Skip to main content
SpringerLink
Log in

QTL analysis of Na+ and K+ concentrations in shoots and roots under NaCl stress based on linkage and association analysis in japonica rice

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Soil salinity is a major constraint to rice production. Na+ and K+ concentrations and ion balance play important roles in the salt tolerance of rice. In the present study, linkage mapping and association mapping were used to identify the QTLs for the visual tolerance score (SES), and the concentrations of Na+ and K+ in shoots (SNC and SKC) and roots (RNC and RKC). A BC2F2:3 population with 137 SSR markers derived from Dongnong425 (a salt-sensitive and widely cultivated variety) as the recurrent parent and Changbai10 (a salt-tolerant variety) as the donor parent was used for linkage mapping. A total of 13 QTLs were identified by the inclusive composite interval mapping method, including 2 for SES, 4 for SNC, 3 for SKC, 3 for RNC, and 1 for RKC. This study was supplemented with association mapping, which was conducted using a panel of 341 japonica rice accessions from different geographical origins with 160 selected SSR markers. A total of 24 significant marker-trait associations (P ≤ 0.01) involving 20 markers were identified using the GLM (Q) and MLM (Q+K) models in TASSEL2.1. Among them, 10 of the SSR markers confirmed or narrowed the genomic regions for salt tolerance that were reported in linkage studies, including six QTLs identified during the present study. The QTLs identified through linkage and association mapping may be useful for marker-assisted selection in rice breeding programs and may accelerate the development of salt-tolerant rice varieties.

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
Fig. 4

Similar content being viewed by others

References

  • Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341–356

    Article  Google Scholar 

  • Ammar MHM, Pandit A, Singh RK, Sameena S, Chauhan MS, Singh AK, Sharma PC, Gaikwad K, Sharma TR, Mohapatra T, Singh NK (2009) Mapping of QTLs controlling Na+, K+ and Cl− ion concentrations in salt tolerant Indica rice variety CSR27. J Plant Biochem Biotechnol 18:139–150

    Article  CAS  Google Scholar 

  • Bonilla P, Mackell D, Deal K, Gregorio G (2002) RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philipp Agric Sci 85:68–76

    Google Scholar 

  • Brachi B, Faure N, Horton M, Flahauw E, Vazquez A, Nordborg M, Bergelson J, Cuguen J, Roux F (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6:e1000940

    Article  PubMed Central  PubMed  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Breseghello F, Sorrells ME (2006) Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172:1165–1177

    Article  PubMed Central  PubMed  Google Scholar 

  • Cheng LR, Wang Y, Meng LJ, Hu X, Cui YR, Sun Y, Zhu LH, Ali J, Xu JL, Li ZK (2011) Identification of salt-tolerant QTLs with strong genetic background effect using two sets of reciprocal introgression lines in rice. Genome 55:45–55

    Article  PubMed  Google Scholar 

  • Cheng YW, Qi YC, Zhu Q, Chen X, Wang N, Zhao X, Chen HY, Cui XJ, Xu L, Zhang W (2009) New changes in the plasma-membrane-associated proteome of rice roots under salt stress. Proteomics 9:3100–3114

  • Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, Frouin J, Rouan L, Goze E, Kilian A, Ahmadi N, Dingkuhn M (2013) Genome-wide association mapping of root traits in a japonica rice panel. PLoS One 11:e78037

    Article  Google Scholar 

  • Doyl JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15

    Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Famoso AN, Zhao K, Clark RT, Tung CW, Wright MH, Bustamante C, Kochian LV, McCouch SR (2011) Genetic architecture of aluminum tolerance in rice (Oryza sativa) determined through genome-wide association analysis and QTL mapping. PLoS Genet 7:e1002221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Bucker ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374

    Article  CAS  PubMed  Google Scholar 

  • Flowers TJ, Koyama ML, Flowers SA, Sudhakar C, Singh KP, Yeo AR (2000) QTL: their place in engineering tolerance of rice to salinity. J Exp Bot 51:99–106

    Article  CAS  PubMed  Google Scholar 

  • Garris AJ, McCouch SR, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759–769

    PubMed Central  PubMed  Google Scholar 

  • Gregorio GB, Senadhira D, Mendoza RD, Manigbas NL, Roxas JP, Guerta CQ (2002) Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crop Res 76:91–101

    Article  Google Scholar 

  • Haq TU, Gorham J, Akhtar J, Akhtar N, Steele KA (2010) Dynamic quantitative trait loci for salt stress components on chromosome 1 of rice. Funct Plant Biol 37:634–645

    Article  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Holland JB (2007) Genetic architecture of complex traits in plants. Curr Opin Plant Biol 10:156–161

