Abstract
Plant diseases caused by seed-borne pathogens cause yield and quality losses and threaten seed production of barley (Hordeum vulgare L.) and food security. The aim of this study was to compare common seed health methods for the diagnosis and detection of Pyrenophora species, and to investigate cell wall degrading enzymes (CWDEs), virulence and aggressiveness of the isolates obtained from pre-basic barley seed fields in Iran. Comparing common seed health methods showed that more fungal isolates were recovered from seeds using the agar plate method compared to freezing blotter, osmotic, embryo count, and seed washing tests. A total of 7 fungal species from 5 genera were identified from 30 different samples of various Iranian barley cultivars. Based on morphological and molecular characteristics, the fungi were identified as Pyrenophora graminea, P. teres f. teres, P. teres f. maculata, Alternaria alternata, Fusarium culmorum, F. graminearum, Rhynchosporium commune and Ustilago nuda f. sp. hordei. This study has shown that barley seed samples carry a wide diversity of fungi. The results showed that the 57 % of the total samples were found to be infected by seed-borne fungi. Among the genera, Pyrenophora was the most abundant fungus. Diverse levels of virulence and aggressiveness were observed for various isolates of Pyrenophora species. Analyzing the activity of CWDEs produced by isolates revealed that xylanase activity was more important than cellulase activity for the virulence of Pyrenophora isolates and enzyme activities affect levels of virulence and aggressiveness of isolates. Therefore, these findings suggest that activity levels of xylanase are correlated with variation in virulence and aggressiveness of Pyrenophora isolates on seedings. This is the first report identifying the seed-borne fungi of Iranian barley cultivars in pre-basic barley seed fields of Iran.
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The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aghnoum R (2019) Leaf stripe disease management in Barley. Ministry of Jihad-e-Agriculture, Agricultural Research Education and Extention Organization
Anonymous (2022). International Seed Testing Association (ISTA); International Rules for Seed Testing. Chapter 7: Validated Seed Health Testing Methods. In K. Sperlingsson & G. Brodal (Eds.), 7-027: Detection of Pyrenophora teres and Pyrenophora graminea in Hordeum vulgare subsp. vulgare (barley) seed. Bassersdorf, Switzerland: International Seed Testing Association; 2022. Available from: https://www.seedtest.org/api/rm/TT74P4C725A2QMV/7-013a-detection-of-ustilago-nuda-in-hordeum-vulga-1.pdf
Ariyawansa HA, Kang JC, Alias SA, Chukeatirote E, Hyde KD (2014) Pyrenophora. Mycosphere 5:351–362
Backes A, Guerriero G, Barka EA, Jacquard C (2021) Pyrenophora teres: Taxonomy, morphology, interaction with Barley, and mode of control. Frontiers in Plant Science 12:614951
Bakri Y, Akeed Y, Jawhar M, Arabi MIE (2020) Evaluation of xylanase production from filamentous fungi with different lifestyles. Acta Alimentaria 49:197–203
Bayraktar H, Akan K (2012) Genetic characterization of Pyrenophora graminea isolates and the reactions of some barley cultivars to leaf stripe disease under greenhouse conditions. Turkish Journal of Agricultural Science 36:329–339
Benkorteby-lyazidi H, Zeghar I, Hanifi-Mekliche L, Bouznad Z (2019) Barley leaf stripe disease in Algeria: evaluation of virulent Pyrenophora graminea isolates and identification of resistant Algerian barley genotypes. Journal of Agricultural Science 25:367–372
