A comparative methylome analysis of brain tissues between fourth instar solitarious and gregarious L. As in S. Wang and colleagues suggest that these genes might be involved in synaptic plasticity and, for the phase transition, point to a crucial role of microtubule dynamics control in locust brains. The role of histone modifications has been less well studied in locusts. Using immunoassays for S. Preliminary data suggest that brains of gregarious S. In migratory locusts, burst expression of retro-elements has been observed in the egg stage, which is thought to be involved in locust development and has been proposed as a regulatory mechanism in phase transition Guo et al.
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The involvement of small ncRNAs in L. The two phases differed strongly in both length distribution and type of small RNAs. Gregarious animals had higher expression of small RNAs below 22 nucleotides, whereas the opposite was true for small RNAs above 22 nucleotides. Moreover, miRNA has been shown to inhibit behavioural aggregation by controlling dopamine synthesis in locusts Yang et al. All this is in strong support of an epigenetic basis for phase polymorphism.
In summary, increasing evidence points to a pivotal role of epigenetics in controlling phase transitions in locusts, yet definite evidence, i. Until recently, evidence for methylation in locusts relied on paper chromatography and photo-spectroscopy Wyatt, , mass spectrometry Boerjan et al. While these methods have their specific value, single base resolution methylome analyses allow detailed analysis of hypothetical changes in DNA methylation status between the solitary and gregarious phase Robinson et al.
Recently, these analyses have been performed in L. Parts of a Schistocerca methylome have also been characterised Falckenhayn et al. Methylome studies to date have been based on whole organisms or brain tissue. However, it is likely that some epigenetic differences might be concealed by these approaches, as they might be specifically directed to particular brain regions or even cells Bonasio, The epigenetic machinery can be experimentally manipulated, e.
In recent years, it has even become possible to manipulate DNA methylation and histone modifications at specific sites see below. Gene regulation by DNA methylation is a complex matter not to mention the intricate interactions with histones, their modifications and ncRNAs , and transitions from one state to another are usually characterised by a dynamic alteration in the methylation pattern.
While some genes or promoters are being methylated, others are demethylated, and as such the total content of methylated cytosines could be more or less constant.
Advances in Insect Physiology
For instance, most cancers are associated with a specific methylation pattern, where tumour suppressor genes are hypermethylated i. It is evident that drugs or other experimental methods that aim at a general lower or higher level of DNA methylation are rather crude tools and will probably not be able to mimic such a delicate balance. Indeed, some cancer forms are associated with global hypomethylation, which also might promote metastasis reviewed in Szyf, A complete demethylation is usually lethal, and Dnmts are often essential during development e.
Zwier et al. Drugs like zebularine Zhou et al. As these drugs do not actively remove methyl groups, they are only effective where DNA replication takes place, limiting their usage to dividing cells. Several other compounds that are not incorporated in DNA have been described as Dnmt inhibitors or DNA demethylating agents reviewed in Szyf, , but their mode of action is not yet understood.
Mechanisms and enzymes that actively demethylate DNA have been described in mammals and plants, the most prominent being TET ten—eleven translocation proteins reviewed in Kohli and Zhang, ; Piccolo and Fisher, ; Wu and Zhang, Some of these demethylating pathways do not require DNA replication and would therefore be attractive to manipulate post-mitotic cells. It should be noted that DNA methylation in insects is not necessarily associated with silencing of gene expression; in fact, DNA methylation in insects is highly correlated with steady gene expression and reduced variability in transcript levels Foret et al.
Besides targeting DNA methylation, another promising avenue would be the manipulation of histone modifications. Some of these enzymes are widely conserved, and could thus serve as targets for pharmaceuticals. In contrast, inhibition of histone demethylases would shift the balance between methylation and demethylation towards higher methylated histones.
So far, however, there are no reports of active demethylation processes in insects. While some drugs have been shown to work in humans and Drosophila alike e. Greiner et al.
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Recent technologies allow mapping of different DNA modifications methylation, hydroxymethylation, formylation, carboxylation at single-base resolution Booth et al. Various methods are available to map DNA methylation, each with their specific advantages and shortcomings Bock et al. Wang and colleagues Wang et al.
This approach allows single-base resolution and absolute quantification of hydroxy methylation [albeit with imperfect quantification Harris et al. Studies of DNA modifications should be complemented by analyses of histone modifications where possible, e. A comparison of the epigenomes of the two phases between L.
Epigenetic changes that are shared between the two species should be prioritised in investigating their role in phase transition. It will be interesting to unravel how the different epigenetic pathways in these two species interact to bring about the phenomenon of phase transition. More specific tools to manipulate particular epigenetic signatures will have to be developed, e.
One strategy might be to target genes with a role in epigenetics using RNAi. Because of the robust systemic RNAi mechanism in locusts Wynant et al. While RNAi has been successfully used for several years in locusts, it has one major drawback: it rarely induces a complete loss of function of the targeted gene.
Locust Collective Motion and Its Modeling
Innovative site-specific genomic engineering tools are currently being explored. Alternatively, methylated DNA sequences of interest might be specifically excised and replaced by unmethylated DNA, or vice versa Ramalingam et al. Even more intriguing was the suggestion that methylating and demethylating enzymes as well as histone modifying enzymes e. This would allow specific de methylation of DNA and histones, thereby enabling manipulation of epigenomes with high precision. While the CRISPR-Cas system has already been shown to work in diverse organisms, such as bacteria, plants, vertebrates and insects, it has not yet been employed in locusts.
Konermann and colleagues Konermann et al. This method is highly versatile, as it allows different DNA sequence recognition systems e. These manipulations would allow functional analyses of specific sites in the epigenome. However, to date, locusts have not been genetically or epigenetically modified.
One of the challenges will be to deliver the modified enzymes into cells of interest Gaj et al. Interestingly, some ZFNs can be delivered directly as proteins across the cell membrane Gaj et al. Bassett and Liu, ; Lee et al. Given the ready use of RNAi in locusts Wynant et al.
If successful, this would open unprecedented opportunities for functional genomics and epigenomics, circumventing the drawbacks of RNAi and pharmaceutical approaches. Future research should aim to reveal the mechanisms of epigenetic control of locust phase transition. Additional insights are to be expected from comparisons with the Australian plague locust, Chortoicetes terminifera , where phase characteristics can change within 72 h in both directions and change abruptly between generations.
Given the advent of new and exciting techniques that allow the specific manipulation of genes and proteins, and the analysis of single cells, these are excellent times to study the molecular mechanics of phase polyphenism in locusts. We apologise to those colleagues whose work we could not cite because of space limitations. We acknowledge the constructive suggestions of two anonymous reviewers that greatly helped to improve the article.
We are grateful for the contributions of Liesbet Temmerman and Isabel Beets to the manuscript. Thanks are due to Tom Fayle for permission to use some of his images, to Roger Jonckers for taking care of our locusts and to Marijke Christiaens for assistance with the figures.
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