Weigel and Colot Genome Biology 2012, 13:249

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REVIEW

Epialleles in plant evolution

Detlef Weigel1,* and Vincent Colot2,3,4,*

differences in the underlying DNA sequence. In eukary-

Abstract otes, most known epigenetic mechanisms are chromatin
Heritable phenotypic differences caused by epigenetic based, and may involve still poorly defined combinations
modifications, rather than DNA sequence mutations, of post-translational histone modifications and histone
pose a challenge to our understanding of natural variants, small or long non-coding RNAs, and DNA
variation. Here, we review what is known about plant methylation [9]. Although the role of epigenetic processes
epialleles and the role of epigenetics in evolution. in development is now well established, the field that
Keywords DNA methylation, epialleles, epigenetics, investigates the transgenerational inheritance of epi-
genetics, plant evolution genetic modifications is still in its infancy.

Natural epialleles in plants

The first natural plant mutant for which the molecular
Introduction basis was determined to be an epimutation rather than a
In college, biologists learn how Darwin and Mendel, change in DNA sequence was a peloric variant of
whose ideas eventually resulted in the modern evolu- toadflax, Linaria vulgaris. Whereas flax normally has
tionary synthesis [1], prevailed over Lamarck and bilaterally symmetrical flowers, the flowers of this variant
Lysenko. Now, from a cursory reading of the literature, it show radial symmetry, a phenotype strikingly similar to
is possible to get the impression that this is changing the one seen in induced cycloidea (cyc) mutants of
[2-4]. But, although epigenetics is clearly enriching snapdragon, Antirrhinum majus [10]. Isolation of a cyc
modern genetic research, reports of the end of genetics homolog from flax revealed that it was genetically linked
have - in our opinion - been an exaggeration. Since the to the peloric phenotype, and that RNA of the cyc
1990s, the molecular basis of hundreds of naturally homolog did not accumulate in the peloric strain [11].
occurring phenotypic variants has been identified in crop The open reading frame of cyc, however, appeared intact,
or wild species and, overwhelmingly, DNA sequence and on DNA blots no gross differences could be detected
differences are involved (for example, [5-7]). Indeed, the around the gene. In contrast, analysis with DNA-methy-
number of natural epialleles that we know of in plants is lation-sensitive restriction enzymes provided evidence
only about a dozen. However, it is very likely that there is for increased methylation of the cyc locus. A direct
an ascertainment bias in favor of DNA sequence changes relationship between DNA methylation and reduced cyc
in the studies carried out so far. Thus, the extent to which expression was deduced from the analysis of spontaneous
epigenetic variation contributes to phenotypic variation somatic revertants ranging in phenotype from semi-
in plants is still not known with certainty. peloric to near wild type. In these plants, DNA methyla-
Epigenetics was a term coined by Waddington, to tion was reduced, which also confirmed that the open
reflect - in modern terms - the causal mechanisms that reading frame was indeed intact and functional. Notably,
lie between genes and phenotypes [8]; however, today it demethylation was less pronounced in semi-peloric than
is mainly used to describe modifications that cause in near-wild-type flowers, both supporting a direct
changes in gene expression that are stably transmitted relationship between DNA methylation and gene expres-
during mitosis or meiosis, but that do not involve sion, and confirming that DNA methylation is not
necessarily an all-or-nothing affair [11,12].
*Correspondence: [email protected], [email protected] A second example of a natural epimutation is provided
1
Department of Molecular Biology, Max Planck Institute for Developmental by the colorless nonripening (CNR) locus from tomato
Biology, Tübingen, 72076, Germany
2
Ecole Normale Supérieure, Institut de Biologie de l’ENS (IBENS), Paris, F-75005,
[13]. As in the example from flax the causal locus, which
France encodes another type of transcription factor, is intact in
Full list of author information is available at the end of the article the non-ripening strain, but expressed at much lower
levels. Again, there were differences in DNA methylation.
© 2010 BioMed Central Ltd © 2012 BioMed Central Ltd This being a more recent study, the authors were able to
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investigate DNA methylation more quantitatively, using ‘epimutability’ of many genes is ultimately conditioned by
bisulfite sequencing. A block of about 300  bp approxi­ the presence of repeat sequences near or within them,
mately 2 kb upstream of the gene was heavily methylated and is thus likely to differ substantially between geno­
in the non-ripening plants. Strikingly, the Liberto wild- types (Figure 1a).
type background, in which the colorless nonripening
variant was found, was also quite highly methylated in Communication between homologous sequences
