The dramatic phenotypes of their silencing are an excellent illustration of epialleles. A more enigmatic example is the generation of over-expressing bal epialleles of the CPR1 constitutive expressor of pathogenesis related proteins 1 locus located in the chromosome 4 Resistance gene cluster in ddm1 mutant backgrounds Stokes and Richards, ; Stokes et al. Surprisingly, these appear to be two different epialleles and neither associated with nucleotide changes. There is also direct evidence that reactivation of transposable elements in the ddm1 background can produce new insertions with phenotypic consequences Miura et al.
Indeed, once activated by ddm1 , transposons can retain their activity even when functional DDM1 is restored Lippman et al. It does not seem too dramatic to suggest that saltational changes in the heritable epigenetic marks and phenotype could arise from even short-term exposure to defective activity of one or a few genes in the epigenetic system.
Environmental and biotic stress may also induce the formation of novel epialleles. Mild inhibition of chaperone activity of the Hsp90 protein in plants by specific pharmacological agents has been shown to produce a diversity of phenotypic changes in Arabidopsis seedlings, such as alterations to plant size, leaf shape and pigmentation Quietsch et al.
When Hsp90 efficiency is reduced, accumulated variation of this kind is rendered non-neutral and alterations to protein function ensue, exposing them to selection Sangster and Queitsch, Definitive genetic proof that the phenotypic effects seen in Arabidopsis are derived in this way has not been presented. Another plausible scenario is that inhibition of full Hsp90 activity can also decrease the functional efficiency of the epigenetic machinery, e. Confirmation that this is the case from molecular epigenetic studies is still lacking. It follows that any environmental insult, such as extreme heat stress, could perturb the activity of epigenetic regulation and heritable effects on epigenetic marks and gene expression changes could arise.
Biotic stress in the form of pathogen attacks may also generate epigenetic aberrations.
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There is evidence that the Bs1 transposable element of maize has been reactivated by viral infection Johns et al. Viral infections may bring about epigenetic changes of this ilk by the virtue of proteins they encode to counteract the defensive RNA pathway machinery of the host plant. The role of these proteins is to inhibit the activity of the defence pathway that destroys viral transcripts, but it also appears that the other RNA pathways are affected.
Dunoyer et al. It seems probable that many of the gross abnormalities of plants infected with viruses forming dsRNA intermediates may be due directly to the upset of miRNA processing that regulates normal development. Evidence for the influence of single epimutations or epialleles on the stable evolution of plant characteristics remains absent, perhaps because changes in DNA sequence during any length of evolutionary time will obfuscate the epigenetic contribution.
Speculation is irresistible though. Chandler and Stam have speculated that paramutation may be a mechanism for transmitting environmentally adapted expression patterns. The adaptive basis of this morphological change is likely to be pollination-based, with Mohavea flowers mimicking the symmetrical flowers of the unrelated Mentzelia in the same desert habitat.
Could epigenetic phenomena have initiated this dramatic shift between two adaptive peaks? Epigenetic explanations may be irresistible for other morphological changes that have repeatedly occurred in plant evolution. The timing of transition from the juvenile vegetative to adult vegetative to reproductive development can differ considerably even between closely related taxa.
Screens for mutations in Arabidopsis genes that alter the timing of these phase changes have revealed several key genes confirmed to be involved in epigenetic processing such as HASTY Bollman et al. Not only does this implicate a number of endogenous small RNA species as essential for controlling the timing of key developmental phase transitions in the life of the plant Peragine et al.
For instance it may take just a few key mutations to generate plants that proceed very rapidly through their life cycle as seen in many desert ephemerals or retain persistently the features of juvenile vegetative growth.
Perhaps the most likely situation where epigenetic changes assist in the generation of an advantageous phenotype is the evolution of apomixis. The evolution of apomixis, in particular autonomous apomixis where an endosperm develops with no paternal genomic contribution, has been seen as problematic to the parent—offspring conflict model Haig and Westoby, As apomixis has evolved repeatedly in the angiosperms, there must be pathways that allow its genesis.
Experimental evidence suggests that alterations in the epigenetic machinery that control gametophyte development, imprinting and endosperm development are the basis of endosperm development without fertilization. Yet none of these mutants promote any substantial development or differentiation of endosperm-like structures. However, loss of function of MET1 , leading to hypomethylation of the maternal gametophyte in fie1 mutants, leads to the production of endosperm more closely resembling sexually derived endosperm Vinkenoog et al.
Recent work by Guitton and Berger has confirmed that these endosperm-like structures are derived from central cells, and report that msi1 mutants also initiate the development of non-viable but polarized, parthenogenetic embryos from the egg cell.
It seems conceivable that full-blown apomixis could evolve from just a few mutations in genes regulating key epigenetic processes. Perhaps by virtue of the highly flexible development allowed by their responsive epigenetic systems, plants are particularly adept at hybridization.
