Molecular Plant Breeding 2024, Vol.15, No.3, 112-131 http://genbreedpublisher.com/index.php/mpb 112 Invited Review Open Access From Ancestors to Modern Cultivars: Tracing the Origin, Evolution, and Genetic Progress in Cucurbitaceae Xuehao Chen , Xiaohua Qi, Xuewen Xu School of Horticulture and Landscape Architecture, Yangzhou University, Yangzhou, 225009, Jiangsu, China Corresponding email: xhchen@yzu.edu.cn Molecular Plant Breeding, 2024, Vol.15, No.3 doi: 10.5376/mpb.2024.15.0013 Received: 20 Feb., 2024 Accepted: 27 Apr., 2024 Published: 27 Jun, 2024 Copyright © 2024 Chen et al., This is an open access article published under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Preferred citation for this article: Chen X.H., Qi X.H., and Xu X.W., 2024, From ancestors to modern cultivars: Tracing the origin, evolution, and genetic progress in Cucurbitaceae, Molecular Plant Breeding, 15(3): 112-131 (doi: 10.5376/mpb.2024.15.0013) Abstract The Cucurbitaceae family, encompassing a wide array of economically significant species, has undergone extensive evolutionary diversification since its origin in the Late Cretaceous period. This systematic review synthesizes the current understanding of the genetic and evolutionary trajectories within the Cucurbitaceae, tracing the lineage from ancestral forms to modern cultivars. We integrate findings from whole-genome analyses, phylogenetic studies, and gene family evolution research to construct a comprehensive picture of the genetic progress in this family. The review highlights the whole-genome duplication event in the Cucurbita genus approximately 30 million years ago, which has led to a rapid turnover and neofunctionalization of protein-coding and long noncoding RNA genes, particularly in Cucurbita argyrosperma. Additionally, the evolution of Benincasa hispida is examined, revealing its unique phylogenetic position and significant gene loss from its common ancestor, alongside the conservation of the phenylalanine ammonia-lyase gene family across six Cucurbitaceae species. The phylogenetic relationships within the family are clarified, with an emphasis on the major clades and their geographical distributions, as well as the need for further ecological and morphological studies. This review provides valuable insights into the genetic mechanisms underlying the diversity and adaptation of Cucurbitaceae species, offering a foundation for future research and breeding programs. Keywords Cucurbitaceae; Evolution; Genome duplication; Gene turnover; Neofunctionalization; Phylogenetics; Phenylalanine ammonia-lyase; Cucurbita argyrosperma; Benincasa hispida; Genetic diversity 1 Introduction The Cucurbitaceae family, encompassing a wide array of economically and nutritionally significant crops, is pivotal to both agriculture and dietary regimes across the globe. This family includes a variety of species such as watermelon, honey melon, cucumber, squash, zucchini, and pumpkin, which are integral to human consumption and cultural practices. The systematic review titled “From Ancestors to Modern Cultivars: Tracing the Origin, Evolution, and Genetic Progress in Cucurbitaceae” aims to delve into the rich tapestry of this plant family’s history, examining its evolutionary trajectory and the genetic advancements that have been achieved through selective breeding practices. Cucurbitaceae crops are some of the world’s most valuable, with their domestication dating back to at least 11 000 years ago in various regions including the New World, Asia, and more recently, Africa (Chomicki et al., 2019). The significance of these crops extends beyond their economic value, as they have played a crucial role in the development of human civilizations, providing sustenance and hydration, especially in arid regions where watermelons were cultivated as a source of fresh water (Paris, 2016). The diversity within the Cucurbitaceae family is remarkable, with a history of widespread dispersal and adaptation. Phylogenetic studies have traced the family’s origin to Asia in the Late Cretaceous, followed by numerous transoceanic dispersal events that have led to their current global distribution (Schaefer et al., 2009). This genetic diversity is not only of academic interest but also has practical implications for breeding programs aimed at improving crop resilience and nutritional content (Velkov and Petkova, 2014). This systematic review will provide a detailed account of the Cucurbitaceae family’s journey from wild ancestors to the diverse and essential cultivars of today, offering insights into the genetic progress that has shaped these crops and setting the stage for future innovations in cucurbit research and cultivation.
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