Pamuk bakteriyel yanıklık etmeni Xanthomonas citri subsp. malvacearum’un izolasyonu, tanılanması ve farklı bitki uçucu yağlarının antibakteriyel etkinliğinin belirlenmesi

Year 2024, , 180 - 191, 21.06.2024

Soner Soylu , Merve Kara , Yusuf Gümüş , Emine Mine Soylu

https://doi.org/10.29050/harranziraat.1434729

Abstract

Pamuk Türkiye’de geniş alanlarda üretimi yapılan önemli endüstri bitkilerin başında
gelir. Pamuk bakteriyel yanıklık hastalığı etmeni Xanthomonas citri subsp.
malvacearum (Syn. Xanthomonas axonopodis pv. malvacearum) tohum kökenli bir
patojendir. Bitki uçucu yağları tohum kökenli fitopatojen türlere karşı kimyasal mücadeleye alternatif olarak kullanım potansiyeline sahip doğal antimikrobiyal bileşiklerdir. Bu çalışmada, Diyarbakır ilinde 2023 yetiştirme sezonunda tipik hastalık belirtileri gösteren pamuk bitkilerinden X. citri subsp. malvacearum bakteriyel
etmenin izolasyonu, tanılanması ve 11 farklı tıbbi bitkiden (Thymus serpyllum, Origanum syriacum, Thymus syriacus, Origanum
onites, Cistus laden, Salvia aramiensis, Laurus nobilis, Hypericum perforatum, Rosmarinus officinalis, Origanum majorana ve
Thymbra spicata) elde edilen uçucu yağların antibakteriyel etkisi disk difüzyon yöntemi ile belirlenmiştir. Tipik hastalık
belirtileri gösteren pamuk bitkilerinden izole edilen izolatlar biyokimyasal ve patojenite testleri ve MALDI-TOF ile tür düzeyinde
X. citri subsp. malvacearum olarak tanılanmıştır. Çalışmada kullanılan bitki uçucu yağları besi yerinde 6.33-46.33 mm çapında
engelleme zonu oluşturmak suretiyle bakteriyel etmene karşı antibakteriyel etkinlik göstermiştir. En etkili uçucun yağlar
sırasıyla T. serpyllum ve T. spicata (43.33 mm), O. syriacum (43.00 mm), T. syriacus (38.33 mm) ve O. onites (37.3 mm) olarak
belirlenmiştir. H. perforatum (9.67 mm), L. nobilis (9.0 mm) ve S. aramiensis (6.33 mm) bitki uçucu yağları hastalık etmene karşı
nispeten daha düşük oranlarda antibakteriyel etkinlik göstermiştir. Elde edilen sonuçlar Thymus spp., Thymbra spp. ve
Origanum spp.’ye ait bitki uçucu yağlarının tohum kökenli bitki patojeni bakteriyel hastalık etmenine karşı kimyasal
mücadeleye alternatif mücadele yöntemi olarak uygulanma potansiyeline sahip olduğunu göstermiştir.

Keywords

pamuk, bakteriyel yanıklık, Xanthomonas, uçucu yağ, antibakteriyel

Ethical Statement

Çalışmada herhangi bir şekilde anket uygulması yapılmamış, hayvansal denek kullanılmamıştır. Etik Kurul Kararına gerek duyulmamaktadır.

Isolation and identification of Xanthomonas citri subsp. malvacearum, cotton bacterial blight disease agent and determination of the antibacterial activity of various plant essential oils

Abstract

Cotton is one of the most important industrial crops produced in large areas in Turkey.
Cotton bacterial blight disease agent Xanthomonas citri subsp. malvacearum (Syn.
Xanthomonas axonopodis pv. malvacearum) is a seed-borne pathogen. Plant essential
oils are natural antimicrobial compounds that have the potential to be used as an
alternative to chemical control of seed-borne phytopathogens. In this study, the
bacterial pathogen X. citri subsp. malvacearum was isolated from cotton plants
showing typical disease symptoms during the 2023 growing season in Diyarbakır
provinces and the antibacterial effect of essential oils obtained from 11 different
medicinal plants (Thymus serpyllum, Origanum syriacum, Thymus syriacus, Origanum
onites, Cistus laden, Salvia aramiensis, Laurus nobilis, Hypericum perforatum,
Rosmarinus officinalis, Origanum majorana and Thymbra spicata) were determined by
disk diffusion method. Bacterial isolates, obtained from cotton plants showing typical
disease symptoms, were identified as X. citri subsp. malvacearum by biochemical and
pathogenicity tests and also MALDI-TOF analysis. The essential oils used in the study
showed antibacterial activity against the bacterial agent by forming an inhibition zone
with a diameter of 6.33-46.33 mm in the nutrient media. T. serpyllum and T. spicata
(43.33 mm), O. syriacum (43.00 mm), T. syriacus (38.33 mm) and O. onites (37.3 mm),
were identified as the most effective essential oils respectively. The essential oils of H.
perforatum (9.67 mm), L. nobilis (9.0 mm) and S. aramiensis (6.33 mm) showed
relatively lower antibacterial activity against the disease agent. The results showed
that essential oils of Thymus spp., Thymbra spp. and Origanum spp. have the potential
to be used as an alternative to chemical control against seed-borne bacterial plant
pathogens.

