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Correlation Analysis Reveals an Important Role of GC Content in Accumulation of Deletion Mutations in the Coding Region of Angiosperm Plastomes

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Abstract

Variation in GC content is assumed to correlate with various processes, including mutation biases, recombination, and environmental parameters. To date, most genomic studies exploring the evolution of GC content have focused on nuclear genomes, but relatively few have concentrated on organelle genomes. We explored the mechanisms maintaining the GC content in angiosperm plastomes, with a particular focus on the hypothesis of phylogenetic dependence and the correlation with deletion mutations. We measured three genetic traits, namely, GC content, A/T tracts, and G/C tracts, in the coding region of plastid genomes for 1382 angiosperm species representing 350 families and 64 orders, and tested the phylogenetic signal. Then, we performed correlation analyses and revealed the variation in evolutionary rate of selected traits using RRphylo. The plastid GC content in the coding region varied from 28.10% to 43.20% across angiosperms, with a few non-photosynthetic species showing highly reduced values, highlighting the significance of functional constraints. We found strong phylogenetic signal in A/T tracts, but weak ones in GC content and G/C tracts, indicating adaptive potential. GC content was positively and negatively correlated with G/C and A/T tracts, respectively, suggesting a trade-off between these two deletion events. GC content evolved at various rates across the phylogeny, with significant increases in monocots and Lamiids, and a decrease in Fabids, implying the effects of some other factors. We hypothesize that variation in plastid GC content might be a mixed strategy of species to optimize fitness in fluctuating climates, partly through influencing the trade-off between AT → GC and GC → AT mutations.

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Acknowledgements

This study was financially supported by the National Natural Science Foundation of China (31970227 and 41571049) and the Science and Technology Basic Resources Investigation Program of China (2019FY100900).

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Correspondence to Yu-Huan Wu or De-Zhu Li.

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All authors declare that they have no conflict of interest.

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Handling Editor: Alexander Platt.

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239_2020_9987_MOESM1_ESM.xlsx

Supplementary file1 Table S1 Three genetic traits in protein-coding regions of plastomes were measured for 1382 angiosperm species representing 350 families and 64 orders using the data set of Li et al (2019). "*" indicates non-photosynthetic plants, including holoparasitic and mycroheterotropic species (Merckx and Freudenstein 2010; Nickrent 2020) (XLSX 194 KB)

239_2020_9987_MOESM2_ESM.xlsx

Supplementary file2 Table S2 Test of phylogenetic signal of three genetic traits using 101 trees, including Li et al.’s MCC and 100 randomly selected trees, using two statistics: Blomberg's K and Pagel's λ. p < 0.001 is considered significant (XLSX 22 KB)

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Yu, Y., Li, HT., Wu, YH. et al. Correlation Analysis Reveals an Important Role of GC Content in Accumulation of Deletion Mutations in the Coding Region of Angiosperm Plastomes. J Mol Evol 89, 73–80 (2021). https://doi.org/10.1007/s00239-020-09987-5

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  • DOI: https://doi.org/10.1007/s00239-020-09987-5

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