Skip to main content
SpringerLink
Log in

A mixed-model QTL analysis for salt tolerance in seedlings of crop-wild hybrids of lettuce

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Cultivated lettuce is more sensitive to salinity stress than its wild progenitor species potentially due to differences in root architecture and/or differential uptake and accumulation of sodium. We have identified quantitative trait locis (QTLs) associated with salt-induced changes in root system architecture (RSA) and ion accumulation using a recombinant inbred line population derived from a cross between cultivated lettuce (Lactuca sativa ‘Salinas’) and wild lettuce (L. serriola). Components of RSA were quantified by replicated measurements of seedling growth on vertical agar plates containing different concentrations of NaCl in a controlled growth chamber environment. Accumulation of sodium and potassium ions was measured in replicates of greenhouse-grown plants watered with 100 mM NaCl water. A total of 14 QTLs were identified using multi-trait linkage analysis, including three major QTLs associated with general root development, root growth in salt stress condition, and ion accumulation. The three major QTLs, qRC9.1, qRS2.1, and qLS7.2, were linked with markers E35/M59-F-425, LE9050, and LE1053, respectively. This study provides regions of lettuce genome contributing to salt-induced changes in RSA and ion accumulation. Future fine-mapping of major QTLs will identify candidate genes underlying salt stress tolerance in cultivated lettuce.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Argyris J, Truco MJ, Ochoa O, Knapp SJ, Still DW, Lenssen GM, Schut JW, Michelmore RW, Bradford KJ (2005) Quantitative trait loci associated with seed and seedling traits in Lactuca. Theor Appl Genet 111:1365–1376

    Article  PubMed  Google Scholar 

  • Armengaud P, Zambaux K, Hills A, Sulpice R, Pattison RJ, Blatt MR, Amtmann A (2009) EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. Plant J 57:945–956

    Article  PubMed  CAS  Google Scholar 

  • Burke JM, Tang SX, Knapp SJ, Rieseberg LH (2002) Genetic analysis of sunflower domestication. Genetics 161:1257–1267

    PubMed  CAS  PubMed Central  Google Scholar 

  • Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196

    Article  CAS  Google Scholar 

  • Collins NC, Tardieu F, Tuberosa R (2008) Quantitative trait loci and crop performance under abiotic stress: where do we stand? Plant Physiol 147:469–486

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • De Smet I, White PJ, Bengough AG, Dupuy L, Parizot B, Casimiro I, Heidstra R, Laskowski M, Lepetit M, Hochholdinger F, Draye X, Zhang H, Broadley MR, Peret B, Hammond JP, Fukaki H, Mooney S, Lynch JP, Nacry P, Schurr U, Laplaze L, Benfey P, Beeckman T, Bennett M (2012) Analyzing lateral root development: how to move forward. Plant Cell 24:15–20

    Article  PubMed  PubMed Central  Google Scholar 

  • DeRose-Wilson L, Gaut BS (2011) Mapping salinity tolerance during Arabidopsis thaliana germination and seedling growth. PLoS One 6:e22832

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Díaz De León JL, Escoppinichi R, Geraldo N, Castellanos T, Mujeeb-Kazi A, Röder MS (2011) Quantitative trait loci associated with salinity tolerance in field grown bread wheat. Euphytica 181:371–383

    Article  Google Scholar 

  • Dubrovsky JG, Forde BG (2012) Quantitative analysis of lateral root development: pitfalls and how to avoid them. Plant Cell 24:4–14

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fang S, Yan X, Liao H (2009) 3D reconstruction and dynamic modeling of root architecture in situ and its application to crop phosphorus research. Plant J 60:1096–1108

    Article  PubMed  CAS  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319

    Article  PubMed  CAS  Google Scholar 

  • Foolad MR, Zhang LP, Lin GY (2001) Identification and validation of QTLs for salt tolerance during vegetative growth in tomato by selective genotyping. Genome 44:444–454

    Article  PubMed  CAS  Google Scholar 

  • French A, Ubeda-Tomas S, Holman TJ, Bennett MJ, Pridmore T (2009) High-throughput quantification of root growth using a novel image-analysis tool. Plant Physiol 150:1784–1795

