High-resolution mapping reveals hotspots and sex-biased recombination in Populus trichocarpa

Chanaka Roshan Abeyratne, David Macaya-Sanz, Ran Zhou, Kerrie W. Barry, Christopher Daum, Kathy Haiby, Anna Lipzen, Brian Stanton, Yuko Yoshinaga, Matthew Zane, Gerald A. Tuskan, Stephen P. DiFazio

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3 Scopus citations

Abstract

Fine-scale meiotic recombination is fundamental to the outcome of natural and artificial selection. Here, dense genetic mapping and haplotype reconstruction were used to estimate recombination for a full factorial Populus trichocarpa cross of 7 males and 7 females. Genomes of the resulting 49 full-sib families (N 829 offspring) were resequenced, and high-fidelity biallelic SNP/INDELs and pedigree information were used to ascertain allelic phase and impute progeny genotypes to recover gametic haplotypes. The 14 parental genetic maps contained 1,820 SNP/INDELs on average that covered 376.7Mb of physical length across 19 chromosomes. Comparison of parental and progeny haplotypes allowed fine-scale demarcation of cross-over regions, where 38,846 cross-over events in 1,658 gametes were observed. Cross-over events were positively associated with gene density and negatively associated with GC content and long-terminal repeats. One of the most striking findings was higher rates of cross-overs in males in 8 out of 19 chromosomes. Regions with elevated male cross-over rates had lower gene density and GC content than windows showing no sex bias. High-resolution analysis identified 67 candidate crossover hotspots spread throughout the genome. DNA sequence motifs enriched in these regions showed striking similarity to those of maize, Arabidopsis, and wheat. These findings, and recombination estimates, will be useful for ongoing efforts to accelerate domestication of this and other biomass feedstocks, as well as future studies investigating broader questions related to evolutionary history, perennial development, phenology, wood formation, vegetative propagation, and dioecy that cannot be studied using annual plant model systems.

Original languageEnglish
Article numberjkac269
JournalG3: Genes, Genomes, Genetics
Volume13
Issue number1
DOIs
StatePublished - Jan 2023

Funding

The work (proposal: 10.46936/10.25585/60001012) conducted by the U.S. Department of Energy Joint Genome Institute (https://ror.org/ 04xm1d337), a DOE Office of Science User Facility, is supported by the Office of Science of the U.S. Department of Energy operated under Contract No. DE-AC02-05CH11231.The authors would like to acknowledge the High-Performance-Computing group at West Virginia University, funded in part by the National Science Foundation EPSCoR Research Infrastructure Improvement Cooperative Agreement #1003907, the state of West Virginia (WVEPSCoR via the Higher Education Policy Commission) and WVU. Finally, we thank the many researchers from the Center for Bioenergy Innovation who contributed to this work. This research was supported by the U.S. Department of Energy (DOE), Office of Biological and Environmental Research through the Center for Bioenergy Innovation (CBI), and a DOE Bioenergy Research Center. The publisher, by accepting the article for publication, acknowledges that the U.S. Government retains a nonexclusive, paid-up, irrevocable, worldwide license to publish, or reproduce the published form of this work, or allow others to do so, for U.S. Government purposes. The views expressed in the article do not necessarily represent the views of the U.S. Department of Energy or the United States Government. Work on heterochiasmy was supported by the National Science Foundation (award 1542509 to SD). The breeding of the 7⨯7 population was initially funded by an award under the Western Sun Grant program to Washington State University (Subgrant T-0013A). Dr Macaya-Sanz was partially supported by “Atracción de Talento Investigador” of the Community of Madrid (ref. 2019-T2/BIO-12780). The project “Conservación y promoción de recursos genéticos forestales con-templadas en el programa nacional de desarrollo rural” (ref. IMP2018-002), funded by the Spanish Ministry of Ecological Transition, also covered some expenses of this study.

FundersFunder number
DOE Bioenergy Research Center
Spanish Ministry of Ecological Transition
U.S. Department of Energy Joint Genome Institute04xm1d337
WVEPSCoR
West Virginia
National Science Foundation1003907, 1542509
U.S. Department of EnergyDE-AC02-05CH11231
Office of Science
Biological and Environmental Research
Washington State University2019-T2/BIO-12780, IMP2018-002
West Virginia University
Center for Bioenergy Innovation
West Virginia Higher Education Policy Commission

    Keywords

    • Populus
    • cross-over
    • heterochiasmy
    • recombination
    • sex-bias

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