Vol. 64 No. 2 (2025)
Articles

Survey for Pyrenophora teres and Ramularia collo-cygni in barley grain from Italy

PDF Suppl. Data
  • Emilio BALDUCCI,
  • Francesco TINI,
  • Laura ROHERIG,
  • Giovanni BECCARI,
  • Andrea ONOFRI,
  • Massimo MONTANARI,
  • Ilaria ALBERTI,
  • Antonio PRODI,
  • Neil D. HAVIS,
  • Paolo BENINCASA,
  • Lorenzo COVARELLI
Emilio BALDUCCI
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
Francesco TINI
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
Laura ROHERIG
Scotland’s Rural College (SRUC), King’s Buildings Campus, West Mains Road, Edinburgh, EH9 3JG, Scotland, UK
Giovanni BECCARI
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
Andrea ONOFRI
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
Massimo MONTANARI
Council for Agricultural Research and Economics (CREA) Research Centre for Cereal and Industrial Crops, Via di Corticella 133, 40128, Bologna, Italy
Ilaria ALBERTI
Council for Agricultural Research and Economics (CREA) Research Centre for Cereal and Industrial Crops, Via G. Amendola 82, 45100, Rovigo, Italy
Antonio PRODI
Department of Agricultural and Food Sciences, Alma Mater Studiorum, University of Bologna, Viale G. Fanin 44, 40127, Bologna, Italy
Neil D. HAVIS
Scotland’s Rural College (SRUC), King’s Buildings Campus, West Mains Road, Edinburgh, EH9 3JG, Scotland, UK
Paolo BENINCASA
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
Lorenzo COVARELLI
Department of Agricultural, Food and Environmental Sciences, University of Perugia, Borgo XX Giugno 74, 06121, Perugia, Italy
DOI: https://doi.org/10.36253/phyto-15998
Categories

Published 2025-09-12

Keywords

  • Cereals,
  • Net blotch,
  • Ramularia leaf spot,
  • qPCR

How to Cite

[1]
E. BALDUCCI, “Survey for Pyrenophora teres and Ramularia collo-cygni in barley grain from Italy”, Phytopathol. Mediterr., vol. 64, no. 2, pp. 255–269, Sep. 2025.

Copyright (c) 2025 Emilio BALDUCCI, Francesco TINI, Laura ROHERIG, Giovanni BECCARI, Andrea ONOFRI, Massimo MONTANARI, Ilaria ALBERTI, Antonio PRODI, Neil D. HAVIS, Paolo BENINCASA, Lorenzo COVARELLI

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

A 2 year study (2019/2020 and 2020/2021 growing seasons) investigated the occurrence and distribution of the barley pathogens Pyrenophora teres and Ramularia collo-cygni (Rcc) in grain in Italy. Pyrenophora teres occurs as two forms causing different host symptoms, P. teres f. teres (Ptt), causing net form net blotch and P. teres f. maculata (Ptm) causing spot form net blotch. Ramularia collo-cygni causes Ramularia leaf spot. Pyrenophora teres and R. collo-cygni cause significant economic damage to barley crops, and their seed-borne stages make their control challenging. Distribution of these two pathogens across different geographic regions was examined in 99 barley grain samples collected from northern, central or southern Italy, characterized by different climatic conditions. Fungal isolates from barley grains onto potato dextrose agar were identified using morphology and polymerase chain reaction (PCR) assays with species-specific primers, and amounts of fungal DNA in grain were quantified using quantitative real-time PCR (qPCR). Traditional isolation methods showed presence of Ptt, but did not provide information to assess Rcc distribution and infection levels, as no Rcc isolates were observed. The qPCR assays also revealed presence of Rcc over the two growing seasons, and amounts of Ptt DNA were greater than for Rcc, particularly in malting barley varieties in2019/2020. Presence of Ptm DNA within grain was detected in only two of the 99 grain samples.

