An Important Pathogen of Barley: Ramularia collo-cygni

Year 2022, Volume: 11 Issue: 1, 205 - 237, 10.06.2022

Zeynep Aslan , Arzu Çelik Oğuz , Aziz Karakaya

https://doi.org/10.55007/dufed.1076555

Abstract

Ramularia collo-cygni is a fungal agent that causes Ramularia leaf spot disease on barley (Hordeum vulgare). It causes necrotic spotting and premature leaf aging, leading to loss of green leaf area in barley, and in case of an epidemic, it causes yield loss up to 70%. Although it was defined more than a hundred years ago due to the late emergence of the disease and the difficulty of diagnosis, it has been accepted as an important pathogen of barley in recent years. Today, it attracts a lot of attention by researchers due to the epidemics it creates around the world. This review describes in detail the biology, epidemiology, host-pathogen relationships of this fungal agent, which has not yet been detected in Turkey and summarizes the current control strategies.

Keywords

Ramularia collo-cygni, Ramularia leaf spot disease, Barley, Hordeum vulgare

Önemli Bir Arpa Patojeni: Ramularia collo-cygni

Abstract

Ramularia collo-cygni, arpada (Hordeum vulgare) Ramularia yaprak lekesi hastalığına neden olan fungal bir etmendir. Nekrotik lekelenmeye ve erken yaprak yaşlanmasına neden olarak arpada yeşil yaprak alanı kaybına yol açmakta ve epidemi yapması durumunda %70’e varan verim kaybına neden olmaktadır. Hastalığın geç dönemde ortaya çıkması ve etmenin tanısının zorluğu nedeni ile yüz yıldan fazla süre önce tanımlanmış olmasına rağmen son yıllarda, arpanın önemli bir patojeni olarak kabul edilmiştir. Günümüzde dünya çapında meydana getirdiği epidemiler nedeni ile araştırmacılar tarafından oldukça ilgi görmektedir. Bu derleme, ülkemizde henüz tespiti yapılmamış olan bu fungal etmenin detaylı olarak biyolojisi, epidemiyolojisi, konukçu patojen ilişkilerini tanımlamakta ve mevcut kontrol stratejilerini özetlemektedir.

Keywords

Ramularia collo-cygni, Ramularia yaprak lekesi hastalığı, Arpa, Hordeum vulgare

References

• B. Leff, N. Ramankutty, and J. A. Foley, ‘Geographic distribution of major crops across the World,’ Global Biogeochemical Cycles, vol. 18, no. 1, pp. 1-33, 2004.
• D. E. Mathre, ‘Compendium of Barley Disease,’ American Phytopathological Society (APS) Press. St. Paul, MN 1982.
• E. Kün, ‘Tahıllar-1 Serin İklim Tahılları, Ankara Üniversitesi Ziraat Fakültesi Yayınları,’ Yayın No:1451. Ankara, s. 332, 1996.
• G. Mızrak ve K. Yalvaç, ‘Genetiği Değiştirilmiş (Aktarma Genli) Organizmalar,’ Rapor, Eylül, Ankara, 2011. Web Sitesi: http://xn--grbzmzrak-q9ac25d.com/Yayinlarim/GdoRaporuEkitap.pdf
• Anonim, T.C Tarım ve Orman Bakanlığı, Arpa, Temmuz-2020, Tarım Ürünleri PiyasaRaporu, WebSitesi: https://arastirma.tarimorman.gov.tr/tepge/Belgeler/PDF. Erişim Tarihi: 20.05.2021.
• E. C. Oerke and H. W. Dehne, ‘Safeguarding production losses in major crops and the role of crop protection,’ Crop Protection, vol. 23, no. 4, pp. 275-285, 2004.
• A. C. Newton, A. J. Flavell, T. S. George, P. Leat, B. Mullholland, L. Ramsay, C. Revoredo-Giha, J. Russell, B. J. Steffenson, J. S. Swanston, W. T. B. Thomas, R. Waugh, P. J. White, and I. J. Bingham, ‘Crops that feed the world 4. Barley: a resilient crop? Strengths and weaknesses in the context of food security,’ Food Security, vol. 3, no. 2, pp. 141-178, 2011.
• S. Savary, L. Willocquet, and S. J. Pethybridge, P. Esker, N. McRoberts, A. Nelson, ‘The global burden of pathogens and pests on major food crops,’ Nature Ecology & Evolution, vol.3, no.3, pp. 430-439, 2019.
• S. Salamati and L. Reitan, ‘Ramularia collo-cygni on spring barley, an overview of its biology and epidemiology,’ Proceedings 1st European Ramularia Workshop, Göttingen, Germany, pp. 19–35, 2006.