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Galkovskyi T, Mileyko Y, Bucksch A, Moore B, Symonova O, Price CA, Topp CN, Pascuzzi ASL, Zurek PR, Fang S, Harer J, Benfey PN, Weitz JS (2012) GiA Roots: software for the high throughput analysis of plant root system architecture. BMC Plant Biol 12:116

    Article  PubMed  PubMed Central  Google Scholar 

  • Gallardo M, Jackson LE, Thmopson RB (1996) Shoot and root physiological responses to localized zones of soil moisture in cultivated and wild lettuce (Lactuca spp.). Plant Cell Environ 19:1169–1178

    Article  Google Scholar 

  • Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Curr Opin Plant Biol 14:296–302

    Article  PubMed  CAS  Google Scholar 

  • Genc Y, Oldach K, Verbyla AP, Lott G, Hassan M, Tester M, Wallwork H, McDonald GK (2010) Sodium exclusion QTL associated with improved seedling growth in bread wheat under salinity stress. Theor Appl Genet 121:877–894

    Article  PubMed  CAS  Google Scholar 

  • Genc Y, Oldach K, Gogel B, Wallwork H, McDonald GK, Smith AB (2013) Quantitative trait loci for agronomic and physiological traits for a bread wheat population grown in environments with a range of salinity levels. Mol Breed 32:39–59

    Article  Google Scholar 

  • Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PM, Tham C, Duan L, Dinneny JR (2013) A spatio–temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25:2132–2154

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Snape J (2010) Meta-QTL analysis of the genetic control of crop height in elite European winter wheat germplasm. Mol Breed 29:159–171

    Article  Google Scholar 

  • Hammer GL, Dong Z, McLean G, Doherty A, Messina C, Schussler J, Zinselmeier C, Paszkiewicz S, Cooper M (2009) Can changes in canopy and/or root system architecture explain historical maize yield trends in the U.S. Corn Belt? Crop Sci 49:299

    Article  Google Scholar 

  • Hartman Y, Hooftman DA, Uwimana B, van de Wiel CC, Smulders MJ, Visser RG, van Tienderen PH (2012a) Genomic regions in crop–wild hybrids of lettuce are affected differently in different environments: implications for crop breeding. Evol Appl 5:629–640

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartman Y, Hooftman DAP, Schranz ME, van Tienderen PH (2012b) QTL analysis reveals the genetic architecture of domestication traits in Crisphead lettuce. Genet Resour Crop Evol 60:1487–1500

    Article  Google Scholar 

  • Huang X, Paulo M, Boer M, Effgen S, Keizer P, Koornneef M, van Eeuwijk FA (2010) Analysis of natural allelic variation in Arabidopsis using a multiparent recombinant inbred line population. Proc Natl Acad Sci USA 108:4488–4493

    Article  Google Scholar 

  • Iyer-Pascuzzi AS, Symonova O, Mileyko Y, Hao Y, Belcher H, Harer J, Weitz JS, Benfey PN (2010) Imaging and analysis platform for automatic phenotyping and trait ranking of plant root systems. Plant Physiol 152:1148–1157

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jackson LE (1995) Root architecture in cultivated and wild lettuce (Lactuca spp.). Plant Cell Environ 18:885–894

    Article  Google Scholar 

  • Jannink JL (2005) Selective phenotyping to accurately map quantitative trait loci. Crop Sci 45:901–908

    Article  CAS  Google Scholar 

  • Jeuken MJ, Lindhout P (2002) Lactuca saligna, a non-host for lettuce downy mildew (Bremia lactucae), harbors a new race-specific Dm gene and three QTLs for resistance. Theor Appl Genet 105:384–391

    Article  PubMed  CAS  Google Scholar 

  • Jeuken MJ, Pelgrom K, Stam P, Lindhout P (2008) Efficient QTL detection for nonhost resistance in wild lettuce: backcross inbred lines versus F2 population. Theor Appl Genet 116:845–857

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Johnson WC, Jackson LE, Ochoa O, van Wijk R, Peleman J, St. Clair DA, Michelmore RW (2000) Lettuce, a shallow-rooted crop, and Lactuca serriola, its wild progenitor, differ at QTL determining root architecture and deep soil water exploitation. Theor Appl Genet 101:1066–1073

