Theoretical and Applied Genetics

, Volume 131, Issue 1, pp 107–126 | Cite as

Genome-wide association study of stem rust resistance in a world collection of cultivated barley

  • Austin J. Case
  • Sridhar Bhavani
  • Godwin Macharia
  • Brian J. SteffensonEmail author
Original Article


Key message

QTL conferring a 14–40% reduction in adult plant stem rust severity to multiple races of Pgt were found on chromosome 5H and will be useful in barley breeding.


Stem rust, caused by Puccinia graminis f. sp. tritici (Pgt) is an important disease of barley. The resistance gene Rpg1 has protected the crop against stem rust losses for over 70 years in North America, but is not effective against the African Pgt race TTKSK (and its variants) nor the domestic race QCCJB. To identify resistance to these Rpg1-virulent races, the Barley iCore Collection, held by the United States Department of Agriculture-Agricultural Research Service National Small Grains Collection was evaluated for adult plant resistance (APR) and seedling resistance to race TTKSK and APR to race QCCJB and the Pgt TTKSK composite of races TTKSK, TTKST, TTKTK, and TTKTT. Using a genome-wide association study approach based on 6224 single nucleotide polymorphic markers, seven significant loci for stem rust resistance were identified on chromosomes 1H, 2H, 3H, and 5H. The most significant markers detected were 11_11355 and SCRI_RS_177017 at 71–75 cM on chromosome 5H, conferring APR to QCCJB and TTKSK composite. Significant markers were also detected for TTKSK seedling resistance on chromosome 5H. All markers detected on 5H were independent of the rpg4/Rpg5 complex at 152–168 cM. This study verified the importance of the 11_11355 locus in conferring APR to races QCCJB and TTKSK and suggests that it may be effective against other races in the Ug99 lineage.



This research was funded, in part, by the Lieberman-Okinow Endowment at the University of Minnesota, American Malting Barley Association, the Bill & Melinda Gates Foundation, the UK Department for International Development to Cornell University for the Borlaug Global Rust Initiative Durable Rust Resistance in Wheat Project, USDA-ARS Cooperative Agreement 58-5062-5-012 (Understanding Stem Rust Resistance in Barley and Germplasm); and Triticeae-CAP project (2011-68002-30029) from the United States Department of Agriculture National Institute of Food and Agriculture. AJC acknowledges financial support from the following University of Minnesota fellowships: Norman E. Borlaug Graduate Fellowship for International Agriculture supported by the Vaale-Henry Endowment, the Minnesota Discovery, Research, and Innovation (MnDRIVE) Fellowship, and the Doctoral Dissertation Fellowship. We thank T. Szinyei and M. Martin for excellent technical assistance and Dr. A. Sallam and Dr. M. Muñoz-Amatriaín for assistance in data analysis.