PDF Suppl. Data

Downloads

Download data is not yet available.

References

  1. AHDB, 2018. Development of UK wide risk forecast scheme for Ramularia leaf spot in barley. UK’s Agriculture and Horticulture Development Board (AHDB). Available at: https://ahdb.org.uk/ramularia-leaf-spot-in-barley. Accessed October 21, 2024.
  2. Ahmed Lhadj W., Boungab K., Righi Assia F., Çelik Oğuz A., Karakaya A., Ölmez F., 2022. Genetic diversity of Pyrenophora teres in Algeria. Journal of Plant Pathology 104(1): 305–315. https://doi.org/10.1007/s42161-021-01010-0. DOI: https://doi.org/10.1007/s42161-021-01010-0
  3. Arabi M.I., Barrault G., Sarrafi A., Albertini L., 1992. Variation in the resistance of barley cultivars and in the pathogenicity of Drechslera teres f. sp. maculata and D. teres f. sp. teres isolates from France. Plant Pathology 41(2): 180–186. https://doi.org/10.1111/j.1365-3059.1992.tb02336.x. DOI: https://doi.org/10.1111/j.1365-3059.1992.tb02336.x
  4. Backes A., Guerriero G., Ait Barka E., Jacquard C., 2021. Pyrenophora teres: taxonomy, morphology, interaction with barley, and mode of control. Frontiers in Plant Science 12: 614951. https://doi.org/10.3389/fpls.2021.614951. DOI: https://doi.org/10.3389/fpls.2021.614951
  5. Bates J.A., Taylor E.J.A., Kenyon D.M., Thomas J.E., 2001. The application of real-time PCR to the identification, detection and quantification of Pyrenophora species in barley seed. Molecular Plant Pathology 2(1): 49–57. https://doi.org/10.1046/j.1364-3703.2001.00049.x. DOI: https://doi.org/10.1046/j.1364-3703.2001.00049.x
  6. Beccari G., Arellano C., Covarelli L., Tini F., Sulyok M., Cowger C., 2019. Effect of wheat infection timing on Fusarium head blight causal agents and secondary metabolites in grain. International Journal of Food Microbiology 290: 214–225. https://doi.org/10.1016/j.ijfoodmicro.2018.10.014. DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.10.014
  7. Beccari G., Caproni L., Tini F., Uhlig S., Covarelli L., 2016. Presence of Fusarium species and other toxigenic fungi in malting barley and multi-mycotoxin analysis by liquid chromatography–high-resolution mass spectrometry. Journal of Agricultural and Food Chemistry 64(21): 4390–4399. https://doi.org/10.1021/acs.jafc.6b00702. DOI: https://doi.org/10.1021/acs.jafc.6b00702
  8. Beccari G., Prodi A., Senatore M.T., Balmas V., Tini F., … Covarelli L., 2020. Cultivation area affects the presence of fungal communities and secondary metabolites in Italian durum wheat grains. Toxins 12(2): 97. https://doi.org/10.3390/toxins12020097. DOI: https://doi.org/10.3390/toxins12020097
  9. Beccari G., Prodi A., Tini F., Bonciarelli U., Onofri A., … Covarelli L., 2017. Changes in the Fusarium head blight complex of malting barley in a three-year field experiment in Italy. Toxins 9(4): 120. https://doi.org/10.3390/toxins9040120. DOI: https://doi.org/10.3390/toxins9040120
  10. Beccari G., Senatore M.T., Tini F., Sulyok M., Covarelli L., 2018. Fungal community, Fusarium head blight complex and secondary metabolites associated with malting barley grains harvested in Umbria, central Italy. International Journal of Food Microbiology 273: 33–42. https://doi.org/10.1016/j.ijfoodmicro.2018.03.005. DOI: https://doi.org/10.1016/j.ijfoodmicro.2018.03.005
