Pyramiding QTLs controlling tolerance against drought, salinity, and submergence in rice through marker assisted breeding

Autoři: Valarmathi Muthu aff001;  Ragavendran Abbai aff001;  Jagadeeshselvam Nallathambi aff001;  Hifzur Rahman aff001;  Sasikala Ramasamy aff001;  Rohit Kambale aff001;  Thiyagarajan Thulasinathan aff001;  Bharathi Ayyenar aff001;  Raveendran Muthurajan aff001
Působiště autorů: Centre for Plant Molecular Biology and Biotechnology Tamil Nadu Agricultural University, Coimbatore, India aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227421


Increases in rice productivity are significantly hampered because of the increase in the occurrence of abiotic stresses, including drought, salinity, and submergence. Developing a rice variety with inherent tolerance against these major abiotic stresses will help achieve a sustained increase in rice production under unfavorable conditions. The present study was conducted to develop abiotic stress-tolerant rice genotypes in the genetic background of the popular rice variety Improved White Ponni (IWP) by introgressing major effect quantitative trait loci (QTLs) conferring tolerance against drought (qDTY1.1, qDTY2.1), salinity (Saltol), and submergence (Sub1) through a marker assisted backcross breeding approach. Genotyping of early generation backcrossed inbred lines (BILs) resulted in the identification of three progenies, 3-11-9-2, 3-11-11-1, and 3-11-11-2, possessing all four target QTLs and maximum recovery of the recurrent parent genome (88.46%). BILs exhibited consistent agronomic and grain quality characters compared to those of IWP and enhanced performance against dehydration, salinity, and submergence stress compared with the recurrent parent IWP. BILs exhibited enhanced tolerance against salinity during germination and increased shoot length, root length, and vigor index compared to those of IWP. All three BILs exhibited reduced symptoms of injury because of salinity (NaCl) and dehydration (PEG) than did IWP. At 12 days of submergence stress, BILs exhibited enhanced survival and greater recovery, whereas IWP failed completely. BILs were found to exhibit on par grain and cooking quality characteristics with their parents. Results of this study clearly demonstrated the effects of the target QTLs in reducing damage caused by drought, salinity, and submergence and lead to the development of a triple stress tolerant version of IWP.

Klíčová slova:

Drought – Drought adaptation – Leaves – Plant resistance to abiotic stress – Quantitative trait loci – Rice – Salinity – Seedlings


1. Ashikari M, Ma JF. Exploring the power of plants to overcome environmental stresses. Springer; 2015.

2. Ray DK, Mueller ND, West PC, Foley JA. Yield trends are insufficient to double global crop production by 2050. PloS one. 2013;8(6):e66428. doi: 10.1371/journal.pone.0066428 23840465

3. Thornton PK. Impacts of climate change on the agricultural and aquatic systems and natural resources within the CGIAR’s mandate. 2012.

4. Dixit S, Singh A, Sandhu N, Bhandari A, Vikram P, Kumar A. Combining drought and submergence tolerance in rice: marker-assisted breeding and QTL combination effects. Molecular breeding. 2017;37(12):143. doi: 10.1007/s11032-017-0737-2 29151804

5. Shamsudin NAA, Swamy BM, Ratnam W, Cruz MTS, Raman A, Kumar A. Marker assisted pyramiding of drought yield QTLs into a popular Malaysian rice cultivar, MR219. BMC genetics. 2016;17(1):30.

6. Todaka D, Nakashima K, Shinozaki K, Yamaguchi-Shinozaki K. Toward understanding transcriptional regulatory networks in abiotic stress responses and tolerance in rice. Rice. 2012;5(1):6. doi: 10.1186/1939-8433-5-6 24764506

7. Pearson GA, Ayers A, Eberhard D. Relative salt tolerance of rice during germination and early seedling development. Soil Science. 1966;102(3):151–6.