Author contribution statement

Austin Case and Brian Steffenson conducted the experiments in the USA and Kenya, performed the analyses, and wrote the manuscript. Sridhar Bhavani and Godwin Macharia coordinated and conducted the experiments in Kenya and revised the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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  1. Arora D, Gross T, Brueggeman R (2013) Allele characterization of genes required for rpg4-mediated wheat stem rust resistance identifies Rpg5 as the R gene. Phytopathology 103:1153–1161CrossRefPubMedGoogle Scholar
  2. Balding DJ (2006) A tutorial on statistical methods for population association studies. Nat Rev Genet 7:781–791CrossRefPubMedGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc Series B 57:289–300Google Scholar
  5. 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 23:2633–2635CrossRefPubMedGoogle Scholar
  6. Browning BL, Browning SR (2016) Genotype imputation with millions of reference samples. Am J Hum Genet 98:116–126CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brueggeman R, Druka A, Nirmala J, Cavileer T, Drader T, Rostoks N, Mirlohi A, Bennypaul H, Gill U, Kudrna D, Whitelaw C, Kilian A, Han F, Sun Y, Gill K, Steffenson B, Kleinhofs A (2008) The stem rust resistance gene Rpg5 encodes a protein with nucleotide-binding-site, leucine-rich, and protein kinase domains. Proc Natl Acad Sci USA 105:14970–14975CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brueggeman R, Steffenson BJ, Kleinhofs A (2009) The rpg4/Rpg5 stem rust resistance locus in barley: resistance genes and cytoskeleton dynamics. Cell Cycle 8:977–981CrossRefPubMedGoogle Scholar
  9. Cantalapiedra CP, Contreras-Moreira B, Silvar C, Perovic D, Ordon F, Gracia MP, Igartua E, Casas AM (2016) A cluster of nucleotide-binding site-leucine-rich Repeat genes resides in a barley powdery mildew resistance quantitative trait loci on 7HL. Plant Genome 9:2CrossRefGoogle Scholar
  10. Case AJ (2017) Genetics, sources, and mapping of stem rust resistance in barley. Ph.D. dissertation, Department of Plant Pathology. University of Minneosta, Proquest Dissertation PublishingGoogle Scholar
  11. 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
  12. Dill-Macky R, Rees RG (1992) Sources of resistance to stem rust in barley. Plant Dis 76:212CrossRefGoogle Scholar
  13. Dill-Macky R, Rees R, Platz G (1990) Stem rust epidemics and their effects on grain yield and quality in Australian barley cultivars. Crop Pasture Sci 41:1057–1063CrossRefGoogle Scholar
  14. Falconer DS (1960) Introduction to quantitative genetics. The Ronald Press Company, New YorkGoogle Scholar
  15. Fetch T, Johnston PA, Pickering R (2009) Chromosomal location and inheritance of stem rust resistance transferred from Hordeum bulbosum into cultivated barley (H. vulgare). Phytopathology 99(4):339–343CrossRefPubMedGoogle Scholar
  16. Fox SL, Harder DE (1995) Resistance to stem rust in barley and inheritance of resistance to race QCC. Can J Plant Sci 75:781–788CrossRefGoogle Scholar
  17. Franckowiak J (1991) BGS 512: resistance to Puccinia graminis Pers. f. sp. tritici Eriks. and E. Henn. (black stem rust), Rpg2b. Barley Genet Newsl 20:116Google Scholar
  18. Franckowiak J, Steffenson B (1997) BGS 512: Resistance to Puccinia graminis Pers. f. sp. tritici Eriks. and E. Henn. (black stem rust), Rpg2b. Barley Genet Newsl 26:439Google Scholar
  19. Jedel P (1991) A gene for resistance to Puccinia graminis f. sp. tritici in PI 382313. Barley Genet Newsl 20:43–44Google Scholar