  11. Bretz F., Hothorn T., Westfall P., 2011. Multiple Comparisons Using R. CRC Press Boca Raton, FL. https://doi.org/10.1201/9781420010909. DOI: https://doi.org/10.1201/9781420010909
  12. Burlakoti R.R., Gyawali S., Chao S., Smith K.P., Horsley R.D., … Neate S.M., 2017. Genome-wide association study of spot form of net blotch resistance in the Upper Midwest barley breeding programs. Phytopathology 107(1): 100–108. https://doi.org/10.1094/PHYTO-03-16-0136-R. DOI: https://doi.org/10.1094/PHYTO-03-16-0136-R
  13. Campbell G.F., Lucas J.A., Crous P.W., 2002. Evidence of recombination between net- and spot-type populations of Pyrenophora teres as determined by RAPD analysis. Mycological Research 106(5): 602–608. https://doi.org/10.1017/S0953756202005853. DOI: https://doi.org/10.1017/S0953756202005853
  14. Carmona M., Barreto D., Moschini R., Reis E.M., 2008. Epidemiology and control of seed-borne Drechslera teres on barley. Cereal Research Communications 36: 637–645. https://doi.org/10.1556/CRC.36.2008.4.13. DOI: https://doi.org/10.1556/CRC.36.2008.4.13
  15. Cavara F., 1893. Ueber einige parasitische pilze auf dem cetreide. Zeitschrift für Pflanzenkrankheiten 3(1): 16–26.
  16. Champion R., 1997. Identifier les Champignons Transmis par les Semences. INRA, Paris, France, 398 pp.
  17. Clemente G., Quintana S., Aguirre N., Rosso A., Cordi N., Havis N.D., 2014. State of art of Ramularia collo-cygni (leaf spot of barley) in Argentina and detection and quantification of R. collo-cygni by real-time PCR in barley plantlets and seeds treated with fungicide. In: Proceedings Conference of the European Foundation for Plant Pathology 8–13 September, 2014, Kraków, Poland, 116-117 (abstract).
  18. Covarelli L., Beccari G., Prodi A., Generotti S., Etruschi F., … Mañes J., 2015. Fusarium species, chemotype characterisation and trichothecene contamination of durum and soft wheat in an area of central Italy. Journal of the Science of Food and Agriculture 95(3): 540–551. https://doi.org/10.1002/jsfa.6772. DOI: https://doi.org/10.1002/jsfa.6772
  19. Deadman M. L., Cooke B.M., 1987. Effects of net blotch on growth and yield of spring barley. Annals of Applied Biology 110(1): 33–42. https://doi.org/10.1111/j.1744-7348.1987.tb03230.x. DOI: https://doi.org/10.1111/j.1744-7348.1987.tb03230.x
  20. Dokhanchi H., Arzanlou M., Abed-Ashtiani F., 2021. Sexual recombination and genetic diversity in Iranian populations of Pyrenophora teres. Journal of Phytopathology 169(7-8): 447–460. https://doi.org/10.1111/jph.13001. DOI: https://doi.org/10.1111/jph.13001
  21. Dussart F., Creissen H.E., Havis N.D., 2020. Ramularia collo-cygni - An enemy in waiting. In: eLS, John Wiley and Sons, Ltd (Ed.). https://doi.org/10.1002/9780470015902.a0028896. DOI: https://doi.org/10.1002/9780470015902.a0028896
  22. Ellwood S.R., Piscetek V., Mair W.J., Lawrence J.A., Lopez‐Ruiz F.J., Rawlinson C., 2019. Genetic variation of Pyrenophora teres f. teres isolates in Western Australia and emergence of a Cyp51A fungicide resistance mutation. Plant Pathology 68(1): 135–142. https://doi.org/10.1111/ppa.12924. DOI: https://doi.org/10.1111/ppa.12924