8. Al-Tamimi N, Brien C, Oakey H, Berger B, Saade S, Ho YS, et al. Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping. Nature Communications. 2016;7:13342. doi: 10.1038/ncomms13342 27853175

9. Mishra S, Senadhira D, Manigbas N. Genetics of submergence tolerance in rice (Oryza sativa L.). Field crops research. 1996;46(1–3):177–81.

10. Kumar R, Venuprasad R, Atlin G. Genetic analysis of rainfed lowland rice drought tolerance under naturally-occurring stress in eastern India: heritability and QTL effects. Field Crops Research. 2007;103(1):42–52.

11. Venuprasad R, Dalid C, Del Valle M, Zhao D, Espiritu M, Cruz MS, et al. Identification and characterization of large-effect quantitative trait loci for grain yield under lowland drought stress in rice using bulk-segregant analysis. Theoretical and Applied Genetics. 2009;120(1):177–90. doi: 10.1007/s00122-009-1168-1 19841886

12. Vikram P, Swamy BM, Dixit S, Ahmed HU, Cruz MTS, Singh AK, et al. qDTY 1.1, a major QTL for rice grain yield under reproductive-stage drought stress with a consistent effect in multiple elite genetic backgrounds. BMC genetics. 2011;12(1):89.

13. Bernier J, Kumar A, Ramaiah V, Spaner D, Atlin G. A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Science. 2007;47(2):507–16.

14. Xu K, Mackill DJ. A major locus for submergence tolerance mapped on rice chromosome 9. Molecular Breeding. 1996;2(3):219–24.

15. Thomson MJ, de Ocampo M, Egdane J, Rahman MA, Sajise AG, Adorada DL, et al. Characterizing the Saltol quantitative trait locus for salinity tolerance in rice. Rice. 2010;3(2):148.

16. Septiningsih EM, Pamplona AM, Sanchez DL, Neeraja CN, Vergara GV, Heuer S, et al. Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Annals of Botany. 2008;103(2):151–60. doi: 10.1093/aob/mcn206 18974101

17. Rahman H, Dakshinamurthi V, Ramasamy S, Manickam S, Kaliyaperumal AK, Raha S, et al. Introgression of submergence tolerance into CO 43, a popular rice variety of India, through marker-assisted backcross breeding. Czech Journal of Genetics and Plant Breeding. 2018;54(3):101–8.

18. Dixit S, Yadaw RB, Mishra KK, Kumar A. Marker-assisted breeding to develop the drought-tolerant version of Sabitri, a popular variety from Nepal. Euphytica. 2017;213(8):184.

19. Thomson MJ, Ocampo D, Egdane J, Katimbang M, Singh R, Gregorio G, et al. QTL mapping and marker-assisted backcrossing for improved salinity tolerance in rice. BioAsia (www bioasia-2007 com), Supplement Papers. 2007:6–12.

20. Singh VK, Singh BD, Kumar A, Maurya S, Krishnan SG, Vinod KK, et al. Marker-Assisted Introgression of Saltol QTL Enhances Seedling Stage Salt Tolerance in the Rice Variety “Pusa Basmati 1”. International journal of genomics. 2018;2018.

21. Valarmathi M, Sasikala R, Rahman H, Jagadeeshselvam N, Kambale R, Raveendran M. Development of salinity tolerant version of a popular rice variety improved white ponni through marker assisted back cross breeding. Indian Journal of Plant Physiology. 2019. doi: 10.1007/s40502-019-0440-x

22. Subramanian M, Sivasubramanian V, Chelliah S. Improved white Ponni released in Tamil Nadu. International Rice Research Newsletter (Philippines). 1986.

23. Bonilla P, Dvorak J, Mackell D, Deal K, Gregorio G. RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philippine Agricultural Scientist (Philippines). 2002.

24. Neeraja CN, Maghirang-Rodriguez R, Pamplona A, Heuer S, Collard BC, Septiningsih EM, et al. A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theoretical and Applied Genetics. 2007;115(6):767–76. doi: 10.1007/s00122-007-0607-0 17657470

25. Ausubel F, Brent R, Kingston R, Moore D, Seidman J, Smith J, et al. Current protocols in molecular biology, vol. 1 John Wiley & Sons. Inc, Brooklyn, New York. 2003;3(1):1994–2005.