• S. Pereyra, ‘Herramientas disponibles para el manejo de dos enfermedades relevantes de la pasada zafra: Fusariosis de la espiga en trigo y Ramularia en cebada,’ Actividades Difusion INIA, vol. 720, pp.33-41, 2013.
• G. R. McGrann and N. D. Havis, ‘Ramularia leaf spot: a newly important threat to barley production,’ Outlooks on Pest Management, vol. 28, no. 2, pp. 65-69, 2017.
• G. Fox and C. D. Li, ‘Achieving sustainable cultivation of barley,’ Burleigh Dodds Science Publishing Limited, pp. 505, 2020.
• H. O. Pinnschmidt and L. N. Jørgensen, ‘Yield effects of Ramularia leaf spot on spring barley,’ Aspects of Applied Biology, vol. 92, pp. 57-66, 2009.
• N. D. Havis, J. K. M. Brown, G. Clemente, P. Frei, M. Jedryczka, J. Kaczmarek, M. Kaczmarek, P. Matusinsky, G. R. D. McGrann, S. Pereyra, M. Piotrowska, H. Sghyer, A. Tellier,and M. Hess, ‘Ramularia collo-cygni-an emerging pathogen of barley crops,’ Phytopathology, vol. 105, no. 7, pp. 895-904, 2015.
• S. J. P. Oxley and N. D. Havis, ‘Development of Ramularia collo-cygni on spring barley and its impact on yield’, In: Crop Protection in Northern Britain, pp. 147-152, 2004.
• F. Cavara, ‘Über einige parasitische Pilze auf dem Getreide,’ Zeitschrift fü Pflanzenkrankheiten, vol. 3, no. 1, pp. 16-26, 1893.
• E. Sachs, P. Greif, D. Amelung, and H. Huss, ‘Ramularia collo-cygni-a rediscovered pathogen of barley in Europe,’ Mitteilungen-Biologischen Bundesanstalt Fur Land Und Forstwirtschaft, vol. 357, pp. 96-96, 1998.
• D. R. Walters, N. D. Havis, and S. J. Oxley, ‘Ramularia collo-cygni: the biology of an emerging pathogen of barley,’ FEMS Microbiology Letters, vol. 279, no.1, pp. 1-7, 2008.
• B. C. Sutton and J. M. Waller, ‘Taxonomy of Ophiocladium hordei, causing leaf lesions on triticale and other Gramineae,’ Transactions of the British Mycological Society, vol. 90, no. 1, pp. 55-61, 1988.
• P. Frei and D. Gindrat, ‘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, vol. 6, pp. 229-234, 2000.
• E. Sachs, ‘A ‘new’ leaf spot disease of barley caused by Ramularia collo-cygni: description, diagnosis and comparison with other leaf spots,’ In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B (eds), Proceeding of the Second International Workshop on Barley Leaf Blights, Aleppo, Syria, pp. 365–369, 2002
• M. J. Piotrowska, J. M. Fountaine, R. A. Ennos, M. Kaczmarek, and F. J. Burnett, ‘Characterisation of Ramularia collo-cygni laboratory mutants resistant to succinate dehydrogenase inhibitors,’ Pest Management Science, vol. 73, no. 6, pp. 1187-1196, 2017.
• N. D. Havis, S. J. P. Oxley, S. R. Piper, and S. R. H. Langrell, ‘Rapid nested PCR-based detection of Ramularia collo-cygni direct from barley,’ FEMS Microbiology Letters, vol. 256, no. 2, pp. 217-223, 2006a.
• P. Frei, K. Gindro, H. Richter, and S. Schürch, ‘Direct‐PCR detection and epidemiology of Ramularia collo‐cygni associated with barley necrotic leaf spot,’ Journal of Phytopathology, vol. 155, no. 5, pp. 281-288, 2007.
• N. D. Havis, N. Evans, and G. Hughes, ‘Development of UK wide risk forecast 17 for Ramularia leaf spot in barley,’ Project Report No. PR600, 2018.
• M. Kaczmarek, M. J. Piotrowska, J. M. Fountaine, K. Gorniak, G. R. D. McGrann, A. Armstrong, K. M. Wright, A. C. Newton, and N. D. Havis, ‘Infection strategy of Ramularia collo‐cygni and development of ramularia leaf spot on barley and alternative graminaceous hosts,’ Plant Pathology, vol. 66, no. 1, pp. 45-55, 2017.
• S. Oxley, N. Havis, A. Evans, S. Waterhouse, and L. Tonguç, ‘A guide to the recognition and understanding of Ramularia and other leaf spots of barley,’ BASF and SAC, pp. 62, 2012.
• N. D. Havis, M. Pastok, S. Pyzalski, and S. J. P. Oxley, ‘Investigating the life cycle of Ramularia collo-cygni,’ In: The Dundee Conference, Crop Protection in Northern Britain, Dundee, UK, pp. 219-224, 2006b.