  20. Jedel PE, Metcalfe DR, Martens JW (1989) Assessment of barley accessions PI-382313, PI-382474, PI-382915, and PI-382976 for stem rust resistance. Crop Sci 29:1473–1477CrossRefGoogle Scholar
  21. Jin Y, Steffenson BJ, Fetch TG (1994a) Sources of resistance to pathotype QCC of Puccinia graminis f. sp. tritici in barley. Crop Sci 34:285–288CrossRefGoogle Scholar
  22. Jin Y, Steffenson BJ, Miller JD (1994b) Inheritance of resistance to pathotypes QCC and MCC of Puccinia graminis f. sp. tritici in barley line Q21861 and temperature effects on the expression of resistance. Phytopathology 84:452–455CrossRefGoogle Scholar
  23. Jin Y, Szabo LJ, Pretorius ZA, Singh RP, Ward R, Fetch T (2008) Detection of virulence to resistance gene Sr24 within race TTKS of Puccinia graminis f. sp. tritici. Plant Dis 92:923–926CrossRefGoogle Scholar
  24. Leng YQ, Wang R, Ali S, Zhao MX, Zhong SB (2016) Sources and genetics of spot blotch resistance to a new pathotype of Cochliobolus sativus in the USDA National Small Grains Collection. Plant Dis 100:1988–1993CrossRefGoogle Scholar
  25. Mamo B (2013) Genetic characterization of multiple disease resistance and agronomical and nutritional traits in Hordeum. Ph.D. dissertation, Department of Plant Pathology. University of Minnesota, UMI Dissertations PublishingGoogle Scholar
  26. Mamo BE, Smith KP, Brueggeman RS, Steffenson BJ (2015) Genetic characterization of resistance to wheat stem rust race TTKSK in landrace and wild barley accessions identifies the rpg4/Rpg5 locus. Phytopathology 105:99–109CrossRefPubMedGoogle Scholar
  27. Mascher M, Muehlbauer GJ, Rokhsar DS, Chapman J, Schmutz J, Barry K, Munoz-Amatriain M, Close TJ, Wise RP, Schulman AH, Himmelbach A, Mayer KF, Scholz U, Poland JA, Stein N, Waugh R (2013) Anchoring and ordering NGS contig assemblies by population sequencing (POPSEQ). Plant J 76:718–727CrossRefPubMedPubMedCentralGoogle Scholar
  28. Mascher M, Gundlach H, Himmelbach A, Beier S, Twardziok SO, Wicker T, Radchuk V, Dockter C, Hedley PE, Russell J, Bayer M, Ramsay L, Liu H, Haberer G, Zhang X-Q, Zhang Q, Barrero RA, Li L, Taudien S, Groth M, Felder M, Hastie A, Šimková H, Staňková H, Vrána J, Chan S, Muñoz-Amatriaín M, Ounit R, Wanamaker S, Bolser D, Colmsee C, Schmutzer T, Aliyeva-Schnorr L, Grasso S, Tanskanen J, Chailyan A, Sampath D, Heavens D, Clissold L, Cao S, Chapman B, Dai F, Han Y, Li H, Li X, Lin C, McCooke JK, Tan C, Wang P, Wang S, Yin S, Zhou G, Poland JA, Bellgard MI, Borisjuk L, Houben A, Doležel J, Ayling S, Lonardi S, Kersey P, Langridge P, Muehlbauer GJ, Clark MD, Caccamo M, Schulman AH, Mayer KFX, Platzer M, Close TJ, Scholz U, Hansson M, Zhang G, Braumann I, Spannagl M, Li C, Waugh R, Stein N (2017) A chromosome conformation capture ordered sequence of the barley genome. Nature 544:427–433CrossRefPubMedGoogle Scholar
  29. McVey DV, Long DL, Roberts J (2002) Races of Puccinia graminis in the United States During 1997 and 1998. Plant Dis 86:568–572CrossRefGoogle Scholar
  30. Miller JD, Lambert J (1955) Variability and inheritance of reaction of barley to race 15B of stem rust. Agron J 47:373–377CrossRefGoogle Scholar
  31. Mirlohi A, Brueggeman R, Drader T, Nirmala J, Steffenson BJ, Kleinhofs A (2008) Allele sequencing of the barley stem rust resistance gene Rpg1 identifies regions relevant to disease resistance. Phytopathology 98:910–918CrossRefPubMedGoogle Scholar
  32. Moscou MJ, Lauter N, Steffenson B, Wise RP (2011) Quantitative and qualitative stem rust resistance factors in barley are associated with transcriptional suppression of defense regulons. PLoS Genet 7:e1002208CrossRefPubMedPubMedCentralGoogle Scholar