    Article  CAS  Google Scholar 

  • Kerbiriou PJ, Stomph TJ, Lammerts van Bueren ET, Struik PC (2013a) Influence of transplant size on the above- and below-ground performance of four contrasting field-grown lettuce cultivars. Front Plant Sci 4:379

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kerbiriou PJ, Stomph TJ, Putten PEL, Lammerts Van Bueren ET, Struik PC (2013b) Shoot growth, root growth and resource capture under limiting water and N supply for two cultivars of lettuce (Lactuca sativa L.). Plant Soil 371:281–297

    Article  CAS  Google Scholar 

  • Koopman WJM, Guetta E, van de Wiel CCM, Vosman B, van den Berg RG (1998) Phylogenetic relationships among Lactuca (Asteraceae) species and related genera based on ITS-1 DNA sequences. Am J Bot 85:1517–1530

    Article  PubMed  CAS  Google Scholar 

  • Koopman WJM, Zevenbergen MJ, van den Berg RG (2001) Species relationships in Lactuca S.L. (Lactuceae, Asteraceae) inferred from AFLP fingerprints. Am J Bot 88:1881–1887

    Article  PubMed  CAS  Google Scholar 

  • Lebeda A, Doležalová I, Křístková E, Kitner M, Petrželová I, Mieslerová B, Novotná A (2009) Wild Lactuca germplasm for lettuce breeding: current status, gaps and challenges. Euphytica 170:15–34

    Article  Google Scholar 

  • Lee GJ, Boerma HR, Villagarcia MR, Zhou X, Carter TE Jr, Li Z, Gibbs MO (2004) A major QTL conditioning salt tolerance in S-100 soybean and descendent cultivars. Theor Appl Genet 109:1610–1619

    Article  PubMed  CAS  Google Scholar 

  • Lin HX, Zhu MZ, Yano M, Gao JP, Liang ZW, Su WA, Hu XH, Ren ZH, Chao DY (2004) QTLs for Na+ and K+ uptake of the shoots and roots controlling rice salt tolerance. Theor Appl Genet 108:253–260

    Article  PubMed  CAS  Google Scholar 

  • Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13

    PubMed  CAS  PubMed Central  Google Scholar 

  • Malosetti M, Ribaut JM, Vargas M, Crossa J, Eeuwijk FA (2007) A multi-trait multi-environment QTL mixed model with an application to drought and nitrogen stress trials in maize (Zea mays L.). Euphytica 161:241–257

    Article  Google Scholar 

  • Malosetti M, van Eeuwijk FA, Boer MP, Casas AM, Elia M, Moralejo M, Bhat PR, Ramsay L, Molina-Cano JL (2011) Gene and QTL detection in a three-way barley cross under selection by a mixed model with kinship information using SNPs. Theor Appl Genet 122:1605–1616

    Article  PubMed  PubMed Central  Google Scholar 

  • Mano Y, Takeda K (1997) Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94:263–272

    Article  Google Scholar 

  • Munns R (2010) Approaches to identifying genes for salinity tolerance and the importance of timescale. Methods Mol Biol 639:25–38

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043

    Article  PubMed  CAS  Google Scholar 

  • Nguyen VL, Ribot SA, Dolstra O, Niks RE, Visser RGF, van der Linden CG (2012) Identification of quantitative trait loci for ion homeostasis and salt tolerance in barley (Hordeum vulgare L.). Mol Breed 31:137–152

    Article  Google Scholar 

  • Pastina MM, Malosetti M, Gazaffi R, Mollinari M, Margarido GR, Oliveira KM, Pinto LR, Souza AP, van Eeuwijk FA, Garcia AA (2012) A mixed model QTL analysis for sugarcane multiple-harvest-location trial data. Theor Appl Genet 124:835–849

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Payne R, Murray D, Harding S, Baird D, Soutar D (2012) Introduction to GenStat for windows, 15th edn. VSN International, Hemel Hempstead. www.vsni.co.uk/software/genstat?ref=genstat.com

  • Ren ZH, Gao JP, Li LG, Cai XL, Huang W, Chao DY, Zhu MZ, Wang ZY, Luan S, Lin HX (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146

