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QTL Mapping of Parthenocarpic Fruit Set in North American Processing Cucumber

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QTL Mapping of Parthenocarpic Fruit Set in North American Processing Cucumber Theor Appl Genet (2016) 129:2387–2401 DOI 10.1007/s00122-016-2778-z ORIGINAL ARTICLE QTL mapping of parthenocarpic fruit set in North American processing cucumber Calvin D. Lietzow1 · Huayu Zhu1 · Sudhakar Pandey1,2 · Michael J. Havey1,3 · Yiqun Weng1,3 Received: 7 July 2016 / Accepted: 24 August 2016 / Published online: 31 August 2016 © Springer-Verlag Berlin Heidelberg (outside the USA) 2016 Abstract expression in cucumber remain largely unknown. Since Key message Through a novel phenotyping method, parthenocarpy is an important yield component, it is dif- four QTLs were consistently associated with increased ficult to separate the true parthenocarpic character from parthenocarpic fruit set in North American processing other yield related traits. In the present study, we devel- cucumber that accounted for over 75 % of observed oped a novel phenotypic approach for parthenocarpic fruit phenotypic variation. set focusing on early fruit development. Two hundred and Abstract Parthenocarpy is a desirable trait with poten- five 3F families derived from a cross between the highly tial for increasing yield and quality in processing cucum- parthenocarpic line 2A and low parthenocarpic line Gy8 ber production. Although many successful parthenocarpic were phenotypically evaluated in three greenhouse experi- fresh market cucumber varieties have been developed, the ments. Seven QTLs associated with parthenocarpic fruit set genetic and molecular mechanisms behind parthenocarpic were detected. Among them, one each on chromosomes 5 and 7 (parth5.1 and parth7.1) and two on chromosome 6 (parth6.1 and parth6.2) were consistently identified in all Communicated by S. Huang. experiments, but their relative contribution to the total phe- notypic variation was dependent on plant growth stages. Electronic supplementary material The online version of this While each of the four QTLs had almost equal contribution article (doi:10.1007/s00122-016-2778-z) contains supplementary material, which is available to authorized users. to the expression of the trait at commercial harvest stage, parth7.1 played an important role in early parthenocarpic * Yiqun Weng fruit set. The results suggested that parthenocarpic fruit [email protected]; [email protected] set can be accurately evaluated with as few as 20 nodes Calvin D. Lietzow of growth. The QTLs identified in this study for partheno- [email protected] carpic fruit set are a valuable resource for cucumber breed- Huayu Zhu ers interested in developing parthenocarpic cultivars and to [email protected] researchers interested in the genetic and molecular mecha- Sudhakar Pandey nisms of parthenocarpic fruit set. [email protected] Michael J. Havey [email protected] Introduction 1 Department of Horticulture, University of Wisconsin- Madison, Madison, WI 53706, USA Fertilization and fruit development are critical to repro- duction and dispersal of flowering plants. Upon success- 2 Indian Institute of Vegetable Research, Varanasi, Uttar Pradesh 221 305, India ful pollination and fertilization, a number of physiologi- cal events occur that lead to the development of fruit and 3 USDA‑ARS Vegetable Crops Research Unit, Horticulture Department, University of Wisconsin-Madison, Madison, seed. In some instances, fruit set can occur independent WI 53706, USA of pollination and/or fertilization, which is referred to as 1 3 2388 Theor Appl Genet (2016) 129:2387–2401 parthenocarpy. Parthenocarpy can be obligatory in which greenhouse production (Sturtevant 1890). Most fresh mar- the plants always produce seedless fruits or facultative in ket cucumbers grown in protected environments today are which production of seedless fruits occurs only when pol- parthenocarpic. Parthenocarpic pickling cultivars are also of lination is prevented. Parthenocarpy is a desirable trait for major importance in Europe. In the US, the majority of pro- the production of fruit and vegetable crops with undesir- cessing cucumbers are grown in a once-over machine har- able large and/or hard seeds. In commercial production, vest production system (Tatlioglu 1992), and parthenocarpic parthenocarpic cultivars are especially beneficial when pol- cultivars have not been widely used. The yields of US pro- lination is difficult or heavily impacted by environmental cessing cucumber have not substantially increased since the conditions. 