  33. Muir C, Nilan R (1973) Registration of ‘Steptoe’ barley. Crop Sci 13:770CrossRefGoogle Scholar
  34. Muñoz-Amatriaín M, Cuesta-Marcos A, Endelman JB, Comadran J, Bonman JM, Bockelman HE, Chao S, Russell J, Waugh R, Hayes PM, Muehlbauer GJ (2014) The USDA barley core collection: genetic diversity, population structure, and potential for genome-wide association studies. PLoS ONE 9:e94688CrossRefPubMedPubMedCentralGoogle Scholar
  35. Mwando EK, Tabu IM, Otaye DO, Njau PN (2012) Effect of Ug99 race of stem rust (Puccinia graminis f. sp. tritici) on growth and yield of barley (Hordeum vulgare L.) in Kenya. J Agr Sci 4:161–168Google Scholar
  36. Myles S, Peiffer J, Brown PJ, Ersoz ES, Zhang Z, Costich DE, Buckler ES (2009) Association mapping: critical considerations shift from genotyping to experimental design. Plant Cell 21:2194–2202CrossRefPubMedPubMedCentralGoogle Scholar
  37. Newcomb M, Olivera PD, Rouse MN, Szabo LJ, Johnson J, Gale S, Luster DG, Wanyera R, Macharia G, Bhavani S, Hodson D, Patpour M, Hovmoller MS, Fetch TG Jr, Jin Y (2016) Kenyan isolates of Puccinia graminis f. sp. tritici from 2008 to 2014: virulence to SrTmp in the Ug99 race group and implications for breeding programs. Phytopathology 106:729–736CrossRefPubMedGoogle Scholar
  38. Newton AC, Flavell AJ, George TS, Leat P, Mullholland B, Ramsay L, Revoredo-Giha C, Russell J, Steffenson BJ, Swanston JS, Thomas WTB, Waugh R, White PJ, Bingham IJ (2011) Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security. Food Secur 3:141–178CrossRefGoogle Scholar
  39. Nirmala J, Rouse M, Chen X, Jin Y (2015) New virulent races of barley leaf and stem rust pathogens in the United States. In: American Malting Barley Association, Barley Improvement Conference, San Diego, CA, Oral PresentationGoogle Scholar
  40. Njau P, Bhavani S, Huerta-Espino J, Keller B, Singh R (2013) Identification of QTL associated with durable adult plant resistance to stem rust race Ug99 in wheat cultivar ‘Pavon 76’. Euphytica 190:33–44CrossRefGoogle Scholar
  41. Oehler E (1950) Die Zu¨chtung der Getreidearten und die Produktion und Anerkennung von Getreidesaatgut in der Schweiz. Druckwerkstatten Koehler & Hennemann, WiesbadenGoogle Scholar
  42. Patterson F, Shands R, Dickson J (1957) Temperature and seasonal effects on seedling reactions of barley varieties to three races of Puccinia graminis f. sp. tritici. Phytopathology 47:395–402Google Scholar
  43. Peterson RF, Campbell A, Hannah A (1948) A diagrammatic scale for estimating rust intensity on leaves and stems of cereals. Can J Res 26:496–500CrossRefGoogle Scholar
  44. Pretorius Z, Singh R, Wagoire W, Payne T (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84:203CrossRefGoogle Scholar
  45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  46. Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180CrossRefPubMedGoogle Scholar
  47. Roelfs AP (1978) Estimated losses caused by rust in small grain cereals in the United States, 1918–76. Online Publication, United States Department of Agriculture-Agricultural Research Service, Cereal Rust LaboratoryGoogle Scholar
  48. Roelfs AP (1982) Effects of barberry eradication on stem rust in the United States. Plant Dis 66:177–181CrossRefGoogle Scholar
  49. Roelfs A (1988) Resistance to Leaf and Stem Rust of Wheat. In: Simmonds NW, Rajaram S (eds) Breeding strategies for resistance to the rusts of wheat. CIMMYT, MexicoGoogle Scholar
