Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Comparative QTL analysis of salinity tolerance in terms of fruit yield using two solanum populations of F7 lines


Salt tolerance has been analysed in two populations of F7 lines developed from a salt sensitive genotype of Solanum lycopersicum var. cerasiforme, as female parent, and two salt tolerant lines, as male parents, from S. pimpinellifolium, the P population (142 lines), and S. cheesmaniae, the C population (116 lines). Salinity effects on 19 quantitative traits including fruit yield were investigated by correlation, principal component analysis, ANOVA and QTL analysis. A total of 153 and 124 markers were genotyped in the P and C populations, respectively. Some flowering time and salt tolerance candidate genes were included. Since most traits deviated from a normal distribution, results based on the Kruskal–Wallis non-parametric test were preferred. Interval mapping methodology and ANOVA were also used for QTL detection. Eight out of 15 QTLs at each population were detected for the target traits under both control and high salinity conditions, and among them, only average fruit weight (FW) and fruit number (FN) QTLs (fw1.1, fw2.1 and fn1.2) were detected in both populations. The individual contribution of QTLs were, in general, low. After leaf chloride concentration, flowering time is the trait most affected by salinity because different QTLs are detected and some of their QTL×E interactions have been found significant. Also reinforcing the interest on information provided by QTL analysis, it has been found that non-correlated traits may present QTL(s) that are associated with the same marker. A few salinity specific QTLs for fruit yield, not associated with detrimental effects, might be used to increase tomato salt tolerance. The beneficial allele at two of them, fw8.1 (in C) and tw8.1 (for total fruit weight in P) corresponds to the salt sensitive parent, suggesting that the effect of the genetic background is crucial to breed for wide adaptation using wild germplasm.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2


  1. Al-Doss AA, Smith SE (1998) Registration of AZ-97MEC and AZ-97MEC-ST very nondormant alfalfa germplasm pools with increased shoot weight and differential response to saline irrigation. Crop Sci 38:568–568

  2. Asins MJ, Breto MP, Carbonell EA (1993) Salt tolerance in Lycopersicon species. 2. Genetic-effects and a search for associated traits. Theor Appl Genet 86:769–774

  3. Ausín I, Alonso-Blanco C, Martinez-Zapater JM (2005) Environmental regulation of flowering. Int J Dev Biol 49:689–705

  4. Basten CJ, Weir BS, Zeng Z-B (2002) QTL Cartographer, Version 1.17. Department of Statistics, North Carolina State University, Raleigh, USA

  5. Blumenthal T, Evans D, Link CD, Guffanti A, Lawson D, Thierry-Mieg J, Thierry-Mieg D, Chiu WL, Duke K, Kiraly M, Kim SK (2002) A global analysis of Caenorhabditis elegans operons. Nature 417:851–854

  6. Bohnert HJ (1995) Coping with water-deficit, application of biochemical principles. Plant Phys 108:5

  7. Bolarín MC, Fernandez FG, Cruz V, Cuartero J (1991) Salinity tolerance in 4 wild tomato species using vegetative yield salinity response curves. J Am Soc Hortic Sci 116:286–290

  8. Chen KY, Tanksley SD (2004) High resolution mapping 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

  9. Cohen BA, Mitra RD, Hughes JD, Church GM (2000) A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat Genet 26:183–186

  10. Cuartero J, Soria T (1997) Productividad de tomates cultivados en condiciones salinas. Actas de horticultura 16:214–221

  11. Cuartero J, Yeo AR, Flowers TJ (1992) Selection of donors for salt-tolerance in tomato using physiological traits. New Phytol 121:63–69

  12. Cuartero J, Bolarín MC, Asins MJ, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57:1045–1058

  13. De Vicente MC, Tanksley SD (1993) Analysis of transgressive segregation in an interspecific tomato cross. Genetics 134:585–596

  14. Dierig DA, Shannon MC, Grieve CM (2001) Registration of WCL-SL1 salt tolerant Lesquerella fendleri germplasm. Crop Sci 41:604–605

  15. Doganlar S, Frary A, Ku HM, Tanksley SD (2002) Mapping quantitative trait loci in inbred backcross lines of Lycopersicon pimpinellifolium (LA1589). Genome 45:1189–1202

