The genomic and epigenomic landscapes of hemizygous genes across crops with contrasting reproductive systems
Abstract
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.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (23)
Yanling Peng
National Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences
Yiwen Wang
Yuting Liu
Xinyue Fang
National Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences
Lin Cheng
Qiming Long
National Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences
Dalu Su
National Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences
Tianhao Zhang
Beijing National Laboratory for Molecular Science, State Key Laboratory of Rare Earth Materials Chemistry and Applications, College of Chemistry and Molecular Engineering
Xiaoya Shi
National Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences
Xiaodong Xu
Qi Xu
School of Optical and Electronic Information (SOEI) and Wuhan National Laboratory for Optoelectronics (WNLO)
Nan Wang
Fan Zhang
Zhongjie Liu
National Key Laboratory of Tropical Crop Breeding, Shenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Key Laboratory of Synthetic Biology, Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences
Hua Xiao
Jin Yao
School of Management, Shenzhen Polytechnic University
Ling Tian
Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Provincial Key Laboratory of Agro-animal Genomics and Molecular Breeding/Guangdong Provincial Sericulture and Mulberry Engineering Research Center, College of Animal Science, South China Agricultural University
Wei Hu
Songbi Chen
National Key Laboratory of Tropical Crop Breeding, Tropical Crops Genetic Resources Institute, Chinese Academy of Tropical Agricultural Sciences
Haibo Wang
Sanwen Huang
Brandon S. Gaut
Department of Ecology and Evolutionary Biology, University of California
Yongfeng Zhou