The genomic and epigenomic landscapes of hemizygous genes across crops with contrasting reproductive systems

Hemizygous genes, which are present on only one of the two homologous chromosomes of diploid organisms, have been mainly studied in the context of sex chromosomes and sex-linked genes. However, these genes can also occur on the autosomes of diploid plants due to structural variants (SVs), such as a deletion/insertion of one allele, and this phenomenon largely unexplored in plants. Here, we investigated the genomic and epigenomic landscapes of hemizygous genes across 22 genomes with varying propagation histories: eleven clonal lineages, seven outcrossed samples, and four inbred and putatively homozygous genomes. We identified SVs leading to genic hemizygosity. As expected, very few genes (0.01 to 1.2%) were hemizygous in the homozygous genomes, representing negative controls. Hemizygosity was appreciable among outcrossed lineages, averaging 8.7% of genes, but consistently elevated for the clonal samples at 13.8% genes, likely reflecting heterozygous SV accumulation during clonal propagation. Compared to diploid genes, hemizygous genes were more often situated in centromeric than telomeric regions and experienced weaker purifying selection. They also had reduced levels of expression, averaging ~20% of the expression levels of diploid genes, violating the evolutionary model of dosage compensation. We also detected higher DNA methylation levels in hemizygous genes and transposable elements, which may contribute to their reduced expression. Finally, expression profiles showed that hemizygous genes were more specifically expressed in contexts related to fruit development, organ differentiation, and stress responses. Overall, hemizygous genes accumulate in clonally propagated lineages and display distinct genetic and epigenetic features compared to diploid genes, shedding unique insights into genetic studies and breeding programs of clonal crops.