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Population genetic structure of Pyrenophora teresDrechs. the causal agent of net blotch in Sardinian landraces of barley (Hordeum vulgare L.)

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Abstract.

Monoconidial cultures of Pyrenophora teres, the causal agent of barley net blotch, were isolated from leaves collected from six populations of the barley landrace "S'orgiu sardu" growing in five agro-ecological areas of Sardinia, Italy, and genotyped using AFLPs. The 150 isolates were from lesions of either the "net form" (P. teres f. sp. teres) or the "spot form" (P. teres f. sp. maculata) of the disease. Of 121 AFLP markers, 42%, were polymorphic. Cluster analysis resolved the isolates into two strongly divergent groups (F ST = 0.79), corresponding to the net (45% of the isolates) and the spot (55% of the isolates) forms (designated the NFR and SFR groups, respectively). The absence of intermediate genotypes and the low number of shared markers between the two groups indicated that hybridization between the two formae is rare or absent under the field condition of Sardinia. Five of the barley populations hosted both forms but in different proportions. The SFR populations were similar in overall polymorphism to the NFR populations. However, compared to the SFR form, the NFR occurred in all fields sampled and showed a higher population divergence (F ST = 0.43 versus F ST = 0.09 with all isolates; F ST = 0.37 versus F ST = 0.06 with clone corrected samples) probably due to a lower migration rate. AFLP fingerprints resolved 117 distinct genotypes among the 150 isolates sampled (78%), 87% in SFR and 68% in NFR isolates. Although the absolute numbers may be a function of the number of AFLP markers assayed, the relative difference suggests that clonality is more prevalent among the NFR isolates (with 11 of 46 haplotypes observed more than once), compared with SFR isolates (7 of 71 haplotypes). Both digenic and multilocus linkage disequilibrium analyses suggested that sexual reproduction occurs at significant levels within the NFR and SFR populations, and that the relative contribution of sexual and asexual reproduction varies among different environments.

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References

  • Afanasenko OS, Hartleb H, Guseva NN, Minarikova V, Janosheva M (1995) A set of differentials to characterize populations of Pyrenophora teres Drechs. for international use. J Phytopathol 143:501–507

    Google Scholar 

  • Attene G, Ceccarelli S, Papa R (1996) The barley (Hordeum vulgare L.) of Sardinia, Italy. Genetic Resour Crop Evol 43:385–393

    Google Scholar 

  • Brown AHD, Feldman MW, Nevo E (1980) Multilocus structure in natural populations of Hordeum spontaneum. Genetics 96:523–536

    Google Scholar 

  • Brown MP, Steffenson BJ, Webster RK (1993) Host range of Pyrenophora teres isolates from California. Plant Dis 77:942–947

    Google Scholar 

  • Bucheli E, Leuchtmann A (1996) Evidence for genetic differentiation between choke-inducing and asymptomatic strains of the Epichloe grass endophyte from Brachypodium sylvaticum. Evolution 50:1879–1887

    Google Scholar 

  • Bucheli E, Gautschi B, Shykoff JA (2001) Differences in population structure of the anther smut fungus Microbotryum violaceum on two closely related host species, Silene latifolia and S. dioica. Mol Ecol 10:285–295

    Article  CAS  PubMed  Google Scholar 

  • Burdon JJ, Abbott DC, Brown AHD, Brown JS (1994) Genetic structure of the scald pathogen (Rhynchosporium secalis) in South Australia: implications for control strategies. Aust J Agric Res 45:1145–1154

    Google Scholar 

  • Burt A, Carter DA, Koenig GL, White TJ, Taylor JW (1996) Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proc Natl Acad Sci USA 93:770–773

    Article  CAS  Google Scholar 

  • Burt A, Koufopanou V, Taylor JW (1999) Population genetics of human-pathogenic fungi. In: Thompson RCA (ed) The molecular epidemiology of infectious diseases. Chapman and Hall, London

