Genetic diversity of Rhynchosporium secalis in Tunisia as revealed by pathotype, AFLP, and microsatellite analyses

Abstract

Genetic variability among 122 Rhynchosporium secalis isolates collected from barley in three regions of Tunisia was investigated using host differentials, amplified fragment length polymorphism (AFLP), and microsatellite markers. The isolates were collected from a widely grown scald-susceptible barley cultivar Rihane and a range of local landrace cultivars in geographically distinct regions with different agroclimatic conditions. Pathotypic diversity (the proportion of unique pathotypes) was high in R. secalis populations from the high (100% diversity), moderate (95%), and low (100%) rainfall areas of Tunisia, and from both Rihane (which is the sole variety grown in the high rainfall region) and local landraces (which predominate in the low rainfall area). This may reflect a general adaptability for aggressiveness and suggests that the widely grown cultivar Rihane has exerted little or no selection pressure on the pathogen population since its release in 1983. Genotypic diversity (GD), defined as the probability that two individuals taken at random had different genotypes, was high for populations from Rihane, local landraces, and different agro-ecological zones (GD = 0.96–0.99). There was low genetic differentiation among pathogen populations from different host populations (G ST ≤ 0.08, θ ≤ 0.12) and agro-ecological zones (G ST ≤ 0.05, θ ≤ 0.04), which may be partly explained by gene flow due to the movement of infected stubble around the country. There was no correlation (r = 0.06, P = 0.39) between virulence phenotype and AFLP haplotype. A phenetic tree revealed groups with low bootstrap values that did not reflect the grouping of isolates based on host, pathotype, or agro-ecological region. The implications of these findings for R. secalis evolutionary potential and scald-resistance breeding in Tunisia are discussed.

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References

  1. 1.

    Xi K, Xue A, Burnett PA, Helm JH, Turkington TK. Quantitative resistance of barley cultivars to Rhynchosporium secalis. Can J Plant Pathol 2000;22:217–23.

    Article  Google Scholar 

  2. 2.

    Yahyaoui AH. Occurrence of barley leaf blights in Central Western Asia and North Africa. In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B, editors. Meeting the challenges of barley blights. Proceedings of the 2nd international workshop on barley leaf blights, 7–11 April 2002. Aleppo, Syria: ICARDA, 2004. p. 13–8.

  3. 3.

    Edney MJ, Choo TM, Kong D, Ferguson TH, Ho KM, May KW, Martin RA. Kernel colour varies with cultivars and environments in barley. Can J Plant Sci 1998;78:217–22.

    Google Scholar 

  4. 4.

    Barr AR, Eglinton JK, Wallwork H, Williams K, Davies PA, Jefferies SP, Brown T. Breeding barley varieties with durable resistance—can the new technologies improve the odds? In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B, editors. Meeting the challenges of barley blights. Proceedings of the 2nd international workshop on barley leaf blights, 7–11 April 2002. Aleppo, Syria: ICARDA; 2004. p. 165–86.

  5. 5.

    Habgood M. Variation in Rhynchosporium secalis. Trans Br Mycol Soc 1973;61:41–7.

    Google Scholar 

  6. 6.

    Williams K, Donnellan S, Smyl C, Scott L, Wallwork H. Molecular variation in Rhynchosporium secalis isolates obtained from hotspots. Australia Plant Pathol 2003;32:257–62.

    Article  CAS  Google Scholar 

  7. 7.

    Jackson LF, Webster RK. The dynamics of a controlled population of Rhynchosporium secalis, changes in race composition and frequencies. Phytopathology 1976a;66:726–8.

    Article  Google Scholar 

  8. 8.

    Newman P, Owen H. Evidence of asexual recombination in Rhynchosporium secalis. Plant Pathol 1985;34:338–40.

    Article  Google Scholar 

  9. 9.

    Newton A. Somatic recombination in Rhynchosporium secalis. Plant Pathol 1989;38:71–4.

    Article  Google Scholar 

  10. 10.

