Abstract
Pyrenophora teres f. teres (Ptt) is the causal agent of net form of net blotch (NFNB) – a major foliar disease of barley (Hordeum vulgare) crops worldwide. Deployment of genetic resistance in cultivars is the preferred method of control, but requires knowledge of the pathogenic variation of Ptt to be effective as spatial and temporal variation is common. In this study, 123 Ptt isolates collected from five states across Australia were examined for pathogenic variation using a set of 31 barley genotypes, composed of 11 international genotypes and 20 Australian cultivars. Barley seedlings were inoculated with spore suspensions from monoconidial isolate cultures and scored for infection response. Phenotypes were used to perform hierarchical cluster analysis for barley genotypes and Ptt isolates. Cluster analysis identified seven line groups, each containing barley genotypes that displayed similar responses to the Ptt isolates. Isolates clustered into four distinct isolate groups shown to harbour differential virulence to four key genotypes: Maritime, Prior, Skiff and Tallon. Isolates with virulence to any one of these genotypes accounted for 96.7% of the samples. Differential virulence was observed on a range of genotypes within each isolate group. The composition of isolate groups in eastern Australia was distinct from Western Australia, whereas all isolate groups were detected in southern Australia. Results suggest that cultivation of regionally adapted barley cultivars has led to regional evolution of Ptt, where the pathogen acquires virulence specific for resistance factors deployed in local cultivars. Detection of Ptt modern isolates that were highly virulent to historic cultivars indicates the long-term survival of virulence gene combinations in the pathogen population.
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References
Afanasenko OS, Jalli M, Pinnschmidt HO, Filatova O, Platz G (2009) Development of an international standard set of barley differential genotypes for Pyrenophora teres f. teres. Plant Pathol 58:665–676
Akhavan A, Turkington TK, Askarian H, Tekauz A, Xi K, Tucker JR, Kutcher HR, Strelkov SE (2016) Virulence of Pyrenophora teres populations in western Canada. Can J Plant Pathol 1–14
Arabi MIE, Al-Safadi B, Charbaji T (2003) Pathogenic variation among isolates of Pyrenophora teres, the causal agent of barley net blotch. J Phytopathol 151:376–382
Beattie AD, Scoles GJ, Rossnagel BG (2007) Identification of molecular markers linked to a Pyrenophora teres avirulence gene. Phytopathology 97:842–849
Bouajila A, Zoghlami N, Al Ahmed M, Baum M, Ghorbel A, Nazari K (2011) Comparative virulence of Pyrenophora teres f. teres from Syria and Tunisia and screening for resistance sources in barley: implications for breeding. Lett Appl Microbiol 53:489–502
Boungab K, Belabid L, Fortas Z, Bayaa B (2012) Pathotype diversity among Algerian isolates of Pyrenophora teres f. teres. Phytopathol Mediterr 51
Cakir M, Gupta S, Platz GJ, Ablett GA, Loughman R, Emebiri LC, Poulsen D, Li CD, Lance RC, Galwey NW, Jones MG (2003) Mapping and validation of the genes for resistance to Pyrenophora teres f. teres in barley (Hordeum vulgare L.). Crop Pasture Sci 54:1369–1377
Cakir M, Gupta S, Li C, Hayden M, Mather DE, Ablett GA, Platz GJ, Broughton S, Chalmers KJ, Loughman R, Jones MG (2011) Genetic mapping and QTL analysis of disease resistance traits in the barley population Baudin × AC Metcalfe. Crop Pasture Sci 62:152–161
Cromey M, Parkes R (2003) Pathogenic variation in Drechslera teres in New Zealand. N Z Plant Prot 56:251–256
De Mendiburu F (2014) Agricolae: statistical procedures for agricultural research. R Packag Version 1:1–6
Deimel H, Hoffmann G (1991) Detrimental effects of net blotch disease to barley plants caused by Drechslera teres (Sacc.) Shoemaker. Zeitschrift fuer Pflanzenkrankheiten und Pflanzenschutz 98:137–161
Douiyssi A, Rasmusson D, Roelfs A (1998) Responses of barley cultivars and lines to isolates of Pyrenophora teres. Plant Dis 82:316–321
ElMor IM (2016) Investigating the virulence of isolates produced by sexual recombination between different Pyrenophora teres isolates. Doctorial dissertation. University of Southern Queensland
Friesen T, Faris J, Lai Z, Steffenson B (2006) Identification and chromosomal location of major genes for resistance to Pyrenophora teres in a doubled-haploid barley population. Genome 49:855–859
Friesen TL, Meinhardt SW, Faris JD (2007) The Stagonospora nodorum-wheat pathosystem involves multiple proteinaceous host-selective toxins and corresponding host sensitivity genes that interact in an inverse gene-for-gene manner. Plant J 51:681–692