  23. Erreguerena I.A., Quiroz F.J., Cambareri M., Pereyra S., Havis N.D., Carmona M.A., 2025. Assessing the impact of Ramularia leaf spot on barley: prospects for fungicide protection strategies and weather-based prediction models in Argentina. Plant Pathology 74(3): 858–872. DOI: https://doi.org/10.1111/ppa.14056
  24. EUROSTAT, 2022. Statistical office of the European Communities (EUROSTAT). Available at: https://ec.europa.eu/eurostat/databrowser/view/tag00051/default/table?lang=en&category=t_agr.t_apro.t_apro_cp. Accessed January 4, 2024.
  25. FAOSTAT, 2022. Food and Agriculture Organization Corporate Statistical Database (FAOSTAT). Available at: https://www.fao.org/faostat/en/#data/QCL. Accessed January 4, 2024.
  26. Fratianni S., Acquaotta F., 2017. The climate of Italy. In: Landscapes and Landforms of Italy (M. Soldati, M. Marchetti, ed.). World Geomorphological Landscapes. Springer Cham. https://doi.org/10.1007/978-3-319-26194-2_4. DOI: https://doi.org/10.1007/978-3-319-26194-2_4
  27. Frei P., Gindrat D., 2000. Le champignon Ramularia collo-cygni provoque une forme de grillures sur les feuilles d’orge d’automne et de graminées adventices. Revue Suisse d’Agriculture 32: 119–125.
  28. Frei P., Gindro K., Richter H., Schürch S., 2007. Direct‐PCR detection and epidemiology of Ramularia collo‐cygni associated with barley necrotic leaf spots. Journal of Phytopathology 155(5): 281–288. https://doi.org/10.1111/j.1439-0434.2007.01228.x. DOI: https://doi.org/10.1111/j.1439-0434.2007.01228.x
  29. Havis N.D., Brown J.K.M., Clemente G., Frei P., Jedryczka M., … Hess M., 2015. Ramularia collo-cygni-An emerging pathogen of barley crops. Phytopathology 105(7): 895–904. https://doi.org/10.1094/PHYTO-11-14-0337-FI. DOI: https://doi.org/10.1094/PHYTO-11-14-0337-FI
  30. Havis N.D., Nyman M., Oxley S.J.P., 2014. Evidence for seed transmission and symptomless growth of Ramularia collo‐cygni in barley (Hordeum vulgare). Plant Pathology 63(4): 929–936. https://doi.org/10.1111/ppa.12162. DOI: https://doi.org/10.1111/ppa.12162
  31. Havis N.D., Oxley S.J.P., Piper S.R., Langrell S.R.H., 2006. Rapid nested PCR-based detection of Ramularia collo-cygni direct from barley: rapid nested PCR-based detection direct from barley. FEMS Microbiology Letters 256(2): 217–223. https://doi.org/10.1111/j.1574-6968.2006.00121.x. DOI: https://doi.org/10.1111/j.1574-6968.2006.00121.x
  32. Hoheneder F., Hofer K., Groth J., Herz M., Heß M., Hückelhoven R., 2021. Ramularia leaf spot disease of barley is highly host genotype-dependent and suppressed by continuous drought stress in the field. Journal of Plant Diseases and Protection 128(3): 749–767. https://doi.org/10.1007/s41348-020-00420-z. DOI: https://doi.org/10.1007/s41348-020-00420-z
  33. Jalli M., 2011. Sexual reproduction and soil tillage effects on virulence of Pyrenophora teres in Finland. Annals of Applied Biology 158(1): 95–105. https://doi.org/10.1111/j.1744-7348.2010.00445.x. DOI: https://doi.org/10.1111/j.1744-7348.2010.00445.x
  34. Khaledi N., Zare L., Hassani F., Osroosh S., 2024. Comparison of diagnostic methods, virulence and aggressiveness analysis of Pyrenophora spp. in pre-basic seeds in the barley fields. Tropical Plant Pathology 49: 304–316. https://doi.org/10.1007/s40858-023-00631-3 DOI: https://doi.org/10.1007/s40858-023-00631-3