    Article  CAS  PubMed  Google Scholar 

  • International Rice Genome Sequencing Project (IRGSP) (2005) The map-based sequence of the rice genome. Nature 436:793–800

  • IRRI (1996) Standard evaluation system for rice, 4th edn. International Rice Research Institute, Manila, p 52

    Google Scholar 

  • Ismail AM, Heuer S, Thomson MJ, Wissuwa M (2007) Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol Biol 65:547–570

    Article  CAS  PubMed  Google Scholar 

  • Jin L, Lu Y, Xiao P, Sun M, Corke H, Bao J (2010) Genetic diversity and population structure of a diverse set of rice germplasm for association mapping. Theor Appl Genet 121:475–487

    Article  PubMed  Google Scholar 

  • Kanneganti V, Gupta AK (2008) Overexpression of OsiSAP8, a member of stress associated protein (SAP) gene family of rice confers tolerance to salt, drought and cold stress in transgenic tobacco and rice. Plant Mol Biol 66:445–462

    Article  CAS  PubMed  Google Scholar 

  • Koyama ML, Levesley A, Koebner RM, Flowers TJ, Yeo AR (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiol 125:406–422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Le Gouis J, Bordes J, Ravel C, Heumez E, Faure S, Praud S, Galic N, Remoue C, Balfourier F, Allard V, Rousset M (2012) Genome-wide association analysis to identify chromosomal regions determining components of earliness in wheat. Theor Appl Genet 124:597–611

    Article  PubMed  Google Scholar 

  • Lee SY, Ahn JH, Cha YS, Yun DW, Lee MC, Ko JC, Lee KS, Eun MY (2007) Mapping QTLs related to salinity tolerance of rice at the young seedling stage. Plant Breed 126:43–46

    Article  Google Scholar 

  • Lewis CM (2002) Genetic association studies: design, analysis and interpretation. Brief Bioinform 3:146–153

    Article  CAS  PubMed  Google Scholar 

  • Li HH, Ye GY, Wang JK (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374

    Article  PubMed Central  PubMed  Google Scholar 

  • Li Y, Huang Y, Bergelson J, Nordborg M, Borevitz JO (2010) Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc Natl Acad Sci 107:21199–21204

    Article  CAS  PubMed Central  PubMed  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  CAS  PubMed  Google Scholar 

  • Luo HL, Song FM, Zheng Z (2005) Overexpression in transgenic tobacco reveals different roles for the rice homeodomain gene OsBIHD1 in biotic and abiotic stress responses. J Exp Bot 56:2673–2682

    Article  CAS  PubMed  Google Scholar 

  • McCouch SR, Cho YG, Yano M, Paul E, Blinstrub M, Morishima H, Kinoshita T (1997) Report on QTL nomenclature. Rice Genet Newsl 14(11):11–131

    Google Scholar 

  • Mir RR, Kumar N, Jaiswal V, Girdharwal N, Prasad M, Balyan HS, Gupta PK (2012) Genetic dissection of grain weight in bread wheat through quantitative trait locus interval and association mapping. Mol Breed 29:963–972

    Article  Google Scholar 

  • Mohammadi-Nejad G, Arzani A, Rezai AM, Singh RK, Gregorio GB (2008) Assessment of rice genotypes for salt tolerance using microsatellite markers associated with the saltol QTL. Afr J Biotechnol 7:31

    Google Scholar 

  • Niu Y, Xu Y, Liu XF, Yang SX, Wei SP, Xie FT, Zhang YM (2013) Association mapping for seed size and shape traits in soybean cultivars. Mol Breed 31:785–794

    Article  CAS  Google Scholar 

  • Ooijen JW, Voorrips RE (2002) JoinMap: version 3.0: software for the calculation of genetic linkage maps. University and Research Center

  • Pandit A, Rai V, Bal S, Sinha S, Kumar V, Chauhan M, Gautam RK, Singh R, Sharma PC, Singh AK (2010) Combining QTL mapping and transcriptome profiling of bulked RILs for identification of functional polymorphism for salt tolerance genes in rice (Oryza sativa L.). Mol Genet Genomics 284:121–136

    Article  CAS  PubMed  Google Scholar 

  • Prasad SR, Bagali PG, Hittalmani S, Shashidhar HE (2000) Molecular mapping of quantitative trait loci associated with seedling tolerance of salt stress in rice (Oryza sativa L.). Curr Sci 78:162–164

    CAS  Google Scholar 

  • Pritchard JK, Stephens M, Rosenberg NA, Donnelly P (2000) Association mapping in structured populations. Am J Hum Genet 67:170–181

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rana P, Jain S, Yadav S, Saini N, Jain RK (2009) Identification of SSR Markers for salt-tolerance in rice variety CSR10 by selective genotyping. J Plant Biochem Biotechnol 18:87–91

