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Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality.

Shen X, De Jonge J, Forsberg SK, Pettersson ME, Sheng Z, Hennig L, Carlborg Ö - PLoS Genet. (2014)

Bottom Line: Here, we used public data from two collections of A. thaliana accessions to associate genetic variability at individual loci with differences in climates at the sampling sites.We use a novel method to screen the genome for plastic alleles that tolerate a broader climate range than the major allele.This approach reduces confounding with population structure and increases power compared to standard genome-wide association methods.

View Article: PubMed Central - PubMed

Affiliation: Swedish University of Agricultural Sciences, Department of Clinical Sciences, Division of Computational Genetics, Uppsala, Sweden; Karolinska Institutet, Department of Medical Epidemiology and Biostatistics, Stockholm, Sweden; University of Edinburgh, MRC Institute of Genetics and Molecular Medicine, MRC Human Genetics Unit, Edinburgh, United Kingdom.

ABSTRACT
As Arabidopsis thaliana has colonized a wide range of habitats across the world it is an attractive model for studying the genetic mechanisms underlying environmental adaptation. Here, we used public data from two collections of A. thaliana accessions to associate genetic variability at individual loci with differences in climates at the sampling sites. We use a novel method to screen the genome for plastic alleles that tolerate a broader climate range than the major allele. This approach reduces confounding with population structure and increases power compared to standard genome-wide association methods. Sixteen novel loci were found, including an association between Chromomethylase 2 (CMT2) and temperature seasonality where the genome-wide CHH methylation was different for the group of accessions carrying the plastic allele. Cmt2 mutants were shown to be more tolerant to heat-stress, suggesting genetic regulation of epigenetic modifications as a likely mechanism underlying natural adaptation to variable temperatures, potentially through differential allelic plasticity to temperature-stress.

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Related in: MedlinePlus

Principle components of the genomic kinship in the RegMap collection for the accessions carrying the alternative alleles at the Chromomethylase 2 locus (CMT2STOP and CMT2WT as filled and empty circles, respectively).Coloring is based on (A) geographical regions (defined as in Figure S37) and (B) temperature seasonality, ranging from dark blue (least variable) to red (most variable).
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pgen-1004842-g003: Principle components of the genomic kinship in the RegMap collection for the accessions carrying the alternative alleles at the Chromomethylase 2 locus (CMT2STOP and CMT2WT as filled and empty circles, respectively).Coloring is based on (A) geographical regions (defined as in Figure S37) and (B) temperature seasonality, ranging from dark blue (least variable) to red (most variable).

Mentions: A strong association to temperature seasonality, i.e. the ratio between the standard deviation and the mean of temperature records over a year, was identified near Chromomethylase 2 (CMT2; Table 1; Fig. 1). Stable areas are generally found near large bodies of water (e.g. London near the Atlantic 11±5°C; mean ± SD) and variable areas inland (e.g. Novosibirsk in Siberia 1±14°C). A premature CMT2 stop codon located on chromosome 4 at 10,414,556 bp (the 31st base pair of the first exon) segregated in the RegMap collection, with minor allele frequency of 0.05. This CMT2STOP allele had a genome-wide significant association with temperature seasonality (P = 1.1×10−7) and was in strong LD (r2 = 0.82) with the leading SNP (Fig. 1B). The geographic distributions of the wild-type (CMT2WT) and the alternative (CMT2STOP) alleles in the RegMap collection shows that the CMT2WT allele dominates in all major sub-populations sampled from areas with low or intermediate temperature seasonality. The plastic CMT2STOP allele is present, albeit at lower frequency, across all sub-populations in low- and intermediate temperature seasonality areas, and is more common in areas with high temperature seasonality (Fig. 2A; Fig. 3; S36 Figure). Such global distribution across the major population strata indicates that the allele has been around in the Eurasian population sufficiently long to spread across most of the native range and that the allele is not deleterious but rather maintained through balancing selection [11], perhaps by mediating an improved tolerance to variable temperatures.


Natural CMT2 variation is associated with genome-wide methylation changes and temperature seasonality.

