Skip to main content
Log in

Association mapping validates previously identified quantitative trait loci for salt tolerance in rice (Oryza sativa L.)

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Salinity is the main abiotic stress that limits rice (Oryza sativa L.) production worldwide. An association mapping project was designed to validate quantitative trait loci (QTLs) in rice associated with Na+, K+ and Ca++ accumulation traits identified in our previous study of linkage mapping. Twenty four varieties/lines of rice were phenotyped for biochemical and yield traits. Among these varieties/lines, two mapping parents, Pokkali and IR-36, of our previous linkage mapping study were also included. For marker-trait assessments, both general linear model (GLM) and mixed linear model (MLM) analyses were performed. Thirteen significant marker-trait associations at P ≤ 0.001 were identified. Associated markers for these marker-trait associations were RM503, RM225, RM152, and RM254 located on chromosomes 3, 6, 8, and 11, respectively. Previously identified QTLs in linkage mapping study for Na+ uptake, Ca++ uptake, total cations uptake, Ca++ uptake ratio, K+ uptake ratio, and Na+/K+ uptake were validated in this study. Heritability values for these traits ranged from 1.00e-05 to 1. Linked markers for these validated QTLs were RM140, RM243, RM203, RM480, RM137, and RM254 located on chromosomes 1, 1, 3, 5, 8, and 11, respectively. These markers will be a valuable resource for marker-assisted breeding (MAB) approach to develop elite salt tolerant rice cultivars. This study demonstrates the potential of association mapping approach to validate previously identified QTLs.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abdurakhmonov IY, Kohel RJ, Yu JZ, Pepper AE, Abdullaev AA, Kushanov FN, Salakhutdinov IB, Buriev ZT, Saha S, Scheffler BE, Jenkins JN, Abdukarimov AA (2008) Molecular diversity and association mapping of fiber quality traits in exotic G. hirsutum L. germplasm. Genomics 92:478–487

    Article  CAS  PubMed  Google Scholar 

  • Abdurakhmonov IY, Saha S, Jenkins JN, Buriev ZT, Shermatov SE, Scheffler BE, Pepper AE, Yu JZ, Kohel RJ, Abdukarimov A (2009) Linkage disequilibrium based association mapping of fiber quality traits in G. hirsutum L. variety germplasm. Genetica 136:401–417

    Article  PubMed  Google Scholar 

  • Ammar MHM, Singh RK, Singh AK, Mohapatra T, Sharma TR, Singh NK (2007) Mapping QTLs for salinity tolerance at seedling stage in rice (Oryza sativa L.). Afr Crop Sci Confer Proceed 8:617–620

    Google Scholar 

  • Asch F, Dingkuln K, Miezan K (2000) Leaf K/Na ratio predicts salinity induced yield loss in irrigated rice. Euphytica 111:109–118

    Article  Google Scholar 

  • Ashkani S, Rafii MY, Rahim HA, Latif MA (2013a) Mapping of the quantitative trait locus (QTL) conferring partial resistance to rice leaf blast disease. Biotechnol Lett 35:799–810

    Article  CAS  PubMed  Google Scholar 

  • Ashkani S, Rafii MY, Rahim HA, Latif MA (2013b) Genetic dissection of rice blast resistance by QTL mapping approach using an F3 population. Mol Biol Reports 40:2503–2515

    Article  CAS  Google Scholar 

  • Aslam M, Ahmed I, Mahmood IA, Akhtar J, Nawaz S (1995) Physiological basis of differential tolerance in rice to salinity. Pak J Soil Sci 10:38–41

    Google Scholar 

  • Atwell S, Huang YS, Vilhjalmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, de Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JD, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, Traw MB, Weigel D, Marjoram P, Borevitz JO, Bergelson J, Nordborg M (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465:627–631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balkunde S, Le H-L, Lee H-S, Kim D-M, Kang J-W, Ahn S-N (2013) Fine mapping of a QTL for the number of spikelets per panicle by using near-isogenic lines derived from an interspecific cross between Oryza sativa and Oryza minuta. Plant Breed 132:70–76

    Article  CAS  Google Scholar 

  • Cheng L, Yang A, Jiang C, Ren M, Zhang Y, Feng Q, Wang S, Guan Y, Luo C (2015) Quantitative trait loci mapping for plant height in tobacco using linkage and association mapping methods. Crop Sci 55:641–647

