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

Authors: GUO, SHAOGUI - Beijing Academy Of Agricultural Sciences; ZHAO, SHENGIE - Chinese Academy Of Agricultural Sciences; SUN, HONGHE - Cornell University; WANG, XIN - Cornell University; WU, SHAN - Cornell University; LIN, TAO - Chinese Academy Of Agricultural Sciences; REN, YI - Beijing Academy Of Agricultural Sciences; DENG, YUN - Chinese Academy Of Agricultural Sciences; ZHANG, JIE - Beijing Academy Of Agricultural Sciences; LU, XUQIANG - Chinese Academy Of Agricultural Sciences; ZHANG, HAIYING - Beijing Academy Of Agricultural Sciences; SHANG, JIANLI - Chinese Academy Of Agricultural Sciences; GONG, GUOYI - Beijing Academy Of Agricultural Sciences; WEN, CHANGLONG - Beijing Academy Of Agricultural Sciences; HE, NAN - Chinese Academy Of Agricultural Sciences; LI, MAOYING - Beijing Academy Of Agricultural Sciences; LIU, JUNPU - Chinese Academy Of Agricultural Sciences; WANG, YANPING - Beijing Academy Of Agricultural Sciences; ZHU, YINGCHUN - Beijing Academy Of Agricultural Sciences; TIAN, SHOUWEI - Beijing Academy Of Agricultural Sciences; Jarret, Robert - Bob; Levi, Amnon; HUANG, SANWEN - Chinese Academy Of Agricultural Sciences; FEI, ZHANGJUN - Cornell University; LIU, WENGE - Chinese Academy Of Agricultural Sciences; XU, YONG - Beijing Academy Of Agricultural Sciences

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/29/2019
Publication Date: 11/1/2019
Citation: Guo, S., Zhao, S., Sun, H., Wang, X., Wu, S., Lin, T., Ren, Y., Deng, Y., Zhang, J., Lu, X., Zhang, H., Shang, J., Gong, G., Wen, C., He, N., Li, M., Liu, J., Wang, Y., Zhu, Y., Tian, S., Jarret, R.L., Levi, A., Huang, S., Fei, Z., Liu, W., Xu, Y. 2019. Resequencing of 414 cultivated and wild watermelon accessions identifies selection for fruit quality traits. Nature Genetics. 51:1616–1623. https://doi.org/10.1038/s41588-019-0518-4.
DOI: https://doi.org/10.1038/s41588-019-0518-4

Interpretive Summary: Watermelon is an important vegetable fruit crop which has been domesticated and consumed by people throughout the world for many decades. Because of the many years of domestication and selection, today’s watermelon cultivars have desirable fruit qualities that do not exist in watermelons that naturally exist in the wild. There is no sufficient information about the genome and genes of watermelon. The main objective of this study was to use advance genomic technologies to elucidate the differences between the genomes of cultivated sweet watermelons versus these of wild watermelons. In this study, ARS scientists collaborated with scientists at Cornell University and scientists at research institutes in China on using advance genomic technologies to sequence and assemble of the watermelon genome. This study not only elucidates the differences between the modern versus wild type watermelon genomes, but also identified important gene sequences associated with resistance to diseases of watermelon which have been lost during the many years of domestication. This study also provides genomic tools valuable for breeders and scientists aiming to improve watermelon with resistance to diseases and pests and with nutritional content.

Technical Abstract: Fruit characteristics of dessert watermelon are largely the results 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 C. amarus and the lineage containing C. lanatus and C. mucosospermus. Our findings indicate that different loci affecting watermelon fruit size have been under selection during evolution, domestication and improvement. A non-bitter allele, arising in the progenitor of dessert watermelon, is largely fixed in Citrullus lanatus. Selection for flesh sweetness started in the progenitor of C. lanatus and continues through modern breeding through 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 shed light on watermelon evolution and breeding history.