Marker Assisted Breeding

  • Michael J. Thomson
  • Abdelbagi M. Ismail
  • Susan R. McCouch
  • David J. Mackill


Recent advances in understanding molecular and physiological mechanisms of abiotic stress responses, along with breakthroughs in molecular marker technologies, have enabled the dissection of the complex traits underlying stress tolerance in crop plants. Quantitative trait loci (QTLs) controlling different abiotic stress traits form the basis for a precise marker-assisted backcrossing (MABC) strategy to rapidly transfer tolerance loci into high-yielding, but stress-sensitive varieties. Case studies are presented to demonstrate the progress and potential for MABC programs to develop rice varieties with increased tolerance to flooding, salinity, phosphorus deficiency and drought, amongst others. Future opportunities exist for employing association genetics for more efficient allele mining for abiotic stress tolerance from germplasm collections, as well as leveraging the power of bioinformatics and genomics data for more efficient trait dissection and use in breeding. Plant breeders now have a wealth of information and tools available to tackle these serious constraints posed by abiotic stresses, with the promise of delivering stable, high yielding varieties, able to thrive in the increasingly degrading soils and the ominously changing environment.


abiotic stresses association mapping Oryza sativa L. QTLs rice 



Arabidopsis Genome Initiative


bacterial artificial chromosome


chromosomal segment substitution lines


European Plant Science Organization


ethylene responsive factors


functional nucleotide polymorphism


transporters high-affinity K+ transporter


International Rice Genome Sequencing Project


International Rice Information System


linkage disequlibrium


scores logarithm of the odds ratio


marker-assisted backcrossing


marker-assisted selection


near-isogenic lines


Oryza sativa cation transporter HKT8


phosphorus uptake 1


quantitative trait loci


restriction fragment length polymorphism


recombinant inbred lines


reactive oxygen species


salt overly sensitive


simple sequence repeat


single nucleotide polymorphism


shoot potassium content 1


submergence 1


  1. Agrama HA, Eizenga GC, Yan W (2007) Association mapping of yield and its components in rice cultivars. Mol Breed 19:341-356CrossRefGoogle Scholar
  2. Andersen JR, Lubberstedt T (2003) Functional markers in plants. Trends Plant Sci 8:554-560PubMedCrossRefGoogle Scholar
  3. Angaji SA, Septiningsih E, Mackill DJ, Ismail AM (2009) QTLs associated with tolerance of flooding during germination in rice (Oryza sativa L.). Euphytica, DOI 10.1007/s10681-009-0014-5Google Scholar
  4. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815CrossRefGoogle Scholar
  5. Ashikari M, Matsuoka M (2006) Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends Plant Sci 11:344-350PubMedCrossRefGoogle Scholar
  6. Babu RC, Nguyen BD, Chamarerk V, Shanmugasundaram P, Chezhian P, Jeyaprakash P, Ganesh SK, Palchamy A, Sadasivam S, Sarkarung S, Wade LJ, Nguyen HT (2003) Genetic analysis of drought resistance in rice by molecular markers: association between secondary traits and field performance. Crop Sci 43:1457-1469CrossRefGoogle Scholar
  7. Bernier J, Kumar A, Ramaiah V, Spaner D, Atlin G (2007) A large-effect QTL for grain yield under reproductive-stage drought stress in upland rice. Crop Sci 47:507-518CrossRefGoogle Scholar
  8. Bonilla P, Dvorak J, Mackill DJ, Deal K, Gregorio GB (2002) RFLP and SSLP mapping of salinity tolerance genes in chromosome 1 of rice (Oryza sativa L.) using recombinant inbred lines. Philipp Agric Sci 85:68-76Google Scholar
  9. Bradbury LMT, Henry RJ, Jin Q, Reinke RF, Waters DLE (2005) A perfect marker for fragrance genotyping in rice. Mol Breed 16:279-283Google Scholar
  10. Bruskiewich RM, Cosico AB, Eusebio W, Portugal AM, Ramos LM, Reyes MT, Sallan MA, Ulat VJ, Wang X, Mcnally KL, Sackville Hamilton R, McLaren CG (2003) Linking genotype to phenotype: The International Rice Information System (IRIS). Bioinformatics. 19(Suppl 1):63-65Google Scholar
  11. Clark JI, Brooksbank C, Lomax J (2005) It’s all GO for plant scientists. Plant Physiol 138:1268-1279PubMedCrossRefGoogle Scholar
  12. Buckler ES IV, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107-111PubMedCrossRefGoogle Scholar