this region, although not quite as extensively as CNR In A. thaliana, tandem repeats in the promoter are also
plants. In contrast, another wild-type strain, Ailsa Craig, associated with gene silencing, in this case of the FWA
had very low levels of DNA methylation at the locus, gene. In wild-type plants, these repeats are methylated,
even though there were no obvious differences in the except in the triploid endosperm, where the two copies of
DNA sequence. Thus, it is possible to speculate the the maternal allele are demethylated and expressed [21].
Liberto strain is more likely to give rise to Cnr mutant Stable epialleles in which the repeats have become
plants than the Alisa Craig strain. unmethylated throughout the life cycle have been
Within 95 kb around the Cnr locus, the epimutant and obtained either after ethyl methanesulfonate (EMS)
the Liberto parent had no DNA sequence differences. muta­genesis, or in plants that are defective in DNA
Since the final mapping interval of 13  kb was approxi­ methylation. Demethylation in the adult plant leads to
mately in the center of this 95 kb region, it is reasonable activation of FWA and late flowering [22,23]. Once fully
to assume that a nearby structural variation is not unmethylated, these tandem repeats very rarely, if ever,
responsible for the modification of Cnr chromatin [13], become spontaneously re-methylated [22,24]. In contrast,
although such a variant might have provided an initial when an unmethylated copy is transformed into wild-
trigger, as discussed below with respect to FOLT in type plants, its repeats become rapidly methylated, shut­
Arabidopsis thaliana [14]. ting down expression of the transgene, apparently
In contrast to cyc and Cnr, several other epialleles are because of information transfer from the endogenous,
clearly associated with alterations in DNA sequences. methylated copies [25]. Such a communication between
Because DNA methylation may spread outwards from alleles may be widespread [26], but is not observed in
repeats and transposable elements [15-17]  - although it crosses of plants with a methylated and silenced FWA
does not always [18] - structural variants could in fact be allele to plants with an unmethylated, activated copy at
the primary causes of differences in the activity of the endogenous locus, and fwa epimutants therefore
adjacent genes, with DNA methylation playing a secon­ behave like normal mutants (as do the examples dis­
dary or mediating role. One such example is provided by cussed above, with the exception of the reversion events).
melon plants, in which the gynoecious (g) locus is Epigenetic interactions at the FWA locus thus differ
inactive and which therefore produce only female flowers from the classic examples of paramutation in maize, in
[19]. The sequences responsible for loss of g expression which silenced alleles frequently induce silencing of
were mapped to a 1.4-kb non-coding sequence, which normal alleles [27,28] (Figure  1). Nonetheless, as FWA,
contained a DNA transposon insertion in all gynoecious paramutation has been linked to tandem repeats in the
plants tested. The transposon was heavily methylated, promoter of paramutable alleles at the maize b1 locus
and high level DNA methylation was also detected in the [29]. Tandem repeats are seemingly also important for
promoter of the adjacent gene, perhaps as a result of para­mutation at the r1 locus, but in this case they are
spreading from the transposon. However, in a recombi­ apparently much larger, as the r1 locus is a tandem array
nant gene in which the transposon was segregated away, of several very similar genes [30]. In contrast, the role of
DNA methylation was reduced and gene expression was repeats in paramutation at the p1 locus is less clear [31].
increased. Moreover, DNA methylation was much lower Just as information between alleles or between endo­ge­
in phenotypically revertant branches, indicating that the nous genes and transgenes can be transferred (relying on
transposon effects were variable, at least to a certain short interfering RNAs (siRNAs) and the DNA
extent. A similar case has been described for rice plants methylation machinery they recruit [28,32]), there is
with a metastable epiallele at the DWARF1 (D1) locus communication between homologous sequences through­
[20], with a large tandem repeat being responsible for out the genome. The first case reported in A.  thaliana
variable DNA methylation. was that of the PAI family of genes. One natural strain of
Thus, all natural epialleles reported to date and for A.  thaliana has two PAI genes in an inverted tandem
which sequence information is available, have involved a arrangement, plus two more dispersed single copies, and
gain or loss of DNA methylation. Moreover, these differ­ all four genes are heavily methylated [33]. Another strain
ences in DNA methylation are often in transposable has only three single copies, which are not methylated,
elements or other types of repeat sequences located near but which become methylated after a cross to the strain
or within the affected genes. This suggests that the with the inverted tandem copies [18,34].
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Trigger present Trigger absent