Gupta S, Loughman R (2001) Current virulence of Pyrenophora teres on barley in Western Australia. Plant Dis 85:960–966
Jalli M (2010) The virulence of Finnish Pyrenophora teres f. teres isolates and its implications for resistance breeding. MTT Agrifood Research Finland
Jebbouj R, El Yousfi B (2009) Barley yield losses due to defoliation of upper three leaves either healthy or infected at boot stage by Pyrenophora teres f. teres. Eur J Plant Pathol 125:303–315
Jebbouj R, El Yousfi B (2010) An integrated multivariate approach to net blotch of barley: Virulence quantification, pathotyping and a breeding strategy for disease resistance. Eur J Plant Pathol 127:521–544
Jonsson R, Bryngelsson T, Jalli M, Gustafsson M (1998) Effect of growth stage on resistance to Drechslera teres f. teres in barley. J Phytopathol 146:261–265
Jordan VWL (1981) Aetiology of barley net blotch caused by Pyrenophora teres and some effects on yield. Plant Pathol 30:77–87
Khan TN (1982) Changes in pathogenicity of Drechslera teres relating to changes in barley cultivars grown in Western Australia. Plant Dis 66:655–656
Khan TN (1987) Relationship between net blotch (Drechslera teres) and losses in grain yield of barley in Western Australia. Crop Pasture Sci 38:671–679
Khan TN, Boyd WJR (1969) Physiologic specialization in Drechslera teres. Aust J Biol Sci 22:1229–1236
Koladia VM, Faris JD, Richards JK, Brueggeman RS, Chao S, Friesen TL (2017) Genetic analysis of net form net blotch resistance in barley lines CIho 5791 and Tifang against a global collection of P. teres f. teres isolates. Theor Appl Genet 130:163–173. doi:10.1007/s00122-016-2801-4
König J, Perovic D, Kopahnke D, Ordon F (2013) Development of an efficient method for assessing resistance to the net type of net blotch (Pyrenophora teres f. teres) in winter barley and mapping of quantitative trait loci for resistance. Mol Breed 32:641–650. doi:10.1007/s11032-013-9897-x
Lamari L, Bernier CC (1989) Toxin of Pyrenophora tritici-repentis: host-specificity, significance in disease, and inheritance of host reaction. Phytopathology 79:740–744
Lehmensiek A, Platz GJ, Mace E, Poulsen D, Sutherland MW (2008) Mapping of adult plant resistance to net form of net blotch in three Australian barley populations. Crop Pasture Sci 58:1191–1197
Liu Z, Ellwood SR, Oliver RP, Friesen TL (2011) Pyrenophora teres profile of an increasingly damaging barley pathogen. Mol Plant Pathol 12:1–19
Liu ZH, Zhong S, Stasko AK, Edwards MC, Friesen TL (2012) Virulence profile and genetic structure of a North Dakota population of Pyrenophora teres f. teres, the causal agent of net form net blotch of barley. Phytopathology 102:539–546
Ma ZQ, Lapitan NLV, Steffenson BJ (2004) QTL mapping of net blotch resistance genes in a doubled-haploid population of six-rowed barley. Euphytica 137:291–296. doi:10.1023/B:EUPH.0000040441.36990.58
Murray GM, Brennan JP (2010) Estimating disease losses to the Australian barley industry. Australas Plant Pathol 39:85–96
Piening L, Kaufmann ML (1969) Comparison of the effects of net blotch and leaf removal on yield in barley. Can J Plant Sci 49:731–735
Platz GJ, Bell KL, Rees RG, Galea VJ (2000) Pathotype variation of the Australian net blotch population. In: 8th International Barley Genetics Symposium, 2000. Adelaide University, Waite Campus, pp 160–162
Qamar MA, Liu ZH, Faris JD, Chao S, Edwards MC, Lai Z, Franckowiak JD, Friesen TL (2008) A region of barley chromosome 6H harbors multiple major genes associated with net type net blotch resistance. Theor Appl Genet 117:1261–1270
Raman H, Platz GJ, Chalmers KJ, Raman R, Read BJ, Barr AR, Moody DB (2003) Mapping of genomic regions associated with net form of netblotch resistance in barley. Crop Pasture Sci 54:1359–1367
Richter K, Schondelmaier J, Jung C (1998) Mapping of quantitative trait loci affecting Drechslera teres resistance in barley with molecular markers. Theor Appl Genet 97:1225–1234
Robinson J, Jalli M (1996) Diversity among Finnish net blotch isolates and resistance in barley. Euphytica 92:81–87
Robinson J, Jalli M (1997) Quantitative resistance to Pyrenophora teres in six Nordic spring barley accessions. Euphytica 94:201–208. doi:10.1023/A:1002996722383
RStudio (2015) RStudio: integrated development for R. Version 0.98.507. Boston, MA: RStudio. Available at: http://www.rstudio.com
Shjerve RA, Faris JD, Brueggeman RS, Yan C, Zhu Y, Koladia V, Friesen TL (2014) Evaluation of a Pyrenophora teres f. teres mapping population reveals multiple independent interactions with a region of barley chromosome 6H. Fungal Genet Biol 70:104–112
