Genome-Wide Analyses Reveal Spatially Structured Genetic Diversity in Indian Rice Shaped by Ancestry, Geography and Environment

Abstract

India is a major centre of rice diversity, where long-term cultivation across contrasting environments has generated substantial genomic and phenotypic variation. We analysed genome-wide SNP variation in 313 Indian rice accessions to resolve ancestry structure, regional diversity, spatial genetic processes, environmental associations and haplotype variation at key domestication and adaptation genes. Population structure analyses resolved eight ancestry groups corresponding to indica, aus, aromatic and japonica lineages. Ancestry explained substantially more genomic differentiation than biogeographic regionalization, while there is extensive historical connectivity among lineages and regions. Genetic diversity considerably varied across biogeographic zones. After balanced resampling, the Himalayan region showed the highest standardized allelic diversity and private-allele richness, whereas the North-East region retained high observed heterozygosity and broad ancestry representation. Isolation-by-distance was weak overall but strongly lineage- and region-dependent. Spatial principal component analysis identified significant ancestry-independent broad-scale genetic gradients, demonstrating geography-influenced structure beyond lineage composition. Redundancy analysis detected significant genome–environment associations (F = 3.07, p = 0.001), with climate explaining more independent genomic variation (2.7%) than soil (0.9%). District-level tribal population proportion showed only a weak negative association with individual heterozygosity (Spearman ρ = −0.155, p = 0.006), although PTP classes exhibited low-to-moderate genetic differentiation. Haplotype analysis revealed strong locus-specific ancestry and geographic structuring at sd1, Wx, GS3 and DRO1. Together, the results show that Indian rice diversity is a reticulate genomic mosaic shaped by ancestry, geography, historical gene flow and environmental heterogeneity. This study provides a landscape-genomic framework for conservation and targeted germplasm utilization in breeding programmes.