• R. Sprague, ‘Additions to the Fungi Imperfecti on grasses in the United States,’ Mycologia, vol. 38, no. 1, pp. 52-64, 1946.
• U. Braun, ‘A monograph of Cercosporella, Ramularia and related genera,’ Phytopathogenic Hyphomycetes, vol. 2, 1998.
• G. R. McGrann, A. Andongabo, E. Sjökvist, U. Trivedi, F. Dussart, M. Kaczmarek, A. Mackenzie, J. M. Fountaine, J. M. G. Taylor, L. J. Paterson, K. Gorniak, F. Burnett, K. Kanyuka, K. E. Hammond-Kosack, J. J. Rudd, M. Blaxter, and N. D. Havis, ‘The genome of the emerging barley pathogen Ramularia collo-cygni,’ BMC Genomics, vol. 17, no. 1, pp. 1-17, 2016.
• M. J. Piotrowska, R. A. Ennos, J. M. Fountaine, F. J. Burnett, M. Kaczmarek, and P. N. Hoebe, ‘Development and use of microsatellite markers to study diversity, reproduction and population genetic structure of the cereal pathogen Ramularia collo-cygni,’ Fungal Genetics and Biology, vol. 87, pp. 64-71, 2016.
• M. S. Kabir, R. J. Ganley, and R. E. Bradshaw, ‘The hemibiotrophic lifestyle of the fungal pine pathogen Dothistroma septosporum,’ Forest Pathology, vol. 45, no. 3, pp. 190 202, 2015.
• A. M. Tiley, S. J. Karki, and A. Feechan, ‘Zymoseptoria tritici,’ eLS, 1-8, 2018, https://doi.org/10.1002/9780470015902.a0027948.
• P. W. Crous, A. Aptroot, J-C. Kang, U. Braun, and M. J. Wingfield, ‘The genus Mycosphaerella and its anamorphs’, Studies in Mycology, vol. 45, pp. 107-121, 2000.
• U. Braun, ‘Ramularia collo-cygni (Ramularia leaf blight of barley)-taxonomy and phylogeny,’ Proceedings of the 2nd International Workshop on Barley Leaf Blights, ICARDA-Aleppo, pp. 343-350, 2004.
• H. Huss, ‘The biology of Ramualaria collo-cygni’, In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B (eds), Proceedings of the Second International Workshop on Barley Leaf Blights, Aleppo, Syria, pp. 321-328, 2004.
• E. Stabentheiner, T. Minihofer, and H. Huss, ‘Infection of barley by Ramularia collo cygni: scanning electron microscopic investigations’, Mycopathologia, vol. 168, no. 3, 135, 2009.
• M. Nyman, N. D. Havis, and S.J.P. Oxley, ‘Importance of seed-borne infection of Ramularia collo-cygni’, Aspects of Applied Biology, vol. 92, pp. 91-96, 2009.
• A. Thirugnanasambandam, K. M. Wright, N. D. Havis, S. C. Whisson, and A. C. Newton, ‘Agrobacterium‐mediated transformation of the barley pathogen Ramularia collo‐cygni with fluorescent marker tags and live tissue imaging of infection development’, Plant Pathology, vol. 60, no. 5, pp. 929-937, 2011.
• H. Huss and E. Sachs, ‘Ramularia-Blattflecken-oder-Sprenkelkrankheit der Gerste’, Der Pflanzenarzt, vol. 51, 1998.
• N. D. Havis, M. Kaczmarek, and J. M. Fountaine, ‘Ramularia collo-cygni-a rapidly developing problem’, In: The Dundee Conference, Crop Protection in Northern Britain, Dundee, UK, pp. 95-100, 2014.
• M. Kaczmarek, J. Fountaine, A. Newton, N. Read, and N. Havis, ‘The life history of Ramularia collo-cygni,’ In: 27th Fungal Genetics Conference, Asilomar, CA, 2013, Online publication, Available: www. fgsc. net/27thFGC/FungalProgramBook2013. Pdf.
• M. Khier, M. Carmona, E. Sachs, R. Delhey, S. Frayssinet, and D. Barreto, ‘Salpicado necrotico, nueva enfermedad de la cebada en Argentina causada por Ramularia collo-cygni’, Resumenes XI Jornadas Fitosanitarias Argentinas, Cordoba, Argentina, 2002.
• I. Heiser, E. Sachs, and B. Liebermann, ‘Photodynamic oxygen activation by rubellin D, a phytotoxin produced by Ramularia collo-cygni,’ Physiological and Molecular Plant Pathology, vol. 62, no. 1, pp. 29-36, 2003.
• I. C. Harvey, ‘Epidemiology and control of leaf and awn spot of barley caused by Ramularia collo cygni,’ New Zealand Plant Protection, vol. 55, pp. 331-335, 2002.
