pires C, Schranz E, Osborn T:
Genome redundancy and plasticity within ancient and recent
Brassica crop species. Biol J Linnean Soc 2004, 82:665-674.
30. Luff B, Pawlowski L, Bender J: An inverted repeat triggers
cytosine methylation of identical sequences in Arabidopsis.
Mol Cell 1999, 3:505-511.
31. Melquist S, Bender J: An internal rearrangement in an
Arabidopsis inverted repeat locus impairs DNA methylation
triggered by the locus. Genetics 2004, 166:437-448.
32. Riddle NC, Richards E: The control of natural variation in
cytosine methylation in Arabidopsis. Genetics 2002,
162:355-363.
33. Riddle NC, Richards E: Genetic variation in epigenetic
inheritance of ribosomal RNA gene methylation in
Arabidopsis. Plant J 2005, 41:524-532.
34. Zilberman D, Cao X, Jacobsen S: Argonaute4 control of locus
specific siRNA accumulation and DNA and histone
methylation. Science 2003, 299:716-719.
35. Xie Z, Johansen L, Gustafson A, Kasschau K, Lellis A, Zilberman D,
Jacobsen S, Carrington J: Genetic and functional diversification
of small RNA pathways in plants. PLOS Biol 2004, 2:0642-0651.
36. Malagnac F, Bartee L, Bender J: An Arabidopsis SET domain
protein required for maintenance but not establishment of
DNA methylation. EMBO J 2002, 21:6842-6852.
37. Ebbs ML, Bartee L, Bender J: H3 Lysine 9 methylation is
maintained on a transcribed inverted repeat by combined
action of SUVH6 and SUVH4 methyltransferases.
Mol Cell Biol 2005, 25:10507-10515.
38. Fieldes M, Schaeffer S, Krech M, Brown J: DNA hypomethylation
in 5-azacytidine-induced early flowering lines of flax.
Theor Appl Genet 2005, 11:136-149.
39. Duvick DN, Cassman KG: Post-green revolution trends in yield
potential of temperate maize in the North-Central United
States. Crop Sci 1999, 39:1622-1630.
40. Tani E, Polidoros AN, Nianiou-Obeidat I, Tsaftaris AS: DNA
methylation patterns are differentially affected by planting
density in maize inbreds and their hybrids. Maydica 2005,
50:19-23.
41. Guo M, Rupe M, Yang X, Crasta O, Zinselmeier C, Smith O,
Bowen B: Genome-wide transcript analysis of maize hybrids:
allelic additive gene expression and yield heterosis.
Theor Appl Genet 2006, 113:831-845.
This report utilizes both field trials and expression analyses to study gene
regulation in several hybrid maize lines. The authors find that the proportion of allelic, additively expressed genes within a hybrid is positively
associated with its yield and heterosis. Hybrids with genes that were
biased toward the expression level of the paternal parent tended to have
lower yields and heterosis.
42. Das OP, Messing J: Variegated phenotype and developmental
methylation changes of a maize allele originating from
epimutation. Genetics 1994, 136:1121-1141.
43. Cubas P, Vincent C, Coen E: An epigenetic mutation
responsible for natural variation in floral symmetry.
Nature 1999, 401:157-161.
44. Lukens LN, Pires JC, Leon E, Vogelzang R, Oslach L, Osborn T:
Patterns of sequence loss and cytosine methylation within a
population of newly resynthesized Brassica napus
allopolyploids. Plant Physiol 2006, 140:336-348.
To measure the frequency of genomic rearrangements and methylation
changes that occur in response to wide crosses, 49 distinct synthetic
allopolyploids were generated from double haploid Brassica parents, and
Current Opinion in Plant Biology 2007, 10:317–322
322 Physiology and metabolism
genomic and methylation changes were surveyed in the S1 generation.
The authors show that genomic rearrangements and CpNpG changes are
rare within the S1. CpG changes are much more frequent and often occur
at the same loci across different lines.
56. Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S:
Specific hypomethylation of DNA is induced by heavy metals
in white clover and industrial hemp. Physiol Plant 2004,
121:472-480.