  35. Kildea S., Mulhare J., Zia R., Hutton F., Creissen H., 2024. Presence and prevalence of Ramularia collo-cygni SDHI resistance in Irish barley seed. Journal of Plant Diseases and Protection 131: 1233–1238. DOI: https://doi.org/10.1007/s41348-024-00910-4
  36. Laitila A., Kotaviita E., Peltola P., Home S., Wilhelmson A., 2007. Indigenous microbial community of barley greatly influences grain germination and malt quality. Journal of the Institute of Brewing 113(1): 9–20. https://doi.org/10.1002/j.2050-0416.2007.tb00250.x. DOI: https://doi.org/10.1002/j.2050-0416.2007.tb00250.x
  37. Lammari H.I., Rehfus A., Stammler G., Fellahi Z.E.A., Benbelkacem A., Benslimane H., 2020. Occurrence and frequency of spot form and net form of net blotch disease of barley in Algeria. Journal of Plant Diseases and Protection 127(1): 35–42. https://doi.org/10.1007/s41348-019-00278-w. DOI: https://doi.org/10.1007/s41348-019-00278-w
  38. Lenth R., 2022. Emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.7.4-9990003. Available at: https://github.com/rvlenth/emmeans. Accessed December 28, 2024.
  39. Liu Z., Ellwood S.R., Oliver R.P., Friesen T.L., 2011. Pyrenophora teres: Profile of an increasingly damaging barley pathogen. Molecular Plant Pathology 12(1): 1–19. https://doi.org/10.1111/j.1364-3703.2010.00649.x DOI: https://doi.org/10.1111/j.1364-3703.2010.00649.x
  40. Makepeace J.C., Havis N.D., Burke J.I., Oxley S.J.P., Brown J.K.M., 2008. A method of inoculating barley seedlings with Ramularia collo-cygni. Plant Pathology 57: 991–999. https://doi.org/10.1111/j.1365-3059.2008.01892.x. DOI: https://doi.org/10.1111/j.1365-3059.2008.01892.x
  41. Mair W.J., Deng W., Mullins J.G., West S., Wang P., … Lopez-Ruiz F.J., 2016. Demethylase inhibitor fungicide resistance in Pyrenophora teres f. sp. teres associated with target site modification and inducible overexpression of Cyp51. Frontiers in Microbiology 7, 1279. https://doi.org/10.3389/fmicb.2016.01279. DOI: https://doi.org/10.3389/fmicb.2016.01279
  42. Matusinsky P., Svobodova-Leisova L., Gubis J., Hudcovicova M., Klcova L., … Minarikova V., 2011. Impact of the seed-borne stage of Ramularia collo-cygni in barley seed. Journal of Plant Pathology 93(3): 679–689.
  43. Matusinsky P., Svobodova-Leisova L., Mariks P., Tvaruzek L., Stemberkova L., … Spitzer T., 2010. Frequency of a mutant allele of cytochrome b conferring resistance to Qol fungicides in the Czech population of Ramularia collo-cygni. Journal of Plant Diseases and Protection 117, 248–252. https://doi.org/10.1007/BF03356369. DOI: https://doi.org/10.1007/BF03356369
  44. Matzen N., Weigand S., Bataille C., Kildea S., Havis N., … Jørgensen L.N., 2024. EuroBarley: control of leaf diseases in barley across Europe. Journal of Plant Diseases and Protection 131: 1239–1244. https://doi.org/10.1007/s41348-023-00852-3. DOI: https://doi.org/10.1007/s41348-023-00852-3
  45. McGrann G.R.D., Havis N.D., 2017. Ramularia leaf spot: a newly important threat to barley production. Outlooks on Pest Management 28: 65–69. https://doi.org/10.1564/v28_apr_05. DOI: https://doi.org/10.1564/v28_apr_05