Keywords

cotton, bacterial blight, Xanthomonas, essential oil, antibacterial

References

• Abdo-Hasan, M., Khalil, H., Debis, B., & Mir, A. N. (2008). Molecular characterisation of Syrian races of Xanthomonas axonopodis pv. malvacearum. Journal of Plant Pathology, 431-439. DOI: https://www.jstor.org/stable/41998535
• Ajene, I. J., Shenge K. C., & Akpa, A. D. (2014). Races of Xanthomonas citri subsp. malvacearum, the causal organism of bacterial blight of cotton in northern Nigeria. Archives of Phytopathology and plant Protection, 47(18), 2263-2269. DOI: https://doi.org/10.1080/03235408.2013.873561
• Aktan, Z. C., & Soylu, S. (2020). Diyarbakır İlinde yetişen badem ağaçlarından endofit ve epifit bakteri türlerinin izolasyonu ve bitki gelişimini teşvik eden mekanizmalarının karakterizasyonu. KSÜ Tarım ve Doğa Dergisi, 23(3), 641-654. DOI: https://doi.org/10.18016/ksutarimdoga.vi.659802
• Anmod, A. B., Ingle, R. W., & Chormale, T.S. (2022). Pathological and cultural characteristics of different isolates of Xanthomonas axonopodis pv. malvacearum. Journal of Plant Disease Sciences, 17(1), 59-62. DOI: https://doi.org/10.48165/jpds.2022.1711
• Atay, M., & Soylu, S. (2022). Biber meyvelerinde hasat sonrası çürümelere sebep olan bazı fungal hastalık etmenlerine karşı Isothiocyanate bileşiklerinin antifungal etkilerinin belirlenmesi. Harran Tarım ve Gıda Bilimleri Dergisi, 26, 290-302. DOI: https://doi.org/10.29050/harranziraat.1136632
• Atay, M., Soylu, S. 2023. Kurutmalık Biber meyvelerinde iç çürüklüğüne neden olan fungal etmenlere karşı bitki uçucu yağlarının in vitro antifungal etkileri. KSU Tarım ve Doğa Dergisi, 26, 76-89. DOI: https://doi.org/10.18016/ksutarimdoga.vi.1085859
• Basim, H., Yegen, O., & Zeller, W. (2000). Antibacterial effect of essential oil of Thymbra spicata L. var. spicata on some plant pathogenic bacteria. Journal of Plant Diseases and Protection, 107(3), 279-84. DOI: https://www.jstor.org/stable/43386995
• Bozkurt, İ. A., Soylu, S., Kara, M., & Soylu, E. M. (2020). Chemical composition and antibacterial activity of essential oils isolated from medicinal plants against gall forming plant pathogenic bacterial disease agents. KSU Journal of Agriculture and Nature, 23(6), 1474-1482. DOI: https://doi.org/10.18016/ksutarimdoga.vi.723544
• Burr, T.J. (2001). Future development of chemical and biological controls for bacterial diseases of plants. In Plant Pathogenic Bacteria: Proceedings of the 10th International Conference on Plant Pathogenic Bacteria, (pp. 19-23), Charlottetown, Prince Edward Island, Canada, July 23-27, Springer Netherlands.
• Churklam, W., Chaturongakul, S., Ngamwongsatit, B., & Aunpad, R. (2020). The mechanisms of action of carvacrol and its synergism with nisin against Listeria monocytogenes on sliced bologna sausage. Food Control, 108, 106864. DOI: https://doi.org/10.1016/j.foodcont.2019.106864
• da Silva, R. S., de Oliveira, M. M. G., de Melo, J. O., Blank, A. F., Correa, C. B., Scher, R., & Fernandes, R. P. M. (2019). Antimicrobial activity of Lippia gracilis essential oils on the plant pathogen Xanthomonas campestris pv. campestris and their effect on membrane integrity. Pesticide Biochemistry and Physiology, 160, 40-48. DOI: https://doi.org/10.1016/j.pestbp.2019.06.014
• Dadasoglu, F., Kotan, R., Çakır, A., Karagöz, K., Dikbas, N., Ozer, H., Kordali, S., & Cakmakci, R. (2016). Use of essential oils and extracts from Satureja and Origanum species as seed disinfectants against Xanthomonas axonopodis pv. vesicatoria (Doidge) dye. Fresenius Environmental Bulletin, 25, 5989-5998.