1980’s (Gusmini and Wehner 2008). A phenomenon known The developmental switch that turns a gynoecium into a as first fruit inhibition, where the first fertilized fruit inhib- growing fruit depends on the fertilization of ovules. In most its the growth of subsequent fruits is thought to be a major angiosperms, the gynoecium dies if not fertilized (O’Neill obstacle to yield improvement in cucumber with once- and Nadeau 1997). Following pollination and fertilization, over machine harvest production systems (Denna 1973; de various phytohormones play critical roles in the initiation Ponti 1976; El-Shawaf and Baker 1981; Sun et al. 2006a). of fruit and seed development (Gillaspy et al. 1993; Sey- A potential solution is the use of gynoecious (expression of mour et al. 2013). As such, parthenocarpic fruit produc- only pistillate flowers) parthenocarpic cucumber varieties. tion can be artificially induced by exogenous application The use of gynoecy in combination with parthenocarpy is of plant growth regulators, such as auxin, gibberellic acid, necessary as cucumber exhibits facultative parthenocarpy, cytokinin, brassinosteroids, or their combinations (e.g., meaning seeded fruit set can occur in parthenocarpic vari- Robinson et al. 1971; Schwabe and Mills 1981; Gorguet eties exposed to a pollen source. Gynoecious varieties et al. 2005; Fu et al. 2008; Vriezen et al. 2008; Pandolfini also benefit from increased numbers of pistillate flowers, 2009; Pascual et al. 2009; Serrani et al. 2010). Partheno- and thus greater opportunities for fruit set. Parthenocarpic carpic expression in crop plants can also be manipulated cucumber varieties offer several advantages over conven- through transgenic expression of regulator genes in hor- tional seeded varieties. Parthenocarpic varieties are able mone signaling pathways. For example, parthenocarpic to set fruits sequentially without suffering from first fruit fruit set has been achieved by expression of the ovule-spe- inhibition (Denna 1973; Sun et al. 2006a). Parthenocarpic cific auxin-synthesizing DefH9-iaaM transgene construct varieties do not require pollination, and are therefore less in tomato, eggplant, strawberry, raspberry, and cucumber vulnerable to poor pollination conditions (abiotic and biotic) (Rotino et al. 1997; Ficcadenti et al. 1999; Donzella et al. and the need for insect pollinators (Pike and Peterson 1969; 2000; Mezzetti et al. 2004; Yin et al. 2006). TPRP-F1-rolB, de Ponti 1976; Varoquaux et al. 2000; Sun et al. 2006a). a second transgenic ovary-specific auxin-synthesizing con- In addition, parthenocarpic varieties often have more uni- struct has also been demonstrated to induce parthenocarpic formly shaped fruit desired by the processing industry (de expression in grape, tomato, and eggplant (Carmi et al. Ponti 1976; Aalbersberg and van Wijchen 1987). 2003; Rotino et al. 2005; Costantini et al. 2007). Parthenocarpic fruit set in cucumber has been manipu- Naturally occurring (genetic) parthenocarpy has been lated both genetically and with the exogenous application observed in many plants and parthenocarpic cultivars are of various synthetic phytohormones. The application of common in citrus (Citrus spp.), grape (Vitis spp), cucur- auxin, cytokinin, gibberellic acid, brassinosteroids, and bit, and solanaceous crops. In several species, the mode of auxin transport inhibitors all result in the induction of par- inheritance for parthenocarpic fruit set has been investi- thenocarpic fruit set in cucumber (e.g., Choudhury and gated and varies from a single gene to multiple quantitative Phatak 1959; Robinson et al. 1971; Beyer and Quebedeaux trait loci (QTLs). For example, in tomato several parthe- 1974; Elassar et al. 1974; Cantliffe and Phatak 1975; Kim nocarpic genes or QTLs have been identified (Mazzucato et al. 1992a; Fu et al. 2008). However, this method has et al. 1998; Fos et al. 2000, 2003; Beraldi et al. 2004; many drawbacks, including the need for continuous appli- Gorguet et al. 2005, 2008). Miyatake et al. (2012) identi- cation of phytohormones throughout growth, increased fied two major-effect QTLs controlling parthenocarpic fruit input costs for growers, environmental impact concerns, set in eggplant (Solanum melongena). In summer squash and human dietary concerns related to consumption of phy- (Cucurbita pepo L.), parthenocarpy was shown to be con- tohormones (Rotino et al. 1997). trolled by a single gene with incomplete dominance (de The mode of genetic inheritance for parthenocarpic fruit Menezes et al. 2005). In citrus, parthenocarpy is controlled set in cucumber remains unresolved although highly suc- by at least two dominant complementary genes (Vardi et al. cessful parthenocarpic greenhouse cultivars have been 2008). developed. Genetic studies have been largely inconsistent Parthenocarpic development of cucumber fruit has on the mode of inheritance for parthenocarpy in cucumber long been recognized as an important characteristic for and have ranged from proposals of a single gene to complex 1 3 Theor Appl Genet (2016) 129:2387–2401 2389 multigenic inheritance (for example, Pike and Peterson 1969; de Ponti and Garretson de Ponti and Garretsen
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