Skip to main content

Genetic dissection of tomato rootstock effects on scion traits under moderate salinity


Key message

Rootstock HKT1 genotype affected fruit [Na + ] and non-commercial fruit yield; QTL analysis of rootstock-mediated scion nutrition is a powerful forward genetic approach to identify wild genes for rootstock breeding.


The present study approaches the QTL dissection of rootstock effects on a commercial hybrid variety grafted on a population of RILs derived from Solanum pimpinellifolium, genotyped for 4370 segregating SNPs from the SolCAP tomato panel and grown under moderate salinity. Results are compared to those previously obtained under high salinity. The most likely functional candidate genes controlling the scion [Na+] were rootstock HKT1;1 and HKT1;2 as it was previously reported for non-grafted genotypes. The higher fruit [Na+] found when rootstock genotype was homozygote for SpHKT1 supports the thesis that scion HKT1 is loading Na+ into the phloem sap in leaves and unloading it in sink organs. A significant increment of small, mostly seedless, fruits was found associated with SlHKT1 homozygous rootstocks. Just grafting increased the incidence of blossom end rot and delayed fruit maturation but there were rootstock RILs that increased commercial fruit yield under moderate salinity. The heritability and number of QTLs involved were lower and different than those found under high salinity. Four large contributing (>17 %) rootstock QTLs, controlling the leaf concentrations of B, K, Mg and Mo were detected whose 2 Mbp physical intervals contained B, K, Mg and Mo transporter-coding genes, respectively. Since a minimum of 3 QTLs (two of them coincident with leaf K and Ca QTLs) were also found governing rootstock-mediated soluble-solids content of the fruit under moderate salinity, grafting desirable crop varieties on stress-tolerant rootstocks tenders an opportunity to increase both salt tolerance and quality.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3


  • Almeida P, de Boer G-J, de Boer A-H (2014) Differences in shoot Na+ accumulation between two tomato species are due to differences in ion affinity of HKT1;2. J Plant Physiol 171:438–447

    Article  CAS  PubMed  Google Scholar 

  • Aloni B, Kami L, Deveturero G, Levin Z, Cohen R, Kazir N, Lotan-Pompan M, Edelstein M, Aktas H, Turhan E, Joel DM, Horey C, Kapulnic Y (2008) Physiological and biochemical changes at the rootstock scion interface in graft combinations between Cucurbita rootstocks and a melon scion. J Hortic Sci Biotechnol 83:777–783

    Google Scholar 

  • Ashrafi H, Kinkade MP, Merk HL, Foolad MR (2012) Identification of novel quantitative trait loci for increased lycopene content and other fruit quality traits in a tomato recombinant inbred line population. Mol Breed 30:549–567

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Asins MJ, Bolarín MC, Pérez-Alfocea F, Estañ MT, Martinez-Andújar C, Albacete A, Villalta I, Bernet GP, Dodd I, Carbonell EA (2010) Genetic analysis of physiological components of salt tolerance conferred by Solanum rootstocks. What is the rootstock doing for the scion? Theor Appl Genet 121:105–115

  • Asins MJ, Villalta I, Aly MM, Olías R, Álvarez De Morales P, Huertas R, Li J, Jaime-Pérez N, Haro R, Raga V, Carbonell EA, Belver A (2013) Two closely linked tomato HKT coding genes are positional candidates for the major tomato QTL involved in Na+/K+ homeostasis. Plant Cell Environ 36:1171–1191

    Article  CAS  PubMed  Google Scholar 

  • Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F, Simonneau T, Essah PA, Tester M, Vèry A-A, Sentenac H, Casse F (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. The EMBO J 22:2004–2014

    Article  CAS  Google Scholar 

  • Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5:28. doi:10.3389/fpls.2014.00028

    Article  PubMed Central  PubMed  Google Scholar 

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

    Google Scholar 

  • Cuartero JM, Fernández-Muñoz R (1999) Tomato and salinity. Sci Hortic 78:83–125

