The haplotype-resolved genome assembly of an ancient citrus variety provides insights into the domestication history and fruit trait formation of loose-skin mandarins

Abstract

Loose-skin mandarins (LSMs) are among the oldest domesticated horticultural crops, yet their domestication history and the genetic basis underlying the formation of key selected traits remain unclear. We provide a chromosome-scale and haplotype-resolved assembly for the ancient Chinese citrus variety Nanfengmiju tangerine. Through the integration of 77 resequenced and 114 published citrus germplasm genomes, we categorize LSMs into 12 distinct groups based on population genomic analyses. We infer that the ancestors of modern cultivated mandarins diverged from wild mandarins in Daoxian approximately 500,000 years ago, when they entered the Yangtze and Pearl River Basins. There, they were domesticated into four ancient cultivation groups, forming the cornerstone of modern Chinese LSM cultivation. We identify selective sweeps underlying quantitative trait loci and genes related to important fruit quality traits, including sweetness and size. We reveal that the co-selection of sugar transporter and metabolism genes are associated with increased fruit sweetness. Significant alterations in the auxin and gibberellin signaling networks may contribute to the enlargement of LSM fruits. We also provide a comprehensive, high-spatiotemporal-resolution atlas of allelic gene expression during citrus fruit development. We detect 5890 allele pairs showing specific expression patterns and a significant increase in variation levels. Our study provides valuable genomic resources and further revises the origin and domestication history of LSMs, offering insights for genetic improvement of citrus plants.