Genetic Architecture of Fruit Size Variation in Cucurbits: a comparative perspective

Authors: PAN, YUPENG - University Of Wisconsin; WANG, YUHUI - University Of Wisconsin; MCGREGOR, CELILIA - University Of Georgia; LIU, SHI - Northeast Agricultural University, China; LUAN, FEISHI - Northeast Agricultural University, China; MEILING, GAO - Qiqihar University; Weng, Yiqun

Submitted to: Theoretical and Applied Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/5/2019
Publication Date: 11/25/2019
Citation: Pan, Y., Wang, Y., McGregor, C., Liu, S., Luan, F., Meiling, G., Weng, Y. 2019. Genetic architecture of fruit size and shape variation in cucurbits: a comparative perspective. Theoretical and Applied Genetics. 133:1-21. https://doi.org/10.1007/s00122-019-03481-3.
DOI: https://doi.org/10.1007/s00122-019-03481-3

Interpretive Summary: Cucurbits include many economically important fruit vegetable crops such as cucumber, melon, watermelon, pumpkin/squash and various gourds. The cucurbits are best known for their diverse fruit size, shape (FS) and color, which is controlled by quantitative trait loci (QTL). However, little is known about the genetic basis and molecular regulation of fruit size variation in cucurbit crops. Rapid progress has been made recently in identification and cloning of fruit size QTL. A systematic review and assessment of the work is lacking. We conducted extensive review of the literature in the last 50 years on work in fruit size variation in cucurbits focusing on cucumber, melon and watermelon. Based on information gathered from numerous studies in these crops, we were able to synthesize QTL information from these studies and establish19, 33, and 21 consensus fruit size QTL in the three crops. Several genes controlling fruit or grain size variation have been cloned in tomato, Archbishops, and rice. These genes encode proteins carrying characteristic domains like CNR, CSR, CYP78A, IQD, OVATE, TRM, and YABBY. Through bioinformatic analysis of the genome data, we identified 107, 102 and 98 homologs of the 7 genes in cucumber, melon and watermelon, respectively. Comparative analysis of consensus QTL locations and candidate gene locations revealed conservation of fruit size gene structure and function among different cucurbit crops. At the same time, some fruit size QTL are mapped in unique position in a particular cucurbit crop. This may imply a novel genetic basis for fruit size control. This work also revealed the pleiotropic effects of the andromonoecious and carpel number genes on fruit size/shape in cucurbits. This is the first comprehensive review of QTL mapping on fruit size variation across cucurbit crops. The present work illustrates the power of comparative analysis in understanding the genetic architecture of fruit size variation, which should greatly facilitate map-based cloning of FS QTL in cucurbit crops. This work provides theoretical basis on the conservation of molecular mechanisms of fruit size variation in cucurbit crops. The results also help cucurbit breeders in marker-assisted selection in cucurbit breeding.

Technical Abstract: The Cucurbitaceae family harbors many economically important fruit vegetable crops (cucurbits) such as cucumber, melon, watermelon, pumpkin/squash and various gourds. The cucurbits are best known for their diverse fruit size and shape (FS), which is controlled by quantitative trait loci (QTL). In cucurbits, little is known on the molecular regulation of FS variation, but rapid progress has been made recently in identification and cloning of FS QTL. Here we conducted extensive literature review and summarized FS QTL identified in cucumber, melon and watermelon; synopsis of QTL information allowed establishment of 19, 33 and 21 draft genome-anchored consensus FS QTL in the three crops. Several genes underlying FS or grain size variation have been cloned in tomato, Arabidopsis, and rice which belong to gene families encoding proteins with following characteristic domains: CNR (cell number regulator), CSR (cell size regulator), CYP78A (P450), IQD/SUN, OVATE/OFP (Ovate Family Protein), TRM (TONNEAU1 Recruiting Motif), and YABBY. We performed domain-based genome-wide searches and identified 107, 102 and 98 homologs of the 7 genes in cucumber, melon and watermelon, respectively. Most consensus FS QTL are co-localized with multiple members of different FS gene families including the cloned FS QTL, CsFS1.2, CsFS2.1 in cucumber, CmFS8.3 in melon, and ClFS3.2 (the O locus) in watermelon suggesting conservation of FS gene structure and function among cucurbits. Some FS QTL are mapped in regions with no homologs of known FS genes, which may imply a novel genetic basis for FS variation in cucurbits. In addition, in three crops, consensus FS QTL are also co-localized with the andromonoecious and carpel number loci which are known to have pleiotropic effects on fruit size/shape in cucurbits. The present work illustrates the power of comparative analysis in understanding the genetic architecture of FS variation, which should greatly facilitate map-based cloning of FS QTL in cucurbit crops.