Intriguingly, the ability to hybridize does seem to have a taxonomic bias with some families showing far greater rates of hybrid formation than others Ellstrand et al.
What does seem common in hybridization events in plants is that it can unlock variation not seen in either parental species. This has been exploited in cultivated plants in particular, but there is also evidence that hybridization could be of major importance in the evolution and diversification of plants in nature for general reviews of plant hybridization see, Stebbins, ; Grant, Where does all the novel variation come from in hybrids?
This has been attributed in the past to the effect of combining the genomes and proteomes of two previously separate, distinct entities; divergence in DNA and protein sequences would allow novel combinations in hybrids with the outcome being altered phenotypes with characteristics different to either parent. The combinations of these quantitative trait loci QTL alleles from both parents that have additive effects in the same direction generate characteristics in excess of either parent.
These combinations, of course, are not possible in the isolated parental populations and only become possible in the hybrids. However, investigation of the epigenetics of hybrids, in particular the use of allopolyploid hybrids between Arabidopsis thaliana and A. This model system is useful as A. This facilitates comparison of established wild allotetraploids to synthetic laboratory populations. A diagram showing the chromosomal genetics of this model system is shown in Fig.
Early studies revealed that formation of hybrids between tetraploid A. A striking observation was that some of the altered phenotypes—such as meristematic fasciation and pigmentation—were unstable in hybrid individuals, indicating that dynamic epigenetic changes affecting gene expression had taken place. This confirms earlier studies where both gene silencing and gene activation were observed, from both parental genomes Comai et al. To confirm that the gene expression changes are due to epigenetic differences from the parents, and could not be attributed to the DNA sequence, the cDNAs displaying these changes have been further analysed.
The first and most compelling question answered by these studies was: what do these arbitrarily identified cDNAs encode? As expected, a range of genes were found even in the first small samples analysed by Comai et al. Determination of DNA methylation of these sequences in the hybrids showed that they exhibited major differences to their parental counterparts. Later work with a broader sampling has shown that many coding genes with different functions, and many with unknown functions, show differential expression in newly synthesized hybrids Wang et al.
Interestingly, some of the cDNAs isolated have not shown simple, stable deactivation or reactivation patterns after hybrid formation; some have shown patterns of reactivation and deactivation across selfed generations of the newly synthesized hybrid Comai et al. This is corroborated by work by Madlung et al. Are the same patterns of gene expression changes, including this instability, also found in established natural populations of A.
This has been addressed by Lee and Chen By using the same AFLP-cDNA technique, it was shown that natural hybrids show differential patterns of gene expression compared with their parental species. Later data from Wang et al. However, these patterns of gene expression are probably much more stable in natural A. Both these treatments cause reactivation of gene expression at some of the silent loci examined.
There is no doubt that this molecular work is hugely impressive but many questions still remain. The most disappointing shortcoming has been the inability to connect an epigenetically derived gene expression change with the generation of a phenotypic alteration in the hybrid. This will certainly be challenging in hybrid systems which are not so easy to work with, but essential to confirm the importance of epigenetics.
Such work would also give an indication of whether epigenetic changes induced by hybridization could be of immediate survival or adaptive value. Our opinion is that both questions will be answered in the affirmative; the current estimates of the proportion of genes in parental genomes affected by hybridization, even if too high, and the fact that coding genes are highly represented supports our view.
Two further fundamental questions also spring to mind. First, is this epigenetic instability in hybrids taxonomically widespread in plants?
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Complex gene expression changes even more subtle than those found in the Arabidopsis hybrids have been found in the homeologous gene pairs of 40 protein-coding genes in Gossypium allopolyploid hybrids Adams et al. However, in a large sample of allopolyploid hybrids involving Triticum and Aegilops species, Shaked et al. In one newly synthesized wheat allotetraploid, gene silencing and methylation changes at multiple loci were observed Kashkush et al. Evidently monocotyledons also exhibit epigenetic instability in hybrid formation.
The other essential question is: what mechanism generates epigenetic instability in hybrids? There is no evidence that the affected genes in A. Clearly, some kind of genome-wide effect is taking place that affects the epigenetic stability of various loci, in some cases over multiple generations. Comai et al.
Their hypothesis is that during evolutionary time, as two populations diverge and develop into different species, there is a slight divergence in the protein components of chromatin regulatory complexes. The sub-units of multi-protein complexes that interact with each other would evolve co-ordinately. When the two species then form a hybrid, the alteration in the structure of these complexes through the combination of protein products encoded by different parental genomes may impair their function to an extent.
This impairment of function in a hybrid could generate genome-wide alterations in chromatin structure, with changes in DNA methylation as a secondary effect. A second component of this hypothesis is that the changes in chromatin regulation allow derepression of silencing of transposable elements, with the hybridization event inducing a burst of transposition. The finding that genes similar to transposable elements and coding genes associated with repetitive DNA show altered expression in hybrids is fitting with this explanation.