  13. Collard BCY, Mackill DJ (2008) Marker assisted selection: an approach for precision plant breeding in the twenty-first century. Phil Trans R Soc Lond B Biol Sci 363:557-572CrossRefGoogle Scholar
  14. 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 142:169-196CrossRefGoogle Scholar
  15. Collard BCY, Vera Cruz CM, McNally KL, Virk PS, Mackill DJ (2008) Rice molecular breeding laboratories in the genomics era: current status and future considerations. Int J Plant Genomics p 25, doi: 10: 1155/2008/524847Google Scholar
  16. Ella E, Kawano N, Yamauchi Y, Tanaka K, Ismail AM (2003) Blocking ethylene perception enhances flooding tolerance in rice seedlings. Funct Plant Biol 30:813-819CrossRefGoogle Scholar
  17. European-Plant-Science-Organization (EPSO) (2005) European plant science: a field of opportunities. J Exp Bot 56:1699-1709CrossRefGoogle Scholar
  18. Flint-Garcia SA, Thornsberry JM, Buckler IV ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357-374Google Scholar
  19. Garris A, McCouch S, Kresovich S (2003) Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759-769PubMedGoogle Scholar
  20. Golldack D, Su H, Quigley F, Kamasani UR, Muñoz-Garay C, Bladeras E, Popova OV, Bennett J, Bohnert HJ, Pantoja O (2002) Characterization of a HKT-type transporter in rice as a general alkali cation transporter. Plant J 31:529-542PubMedCrossRefGoogle Scholar
  21. 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 Crops Res 76:91-101CrossRefGoogle Scholar
  22. Gupta PK, Rustgi S, Kulwal PL (2005) Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol 57:461-485PubMedCrossRefGoogle Scholar
  23. Hartl DL, Clark AG (1997) Principles of population genetics. Sinauer Associates, Sunderland, MAGoogle Scholar
  24. Heuer S, Lu X, Chin J-H, Tanaka JP, Kanamori H, Matsumoto T, De Leon T, Ulat VJ, Ismail AM, Wissuwa M (2009) Comparative sequence analysis of the major quantitative trait locus phosphorus uptake 1 (Pup1) reveal a complex genetic structure. Plant Biotech J 7:456-471CrossRefGoogle Scholar
  25. Horie T, Schroeder JI (2004) Sodium transporters in plants: diverse genes and physiological functions. Plant Physiol 136:2457-2462PubMedCrossRefGoogle Scholar
  26. Horie T, Yoshida K, Nakayama H, Ymada K, Oiki S, Shinmyo A (2001) Two types of HKT transporters with different properties of Na+ and K+ transport in Oryza sativa. Plant J 27:115-128CrossRefGoogle Scholar
  27. Ilic K, Kellogg EA, Jaiswal P, Zapata F, Stevens PF, Vincent LP, Avraham S, Reiser L, Pujar A, Sachs MM, Whitman NT, McCouch SR, Schaeffer ML, Ware DH, Stein LD, Rhee SY (2007) The plant structure ontology, a unified vocabulary of anatomy and morphology of a flowering plant. Plant Physiol 143:587-599PubMedCrossRefGoogle Scholar
  28. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793-800CrossRefGoogle Scholar
  29. Ismail AM, Heuer S, Thomson MJ, Wissuwa M (2007) Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Mol Biol 65:547-570PubMedCrossRefGoogle Scholar
  30. Jackson MB, Ram PC (2003) Physiological and molecular basis of susceptibility and tolerance of rice plants to complete submergence. Ann Bot 91:227-241PubMedCrossRefGoogle Scholar
  31. Jaiswal P, Avaraham S, Ilic K, Kellogg E, McCouch S, Pujar A, Reiser L, Rhee S, Sachs M, Schaeffer M, Stein L, Stevens P, Leszek V, Ware D, Zapata F (2006a) Plant ontology (PO): a controlled vocabulary of plant structures and growth stages. Comp Func Gen 6:388-397CrossRefGoogle Scholar
  32. Jaiswal P, Ni J, Yap I, Ware D, Spooner W, Youens-Clark K, Ren L, Liang C, Zhao W, Ratnapu K, Faga B, Canaran P, Fogleman M, Hebbard C, Avraham S, Schmidt S, Casstevens T, Buckler E, Stein L, McCouch S (2006b) Gramene: a bird’s eye view. Nucleic Acids Res 34:D717-D723; doi: 10.1093/nar/gkj154Google Scholar
  33. Jander G, Norris SR, Rounsley SD, Bush DF, Levin IM, Last RL (2002) Arabidopsis map-based cloning in the post-genome era. Plant Physiol 129:440-450PubMedCrossRefGoogle Scholar
  34. Kruglyak L (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nat Genet 22:139-144PubMedCrossRefGoogle Scholar
  35. Kumar G, Purty RS, Sharma MP, Singla-Pareek SL, Pareek A (2009) Physiological responses among Brassica species under salinity stress show strong correlation with transcript abundance for SOS pathway-related genes. J Plant Physiol 166:507-520PubMedCrossRefGoogle Scholar