• Daferera, D. J., Ziogas, B. N., & Polissiou, M. G. (2003). The effectiveness of plant essential oils on the growth of Botrytis cinerea, Fusarium sp. and Clavibacter michiganensis subsp. michiganensis. Crop Protection, 22(1), 39-44. DOI: https://doi.org/10.1016/S0261-2194(02)00095-9
• Delannoy, E., Lyon, B. R., Marmey, P., Jalloul, A., Daniel, J. F., Montillet, J. L., Essenberg, M., & Nicole, M. (2005). Resistance of cotton towards Xanthomonas campestris pv. malvacearum. Annual Review of Phytopathology, 43(1), 63-82. DOI: https://doi.org/10.1146/annurev.phyto.43.040204.140251
• Dönmez, M. F., Şahin, B. U., & Bozhüyük, A. U. (2020). Antibacterial activities of essential oils and extracts of Satureja species against plant pathogenic bacteria in bean. Journal of Agriculture, 3(2), 57-70. DOI: https://doi.org/10.46876/ja.825656
• EL-Zik, K.M., & Thaxton, P.M. (1994). Breeding for resistance to bacterial blight of cotton in relation to races of the pathogen. Proceedings of the World Cotton Research Conference-1, CSIRO, Melbourne, pp. 236–241.
• Eryılmaz, G. A., Kılıç, O., & Boz, İ. (2019). Evaluation of organic agriculture and good agricultural practices in terms of economic, social and environmental sustainability in Turkey. YYU Journal of Agricultural Science, 29(2), 352-361. DOI: https://doi.org/10.29133/yyutbd.446002
• Ghavam, M., Manca, M. L., Manconi, M., & Bacchetta, G. (2020). Chemical composition and antimicrobial activity of essential oils obtained from leaves and flowers of Salvia hydrangea DC. ex Benth. Scientific Reports, 10(1), 1-10. DOI: https://doi.org/10.1038/s41598-020-73193-y
• Gümüş, Y., Soylu, S., Kara, M., & Türkmen, M. (2022). Chemical compositions and antibacterial activities of essential oils of five aromatic plants against plant pathogenic bacterial disease agents. Journal of Agricultural Food and Environmental Sciences, 76(6), 18-23. DOI: https://journals.ukim.mk/index.php/jafes/article/view/1899/1573
• Hillocks, R. J. (1981). Cotton disease research in Tanzania. Tropical Pest Management, 27(1), 1-12. DOI: https://doi.org/10.1080/09670878109414165
• Hillocks, R. J. (1992). Bacteral Blight. In Hillocks RJ. (ed.) Cotton Diseases, pp. 38-85. CAB International, Wallingford, UK.
• Hunter, R. E., Brinkerhoff, L. A., & Bird, L. S. (1968). The development of a set of upland cotton lines for differentiating races of Xanthomonas malvacearum. Phytopathology, 58, 830-832.
• Kachur, K., & Suntres, Z. (2020). The antibacterial properties of phenolic isomers, carvacrol and thymol. Critical Reviews in Food Science and Nutrition, 60(18), 3042-3053. DOI: https://doi.org/10.1080/10408398.2019.1675585
• Kara, M., Türkmen, M., & Soylu, S. (2022). Chemical compositions and in vitro antifungal activities of essential oils obtained from different Origanum species against postharvest gray mold rot of persimmon fruit. Acta Horticulturae, 1338, 283-290. DOI: https://doi.org/10.17660/ActaHortic.2022.1338.41
• Khan, M. A. (1996). Relationship of Xanthomonas campestris pv. malvacearum population to development of symptoms of bacterial blight of cotton. Pakistan Journal of Phytopathology, 8(2), 152-155.
• Kızıl, S., & Uyar, F. (2006). Antimicrobial activities of some thyme (Tymus, Staureja, Origanum and Thymbra) species against important plant pathogens. Asian Journal of Chemistry, 18(2), 1455-1461.
• Kızıl, S., Uyar, F., & Sağir, A. (2005). Antibacterial activities of some essential oils against plant pathogens. Asian Journal of Plant Sciences, 4(3), 225-228.
