Domestication and improvement history of melon from selection signal and genome-wide association analyses in 297 resequenced accessions

Authors: LIU, SHI - Northeast Agricultural University; GAO, PENG - Northeast Agricultural University; ZHU, QIANGLONG - Northeast Agricultural University; ZHU, ZICHENG - Northeast Agricultural University; LIU, HONGYU - Northeast Agricultural University; WANG, XUEZHENG - Northeast Agricultural University; Weng, Yiqun; GAO, MEILING - Qiqihar University; LUAN, FEISHI - Northeast Agricultural University

Submitted to: Plant Biotechnology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/12/2020
Publication Date: 6/20/2020
Citation: Liu, S., Gao, P., Zhu, Q., Zhu, Z., Liu, H., Wang, X., Weng, Y., Gao, M., Luan, F. 2020. Domestication and improvement history of melon from selection signal and genome-wide association analyses in 297 resequenced accessions. Plant Biotechnology Journal. (2020), pp. 1–14. https://doi.org/10.1111/pbi.13434.
DOI: https://doi.org/10.1111/pbi.13434

Interpretive Summary: Background information: Domestication and improvement are two important stages in crop evolution. Melon is an important vegetable crop with wide phenotypic diversity in many horticultural traits, especially for fruit size, flesh thickness, aroma, and sugar accumulation suggesting extensive selection during its evolution. However, selective signals in the two stages for the remarkable variation in melon remained unclear. Findings: In this manuscript, we reported re-sequencing and analysis of 297 wild, landrace, and improved melon accessions belonging to two different taxonomic groups: ssp. melo and ssp. agrestis. We obtained 2,045,412 high quality single nucleotide polymorphisms (SNPs). Population structure and genetic diversity analyses revealed independent and two-step selections in the two melon subgroups during melon breeding. Genome wide association analysis identified eight fruit size and seven flesh thickness signals overlapping with selective sweeps. Compared with the thin-skinned ssp. agrestis, thick-skinned ssp. melo melons have experienced a stronger selection for thicker edible pulp thickness. We show that in most melon accessions, the carpel number locus, CmCLV3 has pleiotropic effects on both carpel number and fruit shape. Two alcohol acyltransferases genes unique to the melon genome may have undergone strong selection in ssp. agrestis thus contributing to the characteristic aroma in melon as compared with other cucurbits. In contrast, the sucrose phosphate synthase 1 seems to be under a parallel evolution for sweet flesh across multiple cucurbit crops. Who cares? Findings from the present study provide novel insights into melon crop evolution. The work also provides new tools to advance melon breeding.

Technical Abstract: Domestication and improvement are two important stages in crop evolution. Melon (Cucumis melo L.) is an important vegetable crop with wide phenotypic diversity in many horticultural traits, especially for fruit size, flesh thickness, aroma, and sugar accumulation suggesting extensive selection during its evolution. However, selective signals in the two stages for the remarkable variation in melon remained unclear. We re-sequenced 297 wild, landrace, and improved melon accessions belonging to ssp. melo and ssp. agrestis and obtained 2,045,412 high quality single nucleotide polymorphisms (SNPs). Population structure and genetic diversity analyses revealed independent and two-step selections in C. melo ssp. melo and ssp. agrestis during melon breeding. Genome wide association analysis identified eight fruit size and seven flesh thickness signals overlapping with selective sweeps. Compared with the thin-skinned ssp. agrestis, thick-skinned ssp. melo melons have experienced a stronger selection for thicker edible pulp thickness. We show that in most melon accessions, the carpel number locus, CmCLV3 has pleiotropic effects on both carpel number and fruit shape. Two alcohol acyltransferases genes unique to the melon genome may have undergone strong selection in ssp. agrestis thus contributing to the characteristic aroma in melon as compared with other cucurbits. In contrast, the sucrose phosphate synthase 1 seems to be under a parallel evolution for sweet flesh across multiple cucurbit crops. Findings from the present study provide novel insights into melon crop evolution, and new tools to advance melon breeding.