  36. Lafitte HR, Ismail AM, Bennett J (2006) Abiotic stress tolerance in tropical rice: progress and future prospects. Oryza 43:171-186Google Scholar
  37. 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 108:253-260PubMedCrossRefGoogle Scholar
  38. Lukowitz W, Gillmor CS, Scheible WR (2000) Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you? Plant Physiol 123:795-805PubMedCrossRefGoogle Scholar
  39. Martinez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001-1012PubMedCrossRefGoogle Scholar
  40. Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch SR, Purugganan MD (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.) Genetics 177:2223-2232Google Scholar
  41. McCouch SR, Teytelman L, Xu Y, Lobos KB, Clare K, Walton M, Fu B, Maghirang R, Li Z, Zing Y, Zhang Q, Kono I, Yano M, Fjellstrom R, DeClerck G, Schneider D, Cartinhour S, Ware D, Stein L (2002) Development and mapping of 2240 new SSR markers for rice (Oryza sativa L.). DNA Res 9:199-207PubMedCrossRefGoogle Scholar
  42. Mackill DJ (2006) Breeding for resistance to abiotic stresses in rice: the value of quantitative trait loci. In: Lamkey KR and Lee M (eds) Plant breeding: the Arnel R. Hallauer International Symposium. Blackwell, Ames, IA, pp 201-212Google Scholar
  43. Mackill DJ, McNally KL (2005) Molecular markers in rice: a model crop species. In: Lörz H, Wenzel G (eds) Molecular marker systems in plant breeding and crop improvement. Springer Verlag, Heidelberg, Germany, pp 39-54Google Scholar
  44. Moradi F, Ismail AM (2007) Responses of photosynthesis, chlorophyll fluorescence and ROS scavenging system to salt stress during seedling and reproductive stages in rice. Ann Bot 99:1161-1173PubMedCrossRefGoogle Scholar
  45. Moradi F, Ismail AM, Gregorio GB, Egdane JA (2003) Salinity tolerance of rice during reproductive development and association with tolerance at the seedling stage. Ind J Plant Physiol 8:105-116Google Scholar
  46. Morrell PL, Toleno DM, Lundy KE, Clegg MT (2005) Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilization. Proc Natl Acad Sci USA 102:2442-2447PubMedCrossRefGoogle Scholar
  47. Nandi S, Subudhi PK, Senadhira D, Manigbas NL, Sen-Mandi S, Huang N (1997) Mapping QTLs for submergence tolerance in rice by AFLP analysis and selective genotyping. Mol Gen Genet 255:1-8Google Scholar
  48. Neeraja CN, Maghirang-Rodriguez R, Pamplona A, Heuer S, Collard BCY, Septiningsih EM, Vergara G, Sanchez D, Xu K, Ismail AM, Mackill DJ (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115:767-776PubMedCrossRefGoogle Scholar
  49. Ni JJ, Wu P, Senadhira D, Huang N (1998) Mapping QTLs for phosphorus deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:1361-1369CrossRefGoogle Scholar
  50. Nordborg M, Tavare S (2002) Linkage disequilibrium: what history has to tell us? Trend Genet 18:83-90CrossRefGoogle Scholar
  51. Olsen KM, Caicedo AL, Polato N, McClung A, McCouch SR (2006) Selection under domestication: evidence for a sweep in the rice waxy genomic region. Genetics 173:975-983PubMedCrossRefGoogle Scholar
  52. Paran I, Zamir D (2003) Quantitative traits in plants: beyond the QTL. Trends Genet 19:303-306PubMedCrossRefGoogle Scholar
  53. Price AH (2006) Believe it on not, QTLs are accurate!. Trends Plant Sci 11:213-216PubMedCrossRefGoogle Scholar
  54. Pujar A, Jaiswal P, Kellogg E, Ilic K, Vincent L, Avraham S, Stevens P, Zapata F, Reiser L, Rhee S, Sachs M, Schaeffer M, Stein L, Ware D, McCouch S (2006) Whole plant growth stage ontology for angiosperms and its application in plant biology. Plant Physiol 142:414-428PubMedCrossRefGoogle Scholar
  55. Rakshit S, Rakshit A, Matsumura H, Takahashi Y, Hasegawa Y, Ito A, Ishii T, Miyashita NT, Terauchi R (2007) Large scale DNA polymorphism study of Oryza sativa and O. rufipogon reveals the origin and divergence of Asian rice. Theor Appl Genet 114:731-743PubMedCrossRefGoogle Scholar
  56. Remington DL, Thornsberry JM, Matsouka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES 4th (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479-11484PubMedCrossRefGoogle Scholar
  57. 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 37:1141-1146PubMedCrossRefGoogle Scholar
  58. Sahi C, Singh A, Kumar K, Blumwald E, Grover A (2006) Salt stress response in rice: genetics, molecular biology and comparative genomics. Funct Integr Genomics 6:263-284PubMedCrossRefGoogle Scholar