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dorais M, Papadopoulos AP, Gosselin A (2001) Influence of electric conductivity management on greenhouse tomato yield and fruit quality. Agronomie 21:367–383

    Article  Google Scholar 

  • Estañ MT, Medina S, Morales B, Moyano E, Bolarín MC, Asins MJ (2008) Utilización como portainjertos de líneas RILs derivadas de S. lycopersicum x S. chesmaniae y S. lycopersicum x S. pimpinellifolium para mejorar el cultivo de tomate bajo condiciones salinas. In: Monreal LR, Ruiz JM, Blasco B, Rubio MM, Sánchez E, Ríos JJ, Cervilla LM (eds) Presente y Futuro de la Nutrición Mineral de Plantas, Héctor Santillán CP 18183, Granada, pp 225–235. ISBN: 978-84-89780-10-7

  • Estañ MT, Villalta I, Bolarín MC, Carbonell EA, Asins MJ (2009) Identification of fruit yield loci controlling the salt tolerance conferred by solanum rootstocks. Theor Appl Genet 118:305–312

    Article  PubMed  Google Scholar 

  • FAO (2008) FAO land and plant nutrition management service.

  • Farias EAD, Ferreira RLF, Neto SED, Costa FC, Nascimento DS (2013) Organic production of tomatoes in the Amazon Region by plants grafted on wild Solanum rootstocks. Cienc Agrotecnol 37:323–329

    Article  Google Scholar 

  • Fernandez-García N, Martinez V, Cerdá A, Carvajal M (2004) Fruit quality of grafted tomato plants grown under saline conditions. J Hortic Sci Biotech 79:995–1001

    Google Scholar 

  • Foolad MR, Lin GY (1997) Genetic potential for salt tolerance during germination in Lycopersicon species. HortSci 32:296–300

    Google Scholar 

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

    Article  Google Scholar 

  • Hasegawa S, Sogabe Y, Asano T, Nakagawa T, Nakamura H, Kodama H, Ohta H, Yamaguchi MK, Mueller MJ, Nishiuchi T (2011) Gene expression analysis of wounding-induced roots-to-shoot communication in Arabidopsis thaliana. Plant Cell Environ 34:705–716

    Article  CAS  PubMed  Google Scholar 

  • Kacperska A (2004) Sensor types in signal transduction pathways in plant cells responding to abiotic stressors: do they depend on stress intensity? Physiol Plant 122:159–168

    Article  CAS  Google Scholar 

  • King SR, Davis AR, Zhang X, Crosby K (2010) Genetics, breeding and selection of rootstocks for Solanaceae and Cucurbitaceae. Scentia Horticulturae 127:106–111

    Article  Google Scholar 

  • Kromdijk J, Bertin N, Heuvelink E, Molenaar J, de Visser PHB, Marcelis LFM, Struik PC (2014) Crop management impacts the efficiency of quantitative trait loci (QTL) detection and use: case study of fruit loadxQTL interactions. J Exp Bot 65:11–22

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Munnik T, Meijer HJG (2001) Osmotic stress activates distinct lipid and MAPK signalling pathways in plants. FEBS Lett 498:72–178

    Article  Google Scholar 

  • Pascual L, Desplat N, Huang BE, Desgroux A, Bruguier L, Bouchet J-P, Le Q, Chauchard B, Verschave P, Causse M (2014) Potential of a tomato MAGIC population to decipher the genetic control of quantitative traits and detect causal variants in the resequencing era. Plant Biotechnol J. doi:10.1111/pbi.12282

    PubMed  Google Scholar 

  • Price AH (2006) Believe it or not, QTLs are accurate! Trends Plant Sci 11:213–216

    Article  CAS  PubMed  Google Scholar 

  • Raga V, Bernet GP, Carbonell EA, Asins MJ (2014) Inheritance of rootstock effects and their association with salt-tolerance candidate genes in a progeny derived from ‘Volkamer’ lemon. J Am Soc Hort Sci 139:518–528

    CAS  Google Scholar 

  • Rose JKC, Lee HH, Bennett AB (1997) Expression of a divergent expansin gene is fruit-specific and ripening-regulated. Proc Natl Acad Sci USA 94:5955–5960

