Molecular identification and disease management of false smut disease (Graphiola phoenicis) on date palms grown in Türkiye

Year 2025, Volume: 30 Issue: 2, 547 - 559, 21.08.2025

Işılay Lavkor

https://doi.org/10.37908/mkutbd.1652986

Abstract

The date palm (Phoenix dactylifera L.) is a common ornamental tree in Turkey, frequently found in homes, hotels, and public gardens. This study aimed to molecularly identify Graphiola phoenicis, the causal agent of false smut in date palms grown in Turkey, and to determine the efficacy of fungicides in controlling the disease. Characteristic false smut symptoms were observed on date palms during 2020–2021 surveys in Adana. These included numerous cup-shaped black fruiting bodies (sori) that appeared on theauricles and the rachis of the fronds, releasing whitish filaments with powdery yellow spores. Molecular identification of the pathogen was carried out based on the internal transcribed spacer (ITS) region and the large subunit of ribosomal DNA (LSU rDNA). NCBI accession numbers assigned to the ITS sequences are PQ060144 and PQ060145, as well as PQ060146 for the LSU rDNA. Under field conditions, four fungicidal treatments—Boscalid (26.7%) + Pyraclostrobin (6.7%), Prothioconazole (175 g/L) + Trifloxystrobin (88 g/L), Copper oxychloride (700 g/L), and Tea tree oil (222.5 g/L)—were evaluated for disease control. In a two-year trial, a combination of Boscalid + Pyraclostrobin was the most effective, reducing disease incidence by 90.40% and 88.48% in consecutive years. This study not only provides the first molecular characterisation and confirms the presence of G. phoenicis in Türkiye but also proposes an effective fungicide strategy for its control in ornamental date palms.

Keywords

Date palm , Fungicides , Türkiye , Graphiola phoenicis , False smut

Supporting Institution

Gıda ve Kontrol Genel Müdürlüğü

Thanks

This study was financially supported by the Ministry of Agriculture and Forestry, General Directorate of Food and Control of the Republic of Türkiye. I would like to thank Deda BÜYÜKÖZTÜRK, Okan ÖZGÜR, Tahsin AY and Şakir ŞAHİN for their support of this study.

Türkiye’de yetişen hurma ağaçlarında yalancı sürme hastalığının (Graphiola phoenicis) moleküler tanımlanması ve hastalık yönetimi

Abstract

Türkiye’de yaygın bir süs ağacı olan hurma ağacı (Phoenix dactylifera L.) sıklıkla evlerde, otellerde ve halka açık bahçelerde bulunur. Bu çalışmanın amacı, Türkiye’de yetiştirilen hurma ağaçlarında yalancı sürme hastalığına neden olan Graphiola phoenicis’i moleküler olarak tanımlamak ve fungisitlerin hastalığı kontrol etmedeki etkinliğini belirlemektir. Bu kapsamda Adana ilinde 2020-2021 yılları arasında yapılan surveyler sırasında, hurma ağaçlarında yalancı sürme hastalığının karakteristik belirtileri gözlenmiştir. Hastalık belirtileri gösteren ağaçların yaprak ve orta damarında çok sayıda fincan şeklinde siyah meyve gövdeler (sori) ve bu yapılardan beyazımsı ipliksi, toz halinde sarı renkli sporlar gözlenmiştir. Patojenin moleküler tanımlaması, internal transcribed spacer (ITS) ve large subunit ribosomal DNA (LSU rDNA) gen bölgeleri temel alınarak gerçekleştirilmiştir. Fngal etmene ait ITS (PQ060144 ve PQ060145) ve LSU rDNA (PQ060146) gen bölgelerinin dizilerinin Gen Bankası (NCBI) erişim numaraları alınmıştır. Tarla koşulları altında, dört fungisit uygulaması - Boscalid (%26.7) + Pyraclostrobin (%6.7), Prothioconazole (175 g/L) + Trifloxystrobin (88 g/L), Bakır oksiklorür (700 g/L) ve Çay ağacı yağı (222.5 g/L)- hastalık kontrolü için değerlendirilmiştir. İki yıllık bir denemede, Boscalid + Pyraclostrobin kombinasyonu, hastalık insidansını ardışık yıllarda %90.40 ve %88.48 oranında azaltarak en etkili yöntem olmuştur. Bu çalışma, G. phoenicis’in Türkiye’de yetişen hurma ağaçlarında hastalık etmeni olduğuna yönelik ilk moleküler çalışma olup, aynı zamanda süs hurma ağaçlarında hastalığın kontrolünde etkili bir fungisit uygulama stratejisi de önermektedir.