  • Campbell GF, Crows PW, Lucas JA (1999) Pyrenophora teres f. maculata, the cause of Pyrenophora leaf spot of barley in South Africa. Mycol Res 103:257–267

    Article  Google Scholar 

  • Chen RS, McDonald BA (1996) Sexual reproduction plays a major role in the genetic structure of populations of the fungus Mycosphaerella graminicola. Genetics 142:1119–1127

    CAS  PubMed  Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York

  • Deadman ML, Cooke BM (1989) An analysis of rain-mediated dispersal of Drechslera teres conidia in field plots of spring barley. Ann Appl Biol 115:209–214

    Google Scholar 

  • Delmotte F, Bucheli E, Shykoff JA (1999) Host and parasite population structure in a natural plant-pathogen system. Heredity 83:300–308

    Article  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mithocondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Giraud T, Fortini D, Levis C, Leroux P, Brygoo Y (1997) RFLP markers show genetic recombination in Botryotinia fuckeliana (Botrytis cinerea) and transposable elements reveal two sympatric species. Mol Biol Evol 14:1177–1185

    CAS  PubMed  Google Scholar 

  • Harrabi M, Kamel A (1990) Virulence spectrum to barley in some isolates of Pyrenophora teres from the Mediterranean region. Plant Dis 3:230–232

    Google Scholar 

  • Hutcheson K (1970) A test for comparing diversities based on the Shannon formula. J Theoret Biol 26:151–154

    Google Scholar 

  • Jonsson R, Bryngelsson T, Gustafsson M (1997) Virulence studies of Swedish net blotch isolates (Drechslera teres) and identification of resistant barley lines. Euphytica 94:209–218

    Article  Google Scholar 

  • Jordan JWL, Best GR, Allen EC (1985) Effect of Pyrenophora teres on dry matter production and yield component on winter barley. Plant Pathol 34:200–206

    Google Scholar 

  • Kumar J, Nelson RJ, Zeigler RS (1999) Population structure and dynamics of Magnaporthe grisea in the Indian Himalayas. Genetics 152:971–984

    CAS  PubMed  Google Scholar 

  • Lenski RE (1993) Assessing the genetic structure of microbial populations. Proc Natl Acad Sci USA 90:4344–4336

    Google Scholar 

  • Liu YC, Cortesi P, Double ML, McDonald WL, Milgroom MG (1996) Diversity and multilocus structure in populations of Cryphonectria parasitica. Phytopathology 86:1344–1351

    Google Scholar 

  • Majer D, Mithen R, Lewis BG, Vos P, Oliver RP (1996) The use of AFLP fingerprinting for the detection of genetic variation in fungi. Mycol Res 100:1107–1111

    CAS  Google Scholar 

  • Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220

    CAS  PubMed  Google Scholar 

  • Maynard Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria?. Proc Natl Acad Sci USA 90:4384–4388

    PubMed  Google Scholar 

  • Maynard Smith J, Feil EJ, Smith EH (2000) Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays 22:1115–1122

    Article  PubMed  Google Scholar 

  • Martin RA, Clough KS (1984) Relationship of the airborne spore load of the Pyrenophora teres weather variable to net blotch development on barley. Can J Plant Pathol 6:105–110

    Google Scholar 

  • McDermott JM, McDonald BA (1993) Gene flow in a plant pathosystem. Annu Rev Phytopathol 31:353–373

    Article  Google Scholar 

  • McDonald BA, Mundt CC, Chen RS (1996) The role of selection on the genetic structure of pathogen populations. Evidence from field experiments with Mycosphaerella graminicola on wheat. Euphytica 92:73–80

    Google Scholar 

  • McDonald WC (1963) Heterothallism in Pyrenophora teres. Phytopathology 53:771–773

    Google Scholar 

  • Migheli Q, Friard O, Del Tedesco D, Musso MR (1996) Stability of transformed antagonistic Fusarium oxysporum strains in vitro and in soil microcosms. Mol Ecol 5:641–649