  46. McGrann G.R.D., Steed A., Burt C., Goddard R., Lachaux C., … Brown J.K.M., 2015. Contribution of the drought tolerance-related Stress-responsive NAC1 transcription factor to resistance of barley to Ramularia leaf spot. Molecular Plant Pathology 16(2): 201–209. https://doi.org/10.1111/mpp.12173. DOI: https://doi.org/10.1111/mpp.12173
  47. McLean M.S., Howlett B.J., Hollaway G.J., 2009. Epidemiology and control of spot form of net blotch (Pyrenophora teres f. maculata) of barley: A review. Crop and Pasture Science 60(4): 303. https://doi.org/10.1071/CP08173. DOI: https://doi.org/10.1071/CP08173
  48. McLean M.S., Hollaway G.J., 2019. Control of net form of net blotch in barley from seed-and foliar-applied fungicides. Crop and Pasture Science 70: 55–60. https://doi.org/10.1071/CP18142. DOI: https://doi.org/10.1071/CP18142
  49. Morcia C., Tumino G., Ghizzoni R., Badeck F.W., Lattanzio V.M.T., … Terzi V., 2016. Occurrence of Fusarium langsethiae and T-2 and HT-2 Toxins in Italian Malting Barley. Toxins 8(8): 247. https://doi.org/10.3390/toxins8080247. DOI: https://doi.org/10.3390/toxins8080247
  50. Newton A.C., Fitt B.D.L., Atkins S.D., Walters D.R., Daniell T.J., 2010. Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends in Microbiology 18(8): 365–373. https://doi.org/10.1016/j.tim.2010.06.002. DOI: https://doi.org/10.1016/j.tim.2010.06.002
  51. Nicolaisen M., Suproniene S., Nielsen L.K., Lazzaro I., Spliid N.H., Justesen A.F., 2009. Real-time PCR for quantification of eleven individual Fusarium species in cereals. Journal of Microbiological Methods 76(3): 234–240. https://doi.org/10.1016/j.mimet.2008.10.016. DOI: https://doi.org/10.1016/j.mimet.2008.10.016
  52. Nyman M., Havis N.D., Oxley S.J.P., 2009. Importance of seed-borne infection of Ramularia collo-cygni. Aspects of Applied Biology 92: 91–96.
  53. Oğuz A.Ç., Ölmez F., Karakaya A., 2019. Genetic diversity of Net Blotch Pathogens of barley in Turkey. International Journal of Agriculture and Biology 21: 1089–1096.
  54. Oxley S.J.P., Havis N.D., 2010. Managing Ramularia collo-cygni through varietal resistance, seed health and forecasting. HGCA Project report (463).
  55. Parry D.W., Nicholson P., 1996. Development of a PCR assay to detect Fusarium poae in wheat. Plant Pathology 45(2): 383–391. https://doi.org/10.1046/j.1365-3059.1996.d01-133.x. DOI: https://doi.org/10.1046/j.1365-3059.1996.d01-133.x
  56. Pereyra S., Erreguerena I., Couretot L., Pérez C., Palladino C., Havis N. D., 2017. Upsurge of Ramularia leaf spot in South America. In: International Workshop on Barley Leaf Diseases, 2o. Rabat, Morocco: The International Center for Agricultural Research in the Dry Areas (ICARDA), April 5–7, 2017.
  57. Pinheiro J., Bates D., 2000. Mixed-Effect Models in S and S-plus. In: Journal of The American Statistical Association Vol. 96. https://doi.org/10.1007/978-1-4419-0318-1. DOI: https://doi.org/10.1007/978-1-4419-0318-1
  58. Poudel B., Ellwood S.R., Testa A.C., McLean M., Sutherland M.W., Martin A., 2017. Rare Pyrenophora teres Hybridization Events Revealed by Development of Sequence-Specific PCR Markers. Phytopathology 107(7): 878–884. https://doi.org/10.1094/PHYTO-11-16-0396-R. DOI: https://doi.org/10.1094/PHYTO-11-16-0396-R