  59. Salvi S, Tuberosa R (2005) To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10:297-304PubMedCrossRefGoogle Scholar
  60. Sarkar R, Reddy JN, Sharma SG, Ismail AM (2006) Physiological basis of submergence tolerance in rice and implications for crop improvement. Curr Sci 91:899-906Google Scholar
  61. Sax K (1923) The association of size differences with seed-coat pattern and pigmentation in Phaseolus vulgaris. Genetics 8:552-560PubMedGoogle Scholar
  62. Septiningsih EM, Pamplona AM, Sanchez DL, Maghirang-Rodriguez R, Neeraja CN, Vergara GV, Heuer S, Ismail AM, Mackill DJ (2009) Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. Ann Bot 103:151-160PubMedCrossRefGoogle Scholar
  63. Shimizu T, Satoh K, Kikuchi S, Omura T (2007) The repression of cell wall- and plastid-related genes and the induction of defense-related genes in rice plants infected with rice dwarf virus. Mol Plant Microbe Interact 20:247-254PubMedCrossRefGoogle Scholar
  64. Singh S, Mackill DJ, Ismail AM (2009) Responses of SUB1 rice introgression lines to submergence in the field: Yield and grain quality. Field Crops Res 113:12-23CrossRefGoogle Scholar
  65. Sweeney MT, Thomson MJ, Pfeil BE, McCouch SR (2006) Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. Plant Cell 18:283-294PubMedCrossRefGoogle Scholar
  66. Sweeney MT, Thomson MJ, Cho YG, Park YJ, Williamson SH, Bustamante CD, McCouch SR (2007) Global dissemination of a single mutation conferring white pericarp in rice. PLoS Genet 3:e133CrossRefGoogle Scholar
  67. Szalma SJ, Buckler ES, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110:1324-1333PubMedCrossRefGoogle Scholar
  68. Tanksely SD (1993) Mapping polygenes. Annu Rev Genet 27:205-233CrossRefGoogle Scholar
  69. Temnykh S, DeClerck G, Lukashova A, Lipovich L, Cartinhour S, McCouch SR (2001) Computational and experimental analysis of micro-satellites in rice (Oryza sativa L.): Frequency, length variation, transposon associations and genetic marker potential. Genome Res 11:1441-1452PubMedCrossRefGoogle Scholar
  70. Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98:9161-9166PubMedCrossRefGoogle Scholar
  71. Thoday JM (1961) Location of polygenes. Nature 191:368-370CrossRefGoogle Scholar
  72. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, IV BES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286-289PubMedCrossRefGoogle Scholar
  73. Toojinda T, Siangliw M, Tragroonrung S, Vanavichit A (2003) Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann Bot 91:43-253CrossRefGoogle Scholar
  74. Weir B (1996) Genetic Data Analysis II. Sinauer Associates, Sunderland, MA, pp 376Google Scholar
  75. Wilson LM, Whitt SR, Ibanez-Carranza AM, Goodman MM, Rocheford TR, Buckler ES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719-2733PubMedCrossRefGoogle Scholar
  76. Wissuwa M, Ae N (2001a) Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breed 120:43-48CrossRefGoogle Scholar
  77. Wissuwa M, Ae N (2001b) Further characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency. Plant Soil 237:275-286CrossRefGoogle Scholar
  78. Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777-783CrossRefGoogle Scholar
  79. Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor Appl Genet 105:890-897PubMedCrossRefGoogle Scholar
  80. Xu K, Mackill DJ (1996) A major locus for submergence tolerance mapped on rice chromosome 9. Mol Breed 2:219-224CrossRefGoogle Scholar
  81. Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald RC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705-708PubMedCrossRefGoogle Scholar
  82. Yeo AR, Flowers TJ (1986) Salinity resistance in rice (Oryza sativa L.) and a pyramiding approach to breeding varieties for saline soils. Aust J Plant Physiol 13:161-173CrossRefGoogle Scholar
  83. Zhang N, Xu Y, Akash M, McCouch S, Oard J (2005) Identification of candidate markers associated with agronomic traits in rice using discriminant analysis. Theor Appl Genet 110:721-729PubMedCrossRefGoogle Scholar
  84. Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441-445PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Michael J. Thomson
    • 1
  • Abdelbagi M. Ismail
    • 1
  • Susan R. McCouch
    • 1
    • 2
  • David J. Mackill
    • 1
  1. 1.International Rice Research Institute (IRRI)Metro ManilaPhilippines
  2. 2.Department of Plant Breeding and GeneticsCornell UniversityIthacaUSA

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