Abstract
The objective of this study was to identify molecular markers linked to fruit-related traits in the tomato subjected to high temperatures. In total, 160 F2 plants derived from a cross between a heat-tolerant breeding line, CL5915-93D4-1-0-3 (Solanum esculentum), and a heat-sensitive wild accession, L4422 (S. pimpinellifolium), were grown in a greenhouse. Six traits including fruit number, fruit weight, brix, seed number, fruit setting, and flower number were scored. The distributions of fruit number, fruit set, flower number, and seed number were skewed towards heat susceptibility which is known to be characteristic of L4422. Polymorphic bands were generated by PCR-derived methods of RAPD, ISSR and AFLP Polymorphism, the segregation ratio, and distribution over the genome of the above 3 markers were compared. Ten linkage groups, ranging 20.6–151.6 cM in size, were constructed with 62 informative markers spanning a total of 776.3 cM. Fruit-related quantitative trait loci (QTLs) were non-randomly distributed in the tomato genome. For the 6 traits investigated, 21 QTLs were dispersed on linkage groups 2–5. The genetic effects of the various QTLs were differently exhibited, in our study we have respectively found from 10.5% to 30.2% of the variation explained by the QTL for flower number (FRN4) and brix (BX2). Thirteen QTL-mapped markers were unique to 1 trait, and 4 markers were linked to more than 1 trait. Among them, QTLs linked to the I868-470 marker had effects on fruit weight and brix, and a significant positive correlation between these 2 traits was noted (r = 0.35, P < 0.05). Thus, the I868-470 marker may have the potential for simultaneous selection of high fruit weight and brix. These markers also allowed us to align genome linkage maps across distantly related species and to reveal the co-localization between these QTLs and major genes.
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References
AVRDC (1993) Asian Vegetable Research and Development Center report. AVRDC, Taiwan
AVRDC (1997) Asian Vegetable Research and Development Center report. AVRDC, Taiwan
Bai Y, Feng X, Van der Hulst R, Lindhout P (2004) A set of simple PCR markers converted from sequence specific RFLP markers on tomato chromosomes 9 to 12. Mol Breed 13:281–287
Basten CB, Weir BS, Zeng ZS (2002) QTL cartographer: a reference manual and tutorial for QTL map**. Department of Statistics, North Carolina State University, Raleigh, NC
Bernacchi D, Tanksley SD (1997) An interspecific backcross of Lycopersicon esculentum × Lycopersicon hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. Genetics 147:861–877
Bernacchi D, Beck-Bunn T, Eshed Y, Lopez J, Petiard V, Zamir D, Tanksley SD (1998) Advanced backcross QTL analysis in tomato. I. Identification of QTLs for traits of agronomic importance from Lycopersicon hirsutum. Theor Appl Genet 97:381–397
Causse M, Duffe P, Buret M (2004) A genetic map of candidate genes and QTL involved in tomato fruit size and composition. J Exp Bot 55:1671–1685
Chen FQ, Foolad MR (1999) A molecular linkage map of tomato based on a cross between Lycopersicon esculentum and L. pimpinellifolium and its comparison with other molecular maps of tomato. Genome 42:94–103
Chen KY, Tanksley SD (2004) High resolution map** and functional analysis of se2.1: a major stigma exsertion quantitative trait locus associated with the evolution from allogamy to autogamy in the genus Lycopersicon. Genetics 168:1563–1573
Chen FQ, Foolad MR, Hyman J, Clair DA, Beelaman RB (1999) Map** of QTLs for lycopene and other fruit traits in a Lycopersicon esculentum × L. pimpinellifolium cross and comparison of QTLs across tomato species. Mol Breed 5:283–299
Chetelat RT, Meglic V (2000) Molecular map** of chromosome segments introgressed from Solanum lycopersicoides into cultivated tomato (Lycopersicon esculentum). Theor Appl Genet 100:232–241
de Vicent MC, Tanksley SD (1993) QTL analysis of transgressive segregation in an interspecific tmato cross. Genetics 134:585–596
Doerge RW, Churchill GA (1996) Permutation tests for multiple loci affecting a quantitative character. Genetics 142:285–294
Doganlar S, Frary A, Ku HM, Tanksley SD (2002) Map** quantitative trait loci in inbred backcross lines of Lycopersicon pimpinellifolium (LA1589). Genome 45:1189–1202
Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine map** of yield-associated QTLs. Genetics 141:1147–1162
Foolad MR (2007) Genome map** and molecular breeding of tomato. Int J Plant Genome 2007:64358
Fray A, Nesbitt TC, Grandillo S, Knaap E, Liu J, Elber R, Alpert KB, Tanksley SD (2000) fe2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
Fridman E, Pleban T, Zamir D (2000) A recombination hotspot delimits a wild-species quantitative trait locus for tomato sugar content to 484 bp within an invertase gene. Proc Natl Acad Sci USA 97:4718–4723
Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305:1786–1789
Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209
Fulton TM, Beckbunn T, Emmatty D, Eshed Y, Lopez J, Petiard V, Zamir D, Tanksley SD (1997) QTL analysis of an advanced backcross of Lycopersicon peruvianum to the cultivated tomato and comparisons with QTLs found in other wild specifics. Theor Appl Genet 95:881–894
Fulton TM, Grandillo S, Beck-Bunn T, Fridman E, Frampton A, Lopez J (2000) Advanced backcross QTL analysis of a Lycopersicon esculentum × Lycopersicon parviflorum cross. Theor Appl Genet 100:1025–1042
Georgelis N, Scott JW, Baldwin EA (2004) Relationship of tomato fruit sugar concentration with physical and chemical traits and linkage of RAPD markers. J Am Soc Hort Sci 129:839–845
Goldman IL, Paran I, Zamir D (1995) Quantitative trait locus analysis of a recombinant inbred line population derived from a Lycopersicum esculentum × Lycopersicum cheesmanii cross. Theor Appl Genet 90:925–932
Grandillo S, Tanksley SD (1996) Analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92:935–951
Grandillo S, Ku HM, Tanksley SD (1999) Identifying the loci responsible for natural variation in fruit size and shape in tomato. Theor Appl Genet 99:978–987
Gur A, Zamir D (2004) Unused natural variation can lift yield barriers in plant breeding. PLoS Biol 2:1610–1615
Gur A, Semel Y, Cahaner A, Zamir D (2004) Real time QTL of complex phenotypes in tomato interspecific introgression lines. Trends Plant Sci 9:33–39
Haanstra JP, Wye C, Verbakel H, Meijer DF, Van Den BP, Odinot P, Van Heusden AP, Tanksley SD, Lindhout P, Peleman J (1999) An integrated high density RFLP-AFLP map of tomato based on two Lycopersicon esculentum × L. pennellii F2 populations. Theor Appl Genet 99:254–271
Jiang C, Zeng ZB (1995) Multiple trait analysis of genetic map** of quantitative trait loci. Genetics 140:1111–1127
Knaap EV, Tanksley SD (2003) The making of a bell pepper-shaped tomato fruit: identification of loci controlling fruit morphology in Yellow Stuffer tomato. Theor Appl Genet 107:139–147
Kosambi DD (1994) The estimation of map distance from recombination values. Ann Eugenet 12:172–175
Labate JA, Baldo AM (2005) Tomato SNP discovery by EST mining and resequencing. Mol Breed 16:343–349
Lande R, Thompson R (1990) Efficiency of marker-assisted selection in the improvement of quantitative traits. Genetics 124:743–756
Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ (1987) Mapmaker: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genome 1:174–181
Lecomte L, Duffe P, Buret M (2004) Marker-assisted introgression of five QTLs controlling fruit quality traits into three tomato lines revealed interactions between QTLs and genetic backgrounds. Theor Appl Genet 109:658–668
Lin KH, Lo HF, Lee SP, Kuo C, Chen TC, Yeh WL (2006) RAPD markers for the identification of yield traits in tomatoes under heat stress via bulked segregant analysis. Hereditas 143:142–154
Lippmana Z, Tanksley SD (2001) Dissecting the genetic pathway to extreme fruit size in tomato using a cross between the small-fruited wild species Lycopersicon pimpinellifolium and L. esculentum var. Giant Heirloom. Genetics 158:413–422
Lohar DP, Peet WE (1998) Floral characteristics of heat-tolerance and heat-sensitive tomato cultivars at high temperature. HortScience 73:53–60
Marin TB, Moyseeno JB, Monforte AJ, Van Der KE (2007) Morphological variation in tomato: a comprehensive study of quantitative trait loci controlling fruit shape and development. J Exp Bot 58:1339–1349
Messeguer R, Ganal MW, Steffens JC, Tanksley SD (1991) Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol 16:753–770
Mijalski T, Harder A, Halder T, Kersten M, Horsch M (2005) Identification of coexpressed gene clusters in a comparative analysis of transcriptome and proteome in mouse tissues. Proc Natl Acad Sci USA 102:8621–8626
