Phenotypic diversity ultimately traces to variation in genomic sequence and rewiring of regulatory networks. To identify critical genomic sequence in cotton, we constructed a genomic variome based on 1961 allotetraploid cotton accessions, and identified 456 Mb and 357 Mb of sequence with domestication and improvement selection signals, in which 162 agronomic traits-associated loci were identified. We identified 124 presence/absence variation of genes linked to favorable fiber quality and yield. We constructed a pan-genome of the Gossypium genus using 10 representative diploid genomes. We document the genomic evolutionary history and the impact of lineage-specific transposon amplification on differential genome composition. Integration of genomic variation with population transcriptome data allowed us to construct dynamic genetic regulatory networks for the formation of cotton fiber quality. We characterize 1,258 genes comprising 36 genetic modules that control staged fiber development, and uncover genetic components governing their partitioned expression relative to subgenomic duplicated genes (homoeologs). Only about 30% of fiber quality-related homoeologs show phenotypically favorable allele aggregation in a large panel of cultivars, highlighting the unrealized potential for subgenome additivity in fiber improvement. Moreover, we envision a genome-enabled breeding strategy, with a particular attention to 48 favorable alleles related to fiber phenotypes that have been subject to purifying selection during domestication. These studies provide new insights into genetic regulation of cotton fiber development and shed light on new approaches for fiber quality improvement.
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