  50. Roelfs A, Casper D, Long D, Roberts J (1991) Races of Puccinia graminis in the United States in 1989. Plant Dis 75:1127–1130CrossRefGoogle Scholar
  51. Sallam AH, Tyagia P, Brown-Guedira G, Muehlbauer GJ, Hulse A, Steffenson BJ (2017) Genome-wide association mapping of stem rust resistance in Hordeum vulgare subsp. spontaneum. G3 Genes, Genomes, Genetics 7(10):3491–3507 Google Scholar
  52. Sallam A, Endelman J, Jannink J-L, Smith K (2015) Assessing genomic selection prediction accuracy in a dynamic barley breeding population. Plant Genome 8:1–15CrossRefGoogle Scholar
  53. Schilperoord P (2013) Kulturpflanzen in der Schweiz—Gerste. Verein fur alpine Kulturpflanzen Association for Alpine Crops, AlvaneuGoogle Scholar
  54. Shands R (1939) ‘Chevron’ a barley variety resistant to stem rust and other diseases. Phytopathology 29:209–211Google Scholar
  55. Shands R (1964) inheritance and linkage of stem rust and loose smut resistance and starch type in barley. Phytopathology 54:308–316Google Scholar
  56. Singh RP, Hodson DP, Huerta-Espino J, Jin Y, Njau P, Wanyera R, Herrera-Foessel SA, Ward RW (2008) Will stem rust destroy the world’s wheat crop? Adv Agron 98:271–309CrossRefGoogle Scholar
  57. Singh RP, Hodson DP, Jin Y, Lagudah ES, Ayliffe MA, Bhavani S, Rouse MN, Pretorius ZA, Szabo LJ, Huerta-Espino J, Basnet BR, Lan C, Hovmoller MS (2015) Emergence and spread of new races of wheat stem rust fungus: continued threat to food security and prospects of genetic control. Phytopathology 105:872–884CrossRefPubMedGoogle Scholar
  58. Stakman EC, Stewart DM, Loegering WQ (1962) Identification of physiological races of Puccinia graminis f. sp. tritici. Online Publication, United States Department of Agriculture-Agricultural Research Service. Publ E-617. Accessed Mar 2017
  59. Steffenson BJ (1992) Analysis of durable resistance to stem rust in barley. Euphytica 63:153–167CrossRefGoogle Scholar
  60. Steffenson B, Smith K (2006) Breeding barley for multiple disease resistance in the Upper Midwest region of the USA. Czech J Genet Plant Breed 42:79Google Scholar
  61. Steffenson BJ, Wilcoxson RD, Roelfs AP (1984) Inheritance of resistance to Puccinia graminis f.sp. secalis in barley. Plant Dis 68:762–763CrossRefGoogle Scholar
  62. Steffenson BJ, Wilcoxson RD, Roelfs AP (1985) Resistance of barley to Puccinia graminis f. sp. tritici and Puccinia gaminis f. sp. secalis. Phytopathology 75:1108-1111 CrossRefGoogle Scholar
  63. Steffenson B, Jin Y, Rossnagel B, Rasmussen J, Kao K (1995) Genetics of multiple disease resistance in a doubled-haploid population of barley. Plant Breed 114:50–54CrossRefGoogle Scholar
  64. Steffenson BJ, Olivera P, Roy JK, Jin Y, Smith KP, Muehlbauer GJ (2007) A walk on the wild side: mining wild wheat and barley collections for rust resistance genes. Aust J Agr Res 58:532–544CrossRefGoogle Scholar
  65. Steffenson B, Jin Y, Brueggeman R, Kleinhofs A, Sun Y (2009) Resistance to stem rustrace TTKSK maps to the rpg4/Rpg5 complex of chromosome 5H of barley. Phytopathology 99:1135–1141CrossRefPubMedGoogle Scholar
  66. Steffenson BJ, Solanki S, Brueggeman RS (2016) Landraces from mountainous regions of Switzerland are sources of important genes for stem rust resistance in barley. Alpine Bot 126:23–33CrossRefGoogle Scholar
  67. Steffenson BJ, Case AJ, Pretorius Z, Coetzee V, Kloopers FJ, Zhou H, Chai Y (2017) Vulnerability of barley to African pathotypes of Puccinia graminis f. sp. tritici and sources of resistance. Phytopathology 107:950–962CrossRefPubMedGoogle Scholar
