Abstract
The study of phenotypic and genetic diversity in landrace collections is important for germplasm conservation. In addition, the characterisation of very diversified materials with molecular markers offers a unique opportunity to define significant marker-trait associations of biological and agronomic interest. Here, 50 tomato landraces (mainly collected in central Italy), nine vintage and modern cultivars, and two wild outgroups were grown at two locations in central Italy and characterised for 15 morpho-physiological traits and 29 simple sequence repeat (SSR) loci. The markers were selected to include a group of loci in regions harbouring reported quantitative trait loci (QTLs) that affect fruit size and/or shape (Q-SSRs) and a group of markers that have not been mapped or shown to have a priori known linkage (NQ-SSRs). As revealed by univariate and multivariate analyses of morphological data, the landraces grouped according to vegetative and reproductive traits, with emphasis on fruit size, shape and final destination of the product. Compared to the low molecular polymorphism reported in tomato modern cultivars, our data reveal a high level of molecular diversity in landraces. Such diversity has allowed the inference of the existence of a genetic structure that was factored into the association analysis. As the proportion of significant associations is higher between the Q-SSR subset of markers and the subset of traits related to fruit size and shape than for all of the other combinations, we conclude that this approach is valid for establishing true-positive marker-trait relationships in tomato.
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References
Alvarez AE, van de Wiel CCM, Smulders MJM, Vosman B (2001) Use of microsatellites to evaluate genetic diversity and species relationships in the genus Lycopersicon. Theor Appl Genet 103:1283–1292
Aranzana MJ, Kim S, Zhao K, Bakker E, Horton M, Jakob K, Lister C, Molitor J, Shindo C, Tang C, Toomajian C, Traw B, Zheng H, Bergelson J, Dean C, Marjoram P, Nordborg M (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1:531–539. doi:10.1371/journal.pgen.0010060
Archak S, Karihaloo JL, Jain A (2002) RAPD markers reveal narrowing genetic base of Indian tomato cultivars. Curr Sci 82:1139–1143
Areshchenkova T (2000) Isolation, characterization and mapping of microsatellites from the tomato genome and their application in molecular analysis of centromeric regions. Ph.D. Dissertation, University of Sachsen-Anhalt, Germany
Areshchenkova T, Ganal MW (2002) Comparative analysis of polymorphism and chromosomal location of tomato microsatellite markers isolated from different sources. Theor Appl Genet 104:229–235
Bailey LH, Tracy WW, Kyle EJ, Watts RL (1960) Tomato. In: Bailey LH (eds) The standard cyclopedia of horticulture. The Macmillan Company, New York, pp 3353–3359
Barrero LS, Tanksley SD (2004) Evaluating the genetic basis of multiple-locule fruit in a broad cross section of tomato cultivars. Theor Appl Genet 109:669–679
Bredemeijer G, Cooke R, Ganal M, Peeters R, Isaac P, Noordijk Y, Rendell S, Jackson J, Röder MS, Wendehake K, Dijcks M, Amelaine M, Wickaert V, Bertrand L, Vosman B (2002) Construction and testing of a microsatellite database containing more than 500 tomato varieties. Theor Appl Genet 105:1019–1026
Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177
Broun P, Tanksley SD (1996) Characterization and genetic mapping of simple repeat sequences in the tomato genome. Mol Gen Genet 250:39–49
Causse M, Duffe P, Gomez MC, Buret M, Damidaux R, Zamir D, Gur A, Chevalier C, Lemaire-Chamley M, Rothan C (2004) A genetic map of candidate genes and QTLs involved in tomato fruit size and composition. J Exp Bot 55:1671–1685
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Eshed Y, Zamir D (1995) An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141:1147–1162
Esquinas-Alcazar J, Nuez F (1995) Situacion taxonomica, domesticacion y diffusion del tomate. In: Nuez F (eds) El cultivo del tomate. Ed Mundi-Prensa, Madrid, Barcelona, Mexico, pp 13–42
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Flint-Garcia SA, Thuillet A-C, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064