  59. Puglia D., Luzi F., Lilli M., Sbardella F., Pauselli M., … Benincasa P., 2020. Straw fibres from barley hybrid lines and their reinforcement effect in polypropylene-based composites. Industrial Crops & Products 154: 112736. https://doi.org/10.1016/j.indcrop.2020.112736. DOI: https://doi.org/10.1016/j.indcrop.2020.112736
  60. R Core Team, 2023. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: https://www.R-project.org/. Accessed December 28, 2023.
  61. Rau D., Brown A.H.D., Brubaker C.L., Attene G., Balmas V., … Papa R., 2003. Population genetic structure of Pyrenophora teres Drechs. The causal agent of net blotch in Sardinian landraces of barley (Hordeum vulgare L.). Theoretical and Applied Genetics 106(5): 947–959. https://doi.org/10.1007/s00122-002-1173-0. DOI: https://doi.org/10.1007/s00122-002-1173-0
  62. Rehfus A., Matusinsky P., Strobel D., Bryson R., Stammler G., 2019. Mutations in target genes of succinate dehydrogenase inhibitors and demethylation inhibitors in Ramularia collo-cygni. Journal of Plant Diseases and Protection 126: 447–459. https://doi.org/10.1007/s41348-019-00246-4. DOI: https://doi.org/10.1007/s41348-019-00246-4
  63. Rehfus A., Miessner S., Achenbach J., Strobel D., Bryson R., Stammler G., 2016. Emergence of succinate dehydrogenase inhibitor resistance of Pyrenophora teres in Europe. Pest Management Science 72: 1977–1988. https://doi.org/10.1002/ps.4244. DOI: https://doi.org/10.1002/ps.4244
  64. Reis E.M., Danelli A., Casa R.T., 2012. Fungicides, seed dresser adjuvants and storage time in the control of Drechslera teres in barley seeds. Summa Phytopathologica 38: 187–191. https://doi.org/10.1590/S0100-54052012000300001. DOI: https://doi.org/10.1590/S0100-54052012000300001
  65. Retman S., Melnichuk F., Kyslykh T., Shevchuk O., 2022. Complex of barley leaf spots in Ukraine. Chemistry Proceedings 10(1). https://doi.org/10.3390/IOCAG2022-12290. DOI: https://doi.org/10.3390/IOCAG2022-12290
  66. Ronen M., Sela H., Fridman E., Perl-Treves R., Kopahnke D., … Harel A., 2019. Characterization of the Barley Net Blotch Pathosystem at the Center of Origin of Host and Pathogen. Pathogens 8(4): 275. https://doi.org/10.3390/pathogens8040275. DOI: https://doi.org/10.3390/pathogens8040275
  67. Sachs E, 2006. The history of research into Ramularia leaf spot on barley. Proceedings of the 1st European Ramularia Workshop, pp 9-15, Gottingen, Germany.
  68. Senatore M.T., Prodi A., Tini F., Balmas V., Infantino A., … Beccari G., 2023. Different diagnostic approaches for the characterization of the fungal community and Fusarium species complex composition of Italian durum wheat grain and correlation with secondary metabolite accumulation. Journal of the Science of Food and Agriculture 103(9): 4503–4521. https://doi.org/10.1002/jsfa.12526. DOI: https://doi.org/10.1002/jsfa.12526
  69. Serenius M., Manninen O., Wallwork H., Williams K., 2007. Genetic differentiation in Pyrenophora teres populations measured with AFLP markers. Mycological Research 111: 213–223. https://doi.org/10.1016/j.mycres.2006.11.009. DOI: https://doi.org/10.1016/j.mycres.2006.11.009