  68. Sun Y, Steffenson BJ (2005) Reaction of barley seedlings with different stem rust resistance genes to Puccinia graminis f. sp tritici and Puccinia graminis f. sp secalis. Can J Plant Pathol 27:80–89CrossRefGoogle Scholar
  69. Sun YL, Steffenson BJ, Jin Y (1996) Genetics of resistance to Puccinia graminis f sp secalis in barley line Q21861. Phytopathology 86:1299–1302CrossRefGoogle Scholar
  70. Tamang P, Neupane A, Mamidi S, Friesen T, Brueggeman R (2015) Association mapping of seedling resistance to spot form net blotch in a worldwide collection of barley. Phytopathology 105:500–508CrossRefPubMedGoogle Scholar
  71. Technow F (2015) R package mvngGrAd: moving grid adjustment in plant breeding field trials. 0.1.5 edn. Comprehensive R Archive Network. Accessed Jan 2017
  72. Turuspekov Y, Ormanbekova D, Rsaliev A, Abugalieva S (2016) Genome-wide association study on stem rust resistance in Kazakh spring barley lines. BMC Plant Biol 16(1):14–21CrossRefGoogle Scholar
  73. USDA-NASS (2015) United States Department of Agriculture, National Agricultural Statistics Service. Online Publication Quick Stats 2.0. Accessed June 2016
  74. Wamalwa MN, Wanyera R, Njau PN, Okiror MA, Owuoche JO (2016) Inheritance of resistance to Ug99 stem rust pathogen in selected barley lines. S Afr J Plant Soil 33(3):201–206CrossRefGoogle Scholar
  75. Wang X, Richards J, Gross T, Druka A, Kleinhofs A, Steffenson B, Acevedo M, Brueggeman R (2013) The rpg4-mediated resistance to wheat stem rust (Puccinia graminis) in barley (Hordeum vulgare) requires Rpg5, a second NBS-LRR gene, and an actin depolymerization factor. Mol Plant Microbe Interact 26:407–418CrossRefPubMedGoogle Scholar
  76. Wang M, Wan A, Chen X (2015) Barberry as alternate host is important for Puccinia graminis f. sp. tritici but not for Puccinia striiformis f. sp. tritici in the US Pacific Northwest. Plant Dis 99:1507–1516CrossRefGoogle Scholar
  77. Waugh R, Jannink JL, Muehlbauer GJ, Ramsay L (2009) The emergence of whole genome association scans in barley. Curr Opin Plant Biol 12:218–222CrossRefPubMedGoogle Scholar
  78. Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17:155–160CrossRefPubMedGoogle Scholar
  79. Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB (2005) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208CrossRefPubMedGoogle Scholar
  80. Yu L-X, Barbier H, Rouse MN, Singh S, Singh RP, Bhavani S, Huerta-Espino J, Sorrells ME (2014) A consensus map for Ug99 stem rust resistance loci in wheat. Theor Appl Genet 127:1561–1581CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zadoks J, Chang T, Konzak C (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421CrossRefGoogle Scholar
  82. Zhou H (2011) Association mapping of multiple disease resistance in US barley breeding germplasm. Ph.D. dissertation, Department of Plant Pathology. University of Minnesota, UMI Dissertations PublishingGoogle Scholar
  83. Zhou H, Steffenson BJ, Muehlbauer G, Wanyera R, Njau P, Ndeda S (2014) Association mapping of stem rust race TTKSK resistance in US barley breeding germplasm. Theor Appl Genet 127:1293–1304CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Austin J. Case
    • 1
  • Sridhar Bhavani
    • 2
  • Godwin Macharia
    • 3
  • Brian J. Steffenson
    • 1
    Email author
  1. 1.Department of Plant PathologyUniversity of MinnesotaSt. PaulUSA
  2. 2.Centro Internacional de Mejoramiento de Maíz y Trigo (CIMMYT)NairobiKenya
  3. 3.Kenya Agriculture Livestock Research Organization (KALRO)NjoroKenya

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