  16. Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol 50:237–248

  17. Falconer DS (1960) Introduction to quantitative genetics. R Mac Lehose and Com., Glasgow, pp 264–275

  18. Foolad MR (1996) Response to selection for salt tolerance during germination in tomato seed derived from PI 174263. J Am Soc Hortic Sci 121:1006–1011

  19. Foolad MR (1997) Genetic basis of physiological traits related to salt tolerance in tomato, Lycopersicon esculentum Mill. Plant Breed 116:53–58

  20. Gilliam JW (1971) Rapid measurement of chlorine in plant materials. Soil Sci Soc Am Proc 35:512–513

  21. Goldman IL, Paran I, Zamir D (1995) Quantitative trait locus analysis of a recombinant inbred line population derived from a Lycopersicon esculentum × Lycopersicon cheesmanii cross. Theor Appl Genet 90:925–932

  22. Grandillo S, Tanksley SD (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theor Appl Genet 92:935–951

  23. 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

  24. Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol Plant Mol Biol 31:149–190

  25. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499

  26. Infostat (2004) Infostat version 2004. FCA. Universidad Nacional de Córdoba, Argentina

  27. Juenger TE, Sen S, Stowe KA, Simms EL (2005) Epistasis and genotype-environment interaction for quantitative trait loci affecting flowering time in Arabidopsis thaliana. Genetica 123:87–105

  28. Khalf-Allah AM, Pierce LC (1963) A comparison of selection methods for improving earliness, fruit size and yield in tomato. Proc Am Soc Hortic Sci 82:414–419

  29. Korstanje R, Paigen B (2002) From QTL to gene: the harvest begins. Nat Genet 31:235–236

  30. Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugenetics 12:172–175

  31. Lecomte L, Saliba-Colombani V, Gautier A, Gomez-Jimenez MC, Duffe P, Buret M, Causse M (2004) Fine mapping of QTLs of chromosome 2 affecting the fruit architecture and composition of tomato. Mol Breed 13:1–14

  32. Lercher MJ, Urrutia AO, Hurst LD (2002) Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat Genet 31:180–183

  33. Maas E, Hoffmann G (1977) Crop salt tolerance-current assessment. A.S.C.E 103

  34. Malmberg RL, Held S, Waits A, Mauricio R (2005) Epistasis for fitness-related quantitative traits in Arabidopsis thaliana grown in the field and in the greenhouse. Genetics 171:2013–2027

  35. Molinero-Rosales N, Jamilena M, Zurita S, Gomez P, Capel J, Lozano R (1999) FALSIFLORA, the tomato orthologue of FLORICAULA and LEAFY, controls flowering time and floral meristem identity. Plant J 20:685–693

  36. Monforte AJ, Asins MJ, Carbonell EA (1997b) Salt tolerance in Lycopersicon species. 6. Genotype-by-salinity interaction in quantitative trait loci detection: constitutive and response QTLs. Theor Appl Genet 95:706–713

  37. Monforte AJ, Asins MJ, Carbonell EA (1997a) Salt tolerance in Lycopersicon species. 5. Does genetic variability at quantitative trait loci affect their analysis? Theor Appl Genet 95:284–293

  38. Monforte AJ, Asins MJ, Carbonell EA (1999) Salt tolerance in Lycopersicon spp. VII. Pleiotropic action of genes controlling earliness on fruit yield. Theor Appl Genet 98:593–601

  39. 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 utilization. Theor Appl Genet 102:572–590

  40. Morgante M, Salamini F (2003) From plant genomics to breeding practice. Curr Opin Biotechnol 14:214–219

  41. Munns R, Husain S, Rivelli AR, James RA, Condon AG, Lindsay MP, Lagudah ES, Schachtman DP, Hare RA (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant Soil 247:93–105

  42. Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in arabidopsis. Plant Physiol 127:252–261

