Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits

Sheng Guo ,Yun Deng,Shan Wu,Amnon Levi,Nan He,Changlong Wen,Xin Wang,Sanwen Huang,Robert L Jarret ,Yanping Wang,Tao Lin,Wenge Liu,Junpu Liu,Xingrong Lu ,Xingping Zhang,Yi Ren,Haiying Zhang,Shouwei Tian,Lei Gao,Jie Zhang,Yingchun Zhu ,Maoying Li,Jianli Shang,Zhangjun Fei,Guoyi Gong,Honghe Sun,Shengjie Zhao,Yong Xu

doi:10.1038/s41588-019-0518-4

Abstract

Fruit characteristics of sweet watermelon are largely the result of human selection. Here we report an improved watermelon reference genome and whole-genome resequencing of 414 accessions representing all extant species in the Citrullus genus. Population genomic analyses reveal the evolutionary history of Citrullus, suggesting independent evolutions in Citrullus amarus and the lineage containing Citrullus lanatus and Citrullus mucosospermus. Our findings indicate that different loci affecting watermelon fruit size have been under selection during speciation, domestication and improvement. A non-bitter allele, arising in the progenitor of sweet watermelon, is largely fixed in C. lanatus. Selection for flesh sweetness started in the progenitor of C. lanatus and continues through modern breeding on loci controlling raffinose catabolism and sugar transport. Fruit flesh coloration and sugar accumulation might have co-evolved through shared genetic components including a sugar transporter gene. This study provides valuable genomic resources and sheds light on watermelon speciation and breeding history.

Highlights

Watermelon (Citrullus lanatus, 2n = 2 × = 22) is one of the most popular fruit crops worldwide
Combined with previous findings on genome organization differences between C. amarus and C. lanatus shown by ribosomal DNA chromosome landmarks[6,11] and indicated by non-Mendelian segregation in genetic populations derived from crosses between C. amarus and C. lanatus[12], these results suggest that C. amarus and the lineage including C. mucosospermus and C. lanatus might have been derived from different ancestral populations or evolved independently after divergence
The mutants showed substantially reduced soluble sugars, glucose, fructose and sucrose contents in fruit flesh, but had increased raffinose content (Supplementary Fig. 12d). These results indicate that ClAGA2 contributes to sugar accumulation in watermelon fruit flesh through facilitating the metabolism of raffinose into glucose, fructose and sucrose, and could have already been selected for early on in the progenitor of sweet watermelon, as indicated by the already reduced genetic diversity in C. mucosospermus

Summary

Introduction

Watermelon (Citrullus lanatus, 2n = 2 × = 22) is one of the most popular fruit crops worldwide It belongs to the Citrullus genus of the Cucurbitaceae family, and originated in Africa[1]. Modern breeding of sweet watermelon has focused primarily on fruit quality traits, such as sugar content, flesh color and rind pattern, resulting in a narrow genetic base of sweet watermelon[3]. C. colocynthis, C. amarus and C. mucosospermus have been used in breeding programs to identify new sources of disease and pest resistance for the improvement of sweet watermelon[3]. Our study identifies a number of candidate loci associated with fruit quality traits and provides insights into the speciation and domestication of the modern sweet watermelon

Methods

Results

Conclusion