    Article  Google Scholar 

  • Cockram J, White J, Zuluaga DL, Smith D, Comadran J, Macaulay M, Luo ZW, Kearsey MJ, Werner P, Harrap D, Tapsell C, Liu H, Hedley PE, Stein N, Schulte D, Steuernagel B, Marshall DF, Thomas WTB, Ramsay L, Mackay I, Balding DJ, Waugh R, O’Sullivan DM, Consortium A (2010) Genome-wide association mapping to candidate polymorphism resolution in the unsequenced barley genome. Proc Natl Acad Sci U S A 107:21611–21616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Eizenga GC, Prasad B, Jackson AK, Jia MH (2013) Identification of rice sheath blight and blast quantitative trait loci in two different O. sativa/O. nivara advanced backcross populations. Mol Breeding 31:889–907

    Article  Google Scholar 

  • Famoso AN, Zhao K, Clark RT, Tung C-W, 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  PubMed Central  Google Scholar 

  • FAO (2005) Management of irrigation-induced salt-affected soils. ftp://ftp.fao.org/agl/iptrid/salinity_brochure_en.pdf

  • FAO (2009) FAO Statistical Yearbook, 2005. Country Profiles-WEB Edition, Statistics Division FAO-Food and Agriculture Surfed on April 08, at: http://www.fao.org/statistics/yearbook. 22(2):6

  • Flowers TJ, Lauchli A (1983) Sodium versus potassium: substitution and compartmentation. Inorg Plant Nutri 15b:651–681

    CAS  Google Scholar 

  • Gao JP, Lin HX (2013) QTL analysis and map-based cloning of salt tolerance gene in rice. Rice Protocols: Methods Mol Biol 956:69–82

    Article  CAS  Google Scholar 

  • Garciadeblás B, Senn ME, Bañuelos MA, Rodríquez-Navarro A (2003) Sodium transport and HKT transporters: the rice model. Plant J 34:788–801

    Article  PubMed  Google Scholar 

  • Gillingham AG, Sheath GW, Sutton MM (1987) Soil contamination and sample washing effects on major nutrient and soluble sugar concentration of pasture. New Zealand J Agric Res 30:281–285

    Article  CAS  Google Scholar 

  • Hall JL, Flowers TJ (1973) The effect of salt on protein synthesis in the halophyte, Suaeda maritima. Planta 110:361–368

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa G, Nakamura K, Ito H, Saito M, Sato M, Jinno H, Yoshimura Y, Nishimura T, Maejima H, Uehara Y, Kobayashi F, Nakamura T (2014) Association mapping and validation of QTLs for flour yield in the soft winter wheat variety Kitahonami. PLoS One 9:e111337

    Article  PubMed  PubMed Central  Google Scholar 

  • Javed MA (2006) Evaluation of F1 doubled haploid lines and QTL analysis using F2 population for salinity tolerance in rice (Oryza sativa L.). PhD thesis. Grad. School Sci. Tech. Kobe Uni. Kobe, Japan

  • Javed MA, Shabbir G, Misoo S, Ishii T, Kamijima O (2003) Salinity tolerance of three basmati lines: a comparative study of yield related characters. Kinki J Crop Sci Breed 48:7–12

    Google Scholar 

  • Javed MA, Misoo S, Ishii T, Kamijima O (2006) Discrepancy of two ecotypes of Oryza sativa L. to salinity at germination and seedling stages. Ann Biol 22:201–211

    CAS  Google Scholar 

  • Jegadeesan S, Yu K, Poysa V, Gawalko E, Morrison MJ, Shi C, Cober E (2010) Mapping and validation of simple sequence repeat markers linked to a major gene controlling seed cadmium accumulation in soybean [Glycine max (L.) Merr]. Theor Appl Genet 121:283–294

    Article  CAS  PubMed  Google Scholar 

  • Khan MSK, Saeed M, Iqbal J (2015) Identification of quantitative trait loci for Na+, K+ and Ca++ accumulation traits in rice grown under saline conditions using F2 mapping population. Brazilian J Bot 38:555–565

    Article  Google Scholar 

  • Khush GS, Brar DS (2002) Biotechnology for rice breeding: Progress and potential impact. The International Rice Commission (20th Session). Bangkok, Thailand, 23–26 July, 2002

  • Korir PC, Zhang J, Wu K, Zhao T, Gai J (2013) Association mapping combined with linkage analysis for aluminum tolerance among soybean cultivars released in yellow and Changjiang River valleys in China. Theor Appl Genet 126:1659–1675

