Interspecies association mapping links reduced CG to TG substitution rates to the loss of gene-body methylation

Abstract

Comparative genomics can unravel the genetic basis of species differences; however, successful reports on quantitative traits are still scarce. Here we present genome assemblies of 31 so-far unassembled Brassicaceae plant species and combine them with 16 previously published assemblies to establish the Brassicaceae Diversity Panel. Using a new interspecies association strategy for quantitative traits, we found a so-far unknown association between the unexpectedly high variation in CG to TG substitution rates in genes and the absence of CHROMOMETHYLASE3 (CMT3) orthologues. Low substitution rates were associated with the loss of CMT3, while species with conserved CMT3 orthologues showed high substitution rates. Species without CMT3 also lacked gene-body methylation (gbM), suggesting an evolutionary trade-off between the unknown function of gbM and low substitution rates in Brassicaceae, possibly due to low mutability of non-methylated cytosines.

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Fig. 1: Phylogenetic tree of 47 Brassicaceae species including paleo- and meso/neopolyploidization events.
Fig. 2: Polyploidization event identification, their phylogenetic placement and the impact of these events on the gene space.
Fig. 3: PAM and power assessment using simulations based on gene absence/presence patterns.
Fig. 4: PAM of leaf shape complexity.
Fig. 5: Single-nucleotide mutation rates, their association to variation of CMT3 and differences in gbM.

Data availability

All sequencing data, assemblies and gene annotations generated in this project can be found in the European Nucleotide Archive under the project accession number PRJEB26555.

Code availability

The code used to generate associations, the species tree, and the genotypic and phenotypic data can be accessed at https://github.com/schneebergerlab/Scripts_supporting_Kiefer_Willing_et_al_2019.

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Acknowledgements

We would like to thank Bruno Hüttel (Max Planck Genome Centre, Cologne, Germany). This work was supported by the ERC STG Grant INTERACT 802629 (K.S.). Work on BrassiBase was funded within the framework of DFG-SPP 1529 (KO2302-13-1/2) (M.A.K.).

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K.S., M.A.K., E.-M.W. and C.K. designed research. C.K., E.-M.W., W.-B.J., H.S., M.P. and K.S. analysed the data. C.K., U.H. and B.H. performed the plant work. K.S. wrote the paper with the help of all authors.

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Correspondence to Korbinian Schneeberger.

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Supplementary information

Supplementary Information

Supplementary Materials and Methods and Supplementary Figs. 1–16.

Reporting Summary

Supplementary Table 1

Selected species, generated sequencing data and assembly quality.

Supplementary Table 2

Meso-polyploidization prediction (lower part) trained on genomes with known meso-polyploidizations.

Supplementary Table 3

MAPS analysis of species with putatively shared WGD events.

Supplementary Table 4

Leaf shape complexity values.

Supplementary Table 5

Orthologous groups (OG) with highly significant associations to leaf shape complexity.

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Kiefer, C., Willing, E., Jiao, W. et al. Interspecies association mapping links reduced CG to TG substitution rates to the loss of gene-body methylation. Nat. Plants 5, 846–855 (2019). https://doi.org/10.1038/s41477-019-0486-9

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