• Küçükbay, F. Z., Kuyumcu, E., Azaz, A. D., Arabacı, T., & Yücetürk, S. Ç. (2014). Chemical composition of the essential oils of three Thymus taxa from Turkey with antimicrobial and antioxidant activities. Records of Natural Products, 8(2), 110-120.
• Lelliott, R. A., & Stead, D. E. (1987). Methods for the diagnosis bacterial diseases of plants. In: Preece, T.F., Ed., Methods in Plant Pathology, Blackwell Scientific Publications, Oxford.
• Liu, Q. C., Qiao, K., & Zhang, S. A. (2019). Potential of a small molecule carvacrol in management of vegetable diseases. Molecules, 24(10), 1932. DOI: https://doi.org/10.3390/molecules24101932
• Mangalagiri, N. P., Panditi, S. K., & Jeevigunta, N. L. L. (2021). Antimicrobial activity of essential plant oils and their major components. Heliyon, 7(4), e06835. DOI: https://doi.org/10.1016/j.heliyon.2021.e06835
• Mbega, E. R., Mortensen, C. N., Mabagala, R. B., & Wulff, E. G. (2012). The effect of plant extracts as seed treatments to control bacterial leaf spot of tomato in Tanzania. Journal of General Plant Pathology, 78(4), 277-286. DOI: https://doi.org/10.1007/s10327-0120380-z
• Mengulluoglu, M., & Soylu S. (2012). Antibacterial activities of essential oils from several medicinal plants against the seed-borne bacterial disease agent Acidovorax avenae subsp. citrulli. Research on Crops, 13, 641-646. DOI: https://www.researchgate.net/publication/287723650_Antibacterial_activities_of_essential_oils_extracted_from_medicinal_plants_against_seed-borne_bacterial_disease_agent_Acidovorax_avenae_subsp_citrulli
• Meshram, M. K., & Raj, S. (1988). Seed cotton yield and fiber quality as influenced by different grades of bacterial blight under rainfed conditions. Indian Journal of Plant Pathology, 16(2), 257-260.
• Mishra, S.P., & Krishna, A. (2001). Assessment of yield losses due to bacterial blight in cotton. Journal of Mycology and Plant Pathology, 31(2), 232-233.
• Moghaddam, M., Alymanesh, M. R., Mehdizadeh, L., Mirzaei, H., & Pirbalouti, A. G. (2014). Chemical composition and antibacterial activity of essential oil of Ocimum ciliatum, as a new source of methyl chavicol, against ten phytopathogens. Industrial Crops and Products, 59, 144-148. DOI: https://doi.org/10.1016/j.indcrop.2014.05.006
• Mondal, K., Dureja, P., & Prakash, V. J. (2001). Management of Xanthomonas camprestris pv. malvacearum induced blight of cotton through phenolics of cotton rhizobacterium. Current Microbiology, 43, 336-339. DOI: https://doi.org/10.1007/s002840010312
• Naqvi, S. A. H., Iqbal, S., Hafeez-ur-Rehman, Farooq, U., Hassan, M. Z., Shahid, M. N., Noor Shah, A., Abbas, A., Mubeen, I., Farooq, A., Ghareeb, R. Y., Kalaji, H. M., Alrefaei, A. F., & Ahmed, M. A. A. (2022). Evaluation of bacterial perpetuation assays and plant biomolecules antimicrobial activity against cotton blight bacterium Xanthomonas citri subsp. malvacearum; an alternative source for food production and protection. Plants, 11, 1278. DOI: https://doi.org/10.3390/plants11101278
• Oliveira, J.C., Albuquerque, G.M.R., Xavier, A.S., Mariano, R.L.R., Suassuna, N.D., & Souza, E.B. (2011). Characterization of Xanthomonas citri subsp. malvacearum causing cotton angular leaf spot in Brazil. Journal of Plant Pathology, 93, 707-712.
• Orzali, L., Valente, M. T., Scala, V., Loreti, S., & Pucci, N. (2020). Antibacterial activity of essential oils and Trametes versicolor extract against Clavibacter michiganensis subsp. michiganensis and Ralstonia solanacearum for seed treatment and development of a rapid in vivo assay. Antibiotics, 9(9), 628. DOI: https://doi.org/10.3390/antibiotics9090628