    CAS  Google Scholar 

  • Milgroom MG (1996) Recombination and the multilocus structure of fungal populations. Annu Rev Phytopathol 14:457–477

    Article  Google Scholar 

  • Milgroom MG (1997) Genetic variation and the application of genetic markers for studying plant pathogen populations. J Plant Pathol 78:1–13

    Google Scholar 

  • Miller MP (1997) TFPGA. Tools for population genetic analysis. Version 1.3. Northern Arizona University, Arizona

  • Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Tree 14:389–394

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical models for studying genetic variation terms of restriction endonuclease. Proc Natl Acad Sci USA 76:5269–5273

    CAS  PubMed  Google Scholar 

  • Papa R, Attene G, Barcaccia G, Ohgata A, Konishi T (1998) Genetic diversity in landrace populations of Hordeum vulgare L. from Sardinia, Italy, as revealed by RAPDs, isozymes and morphophenological traits. Plant Breed 117:523–530

    Google Scholar 

  • Peever TL, Milgroom MG (1994) Genetic structure of Pyrenophora teres populations determined with random amplified polymorphic DNA markers. Can J Bot 72:915–923

    CAS  Google Scholar 

  • Peltonen S, Jalli M, Kammiovirta K, Karyalainen R (1996) Genetic variation in Drechslera teres populations as indicated by RAPD markers. Ann Appl Biol 128:465–477

    CAS  Google Scholar 

  • Richter K, Shondelmaier J, Jung C (1998) Mapping of quantitative trait loci affecting Drechslera teres in barley with molecular markers. Theor Appl Genet 97:1125–1234

    Article  Google Scholar 

  • Rohlf FJ (1992) NTSYS. Numerical taxonomy and multivariate analysis system, Version 1.70. Exeter, Stauker

  • Rosendahl S, Taylor JW (1997) Development of multiple genetic markers for studies of genetic variation in arbuscular mycorrhizal fungi using AFLP. Mol Ecol 6:821–830

    CAS  Google Scholar 

  • SAS Institut (1995) JMP software, SAS Institut Inc. Copyright 1985–1995

  • Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

  • Shipton WA (1973) Net blotch of barley. Rev Plant Pathol 52:269–290

    Google Scholar 

  • Schneider S, Kueffer JM, Roessli D, Excoffier L (1997) ARLEQUIN Ver. 1.1: a software for population genetic data analysis. Genetic and Biometry Laboratory, University of Geneva, Geneva

  • Scott DB (1991) Identity of Pyrenophora isolates causing net-type and spot-type lesions on barley. Mycopathologia 116:29–36

    Google Scholar 

  • Sicard D, Buchet S, Mikalakis Y, Neema C (1997a) Genetic variability of Colletotrichum lindemunthianum in wild populations of common bean. Plant Pathol 46:355–365

    Google Scholar 

  • Sicard D, Mikalakis Y, Dron M, Neema C (1997b) Genetic diversity and pathogenic variation of Colletotrichum lindemunthianum in the three centers of diversity of its host, Phaseolus vulgaris. Phytopathology 87:807–813

    Google Scholar 

  • Slatkin M (1994) Linkage disequilibrium in growing and stable populations. Genetics 137:331–336

    PubMed  Google Scholar 

  • Smedegård-Petersen V (1971) Pyrenophora teres f. sp. maculata f. nov. and Pyrenophora teres f. teres on barley in Denmark. Royal Veterinary and Agricultural University, Copenhagen, pp 124–144

  • Smedegård-Petersen V (1976) Pathogenesis and genetics of net-spot blotch and leaf stripe of barley caused by Pyrenophora teres and Pyrenophora graminea. DSR Verlag, Royal Veterinary and Agricultural University, Copenhagen, pp 1–76

  • Sokal R (1979) Testing statistical significance of geographic variation pattern. Syst Zool 28:227–232

    Google Scholar 

  • Steffenson BJ, Webster RK (1992) Pathotype diversity of Pyrenophora teres f. sp. teres on barley. Phytopathology 82:170–177