  70. Sharma P., Gujral H.S., 2010. Milling behavior of hulled barley and its thermal and pasting properties. Journal of Food Engineering 97(3): 329–334. https://doi.org/10.1016/j.jfoodeng.2009.10.025 . DOI: https://doi.org/10.1016/j.jfoodeng.2009.10.025
  71. Sierotzki H., Frey R., Wullschleger J., Palermo S., Karlin S., ... Gisi U., 2007. Cytochrome b gene sequence and structure of Pyrenophora teres and P. tritici-repentis and implications for QoI resistance. Pest Management. Science 63: 225–233. doi: 10.1002/ps.1330 DOI: https://doi.org/10.1002/ps.1330
  72. Singh B.K., Delgado-Baquerizo M., Egidi E., Guirado E., Leach J. E., … Trivedi P., 2023. Climate change impacts on plant pathogens, food security and paths forward. Nature Reviews Microbiology 21: 640–656. https://doi.org/10.1038/s41579-023-00900-7. DOI: https://doi.org/10.1038/s41579-023-00900-7
  73. Smedegård-Petersen V., 1971. Pyrenophora teres f. maculata f. nov. and Pyrenophora teres f. teres on barley in Denmark. In: Årsskrift, Kongelige Veterinær- og Landbohøjskole 124, 144.
  74. Sutton B.C., Waller J.M., 1988. Taxonomy of Ophiocladium hordei, causing leaf lesions on Triticale and other Gramineae. Transactions of the British Mycological Society 90(1): 55–61. https://doi.org/10.1016/S0007-1536(88)80180-3. DOI: https://doi.org/10.1016/S0007-1536(88)80180-3
  75. Taylor J.M.G., Paterson L.J., Havis N.D., 2010. A quantitative real-time PCR assay for the detection of Ramularia collo-cygni from barley (Hordeum vulgare). Letters in Applied Microbiology 50(5): 493–499. https://doi.org/10.1111/j.1472-765X.2010.02826.x. DOI: https://doi.org/10.1111/j.1472-765X.2010.02826.x
  76. Tini F., Covarelli L., Ricci G., Balducci E., Orfei M., Beccari G., 2022. Management of Pyrenophora teres f. teres, the causal agent of net form net blotch of barley, in a two-year field experiment in central Italy. Pathogens 11(3): 291. https://doi.org/10.3390/pathogens11030291. DOI: https://doi.org/10.3390/pathogens11030291
  77. Walters D.R., Avrova A., Bingham I.J., Burnett F.J., Fountaine J., Havis N.D., … Newton A.C., 2012. Control of foliar diseases in barley: towards an integrated approach. European Journal of Plant Pathology 133(1): 33–73. https://doi.org/10.1007/s10658-012-9948-x. DOI: https://doi.org/10.1007/s10658-012-9948-x
  78. Walters D.R., Havis N.D., Oxley S.J.P., 2008. Ramularia collo-cygni: The biology of an emerging pathogen of barley. FEMS Microbiology Letters 279(1): 1–7. https://doi.org/10.1111/j.1574-6968.2007.00986.x. DOI: https://doi.org/10.1111/j.1574-6968.2007.00986.x
  79. Weibull J., Walther U., Sato K., Habekuß A., Kopahnke D., Proeseler G., 2003. Chapter 8-Diversity in resistance to biotic stresses. In: Developments in Plant Genetics and Breeding (R. von Bothmer, T. van Hintum, H. Knüpffer, K. Sato, ed.), Elsevier, Denmark, Europe, 7, 143–178. https://doi.org/10.1016/S0168-7972(03)80010-5. DOI: https://doi.org/10.1016/S0168-7972(03)80010-5
  80. Wu H.L., Steffenson B.J., Zhong S., Li Y., Oleson A.E., 2003. Genetic variation for virulence and RFLP markers in Pyrenophora teres. Canadian Journal of Plant Pathology 25(1): 82–90. https://doi.org/10.1080/07060660309507052. DOI: https://doi.org/10.1080/07060660309507052

Most read articles by the same author(s)