45. Liu B, Brubaker CL, Mergeai G, Cronn R, Wendel JF: Polyploid
formation in cotton is not accompanied by rapid genomic
changes. Genome 2001, 44:321-330.
57. Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, RuffiniCastiglione M, Bracale M: Analysis of cytosine methylation
pattern in response to water deficit in pea root tips.
Plant Biol 2002, 4:694-699.
46. Keyte AL, Percifield R, Liu B, Wendel JF: Infrapspecific DNA
methylation polymorphism in cotton (Gossypium hirsutum).
J Hered 2006, 97:444-450.
47. Ashikawa I: Surveying CpG methylation at 50 -CCGG in the
genomes of rice cultivars. Plant Mol Biol 2001, 45:31-39.
58. Xiong LZ, Xu C, Saghai Maroof MA, Zhang Q: Patterns of
cytosine methylation in an elite rice hybrid and its parental
lines, detected by methylation sensitive amplification
polymorphism technique. Mol Gen Genet 1999,
261:439-446.
48. Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM: Analysis of
DNA methylation in Arabidopsis thaliana based on
methylation-sensitive AFLP markers. Mol Genet Genomics
2002, 268:543-552.
59. Shaked H, Kashkush K, Ozkan H, Feldman M, Levy A: Sequence
elimination and cytosine methylation are rapid and
reproducible responses of the genome to wide hybridization
and allopolyploidy in wheat. Plant Cell 2001, 13:1749-1759.
49. Brink RA, Styles D: A collection of pericarp factors.
Maize Genet Coop Newsletter 1966, 40:149-160.
60. Lauria M, Rupe M, Guo M, Kranz E, Pirona R, Viotti A, Lund G:
Extensive maternal DNA hypomethylation in the endosperm of
Zea mays. Plant Cell 2004, 16:510-522.
50. Cocciolone SM, Chopra S, Flint-Garcia S, McMullen M,
Peterson T: Tissue-specific patterns of a maize Myb
transcription factor are epigenetically regulated. Plant J 2001,
27:467-478.
51. Chopra S, Athma P, Li X, Peterson T: A maize Myb homolog is
encoded by a multicopy gene complex. Mol Gen Genet 1998,
260:372-380.
52. Madlung A, Comai L: The effect of stress on genome regulation
and structure. Ann Bot 2004, 94:481-495.
61. Kankel M, Ramsey D, Stokes T, Flowers S, Haag J, Jeddeloh J,
Riddle N, Verbsky M, Richards E: Arabidopsis met1 cytosine
methyltransferase mutants. Genetics 2003, 163:1109-1122.
62. Kakutani T, Munakata K, Richards EJ, Hirochika H: Meiotically
and mitotically stable inheritance of DNA hypomethylation
induced by ddm1 mutation of Arabidopsis thaliana.
Genetics 1999, 151:831-838.
54. Kovarik A, Koukalova B, Bezdek M, Opatrny Z: Hypermethylation
of tobacco heterochromatic loci in response to osmotic
stress. Theor Appl Genet 1997, 95:301-306.
63. Molinier J, Ries G, Zipfel C, Hohn B: Transgeneration memory of
stress in plants. Nature 2006, 442:1046-1049.
Using a b-glucuronidase (GUS)-based construct that allows for quantification of somatic homologous recombination, the authors found that
plants treated with UV light and flagellin had higher rates of homologous recombination. High rates of recombination persisted in subsequent generations and did not depend on the presence of the
construct.
55. Choi CS, Sano H: Abiotic-stress induced demethylation and
transcriptional activation of a gene encoding a
glycerophosphodiesterase-like protein in tobacco plants.
Mol Genet Genomics 2007, in press.
64. Hyten DL, Song Q, Zhu Y, Choi I, Nelson R, Costa J, Specht J,
Shoemaker RC, Cregan PB: Impacts of genetic bottlenecks on
soybean genome diversity. Proc Natl Acad Sci USA 2006,
103:16666-16671.
53. Steward N, Ito M, Yamaguchi Y, Koizumi N, Sano H: Periodic DNA
methylation in maize nucleosomes and demethylation by
environmental stress. J Biol Chem 2002, 277:37741-37746.
Current Opinion in Plant Biology 2007, 10:317–322
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