Cao T, Kim YM, Kav NNV, Strelkov SE (2009) A proteomic evaluation of Pyrenophora tritici-repentis, causal agent of tan spot of wheat, reveals major differences between virulent and avirulent isolates. Proteomics 9:1177–1196
Çelik Y, Karakaya A, Çelik Oğuz A, Mert Z, Akan K, Ergün N, Sayim İ (2016) Determination of the reactions of some barley landraces and cultivars to Drechslera graminea. Mediterranean agricultural sciences 29:43–47
Dokhanchi H, Babai-Ahari A, Arzanlou M (2020) Distribution of mating type alleles in Iranian populations of Pyrenophora graminea, the causal agent of barley leaf stripe disease, using a multiplex PCR approach. European Journal of Plant Pathology 156:343–354
El-Mor IM, Fowler RA, Platz GJ, Sutherland MW, Martin A (2018) An improved detached-leaf assay for phenotyping net blotch of barley caused by Pyrenophora teres. Plant Disease 102:760–763
Etebarian HR (2002) Evaluation of barley cultivars for resistance to leaf stripe. Plant Prot Sci 38:170–173. https://doi.org/10.17221/10347-PPS
Friis P, Olsen CE, Mallert BL (1991) Toxin production in Pyrenophora teres, the ascomycete causing the net-spot blotch disease of Barley (Hordeum vulgare L.). Journal of Biological Chemistry 266:13329–13335
Gangwar OP, Bhardwaj SC, Singh GP, Prasad P, Kumar S (2018) Barley disease and their management: an Indian perspective. Wheat and Barley Research 10:138–150
Gubiš J, Hudcovicová M, Klčová L, Červená V, Bojnanská K, Kraic J (2004) Detection of leaf blotches – causal agents in barley leaves and grains. Czech Journal of Genetics and Plant Breeding 40:111–117
Ismail IA, Godfrey D, Able AJ (2014) Proteomic analysis reveals the potential involvement of xylanase from Pyrenophora teres f. teres in net form net blotch disease of barley. Australasian Plant Pathology 43:715–726
Jalli M, Laitinen P, Latvala S (2011) The emergence of cereal fungal diseases and the incidence of leaf spot diseases in Finland. Agricultural and Food Science 20:62–73
Jawhar M, Arabi MIE (2006) Genetic variability among Pyrenophora graminea isolates. Australas Plant Pathol 35:279–281. https://doi.org/10.1071/AP06001
Khaledi N, Taheri P, Falahati-Rastegar M (2017) Identification, virulence factors characterization and analysis virulence together with aggressiveness of Fusarium spp., causing wheat head blight in Iran. European Journal of Plant Pathology 147:897–918
Lannou C (2012) Variation and selection of quantitative traits in plant pathogens. Annual Review of Phytopathology 50:319–338
Leslie JF, Summerell BA (2006) The Fusarium laboratory manual, 1st edn. Blackwell Publishing Ltd, London.
Lightfoot DJ, Able AJ (2010) Growth of Pyrenophora teres in planta during barley net blotch disease. Australasian Plant Pathology 39:499–507
Liu Z, Ellwood SR, Oliver RP, Friesen TL (2011) Pyrenophora teres: profile of an increasingly damaging barley pathogen. Molecular Plant Pathology 12:1–19
Manning VA, Pandelova I, Dhillon B, Wilhelm LJ, Goodwin SB, Berlin AM, Figueroa M, Freitag M, Hane JK, Henrissat B, Holman WH, Kodira CD, Martin J, Oliver RP, Robbertse B, Schackwitz W, Schwartz DC, Spatafora JW, Turgeon BG et al (2013) Comparative genomics of a plant-pathogenic fungus, Pyrenophora tritici-repentis, reveals transduplication and the impact of repeat elements on pathogenicity and population divergence G3 (Bethesda) 3:41–63
Martin A, Moolhuijzen P, Tao Y, McIlroy J, Ellwood SR, Fowler RA, Platz GJ, Kilian A, Snyman L (2020) Genomic regions associated with virulence in Pyrenophora teres f. teres identified by genome-wide association analysis and biparental mapping. Phytopathology 110:881–891
Mathur SB, Kongsdal O (2003) Common laboratory seed health testing methods for detecting fungi. International Seed Testing Association, Basseradorf, Switzerland.
Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Molecular Plant Pathology 10:311–324
Murray TD, Parry DW, Cattlin ND (2009) Diseases of small grain cereal crops: a colour handbook. Manson Publishing, London
Pecchioni N, Faccioli P, Toubia-Rahme H, Valè G, Terzi V (1996) Quantitative resistance to barley leaf stripe (Pyrenophora graminea) is dominated by one major locus. Theoretical and Applied Genetics 93:97–101
Porta-Puglia A, Delogu G, Vannacci G (1986) Pyrenophora graminea on winter barley seed: effect on disease incidence and yield losses. Phytopathology 117:26–33
Ronen M, Sela H, Fridman E, Perl-Treves R, Kopahnke D, Moreau A, Ben-David R, Harel A (2019) Characterization of the barley net blotch pathosystem at the center of origin of host and pathogen. Pathogens 8:1–16
Sarpeleh A, Tate ME, Wallwork H, Catcheside D, Able AJ (2009) Characterisation of low molecular weight phytotoxins isolated from Pyrenophora teres. Physiological and Molecular Plant Pathology 73:154–162
Sarpeleh A, Wallwork H, Catcheside DEA, Tate ME, Able AJ (2007) Evidence of involvement of proteinaceous toxins from Pyrenophora teres in symptom development of net blotch of barley. Phytopathology 97:907–915
Si E, Meng Y, Ma X, Li B, Wang J, Ren P, Yao L, Yang K, Zhang Y, Shang X, Wang H (2019) Development and characterization of microsatellite markers based on whole-genome sequences and pathogenicity differentiation of Pyrenophora graminea, the causative agent of barley leaf stripe. European Journal of Plant Pathology 154:227–241
Simmons EG (2007) Alternaria: an identification manual. CBS, Utrecht
Stefansson TS, Hallsson JH (2011) Analysis of the species diversity of leaf pathogens in Icelandic barley fields. Icelandic Agricultural Sciences 24:13–23
Taylor EJA, Stevens EA, Bates JA, Morreal G, Lee D, Kenyon DM, Thomas JE (2001) Rapid-cycle PCR detection of Pyrenophora graminea from barley seed. Plant Pathology 50:347–355
Tobias TB, Farrer EC, Rosales A, Sinsabaugh RL, Suding KN, Porras-Alfaro A (2017) Seed-associated fungi in the alpine tundra: both mutualists and pathogens could impact plant recruitment. Fungal Ecol 30:10–18
Turkington TK, Clear RM, Burnett PA, Xi K (2002) Fungal plant pathogens infecting barley and wheat seed from Alberta, 1995-1997. Canadian Journal of Plant Pathology 24:302–308
Vasighzadeh A, Sharifnabi B, Javan-Nikkhah M, Seifollahi E, Landermann-Habetha D, Feurtey A, Holtgrewe-Stukenbrock E (2021) Population genetic structure of four regional populations of the barley pathogen Pyrenophora teres f. maculata in Iran is characterized by high genetic diversity and sexual recombination. Plant Pathol 70:735–744
Vergara M, Cristani C, Vannacci G (2003) Differential transcripts in Pyrenophora graminea and Pyrenophora teres putatively related to pathogenicity. Journal of Plant Pathology 85:157–164
Walters DR, Avrova A, Bingham IJ, Burnett FJ, Fountaine J, Havis ND, Hoad SP, Hughes G, Looseley M, Oxley SJP, Renwick A, Topp CF, Newton AC (2012) Control of foliar diseases in barley: Towards an integrated approach. European Journal of Plant Pathology 133:33–73
Acknowledgements
This present research was financially supported by Seed and Plant Certification and Registration Institute (SPCRI), Iran (Grant Number: 2-08-08-004-000356).
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All authors contributed to the study conception and design. NK and LZ conducted the experiments and has written the manuscript. FH contributed in survey and sample collection. NK supervised and conceptualized the whole research project, also along with FH edited the manuscript. All authors read and approved the final manuscript
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Khaledi, N., Zare, L., Hassani, F. et al. Comparison of diagnostic methods, virulence and aggressiveness analysis of Pyrenophora spp. in pre-basic seeds in the barley fields. Trop. plant pathol. 49, 304–316 (2024). https://doi.org/10.1007/s40858-023-00631-3
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DOI: https://doi.org/10.1007/s40858-023-00631-3