Shoemaker RA (1962) Drechslera Ito. Can J Bot 40:809–836
Smedegård-Petersen V (1974) Reduction in yield and grain size of barley due to attack by the net blotch fungus Pyrenophora teres. R Vet Agric Univ Copenhagen, Den, Yearb 1974:108–117
Smedegård-Petersen V (1977) Isolation of two toxins produced by Pyrenophora teres and their significance in disease development of net-spot blotch of barley. Physiol Plant Pathol 10:203–211
Smith A, Cullis B, Thompson R (2001) Analyzing variety by environment data using multiplicative mixed models and adjustments for spatial field trend. Biometrics 57:1138–1147
Smith AB, Lim P, Cullis BR (2006) The design and analysis of multi-phase plant breeding experiments. J Agric Sci 144:393–409
Somers DJ, Manninen OM, Jalli M, Kalendar R, Schulman A, Afanasenko O, Robinson J (2006) Mapping of major spot-type and net-type net-blotch resistance genes in the Ethiopian barley line CI 9819. Genome 49:1564–1571
Speakman JB, Pommer EH (1986) A simple method for producing large volumes of Pyrenophora teres spore suspension. Bull Br Mycol Soc 20:129–130
Steffenson BJ, Webster RK (1992a) Pathotype diversity of Pyrenophora teres f. teres on barley. Phytopathology 82:170–177
Steffenson BJ, Webster RK (1992b) Quantitative resistance to Pyrenophora teres f. teres in barley. Phytopathology 82:407–411
Steffenson BJ, Webster RK, Jackson LF (1991) Reduction in yield loss using incomplete resistance to Pyrenophora teres f. teres in barley. Plant Dis 75:96–100
Steffenson BJ, Hayes PM, Kleinhofs A (1996) Genetics of seedling and adult plant resistance to net blotch (Pyrenophora teres f. teres) and spot blotch (Cochliobolus sativus) in barley. Theor Appl Genet 92:552–558
Sutton JC, Steele P (1983) Effects of seed and foliar fungicides on progress of net blotch and yield in barley. Can J Plant Sci 63:631–639
Tekauz A (1985) A numerical scale to classify reactions of barley to Pyrenophora teres. Can J Plant Pathol 7:181–183
Tekauz A (1990) Characterization and distribution of pathogenic variation in Pyrenophora teres f. teres and P. teres f. maculata from western Canada. Can J Plant Pathol 12:141–148
Tekauz A, Mills JT (1974) New types of virulence in Pyrenophora teres in Canada. Can J Plant Sci 54:731–734
Tuohy JM, Jalli M, Cooke BM, O’Sullivan E (2006) Pathogenic variation in populations of Drechslera teres f. teres and D. teres f. maculata and differences in host cultivar responses. Eur J Plant Pathol 116:177–185
Usher T, Delacy I, Barsby J, Platz G Rapid detection of adult plant resistance to net form net blotch. In: 14th Australian Barley Technical Symposium, Sunshine Coast, Australia, 13–16 September 2009, 2009.
Wallwork H, Butt M, Capio E (2016) Pathogen diversity and screening for minor gene resistance to Pyrenophora teres f. teres in barley and its use for plant breeding. Australas Plant Pathol 45:527–531. doi:10.1007/s13313-016-0433-4
Ward JH Jr (1963) Hierarchical grouping to optimize an objective function. J Am Stat Assoc 58:236–244
Weiland JJ, Steffenson BJ, Cartwright RD, Webster RK (1999) Identification of molecular genetic markers in Pyrenophora teres f. teres associated with low virulence on ‘Harbin’ barley. Phytopathology 89:176–181
Yoder OC, Gracen VE (1975) Segregation of pathogenicity types and host-specific toxin production in progenies of crosses between races T and O of Helminthosporium maydis (Cochliobolus heterostrophus). Phytopathology 65:273–276
Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421
Acknowledgements
The authors would like to thanks the Grains Research and Development Corporation of Australia for funding this research through the National Barley Foliar Pathogens project (DAQ00178). We would also like to thank the biometrics team in Toowoomba for their valued assistance in conducting data analyses. We also thank the barley scientific community for supplying disease samples, in particular Ciara Beard, Rob Evans, Rob Fromm, Sue Cartledge, I. Goss, Rick Graham, Christy Grime, Dr Sanjiv Gupta, Bruce Hempel, Peter Keys, Dr Mark McLean, Dr David Moody, John Nairn, Blakely Paynter, Richard Prusa, Brian Purdie, Dr Steven Simpendorfer, John Sturgess, Geoff Thomas, Peter Thompson, Ian Wallace and Dr Hugh Wallwork.
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Fowler, R.A., Platz, G.J., Bell, K.L. et al. Pathogenic variation of Pyrenophora teres f. teres in Australia. Australasian Plant Pathol. 46, 115–128 (2017). https://doi.org/10.1007/s13313-017-0468-1
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DOI: https://doi.org/10.1007/s13313-017-0468-1