    Linde CC, Zala M, Ceccarelli S, McDonald BA. Further evidence for sexual reproduction in Rhynchosporium secalis based on distribution and frequency of mating-type alleles. Fungal Genet Biol 2003;40:115–25.

    PubMed  Article  CAS  Google Scholar 

  11. 11.

    McDonald BA, Zhan J, Burdon J. Genetic structure of Rhynchosporium secalis in Australia. Phytopathology 1999;89:639–45.

    PubMed  CAS  Google Scholar 

  12. 12.

    Salamati S, Zhan J, Burdon JJ, McDonald B. The genetic structure of field populations of Rhynchosporium secalis from three continents suggests moderate gene flow and regular recombination. Phytopathology 2000;90:901–8.

    CAS  PubMed  Google Scholar 

  13. 13.

    Tekauz A Pathogenic variation in Rhynchosporium secalis on barley in Canada. Can J Plant Pathol 1991;13:298–304.

    Article  Google Scholar 

  14. 14.

    Ali SM, Mayfield AH, Clare BG. Pathogenicity of 203 isolates of Rhynchosporium secalis on 21 barley cultivars. Plant Pathol 1976;9:135–43.

    Google Scholar 

  15. 15.

    Xi K, Xue A, Turkington TK, Helm JH, Bos C. Pathogenic variation of Rhynchosporium secalis in Alberta. Can J Plant Pathol 2002;24:176–83.

    Article  Google Scholar 

  16. 16.

    Fukuyama T, Yamaji S, Nakamura H. Differentiation of virulence in Rhynchosporium secalis in the Hokuriku district and sources of resistance to the pathogen. Breed Sci 1998;48:23–8.

    Google Scholar 

  17. 17.

    Kiros-Meles A, Udupa S, Abang MM, Abu-Blan H, Baum M, Ceccarelli S, Yahyaoui AH. Amplified fragment length polymorphism among Rhynchosporium secalis isolates collected from a single barley field in Syria. Ann Appl Biol 2005;146:389–94.

    Article  CAS  Google Scholar 

  18. 18.

    Newton AC, Searle J, Guy DC, Hackett CA, Cooke D. Variability in pathotype, aggressiveness, RAPD profile, and rDNA ITSI sequence of UK isolates of Rhynchosporium secalis. Zeitschrift Pflanzenkrankheiten Pflanzenschutz 2001;108:446–58.

    CAS  Google Scholar 

  19. 19.

    Zaffarano PL, McDonald BA, Zala M, Linde CC. Global hierarchical gene diversity analysis suggests the Fertile Crescent is not the center of origin of the barley scald pathogen Rhynchosporium secalis. Phytopathology 2006;96:941–50.

    CAS  PubMed  Google Scholar 

  20. 20.

    Abang MM, Baum M, Ceccarelli S, Grando S, Linde CC, Yahyaoui A, Zhan J, McDonald BA. Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle. Phytopathology 2006;96:1214–22.

    PubMed  Google Scholar 

  21. 21.

    Dinoor A, Eshed N. The analysis of host and pathogen populations in natural ecosystems. In: Wolfe MS, Caten CE editors. Populationsn of plant pathogens: their dynamics and genetics. Oxford: Blackwell Scientific Publications, 1987. p. 75–88.

    Google Scholar 

  22. 22.

    Montarry J, Corbiere R, Lesueur S, Glais I, Andrivon D. Does selection by resistant hosts trigger local adaptation in plant-pathogen systems? J Evol Biol 2006;19:522–31.

    PubMed  Article  CAS  Google Scholar 

  23. 23.

    Zhan J, Mundt CC, Hoffer ME, McDonald BA. Local adaptation and effect of host genotype on the evolution of virulence: an experimental test in a plant pathosystem. J Evol Biol 2002;15:634–47.

    Google Scholar 

  24. 24.

    McDonald BA, Linde C. Pathogen population genetics, evolutionary potential and durable resistance. Annu Rev Phytopathol 2002;40:349–79.

    PubMed  Article  CAS  Google Scholar 

  25. 25.