• H. O. Pinnschmidt and M. S. Hovmøller, ‘Ramularia, a new disease of barley–a review of present knowledge,’ DJF rapport, vol. 89, pp. 313-321, 2003.
• S. J. P. Oxley, N. D. Havis, K. G. Sutherland, and M. Nuttall, ‘Development of a rationale to identify the causal agent of necrotic lesions in spring barley and to identify control mechanisms,’ HGCA Project Report No: 282. HGCA Publications, London, UK. 2002.
• N. D. Havis, M. Nyman, and S. J. P. Oxley, ‘Evidence for seed transmission and symptomless growth of Ramularia collo-cygni in barley (Hordeum vulgare),’ Plant Pathology, vol. 63, no. 4, pp. 929-936, 2004.
• G. R. McGrann, A. Stavrinides, J. Russell, M. M. Corbitt, A. Booth, L. Chartrain, W. T. B. Thomas, and J. K. M. Brown, ‘A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot,’ Journal of Experimental Botany, vol. 65, no. 4, pp. 1025-1037, 2014.
• G. R. McGrann, A. Steed, C. Burt, P. Nicholson, and J. K. M. Brown, ‘Differential effects of lesion mimic mutants in barley on disease development by facultative pathogens,’ Journal of Experimental Botany, vol. 66, no. 11, pp. 3417-3428, 2015a.
• G. R. D. McGrann, A. Steed, C. Burt, R. Goddard, C. Lachaux, A. Bansal, M. Corbitt, K. Gorniak, P. Nicholson, and J. K. M. Brown, ‘Contribution of the drought tolerance related stress‐responsive NAC 1 transcription factor to resistance of barley to Ramularia leaf spot,’ Molecular Plant Pathology, vol. 16, no. 2, pp. 201-209, 2015b.
• J. C. Makepeace, N. D. Havis, J. I. Burke, S J. P. Oxley, and J. K. M. Brown, ‘A method of inoculating barley seedlings with Ramularia collo‐cygni,’ Plant Pathology, vol. 57, no. 6, pp. 991-999, 2008.
• J. K. M. Brown and J. C. Makepeace, ‘The effect of genetic variation in barley on responses to Ramularia collo-cygni,’ Aspects of Applied Biology, vol. 92, pp. 43-47, 2009.
• A. Peraldi, L. L. Griffe, C. Burt, G. R. D. McGrann, and P. Nicholson, ‘Brachypodium distachyon exhibits compatible interactions with Oculimacula spp. and Ramularia collo‐cygni, providing the first pathosystem model to study eyespot and ramularia leaf spot diseases,’ Plant Pathology, vol. 63, no. 3, pp. 554-562, 2014.
• J. M. G. Taylor, L. J. Paterson, and N. D. Havis, ‘A quantitative real‐time PCR assayfor the detection of Ramularia collo‐cygni from barley (Hordeum vulgare),’ Letters in Applied Microbiology, vol. 50, no. 5, pp. 493-499, 2010.
• P. Matusinsky, L. Leisova-Svobodova, J. Gubis, M. Hudcovicova, L. Klcova, M. Gubisova, P. Marik, L. Tvaruzek, and V. Minarikova, ‘Impact of the seed-borne stage of Ramularia collo-cygni in barley seed,’ Journal of Plant Pathology, vol. 93, pp. 679-689, 2011.
• P. Frei, ‘Ramularia collo-cygni: cultivation, storage, and artificial infection of barley and weed grasses under controlled conditions,’ In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B (eds), Proceedings of the Second International Workshop on Barley Leaf Blights, Aleppo, Syria, pp. 351-354, 2004.
• M. G. Cromey, I. C. Harvey, J. E. Sheridan, and N. Grbavag, ‘Occurrence, importance and control of Ramularia collo-cygni in New Zealand’, In Proceedings of the Second International Workshop on Barley Leaf Blights, pp. 7-11, 2002.
• F. Dussart, H. E. Creissen, and N. D. Havis, ‘Ramularia collo-cygni-an enemy in waiting,’ In eLS, pp. 1-8, 2020, doi.org/10.1002/9780470015902.a0028896.
• J. Gubiš and M. Hudcovicova, L. Klčová, ‘First report of Ramularia collo-cygni in Slovakia,’ Journal of Plant Pathology, vol. 90, no. 1, pp. 149, 2008.
• O. S. Afanasenko, N. D. Havis, L. A. Bespalova vd., ‘Ramularia leaf spot is a new barley disease in Russia,’ Plant Protection Quarantine, vol. 1, pp. 11-13, 2012.