    Article  CAS  PubMed  Google Scholar 

  • Kumar V, Singh A, Mithra SVA, Krishnamurthy SL, Parida SK, Jain S, Tiwari KK, Kumar P, Rao AR, Sharma SK, Khurana JP, Singh NK, Mohapatra T (2015) Genome-wide association mapping of salinity tolerance in rice (Oryza sativa). DNA Res:1–13

  • 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 

  • Li N, Shi J, Wang X, Liu G, Wang H (2014) A combined linkage and regional association mapping validation and fine mapping of two major pleiotropic QTLs for seed weight and silique length in rapeseed (Brassica napus L.). BMC Plant Biol 14:114

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Long NV, Dolstra O, Malosetti M, Kilian B, Graner A, Visser RGF, van der Linden CG (2013) Association mapping of salt tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 126:2335–2351

    Article  CAS  PubMed  Google Scholar 

  • Lu W, Wen Z, Li H, Yuan D, Li J, Zhang H, Huang Z, Cui S, Du W (2013) Identification of the quantitative trait loci (QTL) underlying water soluble protein content in soybean. Theor Appl Genet 126:425–433

    Article  CAS  PubMed  Google Scholar 

  • Mace ES, Singh V, Van Oosterom EJ, Hammer GL, Hunt CH, Jordan DR (2012) QTL for nodal root angle in sorghum (Sorghum bicolor L. Moench) co-locate with QTL for traits associated with drought adaptation. Theor Appl Genet 124:97–109

    Article  CAS  PubMed  Google Scholar 

  • Mackay I, Powell W (2007) Methods for linkage disequilibrium mapping in crops. Trends Plant Sci 12:57–63

    Article  CAS  PubMed  Google Scholar 

  • McCouch SR, Wright MH, Tung C-W, Maron LG, McNally KL, Fitzgerald M, Singh N, DeClerck G, Agosto-Perez F, Korniliev P, Greenberg AJ, Naredo MEB, Mercado SMQ, Harrington SE, Shi Y, Branchini DA, Kuser-Falcão PR, Leung H, Ebana K, Yano M, Eizenga G, McClung A, Mezey J (2016) Open access resources for genome-wide association mapping in rice. Nat Commun. doi:10.1038/ncomms10532

    Google Scholar 

  • Mishra KK, Vikram P, Yadaw RB, Swamy BPM, Dixit S, Cruz MTS, Maturan P, Marker S, Kumar A (2013) qDTY12.1: a locus with a consistent effect on grain yield under drought in rice. BMC Genet 14:12

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Murguia JR, Belles JM, Serrano R (1995) A salt-sensitive 3′(2′), 5′-bisphosphate nucleotidase involved in sulfate activation. Science 267:232–234

    Article  CAS  PubMed  Google Scholar 

  • Negrão S, Almadanim MC, Pires IS, Abreu IA, Maroco J, Courtois B, Gregorio GB, McNally KL, Oliveira MM (2013) New allelic variants found in key rice salt-tolerance genes: an association study. Plant Biotechnol J 11:87–100

    Article  PubMed  Google Scholar 

  • Prasad SR, Bagali PG, Hittalmani S, Shashidhar HE (2000) Molecular mapping of quantitative trait loci associated with seedling tolerance to 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  PubMed Central  Google Scholar 

  • Qureshi RH, Aslam M, Mustaga G, Akhtar J (1991) Some aspects of physiology of salt tolerance in wheat (Triticum aestivum L.). Pak J Agric Sci 28:199–209

    Google Scholar 

  • Rains DW, Epstein E (1965) Transport of sodium in plant tissue. Science 148:1611

    Article  CAS  PubMed  Google Scholar 

  • Rajendran K, Tester M, Roy SJ (2009) Quantifying the three main components of salinity tolerance in cereals. Plant Cell Environ 32:237–249

    Article  CAS  PubMed  Google Scholar 

  • Ren Z, Zheng Z, Chinnusami V, Zhu J, Cui X, Iida K, Zhu JK (2010) RAS1, a quantitative trait locus for salt tolerance and ABA sensitivity in Arabidopsis. Proceed Natl Acad Sci USA 107:5669–5674

    Article  CAS  Google Scholar 

  • Riedelsheimer C, Lisec J, Czedik-Eysenberg A, Sulpice R, Flis A, Grieder C, Altmann T, Stitt M, Willmitzer L, Melchinger AE (2012) Genome-wide association mapping of leaf metabolic profiles for dissecting complex traits in maize. PNAS 109:8872–8877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saeed M, Guo W-Z, Ullah I, Tabbasam N, Zafar Y, Rahman M, Zhang T-Z (2011) QTL mapping for physiology, yield and plant architecture traits in cotton (Gossypium hirsutum L.) grown under well-watered versus water-stress conditions. Electron J Biotechnol 14(3). doi:10.2225/vol14-issue3-fulltext-3