    Article  PubMed  CAS  Google Scholar 

  • Schwember AR, Bradford KJ (2010a) A genetic locus and gene expression patterns associated with the priming effect on lettuce seed germination at elevated temperatures. Plant Mol Biol 73:105–118

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Schwember AR, Bradford KJ (2010b) Quantitative trait loci associated with longevity of lettuce seeds under conventional and controlled deterioration storage conditions. J Exp Bot 61:4423–4436

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Crit Rev Plant Sci 32:237–249

    Article  Google Scholar 

  • Sharma S, Xu S, Ehdaie B, Hoops A, Close TJ, Lukaszewski AJ, Waines JG (2011) Dissection of QTL effects for root traits using a chromosome arm-specific mapping population in bread wheat. Theor Appl Genet 122:759–769

    Article  PubMed  PubMed Central  Google Scholar 

  • Thomson MJ, Ocampo M, Egdane J, Rahman MA, Sajise AG, Adorada DL, Tumimbang-Raiz E, Blumwald E, Seraj ZI, Singh RK, Gregorio GB, Ismail AM (2010) Characterizing the saltol quantitative trait locus for salinity tolerance in rice. Rice 3:148–160

    Article  Google Scholar 

  • Truco MJ, Antonise R, Lavelle D, Ochoa O, Kozik A, Witsenboer H, Fort SB, Jeuken MJ, Kesseli RV, Lindhout P, Michelmore RW, Peleman J (2007) A high-density, integrated genetic linkage map of lettuce (Lactuca spp.). Theor Appl Genet 115:735–746

    Article  PubMed  CAS  Google Scholar 

  • Truco MJ, Ashrafi H, Kozik A, van Leeuwen H, Bowers J, Reyes Chin Wo S, Stoffel K, Xu H, Hill T, van Deynze A, Michelmore RW (2013) An ultra high-density, transcript-based, genetic map of lettuce. G3 (Bethesda) 3:617–631

    Article  CAS  Google Scholar 

  • Tuyen DD, Lal SK, Xu DH (2010) Identification of a major QTL allele from wild soybean (Glycine soja Sieb. & Zucc.) for increasing alkaline salt tolerance in soybean. Theor Appl Genet 121:229–236

    Article  PubMed  CAS  Google Scholar 

  • Uwimana B, Smulders MJ, Hooftman DA, Hartman Y, van Tienderen PH, Jansen J, McHale LK, Michelmore RW, van de Wiel CC, Visser RG (2012a) Hybridization between crops and wild relatives: the contribution of cultivated lettuce to the vigour of crop–wild hybrids under drought, salinity and nutrient deficiency conditions. Theor Appl Genet 125:1097–1111

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Uwimana B, Smulders MJ, Hooftman DA, Hartman Y, van Tienderen PH, Jansen J, McHale LK, Michelmore RW, Visser RG, van de Wiel CC (2012b) Crop to wild introgression in lettuce: following the fate of crop genome segments in backcross populations. BMC Plant Biol 12:43

    Article  PubMed  PubMed Central  Google Scholar 

  • Vallejo AJ, Yanovsky MJ, Botto JF (2010) Germination variation in Arabidopsis thaliana accessions under moderate osmotic and salt stresses. Ann Bot Lond 106:833–842

    Article  CAS  Google Scholar 

  • van Eeuwijk FA, Bink MC, Chenu K, Chapman SC (2010) Detection and use of QTL for complex traits in multiple environments. Curr Opin Plant Biol 13:193–205

    Article  PubMed  Google Scholar 

  • van Treuren R, van der Arend AJM, Schut JW (2011) Distribution of downy mildew (Bremia lactucae Regel) resistances in a genbank collection of lettuce and its wild relatives. Plant Genet Resour 11:15–25

    Article  Google Scholar 

  • Vaughn LM, Masson PH (2011) A QTL study for regions contributing to Arabidopsis thaliana root skewing on tilted surfaces. G3 (Bethesda) 1:105–115

    Article  Google Scholar 

  • Vision TJ, Brown DG, Shmoys DB, Durrett RT, Tanksley SD (2000) Selective mapping: a strategy for optimizing the construction of high-density linkage maps. Genetics 155:407–420