• P. Sooväli, M. Tikhonova, and P. Matušinsky, ‘First report of Ramularia leaf spot caused by Ramularia collo-cygni on leaves and seeds of barley in Estonia,’ Plant Disease, vol. 98, no. 7, pp. 997-997, 2014.
• J. M. Fountaine and B. A. Fraaije, ‘Development of QoI resistant alleles in populations of Ramularia collo-cygni,’ Aspects of Applied Biology, vol. 92, pp. 123-126, 2009.
• M. A. Carmona, M. M. Scandiani, A. N. Formento, and A. y Luque, ‘Epidemias de Ramularia collo-cygi, organismo causal dei salpicado necrotico de la cebada,’ In: Campana 2012-2013 Revista Cultivos Invernales en SD de Aapresid, Online puplication, Cultivos Invernales, pp. 44-47, 2013.
• S. Stewart, ‘Manchado necrótico en cebada,’ Actividades Difusion INIA, vol. 254, pp. 47-49, 2001.
• G. Clemente, S. Quintana, N. Aguirre, A. Rosso, N. Cordi, and N. D. Havis, ‘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 fungucide,’ In: Proc. 11th Conf. Eur. Found, Plant Pathol, Poland, 2014.
• A. Mäe, P. Sooväli, and L. Põllumaa, ‘Ramularia collo-cygni: a new pathogen spreading in barley fields in Estonia,’ Agricultural and Food Science, vol. 27, no. 2, pp. 138-145, 2018.
• A. Schützendübel, M. Stadler, D. Wallner, and A. Von Tiedemann, ‘A hypothesis on physiological alterations during plant ontogenesis governing susceptibility of winter barley to ramularia leaf spot’, Plant Pathology, vol. 57, no. 3, pp. 518-526, 2008.
• N. Zamani-Noor, ‘Studies on Ramularia leaf spots on barley—Resistance phenotyping, epidemiology and pathogenicity,’ Ph.D. thesis, Georg-August University Göttingen, Germany, 2011.
• N. Zamani-Noor, A. Schützendübel, B. Koopmann, and A. von Tiedemann, ‘Epidemiology and pathogenicity of Ramularia collo-cygni associated with barley necrotic leaf spot disease,’ Aspects of Applied Biology, vol. 92, pp. 41-42, 2009.
• H. Formayer, H. Huss, and H. Kromb-Kolb, ‘Influence of climatic factors on theformation of symptoms of Ramularia collo-cygni,’ In: Yahyaoui AH, Brader L, Tekauz A, Wallwork H, Steffenson B (eds), Proceeding of the Second International Workshop on Barley Leaf Blights, Aleppo, Syria, pp. 329–330, 2004.
• J. C. Makepeace, ‘The effect of the mlo mildew resistance gene on spotting diseases of barley,’ Doctoral dissertation, University of East Anglia, 2006.
• N. D. Havis, J. M. G. Taylor, M. Nyman, and S. J. P. Oxley, ‘Epidemiology of Ramularia collo cygni,’ Aspects of Applied Biology, vol. 92, pp. 1-7, 2009b.
• P. Marik, Z. Snejdar, and P. Matusinsky, ‘Expression of resistance to Ramularia leaf spot in winter barley cultivars grown in conditions of the Czech Republic,’ Czech Journal of Genetics and Plant Breeding, vol. 47, no. 1, pp. 37-40, 2011.
• G. R. McGrann and J. K. Brown, ‘The role of reactive oxygen in the development of Ramularia leaf spot disease in barley seedlings,’ Annals of Botany, vol. 121, no. 3, pp. 415-430, 2018.
• A. C. Newton, B. D. Fitt, S. D. Atkins, D. R. Walters, and T. J. Daniell, ‘Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions,’ Trends in Microbiology, vol. 18, no. 8, pp. 365-373, 2010.
• Y. X. Wu and A. von Tiedemann, ‘Evidence for oxidative stress involved in physiological leaf spot formation in winter and spring barley,’ Phytopathology, vol. 92, no. 2, pp. 145-155, 2002.
• M. Hess, R. Habeker, M. Kick, M. Martin, and H. Hausladen, ‘Occurrence of the late leaf spot complex of barley and its consequences on optimized disease control,’ Gesunde Pflanzen, vol. 59, no. 2, pp. 47-54, 2007.
• H. Huss, ‘The biology of Ramularia collo-cygni,’ In Proc. Second Int. Workshop Barley Leaf Blights, Aleppo, Syria pp. 321-328, 2002.
• J. C. Zadoks, T. T. Chang, and C. F. Konzak, ‘A decimal code for the growth stages of cereals,’ Weed Research, vol. 14, no. 6, pp. 415-421, 1974.
• C. Toscano‐Underwood, J. S. West, B. D. Fitt, A. D. Todd, and M. Jedryczka, ‘Development of phoma lesionson oilseed rape leaves inoculated with ascospores of A‐group or B‐group Leptosphaeria maculans (stem canker) at different temperatures and wetness durations,’ Plant Pathology, vol. 50, no. 1, pp. 28-41, 2001.
