Dissection of the domestication-shaped genetic architecture of lettuce primary metabolism

Lettuce (Lactuca sativa L.) is an important vegetable crop species worldwide. The primary metabolism of this species is essential for its growth, development and reproduction as well as providing a considerable direct source of energy and nutrition for humans. Here, through investigating 77 primary metabolites in 189 accessions including all major horticultural types and wild lettuce L. serriola we showed that the metabolites in L. serriola were different from those in cultivated lettuce. The findings were consistent with the demographic model of lettuce and supported a single domestication event for this species. Selection signals among these metabolic traits were detected. Specifically, galactinol, malate, quinate and threonate were significantly affected by the domestication process and cultivar differentiation of lettuce. Galactinol and raffinose might have been selected during stem lettuce cultivation as an adaption to the local environments in China. Furthermore, we identified 154 loci significantly associated with the level of 51 primary metabolites. Three genes (LG8749721, LG8763094 and LG5482522) responsible for the levels of galactinol, raffinose, quinate and chlorogenic acid were further dissected, which may have been the target of domestication and/or affected by local adaptation. Additionally, our findings strongly suggest that human selection resulted in reduced quinate and chlorogenic acid levels in cultivated lettuce. Our study thus provides beneficial genetic resources for lettuce quality improvement and sheds light on the domestication and evolution of this important leafy green.