    PubMed  CAS  PubMed Central  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Wang J, Bao Y, Wu Y, Zhang H (2010) Quantitative trait loci controlling rice seed germination under salt stress. Euphytica 178:297–307

    Article  Google Scholar 

  • Wang Z, Chen Z, Cheng J, Lai Y, Wang J, Bao Y, Huang J, Zhang H (2012a) QTL analysis of Na+ and K+ concentrations in roots and shoots under different levels of NaCl stress in rice (Oryza sativa L.). PLoS One 7:e51202

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang Z, Cheng J, Chen Z, Huang J, Bao Y, Wang J, Zhang H (2012b) Identification of QTLs with main, epistatic and QTL × environment interaction effects for salt tolerance in rice seedlings under different salinity conditions. Theor Appl Genet 125:807–815

    Article  PubMed  CAS  Google Scholar 

  • Zhang FZ, Wagstaff C, Rae AM, Sihota AK, Keevil CW, Rothwell SD, Clarkson GJ, Michelmore RW, Truco MJ, Dixon MS, Taylor G (2007) QTLs for shelf life in lettuce co-locate with those for leaf biophysical properties but not with those for leaf developmental traits. J Exp Bot 58:1433–1449

    Article  PubMed  CAS  Google Scholar 

  • Zhang NW, Lindhout P, Niks RE, Jeuken MJW (2009) Genetic dissection of Lactuca saligna nonhost resistance to downy mildew at various lettuce developmental stages. Plant Pathol 58:923–932

    Article  Google Scholar 

  • Zhao Y, Wang T, Zhang W, Li X (2011) SOS3 mediates lateral root development under low salt stress through regulation of auxin redistribution and maxima in Arabidopsis. N Phytol 189:1122–1134

    Article  CAS  Google Scholar 

  • Zhou G, Johnson P, Ryan PR, Delhaize E, Zhou M (2011) Quantitative trait loci for salinity tolerance in barley (Hordeum vulgare L.). Mol Breed 29:427–436

    Article  CAS  Google Scholar 

  • Zhu J, Kaeppler SM, Lynch JP (2005) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310

    Article  CAS  Google Scholar 

  • Zolla G, Heimer YM, Barak S (2010) Mild salinity stimulates a stress-induced morphogenic response in Arabidopsis thaliana roots. J Exp Bot 61:211–224

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

Thanks to China Scholarship Council (http://en.csc.edu.cn/) for providing funding to Z.W. The contributions from the Compositae Genome Project were supported by the National Science Foundation Plant Genome Program Grant # DBI0421630 to RWM. M.M. and C.T. were funded by the STW Learning from Nature program Grant 10987 and NWO ALW Grants 820.02.017 and 846.11.002 awarded to C.T.

Author information

Authors and Affiliations

  1. Biosystematics Group, Wageningen University, 6708 PB, Wageningen, The Netherlands

    Zhen Wei & M. Eric Schranz

  2. Swammerdam Institute for Life Sciences, University of Amsterdam, 1090 GE, Amsterdam, The Netherlands

    Magdalena M. Julkowska & Christa Testerink

  3. Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, 1090 GE, Amsterdam, The Netherlands

    Jacques-Olivier Laloë, Yorike Hartman & Peter H. van Tienderen

  4. EnzaZaden, Enkhuizen, The Netherlands

    Gert-Jan de Boer

  5. Department of Plant Sciences, The Genome Center, University of California, Davis, CA, 95616-8816, USA

    Richard W. Michelmore

Authors
  1. Zhen Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Magdalena M. Julkowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jacques-Olivier Laloë
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yorike Hartman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gert-Jan de Boer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard W. Michelmore
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Peter H. van Tienderen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Christa Testerink
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. M. Eric Schranz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Eric Schranz.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 541 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wei, Z., Julkowska, M.M., Laloë, JO. et al. A mixed-model QTL analysis for salt tolerance in seedlings of crop-wild hybrids of lettuce. Mol Breeding 34, 1389–1400 (2014). https://doi.org/10.1007/s11032-014-0123-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-014-0123-2

Keywords

Search

Navigation