• N. D. Havis, S. J. P. Oxley, F. J. Burnett, and G. Hughes, ‘Epidemiology of Ramularia collo cygni,’ In: The Dundee Conference Crop Protection in Northern Britain, Dundee, UK, pp. 119-124, 2012.
• H. Huss, H. Mayrhofer, and E. Ingolic, ‘Ramularia collo-cygni Sutton and Waller (Fungi imperfecti), ein wirtschaftlich beeunter Parasit der gerste in det Steiermark,’ Mitt Naturwiss Ver Steiermark, vol. 122, pp. 87–95, 1992.
• H. O. Pinnschmidt and M. S. Hovmøller, ‘Resistance against net blotch, scald and Ramularia of barley,’ DJF Rapport, vol. 98, pp. 61-71, 2004.
• H. O. Pinnschmidt, S. A. Sindberg, and J. Willas, ‘Expression of resistance of barley varieties to Ramularia leaf spot and the status of the disease in Denmark,’ In: Proc. First Eur. Ramularia Workshop, Göttingen, Germany, pp. 85-93, 2006.
• E. Sjokvist, R. Lemcke, M. Kamble, F. Turner, M. Blaxter, N. H. D. Havis, M. F. Lyngkjaer, and S. Radutoiu, ‘Dissection of Ramularia leaf spot disease by integrated analysis of barley and Ramularia collo-cygni transcriptome responses,’ Molecular Plant-Microbe Interactions, vol. 32, no. 2, pp. 176-193, 2019.
• D. Godfrey and J. P. Rathjen, ‘Recognition and response in plant PAMP‐triggered immunity,’ Els, 2012.
• M. D. Bolton, H. P. Van Esse, J. H. Vossen, R. de Jonge, I. Stergiopoulos, I. J. E. Stulemeijer, G. C. M. van der Berg, O. Borras-Hidalgo, H. L. Dekker, C. G. De Koster, P. J. G. M. de Wit, M. H. A. J. Joosten, and B. P. H. J. Thomma, ‘The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species,’ Molecular Microbiology, vol. 69, no. 1, pp. 119-136, 2008.
• W-S. Lee, J. J. Rudd, K. E. Hammond-Kosack, and K. Kanyuka, ‘Mycosphaerella graminicola LysM effector-mediated stealth pathogenesis subverts recognition through both CERK1 and CEBiP homologues in wheat,’ Molecular Plant-Microbe Interactions, vol. 27, no. 3, pp. 236-243, 2014.
• J. C. Makepeace, S. J. P. Oxley, N. D. Havis, R. Hackett, J. I. Burke, and J. K. M. Brown, ‘Associations between fungal and abiotic leaf spotting and the presence of mlo alleles in barley,’ Plant Pathology, vol. 56, no. 6, pp. 934-942, 2007.
• A. Dreiseitl, ‘Frequency of powdery mildew resistances in spring barley cultivars in Czech variety trials,’ Plant Protection Science, vol. 48, no. 1, pp. 17-20, 2012.
• M. J. Muria‐Gonzalez, Y. H. Chooi, S. Breen, and P. S. Solomon, ‘The past, present and future of secondary metabolite research in the Dothideomycetes,’ Molecular Plant Pathology, vol. 16, no. 1, pp. 92-107, 2015.
• S. Miethbauer, I. Heiser, and B. Liebermann, ‘The phytopathogenic fungus Ramularia collo‐cygni produces biologically active rubellins on infected barley leaves,’ Journal of Phytopathology, vol. 151, no. 11‐12, pp. 665-668, 2003.
• F. Dussart, R. Douglas, E. Sjökvist, P. N. Hoebe, S. H. Spoel, and G. R. D. McGrann, ‘Genome-based discovery of polyketide derived secondary metabolism pathways in the barley pathogen Ramularia collo cygni,’ Molecular Plant-Microbe Interactions, vol. 31, no. 9, pp. 962-975, 2018a.
• A. Ichihara, H. Oikawa, K. Hayashi, S. Sakamura, A. Furusaki, and T. Matsumoto, ‘Structures of betaenones A and B, novel phytotoxins from Phoma betae Fr,’ Journal of the American Chemical Society, vol. 105, no. 9, pp. 2907-2908, 1983.
• H. Bistrich, J. Breun, G. Emmert, A. Fleck, H. Jaiser, H. Kempe, and M. Lemmens, ‘Screening for leaf spot resistance-results and impact on practical breeding,’ In Proceedings of 1st European Ramularia Workshop, Germany, Göttingen. pp. 83-84, 2006.