  • Saeed M, Dahab AHA, Guo W-Z, Zhang T-Z (2012) A cascade of recently discovered molecular mechanisms involved in abiotic stress tolerance of plants. OMICS: JIB 16:188–199

    Article  CAS  Google Scholar 

  • Saeed M, Guo W-Z, Zhang T-Z (2014) Association mapping for salinity tolerance in cotton (Gossypium hirsutum L.) germplasm from US and diverse regions of China. Aust J Crop Sci 8:338–346

    CAS  Google Scholar 

  • Septiningsih EM, Ignacio JCI, Sendon PMD, Sanchez DL, Ismail AM, Mackill DJ (2013) QTL mapping and confirmation for tolerance of anaerobic conditions during germination derived from the rice landrace Ma-Zhan red. Theor Appl Genet 126:1357–1366

    Article  PubMed  Google Scholar 

  • Shannon MC, Rhoades JD, Draper JH, Scardaci SC, Spyres MD (1998) Assessment of salt tolerance in rice cultivars in response to salinity problems in California. Crop Sci 38:394–398

    Article  CAS  Google Scholar 

  • Spindel J, Begum H, Akdemir D, Virk P, Collard B, Redoña E, Atlin G, Jannink J-L, McCouch SR (2015) Genomic selection and association mapping in rice (Oryza sativa): effect of trait genetic architecture, training population composition, marker number and statistical model on accuracy of rice genomic selection in elite, tropical rice breeding lines. PLoS Genet 11:e1004982

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun L, Ma D, Yu H, Zhou F, Li Y, Luo L, Gao G, Zhang Q, Xu C, He Y (2013) Identification of quantitative trait loci for grain size and the contributions of major grain-size QTLs to grain weight in rice. Mol Breeding 31:451–461

    Article  CAS  Google Scholar 

  • Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K (1999) A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11:1195–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Eeuwijk FA, Kraakman ATW, Niks RE, Van den Berg PMMM, Stam P (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang P, Zhou G, Cui K, Li Z, Yu S (2012) Clustered QTL for source leaf size and yield traits in rice (Oryza sativa L.). Mol Breeding 29:99–113

    Article  CAS  Google Scholar 

  • Yano M, Sasaki T (1997) Genetic and molecular dissection of quantitative traits in rice. Plant Mol Biol 35:145–153

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Flowers TJ, Wang S (2010) Mechanisms of sodium uptake by roots of higher plants. Plant Soil 326:45–60

    Article  CAS  Google Scholar 

  • Zhao J, Paulo MJ, Jamar D, Lou P, van Eeuwijk F, Bonnema G, Vreugdenhil D, Koornneef M (2007) Association mapping of leaf traits, flowering time, and phytate content in Brassica rapa. Genome 50:963–973

    Article  CAS  PubMed  Google Scholar 

  • Zheng H, Wang J, Zhao H, Liu H, Sun J, Guo L, Zou D (2015) Genetic structure, linkage disequilibrium and association mapping of salt tolerance in japonica rice germplasm at the seedling stage. Mol Breeding 35:152

    Article  Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71

    Article  CAS  PubMed  Google Scholar 

  • Zuo S, Yin Y, Pan C, Chen Z, Zhang Y, Gu S, Zhu L, Pan X (2013) Fine mapping of qSB-11 LE, the QTL that confers partial resistance to rice sheath blight. Theor Appl Genet 126:1257–1272

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

First author of this paper was financially supported by Ministry of Education, Government of Pakistan during his entire PhD study program. This work is output of his PhD research project. We are thankful to the Director, Rice Research Institute, Kalashah Kaku, Lahore, Pakistan for providing seeds of different rice varieties used during this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Muhammad Saeed.

Ethics declarations

Conflicts of interest

The authors declare no conflict of interest.

Electronic supplementary material

Table S1

(DOCX 21 kb)

Table S2

(DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, M.S.K., Saeed, M. & Iqbal, J. Association mapping validates previously identified quantitative trait loci for salt tolerance in rice (Oryza sativa L.). Mol Breeding 36, 172 (2016). https://doi.org/10.1007/s11032-016-0605-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-016-0605-5

Keywords

Navigation