    Linde CC, Zala M, Mcdonald BA. Isolation and characterization of microsatellite loci from the barley scald pathogen, Rhynchosporium secalis. Mol Ecol Notes 2005;5:546–8.

    Article  CAS  Google Scholar 

  26. 26.

    von Korff M, Udupa SM, Yahyaoui A, Baum M. Genetic variation among Rhynchosporium secalis populations of West Asia and North Africa as revealed by RAPD and AFLP analysis. J Phytopathol 2004;152:106–13.

    Article  Google Scholar 

  27. 27.

    Bouajila A, Haouas S, Fakhfakh M, Rezgui S, El Ahmed M, Yahyaoui A. Pathotypic diversity of Rhynchosporium secalis (Oudem) in Tunisia. Afr J Biotechnol 2006;5:570–9.

    Google Scholar 

  28. 28.

    Zadoks JC, Chang TT, Conzak CF. A decimal code for the growth stages of cereals. Weed Res 1974;14:415–21.

    Article  Google Scholar 

  29. 29.

    Ceoloni C. Race differentiation and search for sources of resistance to Rhynchosporium secalis in barley in Italy. Euphytica 1980;29:547–53.

    Article  Google Scholar 

  30. 30.

    Vos P, Hogers R, Bleeker M, Reijans M, Van der Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 1995;23:4407–14.

    PubMed  Article  CAS  Google Scholar 

  31. 31.

    Kumar S, Tamura K, Nei M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 2004;5:150–63.

    PubMed  Article  CAS  Google Scholar 

  32. 32.

    Bonnet E, Van de Peer Y. Zt: a software tool for simple and partial Mantel tests. J Stat Software 2002;7:1–12.

    Google Scholar 

  33. 33.

    Hoffmann RJ. Variation in contributions of asexual reproduction to the genetic structure of populations of the sea anemone Metridium senile. Evolution 1986;40:357–65.

    Article  Google Scholar 

  34. 34.

    Agapow P-M, Burt A. Indices of multilocus linkage disequilibrium. Mol Ecol Notes 2001;1:101–2.

    Article  CAS  Google Scholar 

  35. 35.

    Yeh FC, Boyle TJB. Population genetic analysis of co-dominant and dominant markers and quantitative traits. Belgian J Bot 1997;129:157.

    Google Scholar 

  36. 36.

    Nei M. Estimation of average heterozygosity and genetic distance from a small number of samples. Genetics 1978;89:583–90.

    PubMed  CAS  Google Scholar 

  37. 37.

    Nei M. Analysis of gene diversity in subdivided populations. Proc Nat Acad Sci USA 1973;70:3321–3.

    PubMed  Article  CAS  Google Scholar 

  38. 38.

    Weir BS. Genetic data analysis II. Sunderland, MA, USA: Sinauer Associates Inc. Publishers; 1996.

    Google Scholar 

  39. 39.

    Wright S. The genetical structure of populations. Ann Eugenics 1951;15:323–54.

    Google Scholar 

  40. 40.

    McDermott JM, McDonald BA. Gene flow in plant pathosystems. Annu Rev Phytopathol 1993;31:353–73.

    Article  Google Scholar 

  41. 41.

    Williams RJ, Owen H. Physiologic races of Rhynchosporium secalis in Britain. Trans Br Mycol Soc 1973;65:223–34.

    Google Scholar 

  42. 42.

    Hsiang T, Ma XL, Yang L, Cook S. Analyses of RAPD data for detection of host specialization in Sclerotinia homoeocarpa. Plant Pathol 2000;49:269–75.

    Article  Google Scholar 

  43. 43.

    Molina-Cano JL, Fra-Mon P, Salcedo G, Aragoncillo C, Roca de Togores F, Garcia-Olmedo F. Morocco as a possible domestication center for barley: biochemical and agromorphological evidence. Theor Appl Genet 1987;73:531–6.

    Article  CAS  Google Scholar 

  44. 44.

    Molina-Cano JL, Moralejo M, Igartua E, Romagosa I. Further evidence supporting Morocco as a centre of origin of barley. Theor Appl Genet 1999;98:913–8.