Frary A, Nesbitt TC, Frary A, Grandillo S, van der Knaap E, Cong B, Liu J, Meller J, Elber R, Alpert KB, Tnaksley SD (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289:85–88
Frary A, Xu Y, Liu J, Mitchell S, Tedeschi E, Tanksley SD (2005) Development of a set of PCR-based anchor markers encompassing the tomato genome and evaluation of their usefulness for genetics and breeding experiments. Theor Appl Genet 111:291–312
Fulton TM, Bucheli P, Voirol E, López J, Pétiard V, Tanksley SD (2002) Quantitative trait loci (QTL) affecting sugars, organic acids and other biochemical properties possibly contributing to flavor, identified in four advanced backcross populations of tomato. Euphytica 127:163–177
García-Gusano M, García-Martínez S, Ruiz JJ (2004) Use of SNP markers to genotype commercial hybrids and Spanish local cultivars of tomato. Tomato Genet Coop Rep 54:12–15
García-Martínez S, Andreani L, García-Gusano M, Geuna F, Ruiz JJ (2006) Evaluation of amplified fragment length polymorphism and simple sequence repeats for tomato germplasm fingerprinting: utility for grouping closely related traditional cultivars. Genome 49:648–656
Grandillo S, Ku HM, Tanksley SD (1996) Characterization of fs8.1, a major QTL influencing fruit shape in tomato. Mol Breed 2:251–260
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
He C, Poysa V, Yu K (2003) Development and characterization of simple sequence repeat (SSR) markers and their use in determining relationships among Lycopersicon esculentum cultivars. Theor Appl Genet 106:363–373
Herrmann D, Boller B, Studer B, Widmer F, Kölliker R (2006) QTL analysis of seed yield components in red clover (Trifolium pratense L.). Theor Appl Genet 112:536–545
Huang XQ, Borner A, Röder MS, Ganal MW (2002) Assessing genetic diversity of wheat (Triticum aestivum L.) germplasm using microsatellite markers. Theor Appl Genet 105:699–707
Kraakman ATW, van Eeuwijk FA, Dourleijn CJ, Stam P (2001) Fingerprinting of barley to study yield stability. In: Gallais A, Dillman C, Goldgringer I (eds) Quantitative genetics and breeding methods: the way ahead. Proceed 11th meeting of Eucarpia, section Biometrics in Plant breeding. INRA edition, Paris, pp 117–124
Ku HM, Grandillo S, Tanksley SD (2000) fs8.1, a major QTL, sets the pattern of tomato carpel shape well before anthesis. Theor Appl Genet 101:873–878
Lehmann EL, D’Abrera HJM (1975) Nonparametrics: statistical methods based on ranks. Holden-Day series in probability and statistics. Holden-Day, San Francisco
Lippman 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
Liu K, Muse S (2005) PowerMarker: new genetic data analysis software, Version 3.23. Available via DIALOG. http://www.powermarker.net. Accessed 9 Jan 2007
Lynch M, Walsh B (1997) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, pp 413
Mazzucato A (1995) Italian germplasm of Poa pratensis L. I. Variability and mode of reproduction. J Genet Breed 49:111–118
McIntosh MS (1983) Analysis of combined experiments. Agron J 75:153–155
Miller JC, Tanksley SD (1990) RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon. Theor Appl Genet 80:437–448
Monti L, Santangelo E, Corrado G, Rao R, Soressi GP, Scarascia Mugnozza GT (2004) Il “San Marzano”: problematiche e prospettive in relazione alla sua salvaguardia e alla necessità di interventi genetici. Agroindustria 3:161–169
Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 91:153–170
Nesbitt TC, Tanksley SD (2002) Comparative sequencing in the genus Lycopersicon: implication for the evolution of fruit size in the domestication of cultivated tomatoes. Genetics 162:365–379
Noble D (1994) Tantalizing tomatoes from the past. Am Veget Grower 42:44–47
Noli E, Conti S, Maccaferri M, Sanguineti MC (1999) Molecular characterization of tomato cultivars. Seed Sci Technol 27:1–10
Orloci L (1972) An algorith for cluster seeking in ecological collections. Vegetatio 27:339–345
Park YH, West MAL, St Clair DA (2004) Evaluation of AFLPs for germplasm fingerprinting and assessment of genetic diversity in cultivars of tomato (Lycopersicon esculentum L.). Genome 47:510–518
