Intragenic meiotic crossovers generate novel alleles with transgressive expression levels

Sanzhen Liu, James C. Schnable, Alina Ott, Cheng Ting Eddy Yeh, Nathan M. Springer, Jianming Yu, Gary Muehlbauer, Marja C.P. Timmermans, Michael J. Scanlon, Patrick S. Schnable

Research output: Contribution to journalArticlepeer-review

2 Scopus citations

Abstract

Meiotic recombination is an evolutionary force that generates new genetic diversity upon which selection can act. Whereas multiple studies have assessed genome-wide patterns of recombination and specific cases of intragenic recombination, few studies have assessed intragenic recombination genome-wide in higher eukaryotes. We identified recombination events within or near genes in a population of maize recombinant inbred lines (RILs) using RNA-sequencing data. Our results are consistent with case studies that have shown that intragenic crossovers cluster at the 50 ends of some genes. Further, we identified cases of intragenic crossovers that generate transgressive transcript accumulation patterns, that is, recombinant alleles displayed higher or lower levels of expression than did nonrecombinant alleles in any of 100 RILs, implicating intragenic recombination in the generation of new variants upon which selection can act. Thousands of apparent gene conversion events were identified, allowing us to estimate the genome-wide rate of gene conversion at SNP sites (4.9 105). The density of syntenic genes (i.e., those conserved at the same genomic locations since the divergence of maize and sorghum) exhibits a substantial correlation with crossover frequency, whereas the density of nonsyntenic genes (i.e., those which have transposed or been lost subsequent to the divergence of maize and sorghum) shows little correlation, suggesting that crossovers occur at higher rates in syntenic genes than in nonsyntenic genes. Increased rates of crossovers in syntenic genes could be either a consequence of the evolutionary conservation of synteny or a biological process that helps to maintain synteny.

Original languageEnglish (US)
Pages (from-to)2762-2772
Number of pages11
JournalMolecular biology and evolution
Volume35
Issue number11
DOIs
StatePublished - 2018

Bibliographical note

Funding Information:
This work is supported by National Science Foundation grants (IOS-0820610, IOS-1238142). Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.

Publisher Copyright:
© The Author(s) 2018.

Keywords

  • Evolutionary novelty
  • Gene conversion
  • Gene regulation

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