    Article  Google Scholar 

  45. 45.

    Cromey MG, Mulholland RI. Host specialization of Rhynchosporium secalis in New Zeland. J Agric Res 1987;30:345–8.

    Google Scholar 

  46. 46.

    Goodwin SB, Allard RW, Hardy SA, Webster RK. Hierarchical structure of pathogenic variation among Rhynchosporium secalis populations in Idaho and Oregon. Can J Bot 1992;70:810–7.

    Google Scholar 

  47. 47.

    Jørgensen HJ, Smedegaard-Petersen V. Pathogenic variation of Rhynchosporium secalis in Denmark and sources of resistance in barley. Plant Dis 1995;79:297–301.

    Article  Google Scholar 

  48. 48.

    Kelemu S, Badel JL, Moreno CX, Miles JW, Chakraborty S, Fernandes CD, Charchar MJ D’A. Biodiversity, epidemiology and virulence of Colletotrichum gloeosporioides. I. Genetic and pathogenic diversity in Colletotrichum gloeosporioides isolates from Stylosanthes guianensis. Trop Grasslands 1997;31:387–92.

    Google Scholar 

  49. 49.

    Kelemu S, Skinner DZ, Badel JL, Moreno CX, Rodríguez MX, Fernandes CD, Charchar MJ, Chakraborty S. Genetic diversity in South American Colletotrichum gloeosporioides isolates from Stylosanthes guianensis, a tropical forage legume. Eur J Plant Pathol 1999;105:261–72.

    Article  CAS  Google Scholar 

  50. 50.

    Weeds PL, Chakraborty S, Fernandes CD, Charchar MJd’A, Ramesh CR, Kexian Y, Kelemu S. Genetic diversity in Colletotrichum gloeosporioides from Stylosanthes spp. at centers of origin and utilization. Phytopathology 2003;93:176–85.

    CAS  PubMed  Google Scholar 

  51. 51.

    Keller SM, Wolfe MS, McDermott JM, McDonald BA. High genetic similarity among populations of Phaeosphaeria nodorum across cultivars and regions in Switzerland. Phytopathology 1997;87:1134–9.

    PubMed  CAS  Google Scholar 

  52. 52.

    Trail F, Xu H, Loranger R, Gadoury D. Physiological and environmental aspects of ascospore discharge in Gibberella zeae (anamorph Fusarium graminicearum). Mycologia 2002;94:181–9.

    Article  Google Scholar 

  53. 53.

    Jackson LF, Webster RK. Seed and grasses as possible sources of Rhynchosporium secalis for barley in California. Plant Dis Rep 1976b;60:233–6.

    Google Scholar 

  54. 54.

    Kay JG, Owen H. Transmission of Rhynchosporium secalis on barley grain. Trans Br Mycol Soc 1973;60:405–11.

    Article  Google Scholar 

  55. 55.

    Shipton WA, Boyd WJR, Ali SM. Scald of barley. Rev Plant Pathol 1974;53:840–61.

    Google Scholar 

  56. 56.

    Grünwald NJ, Goodwin SB, Milgroom MG, Fry WE. Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 2003;93:738–46.

    Google Scholar 

Download references

Acknowledgments

A. Bouajila was funded through a PhD research fellowship from DANIDA-ICDM Project. The research was also supported in part by the International Center for Agricultural Research in the Dry Areas (ICARDA) and the Phytopathology Group, Institute of Integrative Biology, ETH, Zurich.

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Correspondence to Amor Yahyaoui.

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Bouajila, A., Abang, M.M., Haouas, S. et al. Genetic diversity of Rhynchosporium secalis in Tunisia as revealed by pathotype, AFLP, and microsatellite analyses. Mycopathologia 163, 281–294 (2007). https://doi.org/10.1007/s11046-007-9012-0

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Keywords

  • AFLP
  • Barley scald
  • Genetic structure
  • Microsatellites
  • Pathotype
  • Rhynchosporium secalis