    Google Scholar 

  • Steffenson BJ, Webster RK, Jackson LF (1991) Reduction in yield loss using incomplete resistance to P. teres f. sp. teres in barley. Plant Dis 75:96–100

    Google Scholar 

  • Taylor JW, Geiser DM, Burt A, Koufopanou V (1999a) The evolutionary biology and population genetics underlying fungal strain typing. Clin Microbiol Rev 12:126–146

    CAS  PubMed  Google Scholar 

  • Taylor JW, Jacobson DJ, Fischer MC (1999b) The evolution of asexual fungi: reproduction, speciations and classification. Ann Rev Phytopathol 37:197–246

    Article  CAS  Google Scholar 

  • Tekauz A (1990) Characterization and distribution of pathogenic variation in Pyrenophora teres f. sp. teres and P. teres f. sp. maculata from Western Canada. Can J Plant Pathol 12:141–148

    Google Scholar 

  • Tekauz A (2000) Evaluation of barley cultivar resistance to Pyrenophora teres using combined seedling and adult plant reaction. In: Proc 8th Int Barley Genetic Symposium, 22–27 October 2000, Vol II, pp 182–183

  • Teshome A, Brown AHD, Hodgkin T (2001) Diversity in landraces of cereal and legume crops. Plant Breed Rev 21:221–261

    CAS  Google Scholar 

  • Thrall PH, Burdon J (1997) Host-pathogen dynamics in a metapopulations context: the ecological and evolutionary consequences of being spatial. J Ecol 85:743–753

    Google Scholar 

  • Tybarenc M, Kjellberg F, Arnaud J, Oury B, Frederique Breniere S (1991) Are eukaryotic microorganism clonal or sexual?. A population genetics vantage. Proc Natl Acad Sci USA 88:5129–5133

    PubMed  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Van De Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    CAS  PubMed  Google Scholar 

  • Williams KJ, Lichon A, Gianquitto P, Kretschmer JM, Karakousis A, Manning S, Langridge P, Wallwork H (1999) Identification and mapping of a gene conferring resistance to the spot form of the net blotch (Pyrenophora teres f. maculata) in barley. Theor Appl Genet 99:323–327

    Article  Google Scholar 

  • Williams KJ, Smyl C, Lichon A, Wong KY, Wallwork H (2001) Development and use of an assay based on the polymerase chain reaction that differentiates the pathogens causing spot form and the net form of net blotch of barley. Aust Plant Pathol 30:37–44

    Google Scholar 

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    Google Scholar 

  • Xu J, Mitchell TG, Vilgalys R (1999) PCR-restriction fragment length polymorphism (RFLP) analyses reveal both extensive clonality and local genetic differences in Candida albicans. Mol Ecol 8:59–73

    Article  CAS  PubMed  Google Scholar 

  • Yeh C, Yang RC (1999) POPGENE VERSION 1.31. Microsoft window-based Freeware for population genetic analysis

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Acknowledgements.

We thank R. K. Genger, S. Hoebee, N. Paltridge, A. Becerra Lopez-Lavallé and A. Arba for their assistance during this study, R.K.G. and N.P. for comments on the manuscript, and D. Sicard for frequent discussion and suggestion. D.R. is grateful to CSIRO Plant Industry, where he was a Visiting Scholar while this research was conducted. This work was partially supported by the Italian Government, Project MURST-Cofin99, #9907384522, "Evaluation of 'species-environment' systems for 'in situ' conservation of genetic resources of cultivated species". We thank the anonymous reviewers for thoughtful and helpful suggestions.

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Rau, D., Brown, A.H.D., Brubaker, C.L. et al. Population genetic structure of Pyrenophora teresDrechs. the causal agent of net blotch in Sardinian landraces of barley (Hordeum vulgare L.). Theor Appl Genet 106, 947–959 (2003). https://doi.org/10.1007/s00122-002-1173-0

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