• Pavela, R. (2006). Insecticidal activity of essential oils again stcabbage aphid Brevicoryne brassicae. Journal of Essential Oil Bearing Plants, 9(2), 99-106. DOI: https://doi.org/10.1080/0972060X.2006.10643479
• Pulcrano, G., Roscetto, E., Iula, V. D., Panellis, D., Rossano, F., & Catania, M. R. (2012). MALDI-TOF mass spectrometry and microsatellite markers to evaluate Candida parapsilosis transmission in neonatal intensive care units. European Journal of Clinical Microbiology & Infectious Diseases, 31, 2919-2928. DOI: https://doi.org/10.1007/s10096-012-1642-6
• Raghavendra, V. B., Siddalingaiah, L., & Prakash, H. S. (2009). Role of cultivars, physical, chemical and organic treatments in the management of bacterial blight of cotton. Archives of Phytopathology and Plant Protection, 42(12), DOI: https://do.org/10.1080/03235400701622329
• Regnault-Roger, C., Ribodeau, M., Hamraoui, A., Bareau, I., Blanchard, P., Gil-Munoz, M. I., & Barberan, F. T. (2004). Polyphenolic compounds of Mediterranean Lamiaceae and investigation of Orientational effects on Acanthoscelides obtectus (Say). Journal of Stored Products Research, 40(4), 395-408. DOI: https://doi.org/10.1016/S0022-474X(03)00031-6
• Sarker, S., Sultana, N., & Aminuzzaman, F. M. (2017). Biochemical characterization of Xanthomonas axonopodis pv. malvacearum isolated from infected cotton plant and it’s in vitro sensitivity against some selected chemicals. Artificial Intelligence Review, 11, 1-10. DOI: https://doi.org/10.9734/AIR/2017/35626
• Schaad, N. W., Jones, J. B., & Chun, W. (2001). Laboratory Guide for Identification of Plant Pathogenic Bacteria. 3rd ed.; The American Phytopathological Society: St. Paul, MN, USA.
• Schollenberger, M., Staniek, T. M., Paduch-Cichal, E., Dasiewicz, B., Gadomska-Gajadhur, A., & Mirzwa Mroz, E. (2018). The activity of essential oils obtained from species and interspecies hybrids of the Mentha genus against selected plant pathogenic bacteria. Acta Scientiarum Polonorum Hortorum Cultus, 17(6), 167-174. DOI: https://doi.org/10.24326/asphc.2018.6.17
• Sertkaya, E., Kaya, K., & Soylu, S. (2010). Acaricidal activities of the essential oils from several medicinal plants against the carmine spider mite (Tetranychus cinnabarinus Boisd.) (Acarina: etranychidae). Industrial Crops and Products, 31, 107–112. DOI: https://doi.org/10.1016/j.indcrop.2009.09.009
• Shelke, G. V., Aurangabadkar, L. P., Kashikar, A. R., Wadyalkar, S. A., Phalak, M. S., Kharkarand, H. H., & Umslkarm, G. S. (2012). Identification of resistance source for bacterial blight disease caused by Xanthomonas axonopodis pv. malvacearum and its genetic inheritance in upland cotton. Cotton Research Journal, 3(2), 167-173.
• Shenge, K.C. (2001). Evaluation of plant extracts for the control of Bacterial Blight of Cotton induced by Xanthomonas citri subsp. malvacearum [M.Sc thesis].
• Shirsat, R. P. (2008). Screening of anti-phytopathogenic activity of Terminalia thorelii. Ethnobotanical Leaflets, 12, 538-541.
• Singh, A., Srivastava, S., & Akram, M. (2007). Studies on bacterial leaf blight of cotton (Gossypium spp.). International Journal of Sustainable Crop Production, 2(3), 25-29.
