Dandelions ‘remember’ stress: heritable stress‐induced methylation patterns in asexual dandelions

Plants exhibit a variety of genetic and epigenetic responses to environmental stresses. A well-known response is that transposable elements can be activated (reviewed in Wessler, 1996); other common responses include changes in gene expression levels and patterns (e.g. Kilian et al., 2007), as well as changes in alternative splicing patterns (e.g. Palusa et al., 2007). Among epigenetic phenomena, changes in DNA methylation in response to stress have been investigated in several plants, and both increases and decreases in methylation levels have been discovered (reviewed in Bruce et al., 2007; Lukens & Zhan, 2007; Boyko & Kovalchuk, 2008; Chinnusamy & Zhu, 2009). In some cases the altered methylation levels did not change back to the original levels after the stress was removed (e.g. Steward et al., 2002). In this issue of New Phytologist, Verhoeven et al. (pp. 1108–1118) now show that cytosine methylation patterns in asexual triploid dandelions can change at some loci in response to stress conditions. Moreover, and most notably, some of the altered methylation patterns were heritable in the next generation. …most notably, some of the altered [stress induced] methylation patterns were heritable in the next generation.’ In their study, Verhoeven et al. used asexual, or apomictic, triploid dandelions that reproduce with unfertilized seeds, thus minimizing or eliminating genetic variation among individuals. They used eight plants in each of four stress treatments plus untreated control plants. The stress conditions included high salt, low nutrients, salicylic acid and jasmonic acid stresses; the latter two were used to induce anti-herbivore and anti-pathogen defenses. Changes in methylation were assayed in each plant using the amplified fragment length polymorphism (AFLP) technique with diagnostic methylation-sensitive and methylation-insensitive restriction enzymes. Twenty out of 359 scorable fragments showed evidence of a change in methylation (either gain or loss of methylation) in one or more treatments and in one or more individuals. A large majority (74–92%) of the altered methylation patterns were transmitted to the progeny of the stressed plants that were not exposed to the stresses. The salicylic acid treatments showed the largest number of heritable methylation changes. The fascinating results uncovered by Verhoeven et al. raise many questions about the phenomenon of heritable stress-induced methylation patterns. It will be particularly interesting and important to determine which types of DNA sequences undergo methylation changes in response to environmental stress that are heritable. Are they coding regions, introns, or regulatory regions of genes? Or are they intergenic regions of the genome? Might many of the methylation changes be in transposable elements? Sequencing of the AFLP fragments that displayed the heritable methylation changes in the study by Verhoeven et al. could begin to answer those questions. In addition, the number of methylation changes in a locus could be determined by bisulfite sequencing on some of the loci that were identified by AFLP analysis. In addition, a larger number of loci could be screened by AFLP to identify additional loci that undergo heritable methylation changes in order to shed light on the frequency of different types of DNA sequences involved. If some of the methylation changes occurred in genes it would be important to determine if they affect gene expression. DNA methylation changes are sometimes accompanied by changes in histone modifications, including methylation and acetylation, which affect chromatin structure. Future studies could examine the molecular architecture of chromatin to determine if other epigenetic marks that are affected by stress conditions are also heritable. Verhoeven et al. assayed four stress conditions. Are methylation changes that occur in response to other abiotic and biotic stresses also heritable? Or does the phenomenon occur just after exposure to some types of stresses? Other environmental stresses, such as heat, cold and drought, could be examined. In addition, it would be interesting to expose the plants showing heritable methylation changes to the same stress condition to which their parents were exposed and to compare the responses with plants that had not been treated with the stress in the previous generation. Such experiments might provide insights into the phenotypic consequences of heritable stress-induced methylation changes. Finally, are stress-induced methylation changes heritable in sexual plant species, in addition to apomicts? The dandelions (Taraxicum officinale) provide a nice system in this regard because there are also sexual populations (van Dijk, 2003). In my view, the study of Verhoeven et al. raises more questions than it answers – the authors have opened the door to a potentially vast, unexplored and fascinating avenue of research.

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