Paterson AH, Damon S, Hewitt JD, Zamir D, Rabinowitch HD, Lincoln SE, Lander ES, Tanksley SD (1991) Mendelian factors underlying quantitative traits in tomato: comparison across species generations and environments. Genetics 127:181–197
Podani J (1993) SYN-TAX-pc Version 5.0, User’s Guide. Scientia, Budapest
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rick CM (1976) Tomato, Lycopersicon esculentum (Solanaceae). In: Simmonds NW (eds) Evolution of crop plants. Longman Group, London, pp 268–273
Rick CM, Holle M (1990) Andean Lycopersicon esculentum var. cerasiforme: genetic variation and ist evolutionary significance. Econ Bot 44:69–78
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 Hortic Sci 130:88–94
SAS Institute Inc. (2002) SAS guide for personal computers, 9th edn. SAS Institute, Cary
Smulders MJM, Bredemeijer G, Rus-Kortekaas W, Arens P, Vosman B (1997) Use of short microsatellites from database sequences to generate polymorphisms among Lycopersicon esculentum cultivars and accessions of other Lycopersicon species. Theor Appl Genet 94:264–272
Sneath PHA, Sokal RR (1973) Numerical taxonomy. WH Freeman, San Francisco
Soressi GP (1969) Il pomodoro. Ed Agricole, Bologna
Stevens MA, Rick CM (1986) Genetics and breeding. In: Atherton JG, Rudich J (eds) The tomato crop. Chapman and Hall, London, pp 35–109
Suliman-Pollatschek S, Kashkush K, Shats H, Hillel J, Lavi U (2002) Generation and mapping of AFLP, SSRs and SNPs in Lycopersicon esculentum. Cell Mol Biol Lett 7:583–597
Tam SM, Mhiri C, Vogelaar A, Kerkveld M, Pearce SR, Grandbastien M-A (2005) Comparative analyses of genetic diversities within tomato and pepper collections detected by retrotransposon-based SSAP, AFLP and SSR. Theor Appl Genet 110:819–831
Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16:S181–S189
Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289
Van de Peer Y, De Wachter R (1993) TREECON: a software package for the construction and drawing of evolutionary trees. Comput Applic Biosci 9:177–182
Van der Knaap E, Tanksley SD (2001) Identification and characterization of a novel locus controlling early fruit development in tomato. Theor Appl Genet 103:353–358
Van der Knaap E, Lippman Z, Tanksley SD (2002) Extremely elongated tomato fruit controlled by four quantitative trait loci with epistatic interactions. Theor Appl Genet 104:241–247
Van der Knaap E, 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
Wang L, Guan R, Zhangxiong L, Chang R, Qiu L (2006) Genetic diversity of chinese cultivated soybean revealed by SSR markers. Crop Sci 46:1032–1038
Williams CE, St. Clair DA (1993) Phenetic relationships and levels of variability detected by restriction fragment length polymorphism and random amplified polymorphic DNA analysis of cultivated and wild accessions of Lycopersicon esculentum. Genome 36:619–630
Xu Y, Beachell H, McCouch SR (2005) A marker-based approach to broadening the genetic base of rice in the USA. Crop Sci 44:1947–1959
Zhang N, Xu Y, Akash M, McCouch S, Oard JH (2005) Identification of candidate markers associated with agronomic traits in rice using discriminant analysis. Theor Appl Genet 110:721–729
Acknowledgments
The authors wish to thank Dr Paola Crinò, Dr Rosa Rao and the Tomato Genetic Resource Center, Davis (CA, U.S.A.) for providing some of the seed stocks, two anonymous reviewers for their constructive comments on the manuscript and Dr Christopher Berrie for editorial assistance with the English. This study was supported by the Italian Ministry of Education, Universities and Research (MIUR) in the framework of the SCRIGNO project (Sviluppo e Caratterizzazione delle Risorse Genetiche Native in Ortofrutticoltura), and by the Marche Region––ASSAM (Marche Agency for Agro-food Sector Services).
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Communicated by I. L. Goldman.
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Mazzucato, A., Papa, R., Bitocchi, E. et al. Genetic diversity, structure and marker-trait associations in a collection of Italian tomato (Solanum lycopersicum L.) landraces. Theor Appl Genet 116, 657–669 (2008). https://doi.org/10.1007/s00122-007-0699-6
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DOI: https://doi.org/10.1007/s00122-007-0699-6