Chromosomal sex-determining systems with male heterogamety include actively male-determining-Y and X-A balance systems, both of which are found in animals and plants. The sex-determining genes have been identified in several active-Y plant systems, but the evolution and functioning of X-A balance systems remains mysterious. Here we sequenced and compared the genomes of two hop species. The evolution of the hop X-A balance system involved an ancient recombination suppression event across a large X chromosome region shared by both species. In one species, an autosome fused to this ancestral sex chromosome, and recombination was subsequently suppressed again. The two evolutionary strata created in this neo-X have degenerated to different degrees and evolved correspondingly different dosage compensation levels that correlate with histone modification patterns. Finally, we identified an X-specific ETR1-like ethylene receptor in the ancestral X region. Its dosage may affect sex determination, as part of the counting mechanism of this X-A balance system.

Advanced Genomics Center National Institute of Genetics Mishima Japan

Department of Plant Developmental Genetics Institute of Biophysics of the Czech Academy of Sciences Brno Czech Republic

Division of Microbiology Department of Infectious Medicine Kurume University School of Medicine Kurume Japan

Faculty of Agriculture Iwate University Morioka Japan

Faculty of Science Academic Assembly University of Toyama Gofuku Japan

Graduate School of Environmental and Life Science Okayama University Okayama Japan

Hop Research Institute Co Ltd Žatec Czech Republic

Institute of Ecology and Evolution University of Edinburgh Edinburgh UK

Iwate Biotechnology Research Center Kitakami Japan

Japan Science and Technology Agency PRESTO Kawaguchi shi Japan

Kazusa DNA Research Institute Kisarazu Japan

School of Life Science and Technology Institute of Science Tokyo Tokyo Japan

Suntory Global Innovation Center Ltd Kyoto Japan

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