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ruzicka K, Ljung K, Vanneste S, Podhorska R, Beeckman T, Friml J, Benkova E (2007) Ethylene regulates root growth through effects on auxin biosynthesis and transport–dependent auxin distribution. Plant Cell 19:2197–2212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Sauvage C, Segura V, Bauchet G, Stevens R, Do PT, Nikoloski Z, Fernie A, Causse M (2014) Genome wide association in tomato reveals 44 candidate loci for fruit metabolic traits. Plant Physiol. doi:10.1104//pp.114.241521

  • Savvas D, Colla G, Rouphael Y, Scharz D (2010) Amelioration of heavy metal and nutrient stress in vegetables by grafting. Sci Hortic 127:156–161

    Article  CAS  Google Scholar 

  • Savvas D, Savva A, Ntatsi G, Ropokis A, Karapanos I, Krumbein A, Olympios C (2011) Effects of three commercial rootstocks on mineral nutrition, fruit yield, and quality of salinized tomato. J Plant Nutr Soil Sci 1:154–162

    Article  Google Scholar 

  • Scrase-Field AMG, Knight MR (2003) Calcium: just a chemical switch. Curr Opin Plant Biol 6:500–506

    Article  CAS  PubMed  Google Scholar 

  • Sim S-C, Durstewitz G, Plieske J, Wieseke R, Ganal MW et al (2012) Development of a large SNP genotyping array and generation of high-density genetic maps in tomato. PLoS ONE 7(7):e40563. doi:10.1371/journal.pone.0040563

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Simon EW (1978) The symptoms of calcium deficiency in plants. New Phytol 80:1–15

    Article  CAS  Google Scholar 

  • Steele NM, Mccann MC, Roberts K (1997) Pectin modification in cell walls of ripening tomatoes occurs in distinct domains. Plant Physiol 114:373–381

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sun K, Hunt K, Hauser BA (2004) Ovule abortion in Arabidopsis triggered by stress. Plant Physiol 135:2358–2367

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • The Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641

    Article  Google Scholar 

  • Turhan A, Ozmen N, Serbeci MS, Seniz V (2011) Effects of grafting on different rootstocks on tomato fruit yield and quality. Hortic Sci 38:42–1497

    Google Scholar 

  • Van Ooijen JW (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherlands

  • Van Ooijen JW (2009) MapQTL 6. Software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma BV, Wageningen, Netherlands

  • Villalta I, Bernet GP, Carbonell EA, Asins MJ (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

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Inukaia Y, Yamauchia A (2006) Root development and nutrient uptake. Crit Rev Plant Sci 25:279–301

    Article  CAS  Google Scholar 

  • Witcombe JR, Hollington PA, Howarth CJ, Reader S, Steele KA (2008) Breeding for abiotic stresses for sustainable agriculture. Phil Trans R Soc B 363:703–716

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references


This work was supported in part by grants from the Spanish Government (AGL2008-00197/AGR, RTA2011-00132-C02) and the European Union (FP7-KBBE-2011-5), contract # 289365 (ROOTOPOWER). Authors thank UNIGENIA BIOSCIENCE SLU for the grafting labor, Dr. A.J. Monforte (IBMCP, Valencia, Spain) for comprehensive access to information on SolCAP SNPs, and Dr. G.P. Bernet (IBMCP, Valencia, Spain) for technical assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

The authors declare that the experiment complies with the current laws of Spain.

Author information

Authors and Affiliations


Corresponding author

Correspondence to M. J. Asins.

Additional information

Communicated by Richard G.F. Visser.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 76 kb)

Supplementary material 2 (PDF 198 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Asins, M.J., Raga, V., Roca, D. et al. Genetic dissection of tomato rootstock effects on scion traits under moderate salinity. Theor Appl Genet 128, 667–679 (2015).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


  • Salt Tolerance
  • Total Soluble Solid
  • Fruit Yield
  • Moderate Salinity
  • Bayesian Information Criterion