Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

A walk on the wild side: mining wild wheat and barley collections for rust resistance genes

Brian J. Steffenson A D , Pablo Olivera A , Joy K. Roy A , Yue Jin B , Kevin P. Smith C and Gary J. Muehlbauer C
+ Author Affiliations
- Author Affiliations

A Department of Plant Pathology, University of Minnesota, St. Paul, MN 55108, USA.

B United States Department of Agriculture-Agricultural Research Service, Cereal Disease Laboratory, St. Paul, MN 55108, USA.

C Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, MN 55108, USA.

D Corresponding author. Email: bsteffen@umn.edu

Australian Journal of Agricultural Research 58(6) 532-544 https://doi.org/10.1071/AR07123
Submitted: 26 March 2007  Accepted: 24 May 2007   Published: 26 June 2007

Abstract

Leaf rust, stem rust, and stripe rust are among the most important diseases of wheat and barley worldwide and are best controlled using genetic resistance. To increase the diversity of rust resistance in wheat and barley, a project was initiated to identify and characterise rust resistance genes from the wild species of Aegilops sharonensis (Sharon goatgrass) and Hordeum vulgare ssp. spontaneum (wild barley), respectively. One hundred and two accessions of Sharon goatgrass from Israel and 318 Wild Barley Diversity Collection (WBDC) accessions from the Fertile Crescent, Central Asia, North Africa, and the Caucasus region were evaluated for resistance to leaf rust, stem rust, and/or stripe rust. Sharon goatgrass exhibited a wide range of infection types (ITs) in response to leaf rust, stem rust, and stripe rust. The percentage of resistant accessions in Sharon goatgrass was 58.8–78.4% for leaf rust, 11.8–69.6% for stem rust, and 46.1% for stripe rust, depending on the race used and the plant growth stage. Genetic studies with Sharon goatgrass revealed oligogenic resistance to leaf rust and stem rust. Wild barley also exhibited a wide range of ITs to leaf rust and stem rust; however, the overall frequency of resistance was lower than for Sharon goatgrass. The percentage of resistant accessions in wild barley was 25.8% for leaf rust and 5.7–20.1% for stem rust, depending on the race used. Resistance to the new virulent stem rust race TTKS (i.e. Ug99), present in eastern Africa, was found in both Sharon goatgrass (70% of accessions) and wild barley (25% of 20 accessions tested). Association mapping for stem rust resistance was applied in the WBDC using Diversity Arrays Technology (DArT) markers. Using the highly conservative P value threshold of 0.001, 14 and 15 significant marker associations were detected when the number of subpopulations (K value) was set for 10 and 8, respectively. These significant associations were in 9 and 8 unique chromosome bins, respectively. Two significant marker associations were detected for resistance to the wheat stem rust race MCCF in the same bin as the rpg4/Rpg5 complex on chromosome 7(5H). The presence of a major stem rust resistance gene in this bin on chromosome 7(5H) was validated in a bi-parental mapping population (WBDC accession Damon × cv. Harrington) constructed with DArT markers. The results from this study indicate that Sharon goatgrass and wild barley are rich sources of rust resistance genes for cultivated wheat and barley improvement, respectively, and that association mapping may be useful for positioning disease resistance genes in wild barley.

Additional keywords: allele mining, linkage disequilibrium, wild species, disease resistance.


Acknowledgments

This research was funded by the United States Agency for International Development (USAID) program on Comparative Cereal Genomics and the Lieberman-Okinow Endowment Chair at the University of Minnesota. We thank Stephanie Dahl and Tamas Szinyei for excellent technical assistance, Dr James Kolmer for assistance in the leaf rust evaluations, Dr Jacob Manisterski for assistance in the stripe rust evaluation, and Koffi Adragni for statistical assistance. We are indebted to Dr Yehoshua Anikster for suggesting the Sharon goatgrass project and providing the germplasm used in this study. We thank Dr Andrzej Kilian, Ben Alsop, and Jason Carling for their assistance in genotyping the wild barley collection. BJS dedicates this paper to Professor Robert A. McIntosh for his valuable mentoring.


References


Alam KB, Gustafson JP (1988) Tan-spot resistance screening of Aegilops species. Plant Breeding 100, 112–118.
CrossRef |

Alsop BP , Kilian A , Carling J , Pickering RA , Steffenson BJ (2007) DArT marker-based linkage analysis and inheritance of multiple disease resistance in a wild × cultivated barley population. In ‘Plant and Animal Genome XV Conference’. 13–17 January 2007, San Diego, CA.

