Genome assembly and population genomic analysis reveal the genetic basis of popcorn evolution

Abstract

Popcorn, one of the world's most popular snack foods, represents the most ancient type of maize domesticated by humans. However, the genetic basis underlying popcorn evolution and kernel-popping traits remains largely unknown. In this study, we assembled a high-quality genome sequence of the popcorn landrace Strawberry Popcorn (SP) and conducted extensive population genomic analyses. The SP genome spans 2.3 Gb and harbours a large inversion on chromosome 8, along with millions of genetic variants that enable the discovery of beneficial alleles. Translocations and substantial duplications of the Ga1 gene occurred in the locus associated with unilateral cross-incompatibility on chromosome 4. Tandemly duplicated Ga1 genes underwent pseudogenisation and truncation with complete loss of gene function. The P1 gene experienced gene expansion and regulatory modifications, leading to downregulation of transcription and subsequent loss of pericarp colour during maize domestication and improvement. Population genomic analysis further identified a subset of 12 marker genes from over 2494 genes under human selection, which were reshaped to enhance kernel-popping traits during domestication. These marker genes include Pl1 and Dek1 for pericarp and aleurone layer thickness; THP9, Sh2, SUS1, Smk10, KW1, O7, and NKD1 for protein and starch biosynthesis; and VP5, CCD7, and Crti3 for carotene biosynthesis, which all influence endosperm vitreousness, a key factor determining kernel hardness for popping. Among these genes, KW1 and O7 stand out as pivotal genes with a significant impact on kernel-popping performance. These results provide a wealth of gene targets to greatly accelerate the molecular breeding of improved popcorn varieties.