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Genetic Mapping of a Major Gene Affecting Onion Bulb Fructan Content

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Genetic Mapping of a Major Gene Affecting Onion Bulb Fructan Content Theor Appl Genet (2006) 112: 958–967 DOI 10.1007/s00122-005-0199-5 ORIGINAL PAPER John McCallum Æ Andrew Clarke Meeghan Pither-Joyce Æ Martin Shaw Æ Ruth Butler Don Brash Æ John Scheffer Æ Ian Sims Sjaak van Heusden Æ Masayoshi Shigyo Michael J. Havey Genetic mapping of a major gene affecting onion bulb fructan content Received: 13 October 2005 / Accepted: 14 December 2005 / Published online: 11 January 2006 Ó Springer-Verlag 2006 Abstract The non-structural dry matter content of onion analysed on a dry weight basis, reducing sugar and bulbs consists principally of fructose, glucose, sucrose fructan content exhibited high negative correlations and and fructans. The objective of this study was to under- bimodal segregation suggestive of the action of a major stand the genetic basis for the wide variation observed in gene. A polymorphic SSR marker, ACM235, was iden- the relative amounts of these carbohydrates. Bulb car- tified which exhibited strong disequilibrium with bulb bohydrate composition was evaluated in progeny from fructan content in F2:3 families from the ‘W202A’ · crosses between high dry matter storage onion varieties ‘Texas Grano 438’ mapping population evaluated in two and sweet, low dry matter varieties. When samples were environments. This marker was mapped to chromosome 8 in the interspecific population ‘Allium cepa · A. roylei’. Mapping in the ‘Colossal Grano PVP’ · ‘Early Long- Communicated by P. Langridge keeper P12’ F2 population showed that a dominant J. McCallum (&) Æ M. Pither-Joyce Æ M. Shaw Æ R. Butler major gene conditioning high-fructan content lay in the New Zealand Institute for Crop and Food Research Limited, same genomic region. QTL analysis of total bulb fructan Private Bag 4704, Christchurch, New Zealand content in the intraspecific mapping population E-mail: [email protected] Tel.: +64-3-3256400 ‘BYG15-23’ · ‘AC43’ using a complete molecular mar- Fax: +64-3-3252074 ker map revealed only one significant QTL in the same chromosomal region. This locus, provisionally named A. Clarke Frc, may account for the major phenotypic differences in Institute of Molecular BioSciences, Massey University, Private Bag 11 222, Palmerston North, New Zealand bulb carbohydrate content between storage and sweet onion varieties. D. Brash New Zealand Institute for Crop and Food Research Limited, Private Bag 11600, Palmerston North, New Zealand J. Scheffer Abbreviations DM: Dry matter content Æ SSC: Soluble New Zealand Institute for Crop and Food Research Limited, solids content Æ PCA: Principal components analysis Cronin Rd, RD 1, Pukekohe, New Zealand REML: Restricted maximum likelihood Æ SSCP: Single-stranded conformation polymorphism I. Sims Industrial Research Limited, PO Box 31 310, Lower Hutt, New Zealand Introduction S. van Heusden Laboratory of Plant Breeding, Department of Plant Sciences, Wageningen University & Research Centre, AJ, Wageningen, Onions have been valued over millennia not only for The Netherlands their culinary qualities but also for their medicinal value, which has been confirmed by modern medical science M. Shigyo (Griffiths et al. 2002). Selection by growers and breeders Faculty of Agriculture, Yamaguchi University, 753-8515, Yamaguchi, Japan has produced cultivars with widely varying adaptation, bulb size, sweetness, storability and processing quality, M. J. Havey with correspondingly large variation in bulb carbohy- Agricultural Research Service, USDA, Department drate composition. Bulbs of onion and other Allium of Horticulture, , University of Wisconsin, species store fructans, fructose polysaccharides formed 1575 Linden Drive, Madison, WI 53706, USA by the cumulative addition of a fructosyl group to a 959 sucrose molecule, which also function as protectants Onion is an outcrossing, biennial diploid against cold and drought stress (Ritsema and Smeekens (2n=2x=16) with a very large genome (32 pg/2n; Jones 2003). Onions are a major source of dietary fructans, 1990). Genetic analyses in onion have previously been contributing 25% of the average American intake limited by laborious breeding systems, population het- (Moshfegh et al. 1999). Fructans enhance the value of erozygosity, limited genetic and DNA sequence re- onion as a functional food by conferring prebiotic sources, and poor knowledge of population structure. properties and lowering blood lipid and insulin levels The only extensive genetic dissection of bulb traits to (Ritsema and Smeekens 2003). date has been conducted in the cross ‘BYG15–23’ · Fructans, glucose, fructose and sucrose comprise the ‘AC43’ made between the storage onion ‘Brigham Yel- majority (65–80%) of onion bulb dry matter content low Globe’ and the low DM onion ‘Alisa Craig’ (King (Darbyshire and Henry 1978). Dry matter content (DM) et al. 1998). An initial QTL analysis identified several exhibits wide genetic variation, from around 6% in genomic regions affecting DM, soluble solids and other sweet onions up to over 25% in dehydration varieties correlated traits (Galmarini et al. 2001). A subsequent (Jones and Mann 1963) and is commonly estimated study based on analysis of fructan content from repli- indirectly as soluble solids content (SSC) by refractom- cated field trials confirmed that a genome region con- etry (Mann and Hoyle 1944). Although higher DM is taining a functionally characterised acid invertase gene associated with higher total fructan content, higher (Vijn et al. 1998) was associated with bulb sugar content degree of polymerisation (DP) and lower content of (Havey et al. 2004). fructose, glucose and sucrose (Darbyshire and Henry The objective of this research was therefore to iden- 1979), the relationship between carbohydrate content tify genome regions affecting onion bulb carbohydrate and bulb water content is poorly understood (Sinclair composition in crosses between commercially relevant et al. 1995a, b). storage and sweet onion varieties using PCR-based Onion contains fructans with DP 3–15 of the inulin markers. Analysis of phenotypic variation in several neo-series, in which b(1–2)-linked fructose chains can be independent pedigrees showed common patterns of attached to the fructose C1 or the glucose C6 of the variation, suggesting segregation of a major gene sucrose starter unit (Darbyshire and Henry 1978; Ernst affecting fructan content. Following identification of a et al. 1998; Vijn et al. 1997). Comparative chromato- linked marker, the onion linkage map (Martin et al. graphic analyses of bulb fructo-oligosaccharides from 2005) was used to confirm that a major gene in the same sweet, storage and dehydrator-type cultivars have shown genome region was the main determinant of fructan that C6-linked (neokestose) derivatives predominate content in all these populations. over C1-linked (1-kestose) types and that cultivar dif- ferences are primarily quantitative (Shiomi et al. 1997). Fructan biosynthesis is initiated by the enzyme sucrose- Materials and methods sucrose 1-fructosyltransferase (SS1FT), which catalyses the formation of 1-kestose from sucrose (Vijn et al. Plant material 1998). Chain elongation is catalysed by fructan:fructan 6G-fructosyltransferase (6G-FFT) and fructan:fructan Pair- and self-pollinations were carried out by enclosing 1-fructosyltransferase (1-FFT) activities. An onion umbels in perforated plastic bags and introducing blow- fructan:fructan fructosyltransferase cloned by Vijn et al. fly pupae. Mass pollinations were performed in 1.5 m3 (1998) was subsequently shown to be a bi-functional cages with honeybees. General plant husbandry and enzyme possessing both 6G-FFT and 1-FFT activities post-harvest practices were as described in McCallum capable of producing the entire range of fructans ob- et al. (2001a). Field evaluations of F2 populations were served in onion (Fujishima et al. 2005; Ritsema et al. conducted by transplanting three plots of 40 plants each 2003). In vitro (Kahane et al. 2001a) and field-based of the F2, maternal and paternal populations in a 3·3 (Kahane et al. 2001b) studies of bulb fructan accumu- Latin Square design. lation during development have shown that lines with The ‘Colossal Grano’ · ‘Early Longkeeper P12’ high DM continue to accumulate fructan throughout (C·P12) population was derived by self-pollinating an bulbing but low DM lines plateau early, suggesting F1 bulb from the pair cross ‘Colossal PVP’ (lot 37018 stronger sink strength in high DM lines. Sunseeds) · ‘Early Longkeeper P12’ (Crop & Food Onion bulb carbohydrate content is highly heritable. Research). Parental and F2 plants were grown hydro- Several studies have obtained broad-sense heritability ponically without supplementary lighting in the glass- estimates of 0.6–0.83 for bulb SSC and also reported house at Lincoln, New Zealand (lat 43°39¢), in a high significant correlation with other traits such as bulb size sulphur medium (4 Meq lÀ1 S) as described previously and pungency (Galmarini et al. 2001; Kadams and (McCallum et al. 2002; Randle et al. 1995). Six 18 l tubs Nwasike 1986; Lin et al. 1995; McCollum 1968; Simon each containing nine F2 plants and two tubs of nine 1995). Many dehydration onion breeding programmes plants of each parental line were transplanted in October have also made substantial progress in raising DM 1999 and 2000, harvested in late January and cured for through selection (Wall and Corgan 1999). 2 weeks in the glasshouse. 960 The ‘W429A’ · ‘Houston Grano’ F2 population was fractionated by HPLC on a 220·4.6 mm Applied derived by self-pollinating a single F1 bulb from the pair Biosystems (Foster City, CA, USA) Brownlee
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