Anikster Y, Long DL, Manisterski J (1992) Response to wheat leaf rust of Aegilops spp. collected in Israel. Phytopathology 82, 114.

Anikster Y, Manisterski J, Long DL, Leonard KJ (2005) Resistance to leaf rust, stripe rust, and stem rust in Aegilops spp. in Israel. Plant Disease 89, 303–308.
CrossRef |

Antonov AI, Marais GF (1996) Identification of leaf rust resistance genes in Triticum species for transfer to common wheat. South African Journal of Plant Soil 13, 55–60.

Baum M, Grando S, Backes G, Jahoor A, Sabbagh A, Ceccarelli S (2003) QTLs for agronomic traits in the Mediterranean environment identified in recombinant inbred lines of the cross ‘Arta’ x H. spontaneum 41-1. Theoretical and Applied Genetics 107, 1215–1225.
CrossRef | PubMed |

von Bothmer R , Sato K , Komatsuda T , Yasuda S , Fishbeck G (2003) The domestication of cultivated barley. In ‘Diversity in barley (Hordeum vulgare)’. (Eds R von Bothmer, T van Hintum, H Knupffer, K Sato) pp. 9–27. (Elsevier: New York)

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

Brown WM, Hill JP, Velasco VR (2001) Barley yellow rust in North America. Annual Review of Phytopathology 39, 367–384.
CrossRef | PubMed |

Buntjer JB, Sørensen AP, Peleman JD (2005) Haplotype diversity: the link between statistical and biological association. Trends in Plant Science 10, 466–471.
CrossRef | PubMed |

Caldwell KS, Russell J, Langridge P, Powell W (2006) Extreme population-dependent linkage disequilibrium detected in an inbreeding plant species, Hordeum vulgare. Genetics 172, 557–567.
CrossRef | PubMed |

Chen XM, Moore M, Milus EA, Long DL, Line RF, Marshall D, Jackson L (2002) Wheat stripe rust epidemics and races of Puccinia striiformis f. sp. tritici in the United States in 2000. Plant Disease 86, 39–46.
CrossRef |

Clifford BC (1985) Barley leaf rust. In ‘The Cereal Rusts Vol. II: Diseases, distribution, epidemiology and control’. (Eds AP Roelfs, WR Bushnell) pp. 173–205. (Academic Press: Orlando, FL)

Cook RJ, Hims MJ, Vaughan TV (1999) Effects of fungicide spray timing on winter wheat disease control. Plant Pathology 48, 33–50.
CrossRef |

Ecker R, Cahaner A, Dinoor A (1990) The inheritance of resistance to Septoria glume blotch II. The wild wheat species Aegilops speltoides. Plant Breeding 104, 218–223.
CrossRef |

Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.
PubMed |


Fetch TG, Steffenson BJ, Nevo E (2003) Diversity and sources of multiple disease resistance in Hordeum spontaneum. Plant Disease 87, 1439–1448.
CrossRef |

Friebe B, Jiang J, Raupp WJ, McIntosh RA, Gill BS (1996) Characterization of wheat-alien translocations conferring resistance to diseases and pests: current status. Euphytica 91, 59–87.

Gerechter-Amitai ZK, Loegering WQ (1977) Genes for low reaction to Puccinia graminis tritici in Aegilops and Triticum. Crop Science 17, 830–832.

Gill BS , Friebe B (2002) Cytogenetics, phylogeny and evolution of cultivated wheats. In ‘Bread wheat. Improvement and production’. (Eds BC Curtis, S Rajaram, H. Gomez Macpherson) pp. 71–88. (FAO: Rome)

Gill BS, Sharma HC, Raupp WJ, Browder LE, Hatchett JH, Harvey TL, Moseman GJ, Waines JG (1985) Evaluation of Aegilops species for resistance to wheat powdery mildew, wheat leaf rust, Hessian fly and greenbug. Plant Disease 69, 314–316.

Huelsenbeck JP, Andolfatto P (2007) Inference of population structure under a Dirichlet process model. Genetics 175, 1787–1802.
CrossRef | PubMed |

Jaccoud D, Peng K, Feinstein D, Kilian A (2001) Diversity Arrays: a solid state technology for sequence information independent genotyping. Nucleic Acids Research 29, e25.
CrossRef | PubMed |

Jiang J, Friebe B, Gill BS (1994) Recent advances in alien gene transfer in wheat. Euphytica 73, 199–212.
CrossRef |

Jin Y, Singh R (2006) Resistance to recent eastern African stem rust isolates with virulence to Sr31 in US wheat. Plant Disease 90, 476–480.
CrossRef |

Jin Y, Steffenson BJ (1994) Inheritance of leaf rust resistance in cultivated and wild barley. Heredity 85, 451–454.