    Article  CAS  Google Scholar 

  • 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  CAS  PubMed  Google Scholar 

  • Rosenberg NA, Burke T, Elo K, Feldman MW, Freidlin PJ, Groenen MA, Hillel J, Mki-Tanila A, Tixier-Boichard M, Vignal A, Wimmers K, Weigend S (2001) Empirical evaluation of genetic clustering methods using multilocus genotypes from 20 chicken breeds. Genetics 159:699–713

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sabouri H, Rezai AM, Moumeni A, Kavousi A, Katouzi M, Sabouri A (2009) QTLs mapping of physiological traits related to salt tolerance in young rice seedlings. Biol Plant 53:657–662

    Article  Google Scholar 

  • Singh RK, Redoña E, Refuerzo L (2010) Varietal improvement for abiotic stress tolerance in crop plants: special reference to salinity in rice. In: Abiotic stress adaptation in plants. Springer, Dordrecht, pp 387–415

  • Sun SJ, Guo SQ, Yang X, Bao YM, Tang HJ, Sun H, Huang J, Zhang HS (2010) Functional analysis of a novel Cys2/His2-type zinc finger protein involved in salt tolerance in rice. J Exp Bot 61:2807–2818

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tanksley SD, Nelson JC (1996) Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines. Thero Appl Genet 92:191–203

    Article  CAS  Google Scholar 

  • Thomson MJ, de 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 

  • Tian L, Tan LB, Liu FX, Cai HW, Sun CQ (2011) Identification of quantitative trait loci associated with salt tolerance at seedling stage from Oryza rufipogon. J Genet Genomics 38:593–601

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang ZF, Chen ZW, Cheng JP, Lai YY, Wang JF, Bao YM, Huang J, Zhang HS (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  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang ZF, Cheng JP, Chen ZW, Huang J, Bao YM, Wang JF, Zhang HS (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  CAS  PubMed  Google Scholar 

  • Wassmann R, Hien NX, Hoanh CT, Tuong TP (2004) Sea level rise affecting the Vietnamese Mekong Delta: water elevation in the flood season and implications for rice production. Clim Chang 66:89–107

    Article  Google Scholar 

  • Weng JF, Xie CX, Hao ZF, Wang JJ, Liu CL, Li MS, Zhang DG, Bai L, Zhang SH, Li XH (2011) Genome-wide association study identifies candidate genes that affect plant height in Chinese elite maize (Zea mays L.) inbred lines. PLoS One 6:e29229

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu R, Garg A (2003) Engineering rice plants with trehalose-producing genes improves tolerance to drought, salt, and low temperature. ISB news report

  • Wu Y, Hu Y, Xu G (2009) Interactive effects of potassium and sodium on root growth and expression of K/Na transporter genes in rice. Plant Growth Regul 57:271–280

    Article  CAS  Google Scholar 

  • Xie XB, Song MH, Jin FX, Ahn SN, Suh JP, Hwang HG, McCouch SR (2006) Fine mapping of a grain weight quantitative trait locus on rice chromosome 8 using near-isogenic lines derived from a cross between Oryza sativa and Oryza rufipogon. Thero Appl Genet 113:885–894

    Article  CAS  Google Scholar 

  • Yeo AR, Yeo ME, Flowers SA, Flowers TJ (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theor Appl Genet 79:377–384

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice. International Rice Research Institute, Manila, p 38

    Google Scholar 

  • Zheng TQ, Yang J, Zhong WG, Zhai HQ, Zhu LH, Fan FJ, Ali AJ, Yang JH, Wang J, Zhu JY, Uzokwe VNE, Xu JL, Li ZK (2012) Novel loci for field resistance to black-streaked dwarf and stripe viruses identified in a set of reciprocal introgression lines of rice (Oryza sativa L.). Mol Breed 29:925–938

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Tackle Key Program in Science and Technology of the Science and Technology Ministry of China (2011BAD35B02-01) and by the Program in Science and Technology of the Science and Technology Ministry of China (2011BAD16B11).

Author information

Authors and Affiliations

  1. Rice Research Institute, College of Agriculture, Northeast Agriculture University, 59 Mucai Street, Harbin, 150030, China

    Hongliang Zheng, Hongwei Zhao, Hualong Liu, Jingguo Wang & Detang Zou

Authors
  1. Hongliang Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hongwei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hualong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jingguo Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Detang Zou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Detang Zou.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, H., Zhao, H., Liu, H. et al. QTL analysis of Na+ and K+ concentrations in shoots and roots under NaCl stress based on linkage and association analysis in japonica rice. Euphytica 201, 109–121 (2015). https://doi.org/10.1007/s10681-014-1192-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-014-1192-3

Keywords

Search

Navigation