  43. Owen PA, Nickell CD, Noel GR, Thomas DJ, Frey K (1994) Registration of saline soybean. Crop Sci 34:1689–1689

  44. Paran I, Zamir D (2003) Quantitative traits in plants: beyond the QTL. Trends Genet 19:303–306

  45. Paterson AH, Deverna JW, Lanini B, Tanksley SD (1990) Fine mapping of quantitative trait loci using selected overlapping recombinant chromosomes, in an interspecies cross of tomato. Genetics 124:735–742

  46. Pérez-Alfocea F, Estan MT, Caro M, Bolarín MC (1993) Response of tomato cultivars to salinity. Plant Soil 150:203–211

  47. Pérez-Alfocea E, Guerrier G, Estan MT, Bolarín MC (1994) Comparative salt responses at cell and whole-plant levels of cultivated and wild tomato species and their hybrid. J Hortic Sci 69:639–644

  48. Sablowski RWM, Meyerowitz EM (1998) A homolog of NO APICAL MERISTEM is an immediate target of the floral homeotic genes APETALA3/PISTILLATA. Cell 92:93–103

  49. Sacher RF, Staples RC, Robinson RW (1983) Ion regulation and response of tomato to sodium-chloride—a homeostatic system. J Am Soc Hortic Sci 108:566–569

  50. Saliba-Colombani V, Causse M, Langlois D, Philouze J, Buret M (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 102:259–272

  51. Santa-Cruz A, Perez-Alfocea F, Caro M, Acosta M (1998) Polyamines as short-term salt tolerance traits in tomato. Plant Sci 138:9–16

  52. Steiner JJ, Banuelos GS (2003) Registration of ARS NLT-SALT and ARS-NLT-SALT/B saline tolerant narrow-leaf trefoil germplasm. Crop Sci 43:1888–1889

  53. Storey R, Walker RR (1999) Citrus and salinity. Sci Hortic 78:39–81

  54. Tal M, Shannon MC (1983) Effects of dehydration and high-temperature on the stability of leaf membranes of Lycopersicon esculentum, L. cheesmanii, Lycopersicon. peruvianum and Solanum pennellii. Z Pflanzenphysiol 112:411–416

  55. Tanksley SD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16:S181–S189

  56. Thomas DSG, Middleton NJ (1993) Salinization—new perspectives on a major desertification issue. J Arid Environ 24:95–105

  57. Van Ieperen W (1996) Effects of different day and night salinity levels on vegetative growth, yield and quality of tomato. J Hortic Sci 71:99–111

  58. Van Ooijen JW, Maliepaard C (1996) MapQTL (tm) Version 3.0: Software for the calculation of QTL positions on genetic maps. DLO-Centre for Plant Breeding and Reproduction Research, Wageningen, The Netherlands

  59. Van Ooijen JW, Voorrips R E (2001) Joinmap Version 3.0: Software for the calculation of genetic linkage maps Release 3.0. Plant Research International, Wageningen, The Netherlands

  60. 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

  61. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu JH, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45:523–539

  62. Villalta I, Reina-Sanchez A, Cuartero J, Carbonell EA, Asins MJ (2005) Comparative microsatellite linkage analysis and genetic structure of two populations of F-6 lines derived from Lycopersicon pimpinellifolium and L. cheesmanii. Theor Appl Genet 110:881–894

  63. Xu GH, Magen H, Tarchitzky J, Kafkafi U (2000) Advances in chloride nutrition of plants. Adv Agronomy 68:97–150

Download references


This work was supported in part by grants from IVIA (IV), and INIA (RTA01-113-C2 and RTA04-075-C2). Authors thank Drs. Jimenez-Diaz and Martinez-Zapater for the information on the flowering time gene candidates, and I. Pereira, J. Pérez-Panadés, P. Cirujeda and J. Puchades for technical assistance.

Author information

Correspondence to M. J. Asins.

Additional information

Communicated by C. Hackett.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Villalta, I., Bernet, G.P., Carbonell, E.A. et al. Comparative QTL analysis of salinity tolerance in terms of fruit yield using two solanum populations of F7 lines. Theor Appl Genet 114, 1001–1017 (2007).

Download citation


  • Salt Tolerance
  • Fruit Weight
  • Stem Length
  • Fruit Yield
  • Fruit Number