Jin Y, Steffenson BJ, Miller JD (1994) Inheritance of resistance to pathotypes QCC and MCCF of Puccinia graminis f. sp. tritici in barley line Q21861 and temperature effects on the expression of resistance. Phytopathology 84, 452–455.
CrossRef |

Kennedy BW, Quinton M, Vanarendonk JAM (1992) Estimation of effects of single genes on quantitative traits. Journal of Animal Science 70, 2000–2012.
PubMed |


Kimber G , Feldman M (1987) ‘Wild wheat—An introduction.’ Special Report 353. (College of Agriculture, University of Missouri: Columbia, MO)

Kleinhofs A , Graner A (2001) An integrated map of the barley genome. In ‘DNA-based markers in plants’. 2nd edn (Eds RL Phillips, I Vasil) pp 187–199. (Kluwer: Boston)

Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annual Review of Phytopathology 34, 435–455.
CrossRef | PubMed |

Kolmer JA, Long DL, Huges ME (2004) Physiologic specialization of Puccinia triticina on wheat in the United States in 2002. Plant Disease 88, 1079–1084.
CrossRef |

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

Kutiel P (1998) Annual vegetation of the coastal sand dunes of the northern Sharon Israel. Israeli Journal of Plant Sciences 46, 287–298.

Labate JA (2000) Software for population genetics analyses of molecular data. Crop Science 40, 1521–1528.

Legge WG, Metcalfe DR, Chiko AW, Martens JW, Tekauz A (1996) Reaction of Turkish barley accessions to Canadian barley pathogens. Canadian Journal of Plant Science 76, 927–931.

Levine MN , Cherewick WJ (1952) Studies on dwarf leaf rust of barley. US Department of Agriculture Technical Bulletin No. 1057.

Long DL , Hughes ME (2000). Small grain losses due to rust. Publication No. CDL-EP#007. Available at: www.cdl.umn.edu (accessed on: 12/01/06).

Malysheva-Otto LV, Ganal MW, Röder MS (2006) Analysis of molecular diversity, population structure and linkage disequilibrium in a worldwide survey of cultivated barley germplasm (Hordeum vulgare L.). BMC Genetics Paper 6 (online) 7,
CrossRef | PubMed |

Manisterski J, Segal A, Levy AA, Feldman M (1988) Evaluation of Israeli Aegilops and Agropyron species for resistance to wheat leaf rust. Plant Disease 72, 941–944.
CrossRef |

Marais GF, McCallum B, Marais AS (2006) Leaf Rust and Stripe Rust Resistance Genes Derived from Aegilops sharonensis. Euphytica 149, 373–380.
CrossRef |

Marais GF, Pretorius ZA, Marais AS, Wellings CR (2003) Transfer of rust resistance genes from Triticum species to common wheat. South African Journal of Plant and Soil 20, 193–198.

Metcalfe DR, Chiko AW, Martens JW, Tekauz A (1977) Reaction of barleys from the Middle East to Canadian pathogens. Canadian Journal of Plant Science 57, 995–999.

Miller JD, Lambert JW (1955) Variability and inheritance of reaction of barley to race 15B of stem rust. Agronomy Journal 47, 373–377.

Millet E, Agami M, Ezrati S, Manisterski J, Anikster Y (2006) Distribution of Sharon goat grass (Aegilops sharonensis Eig) in Israel. Israeli Journal of Plant Science 54, 243–248.
CrossRef |


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. Proceedings of the National Academy of Sciences of the United States of America 102, 2442–2447.
CrossRef | PubMed |

Moseman JG, Nevo E, El-Morshidy MA (1990) Reactions of Hordeum spontaneum to infection with two cultures of Puccinia hordei from Israel and United States. Euphytica 49, 169–175.
CrossRef |

Olivera PD, Anikster Y, Kolmer JA, Steffenson BJ (2007) Resistance of Sharon goatgrass (Aegilops sharonensis) to fungal diseases of wheat. Plant Disease in press 91,

Pasquini M (1980) Disease resistance in wheat: II. Behaviour of Aegilops species with respect to Puccinia recondite f. sp. tritici, Puccinia graminis f. sp. tritici and Erysiphe graminis f. sp. tritici. Genetica Agraria 34, 133–148.

