Structural variations contribute to subspeciation and yield heterosis in rice

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Yield heterosis has been extensively exploited in hybrid breeding, with inter-subspecies hybrids often exhibiting the most pronounced effects. However, developing elite hybrids remains a laborious and time-consuming process. The genetic basis of heterosis has been debated for over a century, hindered largely by the lack of high-quality genomes. Here, we assembled genomes for 12 representative indica and japonica rice accessions. Using sequence variants of the Phr1 gene, we functionally validated two deletions responsible for phenol reaction variation between the subspecies. Comparative genomic analyses revealed extensive sequence variation among these inbred lines and highlighted the pivotal role of structural variants (SVs) in rice subspeciation. Importantly, the number of SVs between parental inbred lines significantly correlated with heterosis across 17 agronomic traits, with distinct correlation patterns for intra- and inter-subspecific F 1 hybrids. We identified SVs associated with S5-ORF5 and OsBZR1 and validated their function to heterosis for seed setting rate and yield heterosis, respectively, underscoring the importance of SVs in breeding inter-subspecific hybrids. The genomic SVs altered gene expression and these transcriptional changes effectively explained the variances in heterosis. Furthermore, translocations outperformed other SVs and their heterozygous haplotypes exhibited heterosis over homozygous ones. Our findings establish SVs as pivotal drivers in subspeciation and highlight the overdominance model for harnessing rice heterosis.