(a) ( )

(b)

(c)
Figure 1. Classes of epialleles. (a) Epigenetic modifications and associated silencing of the adjacent gene is dependent on a specific cis-element,
often a repetitive element. (b) Epigenetic modification is triggered by another locus or allele. Once the modification has been established, the
trigger is no longer required for its maintenance. (c) Epigenetic modification is triggered by another locus or allele, but the trigger is permanently
required.

A similar situation, with interesting phenotypic Spontaneous changes in DNA methylation patterns
consequences, is seen at the FOLT1 and FOLT2 loci in The examples discussed so far indicate that changes in
A. thaliana [14]. In one strain, the FOLT2 locus contains DNA methylation patterns are far from random, but that
multiple truncated copies, and siRNAs produced by these they are also not always entirely predictable. To dis­tin­
truncated versions target the intact FOLT1 copy and guish the effects of interactions between different
silence it. Notably, FOLT2 itself escapes complete genomes, and of new structural variants from spon­ta­
silencing, preserving FOLT activity. Another strain lacks neous changes, whole-genome methylation patterns were
the FOLT2 locus, which induces silencing, but has an studied in isogenic A.  thaliana lines [38,39]. Lines were
active FOLT1 copy. When this copy is replaced by the derived from a single progenitor and then propagated in
silenced FOLT1 allele from the other strain through a benign greenhouse environment by single-seed descent.
crossing, plants lack FOLT activity and almost always die After thirty generations, almost 10% of all methylated
[14]. Important for this phenomenon is that FOLT1 stays cytosines in the genome had increased or decreased
silenced even after the FOLT2 locus that induces methylation in at least one out of ten lines examined.
silencing has been segregated away (Figure 1b). In other However, there is little evidence that such differentially
words, FOLT1 may be seen as a ‘pure’ epiallele [35], but methylated positions (DMPs) can have major effects on
without complete information about the history of the the activity of adjacent genes. Rather, it is large contigu­ous
genetic background it has passed through, it is impossible regions of differential methylation (differen­tially methy­
to know whether it reached this state without any lated regions, or DMRs), as in the epialleles dis­cussed
external influence. Genome-wide analyses with genetic above, which normally matter. In contrast to DMPs, there
material derived from crossing closely related tomato were very few DMRs in the studied A.  thaliana lines
species have recently confirmed that such trans inter­ [38,39].
actions are likely to be quite common, and that they may In agreement with what is known about the establish­
underlie many aspects of the superior or inferior perfor­ ment and maintenance of DNA methylation, DMPs were
mances of hybrid plants [36]. An important finding in not randomly distributed. DNA methylation on and near
this case was that silencing was only established gradually - transposons was highly stable, whereas it often changed
similar to what has been observed in A.  thaliana [37]  - over genes and far away from transposons. Moreover, the
which is discussed below. Once com­plete genome same changes were seen much more often than expected
sequences for the tomato lines become available, it will by chance in different lines, indicating that certain sites
also be possible to address systematically the question of are considerably less stable than others. The bias in
whether there are epialleles that are absolutely dependent spontaneous DNA methylation changes parallels what
on a trans-acting trigger (Figure 1c). has been reported for differences between wild strains, in
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Environment Constant Random Episodic