• S. Oxley, N. Havis, and R. Hackett, ‘Impact of fungicides and varietal resistance on Ramularia collo-cygni in spring barley,’ In: Proceedings 1st European Ramularia Workshop, Germany, Göttingen, pp. 103-112, 2006.
• I. Heiser, M. Heß, K. U. Schmidtke, U. Vogler, S. Miethbauer, and B. Liebermann, ‘Fatty acid peroxidation by rubellin B, C and D, phytotoxins produced by Ramularia collo-cygni,’ Physiological and Molecular Plant Pathology, vol. 64, no. 3, pp. 135-143, 2004.
• S. Miethbauer, S. Haase, K. U. Schmidtke, W. Günther, I. Heiser, and B. Liebermann, ‘Biosynthesis of photodynamically active rubellins and structure elucidation of new anthraquinone derivatives produced by Ramularia collo-cygni,’ Phytochemistry, vol. 67, no. 12, pp. 1206-1213, 2006.
• H. L. Hjortshøj, A. R. Ravnshøj, M. Nyman, J. Orabi, G. Backes, H. Pinnschmidt, N. Havis, J. Stougaard, and E. Stukenbrock, ‘High levels of genetic and genotypic diversity in field populations of the barley pathogen Ramularia collo cygni,’ European Journal of Plant Pathology, vol. 136, no. 1, pp. 51-60, 2013.
• L. Leisova‐Svobodova, P. Matusinsky, and L. Kucera, ‘Variability of the Ramularia collo‐cygni population in Central Europe,’ Journal of Phytopathology, vol. 160, no. 11/12, pp. 701-709, 2012.
• A. Piotrowska-Niczyporuk and A. Bajguz, ‘The effect of natural and synthetic auxins on the growth, metabolite content and antioxidant response of green alga Chlorella vulgaris (Trebouxiophyceae),’ Plant Growth Regulation, vol. 73, no. 1, pp. 57-66, 2014.
• R. Stam, H. Sghyer, A. Tellier, M. Hess, and R. Hückelhoven, ‘The current epidemic of the barley pathogen Ramularia collo-cygni derives from a population expansion and shows global admixture,’ Phytopathology, vol. 109, no. 12, pp. 2161-2168, 2019.
• M. Hess, S. Weigand, and H. Hausladen, ‘Studying the epidemics of Ramularia collo-cygni in Germany and Austria with different diagnostic tools; development of field diagnostics and implications for integrated disease control,’ Aspects of Applied Biology, vol. 92, pp. 9-16, 2009.
• B. A. Fraaije, H. J. Cools, J. Fountaine, D. J. Lovell, J. Motteram, J. S. West, and J. A. Lucas, ‘Role of ascospores in further spread of QoI-resistant cytochrome b alleles (G143A) in field populations of Mycosphaerella graminicola,’ Phytopathology, vol. 95, no. 8, pp. 933-941, 2005.
• P. Matusinsky, L. Svobodova-Leisova, P. Mariks, L. Tvaruzek, L. Stemberkova, M. Hanusova, V. Minarikova, M. Vysohlidova, and T. Spitzer, ‘Frequency of a mutant allele of cytochrome b conferring resistance to Ool fungicides in the Czech population of Ramularia collo-cygni,’ Journal of Plant Diseases and Protection, vol. 117, no. 6, pp. 248-252, 2010.
• A. Rehfus, P. Matusinsky, D. Strobel, R. Bryson, and G. Stammler, ‘Mutations in target genes of succinate dehydrogenase inhibitors and demethylation inhibitors in Ramularia collo-cygni in Europe,’ Journal of Plant Diseases and Protection, vol. 126, no. 5, pp. 447-459, 2019.
• S. A. Pereyra, J. P. Viera, and N. Havis, ‘Managing Ramularia leaf spot of barley in Uruguay,’ In: Proc. APS-CPS Joint Meeting, Minneapolis, MN, Poster-297, 2014.
• FRAC, Mode of Action of Fungicides. (2014). Erişim Tarihi: 04.04.2021. Online publication. http://www. frac.info/publications/downloads.
• D. R. Walters, N. D. Havis, C. Sablou, and D. J. Walsh, ‘Possible trade-off associated with the use of a combination of resistance elicitors,’ Physiological and Molecular Plant Pathology, vol. 75, no. 4, pp. 188-192, 2011.
• I. A. Erreguerena, F. J. Quiroz, M. R. A. Montoya, C. A. Maringolo, N. Lazzaro, and F. Gimenez, ‘Ventana de protección para el control quımico de Ramularia collo-cygni y Rhynchosporium secalis en cebada en el sudeste bonaerense,’ Resúmenes III Cong. Argentino Fitopatol. San Miguel de Tucumán, Argentina, 2014.