• Soylu, S., Evrendilek, G.A., & Soylu, E.M. (2009). Chemical compositions and antibacterial activities of bitter fennel (Foeniculum vulgare Mill. var. vulgare) and dill (Anethum graveolens L.) essential oils against the growth of food-borne and seed-borne plant pathogenic bacteria. Italian Journal of Food Science, 21, 347-355. DOI: https://www.researchgate.net/publication/284790594.
• Soylu, S., Kara, M., Türkmen, M., & Şahin, B. (2022). Synergistic effect of Foeniculum vulgare essential oil on the antibacterial activities of Ag- and Cu substituted ZnO nanorods (ZnO-NRs) against food, human and plant pathogenic bacterial disease agents. Inorganic Chemistry Communications, 146, 110103. DOI: https://doi.org/10.1016/j.inoche.2022.110103
• Soylu, S., Atay, M., Kara, M., Uysal, A., Soylu, E.M., & Kurt, Ş. (2023). Morphological and molecular characterization of Fusarium incarnatum as a causal disease agent of pepper (Capsicum annuum) fruit rot. Journal of Phytopathology, 171, 688-699. DOI: https://doi.org/10.1111/jph.13228
• Temtek, E. (2021). Kavunda bakteriyel meyve lekesi hastalığına neden olan Acidovorax citrulli’nin bazı bitki uçucu yağları ile in vitro koşullarda kontrolü. Yüksek Lisans Tezi, Iğdır University.
• Thaxton, P. M., & El-Zik, K. M. (2001). Bacterial blight. In: Kirk- patrick T.L., Rothrock C.S. (eds) Compendium of Cotton Diseases. 2nd ed., pp. 34-35.
• Türkmen, M., Kara, M., Maral, H., & Soylu, S. (2022). Determination of chemical component of essential oil of Origanum dubium plants grown at different altitudes and antifungal activity against Sclerotinia sclerotiorum. Journal of Food Processing and Preservation, 46, e15787. DOI: https://doi.org/10.1111/jfpp.15787
• Türkmenoğlu, Z. (1969). Ege Bölgesi pamuklarında zarar yapan pamuk köşeli yaprak leke hastalığı (Xanthomonas malvacearum Erw. Smith)’na karşı tohum ilaçlama denemeleri. Bitki Koruma Bülteni, 9, 223-237.
• Uysal, A., Kurt, Ş., Soylu, S., Soylu, E.M., & Kara, M., (2019). Yaprağı yenen sebzelerdeki mikroorganizma türlerinin MALDI-TOF MS (Matris Destekli Lazer Desorpsiyon/İyonizasyon Uçuş Süresi Kütle Spektrometresi) tekniği kullanılarak tanılanması. Yüzüncü Yıl Üniversitesi Tarım Bilimleri Dergisi, 29, 595-603. DOI: https://doi.org/10.29133/yyutbd.627850
• Ünlü, N., & Elçi, E. (2019). Antibacterial effects of eucalyptus and some commercial plant essential oils on tomato bacterial canker disease (Clavibacter michiganensis subsp. michiganensis). Plant Protection Bulletin, 59(2), 39-47. DOI: https://doi.org/10.16955/bitkorb.471162
• Verma, J. P. (1986). Bacterial Blight of Cotton. CRC Press, Boca Ratoon, FL, USA.
• Verma, J. P., & Singh, R. P. (1974). Recent studies on the bacterial diseases of fiber and oil seed crops in India. Plant Pathology, 134-145.
• Wallace, T.P., & El-Zik, K.M. (1990). Quantitative analysis of resistance in cotton to three new isolates of the bacterial blight pathogen. Theoretical and Applied Genetics, 79, 443-448. DOI: https://doi.org/10.1007/BF00226150.
• Watkins, G. M. (1981). Compendium of Cotton Diseases, 240. St Paul, MN: American Phytopathology Society.
• Zachowski, M.A., Çınar, Ö., & Rudolph, K. (1989). Characterization of Xanthomonas campestris pv. malvacearum (angular leaf spot of Cotton) isolates from Turkey and resistance tests of Turkish cotton cultivars. Phytopathologia Mediterranea, 28, 10-15.
• Zenelt, W., Krawczyk, K., & Borodynko-Filas, N. (2021). Biodiversity and scope of endophytic and phytopathogenic bacterial species identified in plant samples investigated in the Plant Disease Clinic laboratory. Journal of Plant Protection Research, 61(1), 63-82, DOI: https://doi.org/10.24425/jppr.2021.136274