Genetic and epigenetic changes during the invasion of a cosmopolitan species (<i>Phragmites australis</i>)

Liu, Lele; Cuiping, Pei; Liu, Shuna; Guo, Xiao; Du, Ning; Guo, Weihua

doi:10.1002/ece3.4144

Cited by 30 publications

(27 citation statements)

References 72 publications

(127 reference statements)

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“… Amarasinghe et al. (2014) found a global erasure of DNA methylation increased reproductive behavior, Liu et al. (2018) found differences in expression in genes responsible for methylation between castes and Marshall et al.…”

Section: Discussionmentioning

confidence: 99%

Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

Marshall

Jones

Lonsdale

et al. 2020

Genome Biology and Evolution

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Allele-specific expression is when one allele of a gene shows higher levels of expression compared to the other allele, in a diploid organism. Recent work has identified allele-specific expression in a number of Hymenopteran species. However, the molecular mechanism which drives this allelic expression bias remains unknown. In mammals DNA methylation is often associated with genes which show allele-specific expression. DNA methylation systems have been described in species of Hymenoptera, providing a candidate mechanism. Using previously generated RNA-Seq and whole genome bisulfite sequencing from reproductive and sterile bumblebee (Bombus terrestris) workers we have identified genome-wide allele-specific expression and allele-specific DNA methylation. The majority of genes displaying allele-specific expression are common between reproductive and sterile workers and the proportion of allele-specific expression bias generally varies between genetically distinct colonies. We have also identified genome-wide allele-specific DNA methylation patterns in both reproductive and sterile workers, with reproductive workers showing significantly more genes with allele-specific methylation. Finally, there is no significant overlap between genes showing allele-specific expression and allele-specific methylation. These results indicate that cis-acting DNA methylation does not directly drive genome-wide allele-specific expression in this species.

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Section: Discussionmentioning

confidence: 99%

Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

Marshall

Jones

Lonsdale

et al. 2020

Genome Biology and Evolution

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“…These findings support previous research which suggests methylation is associated with worker reproductive behaviour. Amarasinghe et al (2014) found a global erasure of DNA methylation increased reproductive behaviour, Liu et al (2018) found differences in expression in genes responsible for methylation between castes and Marshall et al (2019) found differentially methylated genes between B. terrestris castes, some of which were involved in reproductive processes. Numerous other studies have linked methylation to caste differences in various other social insect species, such as; Apis mellifera (Lyko et al , 2010; Elango et al , 2009), Camponotus floridanus and Harpegnathos saltator (Bonasio et al , 2012), Polistes dominula (Weiner et al , 2013) and Zootermopsis nevadensis (Glastad et al , 2016).…”

Section: Discussionmentioning

confidence: 99%

Bumblebee worker castes show differences in allele-specific DNA methylation and allele-specific expression

Marshall

Jones

Lonsdale

et al. 2020

Preprint

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word count: 226. 2 1Allele-specific methylation and expression in bumblebees. Abstract 4Allele-specific expression is when one allele of a gene shows higher levels of expression compared 5 to the other allele, in a diploid organism. Genomic imprinting is an extreme example of this, 6 where some genes exhibit allele-specific expression in a parent-of-origin manner. Recent work 7 has identified potentially imprinted genes in species of Hymenoptera. However, the molecular 8 mechanism which drives this allelic expression bias remains unknown. In mammals DNA 9 methylation is often associated with imprinted genes. DNA methylation systems have been 10 described in species of Hymenoptera, providing a candidate imprinting mechanism. Using 11 previously generated RNA-Seq and whole genome bisulfite sequencing from reproductive and 12 sterile bumblebee (Bombus terrestris) workers we have identified genome-wide allele-specific 13 expression and allele-specific DNA methylation. The majority of genes displaying allele-specific 14 expression are common between reproductive castes and the proportion of allele-specific 15 expression bias generally varies between colonies. We have also identified genome-wide 16 allele-specific DNA methylation patterns in both castes. There is no significant overlap between 17 genes showing allele-specific expression and allele-specific methylation. These results indicate 18 that DNA methylation does not directly drive genome-wide allele-specific expression in this 19 species. Only a small number of the genes identified may be 'imprinted' and it may be these genes 20 which are associated with allele-specific DNA methylation. Future work utilising reciprocal 21 crosses to identify parent-of-origin DNA methylation will further clarify the role of DNA 22 methylation in parent-of-origin allele-specific expression. 23 42 species, see Standage et al. (2016). Additionally, allele-specific expression has been associated with 43 allele-specific methylation in two ant species, Camponotus floridanus and Harpegnathos saltator 44 (Bonasio et al., 2012). Another study did not find any relationship between allele-specific expression 45 and methylation in a hybrid cross of two non-social wasp species, Nasonia vitripennis and Nasonia 46 giraulti (Wang et al., 2016). 47Bumblebees provide an ideal system to further investigate the relationship between allele-specific 48 3 Allele-specific methylation and expression in bumblebees. methylation and allele-specific expression, specifically with a view of elucidating potential 49 mechanisms involved in genomic imprinting in social insects. Using a candidate gene approach, 50 previous research identified allele-specific expression in a gene (ecdysone 20-monooxygenase-like) 51 related to worker reproductive behaviour in B. terrestis (Amarasinghe et al., 2015). Additional 52 research has since used RNA-seq data to identify >500 loci showing allele-specific expression 53 throughout the B. terrestris genome (Lonsdale et al., 2017). This same study also...