• M. Hess, H. Sghyer, H. Hausladen, and S. Weigand, ‘Studying the epidemiology of Ramularia collo-cygni for the improvement of an Integrated Pest Management system in a changing climate,’ In: Proc. 11th Conf. Eur. Found, Plant Pathol, Poland, 2014.
• N. D. Havis, L. Paterson, J. M. G. Taylor, and D. R. Walters, ‘Use of resistance elicitors to control Ramularia collo-cygni in spring barley,’ Aspects of Applied Biology, vol. 92, pp. 127-132, 2009a.
• D. R. Walters, A. Avrova, I. J. Bingham, F. J. Burnett, J. Fountaine, N. D. Havis, S. P. Hoad, G. Hughes, M. Looseley, S. J. P. Oxley, A. Renwick, C. F. E Topp, and A. C. Newton, ‘Control of foliar diseases in barley: towards an integrated approach,’ European Journal of Plant Pathology, vol. 133, no. 1, pp. 33-73, 2012.
• N. D. Havis, M. Nyman, and S. J. P. Oxley, ‘Potential of seed treatment to control Ramularia collo-cygni in barley,’ In: The Dundee Conference, Crop Protection in Northern Britain, Dundee, UK, pp. 97-102, 2010.
• M. Kaczmarek, M. J. Piotrowska, J. M. Fountaine, K. Gorniak, G. R. D. McGrann, A. Armstrong, K. M. Wright, A. C. Newton, and N. D. Havis, ‘Infection strategy of Ramularia collo‐cygni and development of ramularia leaf spot on barley and alternative graminaceous hosts,’ Plant Pathology, vol. 66, no. 1, pp. 45-55, 2017.
• B. Korić, Z. Tomić, M. Šimala, and T. M. Milek, ‘Ramularia leaf spot on barley in the Republic of Croatia,’ Zbornik predavanj in referatov 9. Slovenskega Posvetovanja o Varstvu Rastlin, Nova Gorica, Slovenije, pp. 273-279, 2009.
• N. D. Havis, F. Burnett, G. Hughes, and T. Yoxall, ‘Development of a risk forecast model for the barley disease Ramularia leaf spot,’ In: Proc. Future IPM Eur. Conf. Riva del Garda, Italy, 2013.
• J. E. Sheridan, ‘Cereal diseases 1999-2000 (including pea diseases and gooseberry mildew) disease survey and disease control in the Wairarapa, New Zealand,’ Mycology and Plant Pathology Report, 37. 2000.
• A. Leistrumaite and Z. Liatukas, ‘Resistance of spring barley cultivars to the new disease Ramularia leaf spot, caused by Ramularia collo-cygni,’ Agronomy Research, vol. 4, pp. 251-255, 2006.
• S. J. P. Oxley, J. K. M. Brown, and N. D. Havis, ‘Impact and interactions of Ramularia collo-cygni and oxidative stress in barley,’ Project Report No. 431, 2008.
• P. Matušinsky, M. Hanusová, L. Stemberková, P. Mařík, V. Minaříková, L. Tvarůžek, I. Langer, and T. Spitzer, ‘Response of spring barley cultivars to Ramularia leaf spot in conditions of the Czech Republic,’ Cereal Research Communications, vol. 41, no. 1, pp. 126-132, 2013.
• I. H. Jørgensen, ‘Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley,’ Euphytica, vol. 63, no. 1, pp. 141-152, 1992.
• H. O. Pinnschmidt and S. A. Sindberg, ‘Assessing Ramularia leaf spot resistance of spring barley cultivars in the presence of other diseases,’ Aspects of Applied Biology, vol. 92, pp. 71-80, 2009.
• R. L. Hjortshøj, ‘Improving resistance to Ramularia leaf spot in barley,’ Ph.D. thesis, Aarhus University, Denmark, 2012.
• D. Tilman, ‘Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices,’ Proceedings of the National Academy of Sciences, vol. 96, no. 11, pp. 5995-6000, 1999.
• E. H. Stukenbrock and B. A. McDonald, ‘The origins of plant pathogens in agro-ecosystems,’ Annual Review of Phytopathology, vol. 46, pp. 75-100, 2008.
• D. W. Hollomon and K. J. Brent, ‘Combating plant diseases—the Darwin connection,’ Pest Management Science, vol. 65, no. 11, pp. 1156-1163, 2009.
• J. M. Cornuet and G. Luikart, ‘Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data’ Genetics, vol. 144, no. 4, pp. 2001-2014, 1996.
• J. Wakeley, Coalescent theory: an introduction. Roberts and Company, Greenwood Village, No. 575: 519.2 WAK, 2009.
• B. A. McDonald and C. Linde, ‘Pathogen population genetics, evolutionary potential, and durable resistance,’ Annual Review of Phytopathology, vol. 40, no. 1, pp. 349-379, 2002.