epimutations random induced induced

Generation 0

Generation 1

Generation 2

Generation 3

Generation 4

Figure 2. The potential role of inherited epigenetic changes, comparing the effects of spontaneous and induced epimutations. A
population of genotypically identical individuals is shown, which contain a single locus that can exist in two epigenetic states. Like spontaneous
epimutations, induced epimutations are maintained across generations, but revert randomly without the inducing environment (which almost
never happens for DNA mutations). The epiallele marked in purple is disadvantageous in a normal environment (leading to increased death;
red crosses). In a stress environment (indicated by a thunder bolt), the unmodified allele (shown in grey) is disadvantageous. If the environment
changes randomly from generation to generation, induced epivariation is unlikely to be advantageous. If there are longer episodes of stress,
induced epivariation could be advantageous, and Darwinian selection might favor alleles that can become subject to induced epivariation.
However, formalization is needed to determine the boundary conditions for such a scenario.

which transposon methylation is much more similar than main DNA methyltransferase responsible for maintaining
genic methylation [40]. It is also consistent with trans­ CG methylation in repeat sequences, as well as in gene
poson methylation being under much greater selective bodies. In another case [45], a wild-type individual was
pressure. Loss of DNA methylation has comparatively crossed with a plant mutant for DDM1, which encodes a
few effects on the expression of protein-coding genes, but putative chromatin remodeler involved in maintaining all
it greatly reduces transposon silencing [41-43]. In turn, types of DNA methylation (CG, CHG and CHH), specifi­
active transposons are powerful mutagens. cally over repeat sequences. After the initial cross, a
single F1 individual was either selfed [44], or backcrossed
Lessons from crosses between methylated and to the wild-type parent [45]. F2 progeny homozygous for
demethylated genomes the wild-type MET1 or DDM1 allele were selected, and
Given the frequent implication of repeat elements in the epiRILs were propagated through seven rounds of selfing.
epimutability of genes, an important question is the Analysis of these lines indicated that met1- and ddm1-
extent to which the accidental loss of DNA methylation induced hypomethylation of repeat sequences could be
over transposons and other repeats can be inherited and either stably inherited for at least eight generations or
affect phenotypes. Two experimental studies have pro­ else fully reversed [44,45]. Reversion was mediated by
vided genome-wide answers to this question in small RNAs mainly acting in cis, and often occurred in
A. thaliana [44,45]. Both studies relied on the creation of several steps over successive generations [37]. Moreover,
epigenetic recombinant inbred lines (epiRILs). In one heritable variation for several complex traits was ob­
case [44], the epiRILS were derived from the cross of a served in the epiRILs [44-47], highlighting the potentially
wild-type individual with a near-isogenic plant homozy­ important role of repeat-associated epigenetic changes in
gous for a mutant allele of MET1, which encodes the generating heritable phenotypic diversity.
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Competing interests 12:1447-1451.
The authors declare that they have no competing interests. 23. Soppe WJ, Jacobsen SE, Alonso-Blanco C, Jackson JP, Kakutani T, Koornneef
M, Peeters AJ: The late flowering phenotype of fwa mutants is caused by
Acknowledgments gain-of-function epigenetic alleles of a homeodomain gene. Mol Cell 2000,
Our studies of epigenetic inheritance are supported by the European Union 6:791-802.
FP7 Collaborative Project AENEAS (contract KBBE-2009-226477, to DW), the 24. Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N,
European Union FP7 Network of Excellence Epigenesys (to VC) and the French Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P,
Agence Nationale de la Recherche project EPIMOBILE (to VC). Hospital F, Colot V: Assessing the impact of transgenerational epigenetic
variation on complex traits. PLoS Genet 2009, 5:e1000530.
Author details 25. Chan SW, Zhang X, Bernatavichute YV, Jacobsen SE: Two-step recruitment of
1
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Biology 2012, 13:249.
Lavine K, Mittal V, May B, Kasschau KD, Carrington JC, Doerge RW, Colot V,