Pretorius ZA, Singh RP, Wagoire WW, Payne TS (2000) Detection of virulence to wheat stem rust resistance genes Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Disease 84, 203.
CrossRef |


Pritchard JK, Przeworski M (2001) Linkage disequilibrium in humans: Models and Data. Amercan Journal of Human Genetics 69, 1–14.
CrossRef |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
PubMed |


Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Current Opinion in Plant Biology 5, 94–100.
CrossRef | PubMed |

Roelfs AP (1985) Wheat and rye stem rust. In ‘The Cereal Rusts Vol. II: Diseases, distribution, epidemiology and control’. (Eds AP Roelfs, WR Bushnell) pp. 4–37. (Academic Press: Orlando, FL)

Rostoks N, Ramsay L, MacKenzie K, Cardle L, Bhat PR , et al. (2006) Recent history of artificial outcrossing facilitates whole-genome association mapping in elite inbred crop varieties. Proceedings of the National Academy of Sciences of the United States of America 103, 18656–18661.
CrossRef | PubMed |

Segal A , Manisterski J , Fischerbeck G , Wahl I (1980) How plant populations defend themselves in natural ecosystems. In ‘Plant disease: an advanced treatise’. Vol. 5. (Eds JG Horsfall, EB Cowling) pp. 75–102. (Academic Press: New York)

Singh RP , Hodson DP , Jin Y , Huerta-Espino J , Kinyua MG , Wanyera R , Njau P , Ward RW (2006) Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources. 1 (No. 054), 13 pp.

van Slageren M (1993) Taxonomy and distribution of Aegilops. In ‘Biodiversity and wheat improvement’. (Ed. AB Damania) pp. 67–79. (John Wiley & Sons.: Chichester, UK)

Snyman JE, Pretorius ZA, Kloppers FJ, Marais GF (2004) Detection of adult-plant resistance to Puccinia triticina in a collection of wild Triticum species. Genetic Resources and Crop Evolution 51, 591–597.
CrossRef |

Steffenson BJ, Jin Y (2006) Resistance to race TTKS of Puccinia graminis f. sp. tritici in barley. Phytopathology 96, S110.

Steffenson BJ, Miller JD, Jin Y (1993) Detection of the stem rust resistance gene Rpg1 in barley seedlings. Plant Disease 77, 626–629.

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. Canadian Journal of Plant Pathology 27, 80–89.

Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES, IV (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nature Genetics 28, 286–289.
CrossRef | PubMed |

Wahl I , Anikster Y , Manisterski J , Segal A (1984) Evolution at the center of origin. In ‘The cereal rusts. Vol. I. Origins, specificity, structure, and physiology’. (Eds AP Roelfs, WR Bushnell) pp. 33–77. (Academic Press: Orlando, FL)

Wanyera R, Kinyua MG, Jin Y, Singh RP (2006) The spread of stem rust caused by Puccinia graminis f. sp. tritici, with virulence on Sr31 in wheat in Eastern Africa. Plant Disease 90, 113.
CrossRef |

Wenzl P, Carling J, Kudrna D, Jaccoud D, Huttner E, Kleinhofs A, Kilian A (2004) Diversity arrays technology (DArT) for whole-genome profiling of barley. Proceedings of the National Academy of Sciences of the United States of America 101, 9915–9920.
CrossRef | PubMed |

Wenzl P, Li H, Carling J, Zhou M, Raman H , et al. (2006) A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics Paper 6 (online) 7,
CrossRef | PubMed |

Wolfinger R, O’Connell M (1993) Generalized linear mixed models: a pseudo-likelihood approach. Journal of Statistical Computation and Simulation 48, 233–243.

Yang W-Y, Yu Y, Zhang Y, Hu X-R, Wang Y, Zhou Y-C, Lu B-R (2003) Inheritance and expression of stripe rust resistance in common wheat (Triticum aestivum) transferred from Aegilops tauschii and its utilization. Hereditas 139, 49–55.
CrossRef | PubMed |

Yu J, Pressoir G, Briggs WH, Bi IV, Yamasaki M , et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics 38, 203–208.
CrossRef | PubMed |

Yun SJ, Gyenis L, Bossolini E, Hayes PM, Matus I, Smith KP, Steffenson BJ, Tuberosa R, Muehlbauer GJ (2006) Validation of quantitative trait loci for multiple disease resistance in barley using advanced backcross lines developed with a wild barley. Crop Science 46, 1179–1186.
CrossRef |

Yun SJ, Gyenis L, Hayes PM, Matus I, Smith KP, Steffenson BJ, Muehlbauer GJ (2005) Quantitative trait loci for multiple disease resistance in wild barley. Crop Science 45, 2563–2572.
CrossRef |








Rent Article (via Deepdyve) Export Citation Cited By (42)

View Altmetrics