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The genome-wide dynamics of purging during selfing in maize

Abstract

Self-fertilization (also known as selfing) is an important reproductive strategy in plants and a widely applied tool for plant genetics and plant breeding. Selfing can lead to inbreeding depression by uncovering recessive deleterious variants, unless these variants are purged by selection. Here we investigated the dynamics of purging in a set of eleven maize lines that were selfed for six generations. We show that heterozygous, putatively deleterious single nucleotide polymorphisms are preferentially lost from the genome during selfing. Deleterious single nucleotide polymorphisms were lost more rapidly in regions of high recombination, presumably because recombination increases the efficacy of selection by uncoupling linked variants. Overall, heterozygosity decreased more slowly than expected, by an estimated 35% to 40% per generation instead of the expected 50%, perhaps reflecting pervasive associative overdominance. Finally, three lines exhibited marked decreases in genome size due to the purging of transposable elements. Genome loss was more likely to occur for lineages that began with larger genomes with more transposable elements and chromosomal knobs. These three lines purged an average of 398 Mb from their genomes, an amount equivalent to three Arabidopsis thaliana genomes per lineage, in only a few generations.

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Fig. 1: Study design and estimates of genome size.
Fig. 2: Various components of the genome compared between GSΔ and GScon groups and between S1 and S6.
Fig. 3: Proportion of derived allele across SNP types, generations and recombination categories.
Fig. 4: Inference of heterozygous and homozygous genomic regions, based on SNPs inferred to be heterozygous in the parent.

Data availability

Sequence data that support the findings of this study have been deposited in NCBI Short Read Archive under project code SRP158803. The gff files used in this study, the GS flow cytometry data and the raw mapping count data are available on figshare.com (https://doi.org/10.6084/m9.figshare.783825.v2) or from the corresponding author. The SNP VCF files and dataset are available from the corresponding authors upon request.

Code availability

Custom code used in SNP analyses is available from the corresponding authors upon request.

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Acknowledgements

A.M. is supported by an EMBO Postdoctoral Fellowship ALTF 775-2017 and by HFSPO Fellowship LT000496/2018-L. A.B. is supported by The Royal Society (award numbers UF160222 and RGF/R1/180006). M.C.S. is supported by an NSF Graduate Research Fellowship to UC Davis (1148897). D.K.S. is supported by a Postdoctoral Fellowship from the National Science Foundation (NSF) Plant Genome Research Program (1609024). J.F.D. is supported by NSF grant IOS 1238014. Q.L. is supported by a National Natural Science Foundation of China grant (no. 31471431) and the Training Program for Outstanding Young Talents of Zhejiang A&F University to Q.L. B.S.G. is supported by NSF grants 1542703 and 1655808.

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K.R., A.M. and B.S.G. contributed analyses, ideas and writing. G.R.J.G. and Q.L. performed analyses. K.R., C.M.D. and B.S.G. helped design the experiment, grew plants and measured phenotypes; A.B., G.R.J.G., Q.L., D.K.S., J.F.D. and M.C.S. provided materials, data and/or critical ideas. B.S.G. conceived of the project.

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Correspondence to Qingpo Liu or Brandon S. Gaut.

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Roessler, K., Muyle, A., Diez, C.M. et al. The genome-wide dynamics of purging during selfing in maize. Nat. Plants 5, 980–990 (2019). https://doi.org/10.1038/s41477-019-0508-7

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