Monforte AJ, Friedman E, Zamir D, Tanksley SD (2001) Comparison of a set of allelic QTL-NILs for chromosome 4 of tomato: deductions about natural variation and implications for germplasm ultilization. Theor Appl Genet 102:572–590
Nesbitt TN, Tanksley SD (2002) Comparative sequencing in the genus Lycopersicon: implications for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162:365–379
Paran I, Zamir D (2003) Quantitative traits in plants: beyond the QTL. Trends Genet 19:303–306
Paterson AH, Damon S, Hewitt JD (1991) Mendelian factors underlying quantitative traits in tomato: comparison across species, generations and environments. Genetics 127:181–197
Ruiz JJ, García-Martínez S, Picó B, Gao M, Quiros CF (2005) Genetic variability and relationship of closely related Spanish traditional cultivars of tomato as detected by SRAP and SSR markers. J Am Soc Hort Sci 130:88–94
Saliba-Colombani V, Causse M, Gervais L, Philouze J (2000) Efficiency of RFLP, RAPD, and AFLP markers for the construction of an intraspecific map of the tomato genome. Genome 43:29–40
Saliba-Colombani V, Causse M, Langlois D (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Map** QTLs for physical and chemical traits. Theor Appl Genet 102:259–272
Semel Y, Nissenbaum J, Menda N, Zinder M, Krieger U, Issman N (2006) Overdominant quantitative trait loci for yield and fitness in tomato. Proc Natl Acad Sci USA 103:12981–12986
Sharma A, Zhang L, Niño-Liu D, Ashrafi H, Foolad MR (2008) A Solanum lycopersicum × Solanum pimpinellifolium linkage map of tomato displaying genomic locations of R-genes, RGAs, and candidate resistance/defense-response ESTs. Int J Plant Genome 2008:926090
Stevens MA (1986) Inheritance of tomato fruit quality components. Plant Breed Rev 4:273–311
Suliman-Pollatschek S, Kashkush K, Shats H, Hillel J, Lavi U (2002) Generation and map** of AFLP, SSRs and SNPs in Lycopersicon esculentum. Cell Mol Biol Let 7:583–597
Swamy MBP, Sarla M (2008) Yield-enhancing quantitative trait loci (QTLs) from wild species. Biotech Adv 26:106–120
Tanksley SD (1993) Map** polygenes. Ann Rev Genet 27:205–233
Tanksley SD, Nelson JC (1996) Advanced backcross QTL analysis, a method for the simultaneous discovery and transfer of valuable QTL from unadapted germplasm into elite breeding lines. Theor Appl Genet 92:191–203
Tanksley SD, Ganal MW, Prince JP, de Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Riider MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160
Tanksley SD, Grandillo S, Fultom TM, Zamir D, Eshed Y, Petiard V (1996) Advanced backcross QTL analysis in a cross between an elite processing line of tomato and its wild relative L. pimpinellifolium. Theor Appl Genet 92:213–224
Villalta I, Bernet GP, Carbonell EA, Asins MI (2007) Comparative QTL analysis of salinity tolerance in terms of fruit yield using two solanum populations of F7 lines. Theor Appl Genet 114:1001–1017
Villareal RL, Lai SH, Wong SH (1978) Screening for heat tolerance in the genus Lycopersicon. HortScience 13:479–481
Vos P, Hogers R, Bleeker M, Reijans M, Van De Lee T, Hornes M, Frijers A, Pot J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Yang W, Bai X, Kabelka E (2004) Discovery of singly nucleotide polymorphisms in Lycopersicon esculentum by computer aided analysis of expressed sequence tags. Mol Breed 14:21–34
Yates HE, Frary A, Doganlar S (2004) Comparative fine map** of fruit quality QTLs on chromosome 4 introgressions derived from two wild tomato species. Euphytica 135:283–296
Zeng ZB (1994) Precision map** of quantitative trait loci. Genetics 136:1468–1475
Acknowledgements
The authors are grateful to D. L. Lo, Z. Y. Chang, and numerous students for assistance in the greenhouse at Chinese Culture University. We also thank anonymous reviewers for their comments on the revision of this article. This work was supported in part by grants from the Council of Agriculture (93-AS-1.3.1-Z2), Executive Yuan, Taiwan.
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Lin, KH., Yeh, WL., Chen, HM. et al. Quantitative trait loci influencing fruit-related characteristics of tomato grown in high-temperature conditions. Euphytica 174, 119–135 (2010). https://doi.org/10.1007/s10681-010-0147-6
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DOI: https://doi.org/10.1007/s10681-010-0147-6