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Watermelon domestication was shaped by stepwise selection and regulation of the metabolome

Science China(Life Sciences) 2023年第3期66卷 579-594页

作者： Pingli Yuan Congping Xu Nan He Xuqiang Lu Xingping Zhang Jianli Shang Hongju Zhu Chengsheng Gong Hanhui Kuang Tang Tang Yong Xu Shuangwu Ma Dexi Sun Weiqin Zhang Muhammad J.Umer Jian Shi Alisdair R.Fernie Wenge Liu Jie Luo Henan Joint International Research Laboratory of South Asian Fruits and Cucurbits Zhengzhou Fruit Research InstituteChinese Academy of Agricultural SciencesZhengzhou 450009China Hainan Yazhou Bay Seed Laboratory Sanya Nanfan Research Institute of Hainan UniversitySanya 572025China Peking University Institute of Advanced Agricultural Sciences Weifang 261325China College of Horticulture and Forestry Sciences Huazhong Agricultural UniversityWuhan 430070China Wuhan Metware Biotechnology Co. Ltd.Wuhan 430070China National Watermelon and Melon Improvement Center Beijing Academy of Agricultural and Forestry SciencesBeijing 100097China Max-Planck-Institute of Molecular Plant Physiology Potsdam-Golm 144776Germany College of Tropical Crops Hainan UniversityHaikou 572208China

Although crop domestication has greatly aided human civilization,the sequential domestication and regulation of most quality traits remain poorly understood.Here,we report the stepwise selection and regulation of major fruit quality traits that occurred during watermelon evolution.The levels of fruit cucurbitacins and flavonoids were negatively selected during speciation,whereas sugar and carotenoid contents were positively selected during domestication.Interestingly,fruit malic acid and citric acid showed the opposite selection trends during the improvement.We identified a novel gene cluster(CGC1,cucurbitacin gene cluster on chromosome 1)containing both regulatory and structural genes involved in cucurbitacin biosynthesis,which revealed a cascade of transcriptional regulation operating mechanisms.In the CGC1,an allele caused a single nucleotide change in Cl ERF1 binding sites(GCC-box)in the promoter of Cl Bh1,which resulted in reduced expression of Cl Bh1 and inhibition of cucurbitacin synthesis in cultivated watermelon.Functional analysis revealed that a rare insertion of 244 amino acids,which arose in C.amarus and became fixed in sweet watermelon,in Cl OSC(oxidosqualene cyclase)was critical for the negative selection of cucurbitacins during watermelon evolution.This research provides an important resource for metabolomics-assisted breeding in watermelon and for exploring metabolic pathway regulation mechanisms.

关键词： metabolome mGWAS gene cluster domestication cucurbitacin biosynthesis

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