Fitness Costs and Variation in Transmission Distortion Associated with the Abnormal Chromosome 10 Meiotic Drive System in Maize

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 2017 Nov 11

PMID 29122827

Citations 13

Authors

David M Higgins

Elizabeth G Lowry

Lisa B Kanizay

Philip W Becraft

David W Hall

R Kelly Dawe

Affiliations

Soon will be listed here.

Abstract

Meiotic drive describes a process whereby selfish genetic elements are transmitted at levels greater than Mendelian expectations. Maize abnormal chromosome 10 (Ab10) encodes a meiotic drive system that exhibits strong preferential segregation through female gametes. We performed transmission assays on nine Ab10 chromosomes from landraces and teosinte lines and found a transmission advantage of 62-79% in heterozygotes. Despite this transmission advantage, Ab10 is present at low frequencies in natural populations, suggesting that it carries large negative fitness consequences. We measured pollen transmission, the percentage of live pollen, seed production, and seed size to estimate several of the possible fitness effects of Ab10. We found no evidence that Ab10 affects pollen transmission, , Ab10 and N10 pollen are transmitted equally from heterozygous fathers. However, at the diploid (sporophyte) level, both heterozygous and homozygous Ab10-I-MMR individuals show decreased pollen viability, decreased seed set, and decreased seed weight. The observed fitness costs can nearly but not entirely account for the observed frequencies of Ab10. Sequence analysis shows a surprising amount of molecular variation among Ab10 haplotypes, suggesting that there may be other phenotypic variables that contribute to the low but stable equilibrium frequencies.

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References

Mezmouk S, Ross-Ibarra J . The pattern and distribution of deleterious mutations in maize. G3 (Bethesda). 2013; 4(1):163-71. PMC: 3887532. DOI: 10.1534/g3.113.008870. View

Lyttle T . Experimental Population Genetics of Meiotic Drive Systems II. Accumulation of Genetic Modifiers of Segregation Distorter (SD) in Laboratory Populations. Genetics. 1979; 91(2):339-57. PMC: 1216371. DOI: 10.1093/genetics/91.2.339. View

Ananiev E, Phillips R, Rines H . A knob-associated tandem repeat in maize capable of forming fold-back DNA segments: are chromosome knobs megatransposons?. Proc Natl Acad Sci U S A. 1998; 95(18):10785-90. PMC: 27973. DOI: 10.1073/pnas.95.18.10785. View

Pieper K, Dyer K . Occasional recombination of a selfish X-chromosome may permit its persistence at high frequencies in the wild. J Evol Biol. 2016; 29(11):2229-2241. PMC: 5089913. DOI: 10.1111/jeb.12948. View

McLaren W, Gil L, Hunt S, Riat H, Ritchie G, Thormann A . The Ensembl Variant Effect Predictor. Genome Biol. 2016; 17(1):122. PMC: 4893825. DOI: 10.1186/s13059-016-0974-4. View

Hiatt E, Dawe R . Four loci on abnormal chromosome 10 contribute to meiotic drive in maize. Genetics. 2003; 164(2):699-709. PMC: 1462598. DOI: 10.1093/genetics/164.2.699. View

Fishman L, Kelly J . Centromere-associated meiotic drive and female fitness variation in Mimulus. Evolution. 2015; 69(5):1208-18. PMC: 5958614. DOI: 10.1111/evo.12661. View

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S . TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14(4):R36. PMC: 4053844. DOI: 10.1186/gb-2013-14-4-r36. View

Hartl D . Meiotic drive in natural populations of Drosophila melanogaster. IX. Suppressors of segregation distorter in wild populations. Can J Genet Cytol. 1970; 12(3):594-600. DOI: 10.1139/g70-079. View

10.

Rhoades M . Preferential Segregation in Maize. Genetics. 1942; 27(4):395-407. PMC: 1209167. DOI: 10.1093/genetics/27.4.395. View

11.

Dawe R, Hiatt E . Plant neocentromeres: fast, focused, and driven. Chromosome Res. 2004; 12(6):655-69. DOI: 10.1023/B:CHRO.0000036607.74671.db. View

12.

Dobin A, Davis C, Schlesinger F, Drenkow J, Zaleski C, Jha S . STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2012; 29(1):15-21. PMC: 3530905. DOI: 10.1093/bioinformatics/bts635. View

13.

Van der Auwera G, Carneiro M, Hartl C, Poplin R, Del Angel G, Levy-Moonshine A . From FastQ data to high confidence variant calls: the Genome Analysis Toolkit best practices pipeline. Curr Protoc Bioinformatics. 2014; 43:11.10.1-11.10.33. PMC: 4243306. DOI: 10.1002/0471250953.bi1110s43. View

14.

Schnable P, Ware D, Fulton R, Stein J, Wei F, Pasternak S . The B73 maize genome: complexity, diversity, and dynamics. Science. 2009; 326(5956):1112-5. DOI: 10.1126/science.1178534. View

15.

Mroczek R, Melo J, Luce A, Hiatt E, Dawe R . The maize Ab10 meiotic drive system maps to supernumerary sequences in a large complex haplotype. Genetics. 2006; 174(1):145-54. PMC: 1569779. DOI: 10.1534/genetics.105.048322. View

16.

Trapnell C, Williams B, Pertea G, Mortazavi A, Kwan G, van Baren M . Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010; 28(5):511-5. PMC: 3146043. DOI: 10.1038/nbt.1621. View

17.

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A . The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010; 20(9):1297-303. PMC: 2928508. DOI: 10.1101/gr.107524.110. View

18.

Bolger A, Lohse M, Usadel B . Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30(15):2114-20. PMC: 4103590. DOI: 10.1093/bioinformatics/btu170. View

19.

Chmatal L, Gabriel S, Mitsainas G, Martinez-Vargas J, Ventura J, Searle J . Centromere strength provides the cell biological basis for meiotic drive and karyotype evolution in mice. Curr Biol. 2014; 24(19):2295-300. PMC: 4189972. DOI: 10.1016/j.cub.2014.08.017. View

20.

Herrmann B, Koschorz B, Wertz K, McLaughlin K, Kispert A . A protein kinase encoded by the t complex responder gene causes non-mendelian inheritance. Nature. 2000; 402(6758):141-6. DOI: 10.1038/45970. View