Shen X, De Jonge J, Forsberg SK, Pettersson ME, Sheng Z, Hennig L, Carlborg Ö - PLoS Genet. (2014)

Principle components of the genomic kinship in the RegMap collection for the accessions carrying the alternative alleles at the Chromomethylase 2 locus (CMT2STOP and CMT2WT as filled and empty circles, respectively).Coloring is based on (A) geographical regions (defined as in Figure S37) and (B) temperature seasonality, ranging from dark blue (least variable) to red (most variable).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263395&req=5

pgen-1004842-g003: Principle components of the genomic kinship in the RegMap collection for the accessions carrying the alternative alleles at the Chromomethylase 2 locus (CMT2STOP and CMT2WT as filled and empty circles, respectively).Coloring is based on (A) geographical regions (defined as in Figure S37) and (B) temperature seasonality, ranging from dark blue (least variable) to red (most variable).
Mentions: A strong association to temperature seasonality, i.e. the ratio between the standard deviation and the mean of temperature records over a year, was identified near Chromomethylase 2 (CMT2; Table 1; Fig. 1). Stable areas are generally found near large bodies of water (e.g. London near the Atlantic 11±5°C; mean ± SD) and variable areas inland (e.g. Novosibirsk in Siberia 1±14°C). A premature CMT2 stop codon located on chromosome 4 at 10,414,556 bp (the 31st base pair of the first exon) segregated in the RegMap collection, with minor allele frequency of 0.05. This CMT2STOP allele had a genome-wide significant association with temperature seasonality (P = 1.1×10−7) and was in strong LD (r2 = 0.82) with the leading SNP (Fig. 1B). The geographic distributions of the wild-type (CMT2WT) and the alternative (CMT2STOP) alleles in the RegMap collection shows that the CMT2WT allele dominates in all major sub-populations sampled from areas with low or intermediate temperature seasonality. The plastic CMT2STOP allele is present, albeit at lower frequency, across all sub-populations in low- and intermediate temperature seasonality areas, and is more common in areas with high temperature seasonality (Fig. 2A; Fig. 3; S36 Figure). Such global distribution across the major population strata indicates that the allele has been around in the Eurasian population sufficiently long to spread across most of the native range and that the allele is not deleterious but rather maintained through balancing selection [11], perhaps by mediating an improved tolerance to variable temperatures.

Bottom Line: Here, we used public data from two collections of A. thaliana accessions to associate genetic variability at individual loci with differences in climates at the sampling sites.We use a novel method to screen the genome for plastic alleles that tolerate a broader climate range than the major allele.This approach reduces confounding with population structure and increases power compared to standard genome-wide association methods.

View Article: PubMed Central - PubMed

Affiliation: Swedish University of Agricultural Sciences, Department of Clinical Sciences, Division of Computational Genetics, Uppsala, Sweden; Karolinska Institutet, Department of Medical Epidemiology and Biostatistics, Stockholm, Sweden; University of Edinburgh, MRC Institute of Genetics and Molecular Medicine, MRC Human Genetics Unit, Edinburgh, United Kingdom.

ABSTRACT
As Arabidopsis thaliana has colonized a wide range of habitats across the world it is an attractive model for studying the genetic mechanisms underlying environmental adaptation. Here, we used public data from two collections of A. thaliana accessions to associate genetic variability at individual loci with differences in climates at the sampling sites. We use a novel method to screen the genome for plastic alleles that tolerate a broader climate range than the major allele. This approach reduces confounding with population structure and increases power compared to standard genome-wide association methods. Sixteen novel loci were found, including an association between Chromomethylase 2 (CMT2) and temperature seasonality where the genome-wide CHH methylation was different for the group of accessions carrying the plastic allele. Cmt2 mutants were shown to be more tolerant to heat-stress, suggesting genetic regulation of epigenetic modifications as a likely mechanism underlying natural adaptation to variable temperatures, potentially through differential allelic plasticity to temperature-stress.

Show MeSH
Related in: MedlinePlus