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“…They grew populations from different environments under controlled common garden conditions to test the stability of epigenetic inheritance and to partition genetic from epigenetic variation. While they found epigenetic variation to be greater than genetic variation across populations, they did not find convergence in epigenetic markings between populations occupying similar environments, suggesting the relationship between environmentally heritable induced epigenetic variations may not be stable and also dependent on the genetic background (Liu et al, ). In comparison with two saltmarsh species, Foust et al () found while one species showed a significant correlation between epigenetic variation and habitat, the other species did not.…”

Section: Epigenetic Mechanisms a Component Of The Rapid Response To mentioning

confidence: 99%

“…Yet, the relationship between epigenetic variation, population divergence and transgenerational inheritance across environments is not universal. Recently, Liu et al () examined genetic and epigenetic variation of native and invasive lineages of the common reed ( Phragmites australis ) in North America. They grew populations from different environments under controlled common garden conditions to test the stability of epigenetic inheritance and to partition genetic from epigenetic variation.…”

Section: Epigenetic Mechanisms a Component Of The Rapid Response To mentioning

confidence: 99%

“…In comparison with two saltmarsh species, Foust et al () found while one species showed a significant correlation between epigenetic variation and habitat, the other species did not. Both Foust et al () and Liu et al () found a correlation between the amount of genetic and epigenetic variation within a population, suggesting that separating the contribution from these sources of variation will present challenges for interpretation of these patterns.…”

Section: Epigenetic Mechanisms a Component Of The Rapid Response To mentioning

confidence: 99%

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Biological invasion: The influence of the hidden side of the (epi)genome

et al. 2019

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Understanding the mechanisms underlying biological invasions and rapid adaptation to global change remains a fundamental challenge, particularly in small populations lacking in genetic variation. Two understudied mechanisms that could facilitate adaptive evolution and adaptive plasticity are the increased genetic variation due to transposable elements (TEs), and associated or independent modification of gene expression through epigenetic changes. Here, we focus on the potential role of these genetic and non‐genetic mechanisms for facilitating invasion success. Because novel or stressful environments are known to induce both epigenetic changes and TE activity, these mechanisms may play an underappreciated role in generating phenotypic and genetic variation for selection to act on. We review how these mechanisms operate, the evidence for how they respond to novel or stressful environments, and how these mechanisms can contribute to the success of biological invasions by facilitating adaptive evolution and phenotypic plasticity. Because genetic and phenotypic variations due to TEs and epigenetic changes are often well regulated or “hidden” in the native environment, the independent and combined contribution of these mechanisms may only become important when populations colonize novel environments. A focus on the mechanisms that generate and control the expression of this variation in new environments may provide insights into biological invasions that would otherwise not be obvious. Global changes and human activities impact on ecosystems and allow new opportunities for biological invasions. Invasive species succeed by adapting rapidly to new environments. The degree to which rapid responses to environmental change could be mediated by the epigenome—the regulatory system that integrates how environmental and genomic variation jointly shape phenotypic variation—requires greater attention if we want to understand the mechanisms by which populations successfully colonize and adapt to new environments. A free Plain Language Summary can be found within the Supporting Information of this article.

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Genetic and epigenetic changes during the invasion of a cosmopolitan species (Phragmites australis)

Cited by 30 publications

References 72 publications

Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

Bumblebee Workers Show Differences in Allele-Specific DNA Methylation and Allele-Specific Expression

Bumblebee worker castes show differences in allele-specific DNA methylation and allele-specific expression

Biological invasion: The influence of the hidden side of the (epi)genome

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