26. Abdul-Baki AA, Anderson JD. Vigor determination in soybean seed by multiple criteria 1. Crop science. 1973;13(6):630–3.

27. Chaudhary R, Ahn S. International network for genetic evaluation of rice (INGER) and its modus operandi for multi-environment testing. 1996.

28. Munns R, Wallace PA, Teakle NL, Colmer TD. Measuring soluble ion concentrations (Na+, K+, Cl−) in salt-treated plants. Plant stress tolerance: Springer; 2010. p. 371–82.

29. IRRI. Standard Evaluation System for Rice. Los Banos, Philippines: IRRI; 2002. 29 p.

30. Unnevehr L, Juliano B, Perez C. Consumer demand for rice grain quality in Southeast Asia. Rice Grain Quality Mark International Rice Research Institute. 1985;933:15–23.

31. Little RR. Differential effect of dilute alkali on 25 varieties of milled white rice. Cereal Chem. 1958;35:111–26.

32. Kongseree N, Juliano BO. Physicochemical properties of rice grain and starch from lines differing in amylose content and gelatinization temperature. Journal of Agricultural and Food Chemistry. 1972;20(3):714–8.

33. Cagampang GB, Perez CM, Juliano BO. A gel consistency test for eating quality of rice. Journal of the Science of Food and Agriculture. 1973;24(12):1589–94. doi: 10.1002/jsfa.2740241214 4771843

34. Azeez M, Shafi M. Quality in rice. Department of Agricultural East Pakistan Technology Bulletin. 1966;(13):50.

35. Sidhu JS, Gill MS, Bains GS. Milling of paddy in relation to yield and quality of rice of different Indian varieties. Journal of Agricultural and Food Chemistry. 1975;23(6):1183–5.

36. Juliano B. A simplified assay for milled rice amylase. Cereal Sci Today. 1971;16:360.

37. Yamori W. Improving photosynthesis to increase food and fuel production by biotechnological strategies in crops. Journal of Plant Biochemistry & Physiology. 2013.

38. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, et al. Solutions for a cultivated planet. Nature. 2011;478(7369):337. doi: 10.1038/nature10452 21993620

39. Dilley M, Chen RS, Deichmann U, Lerner-Lam AL, Arnold M. Natural disaster hotspots: a global risk analysis: The World Bank; 2005.

40. Shrivastava P, Kumar R. Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi journal of biological sciences. 2015;22(2):123–31. doi: 10.1016/j.sjbs.2014.12.001 25737642

41. Li Z-K, Xu J-L. Breeding for drought and salt tolerant rice (Oryza sativa L.): progress and perspectives. Advances in molecular breeding toward drought and salt tolerant crops: Springer; 2007. p. 531–64.

42. Hoang T, Tran T, Nguyen T, Williams B, Wurm P, Bellairs S, et al. Improvement of salinity stress tolerance in rice: challenges and opportunities. Agronomy. 2016;6(4):54.

43. Septiningsih EM, Hidayatun N, Sanchez DL, Nugraha Y, Carandang J, Pamplona AM, et al. Accelerating the development of new submergence tolerant rice varieties: the case of Ciherang-Sub1 and PSB Rc18-Sub1. Euphytica. 2015;202(2):259–68.

44. Toledo AMU, Ignacio JCI, Casal C, Gonzaga ZJ, Mendioro MS, Septiningsih EM. Development of improved Ciherang-Sub1 having tolerance to anaerobic germination conditions. Plant Breeding and Biotechnology. 2015;3(2):77–87.

45. Dixit S, Huang BE, Cruz MTS, Maturan PT, Ontoy JCE, Kumar A. QTLs for tolerance of drought and breeding for tolerance of abiotic and biotic stress: an integrated approach. PLoS One. 2014;9(10):e109574. doi: 10.1371/journal.pone.0109574 25314587

46. Gregorio G, Senadhira D, Mendoza R, Manigbas N, Roxas J, Guerta C. Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crops Research. 2002;76(2–3):91–101.

47. Visscher PM, Haley CS, Thompson R. Marker-assisted introgression in backcross breeding programs. Genetics. 1996;144(4):1923–32. 8978075

48. Servin B, Hospital F. Optimal positioning of markers to control genetic background in marker-assisted backcrossing. Journal of Heredity. 2002;93(3):214–7. doi: 10.1093/jhered/93.3.214 12195040

49. Vikram P, Swamy BM, Dixit S, Singh R, Singh BP, Miro B, et al. Drought susceptibility of modern rice varieties: an effect of linkage of drought tolerance with undesirable traits. Scientific reports. 2015;5:14799. doi: 10.1038/srep14799 26458744

50. Muthukumar M. SR, Robin S. And Raveendran M. Developing improved versions of a popular rice variety (Improved White Ponni) through marker assisted backcross breeding. Green Farming 2017;Vol. 8(3).

51. Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, Close TJ. Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant molecular biology. 2007;63(5):609–23. doi: 10.1007/s11103-006-9112-0 17160619

52. Platten JD, Thomson MJ, Ismail AM. Genomics Applications to Salinity Tolerance Breeding in Rice. Translational Genomics for Crop Breeding: Improvement for Abiotic Stress, Quality and Yield Improvement. 2013:31.

53. Ingram J, Bartels D. The molecular basis of dehydration tolerance in plants. Annual review of plant biology. 1996;47(1):377–403.

54. Cabuslay GS, Ito O, Alejar AA. Physiological evaluation of responses of rice (Oryza sativa L.) to water deficit. Plant Science. 2002;163(4):815–27.

55. Hampson CR, Simpson G. Effects of temperature, salt, and osmotic potential on early growth of wheat (Triticum aestivum). I. Germination. Canadian Journal of Botany. 1990;68(3):524–8.

56. Priyadarshini S. Marker assisted introgression of mega effect qtls controlling drought tolerance from upland variety apo into popular rice (oryza sativa l.) varieties of tamil nadu: TAMIL NADU AGRICULTURAL UNIVERSITY COIMBATORE; 2013.

57. Vikram P, Swamy BM, Dixit S, Trinidad J, Cruz MTS, Maturan PC, et al. Linkages and interactions analysis of major effect drought grain yield QTLs in rice. PLoS One. 2016;11(3):e0151532. doi: 10.1371/journal.pone.0151532 27018583

58. Juliano BO, Villareal C. Grain quality evaluation of world rices: Int. Rice Res. Inst.; 1993.

59. Huang B, Duncan R, Carrow R. Drought-resistance mechanisms of seven warm-season turfgrasses under surface soil drying: II. Root aspects. Crop Science. 1997;37(6):1863–9.

60. Hittalmani S, Parco A, Mew T, Zeigler R, Huang N. Fine mapping and DNA marker-assisted pyramiding of the three major genes for blast resistance in rice. Theoretical and Applied Genetics. 2000;100(7):1121–8.

61. Linh LH, Linh TH, Xuan TD, Ham LH, Ismail AM, Khanh TD. Molecular breeding to improve salt tolerance of rice (Oryza sativa L.) in the Red River Delta of Vietnam. International journal of plant genomics. 2012;2012.

62. Swamy BM, Kumar A. Genomics-based precision breeding approaches to improve drought tolerance in rice. Biotechnology advances. 2013;31(8):1308–18. doi: 10.1016/j.biotechadv.2013.05.004 23702083

63. Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M, Hara N, et al. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nature genetics. 2013;45(9):1097. doi: 10.1038/ng.2725 23913002

64. Dixit S, Grondin A, Lee C-R, Henry A, Olds T-M, Kumar A. Understanding rice adaptation to varying agro-ecosystems: trait interactions and quantitative trait loci. BMC genetics. 2015;16(1):86.

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