Keywords

Graphiola phoenicis , Türkiye , Hurma ağaçları , Yalancı sürme , Fungusit

References

• Abbas, E.H., & Abdulla, A.S. (2004). First report of false smut disease caused by Graphiola phoenicis on date palm trees in Qatar. Plant Pathology, 53, 815. https://doi.org/10.1111/j.1365-3059.2004.01084.x
• Barnes, C.W., & Szabo, L.J. (2007). Detection and identification of four common rust pathogens of cereals and grasses using real-time polymerase chain reaction. Phytopathology, 97 (6), 717-727. https://doi.org/10.1094/PHYTO-97-6-0717
• Begerow, D., Bauer, R., &. Oberwinkler, F. (1997). Phylogenetic studies on nuclear large subunit ribosomal DNA sequences of smut fungi and related taxa. Canadian Journal of Botany, 75, 2045-2056.
• CAB International (2003). Crop protection compendium Wallingford, CABI Publishing, UK.
• Cabrera, R., Hodgson, F., Armas, M.D., Santiago, C.T., Lorenzo, C.D., Prendes, C., & Plata, P. (1990). A fungus disease of canary palm (Phaenix canariensis chab. ) produced by Graphiola phoenicis (Mong)Poit. Fisher in the Canary Islands. Phytoma Espana, 18, 21-25.
• Chohan, J.S. (1972). Diseases of date palm (Phoenix dactylifera L.) and their control. Punjab Horticulture Journal, 12, 25-32.
• Cole, G. (1983). Graphiola phoenicis: A taxonomic enigma. Mycologia, 75, 93-116.
• Cúndom, M.A. (2009). Graphiola phoenicis manifestation over Roebelenii phoenicis in Argentina. Summa Phytopathologica, 35, 239-239.
• Djerbi, M. (1983). Diseases of the date palm (Phoenix dactylifera). F.A.O Regional Project for Palm and Dates Research Center in the Near East and North Africa.
• Edongali, E.A. (1996). Disease of date palms (Phaenix dactilifera L.) of Libya. Arab Journal of Plant Protection, 14, 41-43.
• El Deeb, H.M., Lashin, S.M., & Arab, Y.A. (2007). Distribution and pathogenesis of date palm fungi in Egypt. Acta Horticulturae, 736, 421-429.
• El Gariani, N.K., El Rayani, A.M., & Edongali, E.A. (2007). Distribution of phytopathogenic fungi on the coastal region of Libya and their relationships with date cultivars. Acta Horticulturae, 736, 449-455. https://doi.org/10.17660/ActaHortic.2007.736.42
• Er, Ö., & Akgül, D.S. (2021). Osmaniye ili buğday ekim alanlarında sap çürüklüğü hastalığıyla ilişkili Fusarium türleri. Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi, 26 (2), 292-302. https://doi.org/10.37908/mkutbd.884544
• Felsenstein, J. (1985). Confidence limits in phylogenies: an approach using the bootstrap. Evolution, 39, 783-791.
• Guar, V.K. (2000). Studies on Graphiola leaf spot disease of date palm. Integrated Plant disease management for sustainable agriculture. Proceedings of International Conference, India, 471-472.
• Gupta P.C., & Mehta, N. (1985). Recommendations regarding various diseases of arid zone fruit crops from hisar centre. AICRP Arid Zone Fruits.
• Habana Parveen, H., Saharan, M.S., Verma, A., & Sharma, I. (2015). Pathogenic variability among Tilletia indica isolates and distribution of heterothallic alleles in the Northwestern Plains Zone of India. Turkish Journal of Agriculture and Forestry, 39 (1), 63-73. https://journals.tubitak.gov.tr/agriculture/vol39/iss1/8
• Haldhar, S.M., Maheshwari, S.K., & Muralidharan, C.M. (2017). Pest status of date palm (Phoenix dactylifera) in arid regions of India: A review. Journal of Agriculture and Ecology, 3, 1-11.
• Hawksworth, D.L., Kirk, P.M., Sutton, B.C., & Pegler, D.N. (1995). Ainsworth & Bisby’s dictionary of the fungi. 8th Edition, CAB International, Wallingford, UK.
• Hyde, K.D., Nilsson, R.H., Alias, S.A., Ariyawansa, H.A., Blair, J.E., Cai, L., de Cock, A.W.A.M., Dissanayake, A.J., Glockling, S.L., Goonasekara, I.D., Gorczak, M., Hahn, M,. Jayawardena, R.S., Van Kan, J.A.L., Laurence, M.H., Lévesque, C.A., Li, X., Liu, J.K., Maharachchikumbura, S.S.N., Manamgoda, D.S., Martin, F.N., McKenzie, E.H.C., McTaggart, A.R., Mortimer, P.E., Nair, P.V.R., Pawłowska, J., Rintoul, T.L., Shivas, R.G., Spies, C.F.J., Summerell, B.A., Taylor, P.W.J., Terhem, R.B., Udayanga, D., Vaghefi, N., Walther, G., Wilk, M., Wrzosek, M., Xu, J.C., Yan, J.Y., & Zhou, N. (2014). One stop shop: Backbones trees for important phytopathogenic generates: I. Fungal Diversity, 67, 21-125. https://link.springer.com/article/10.1007/s13225-014-0298-1#Sec3
• Kurt, Ş., Soylu, S., Uysal, A., Soylu, E.M., & Kara, M. (2020). Ceviz gövde kanseri hastalığı etmeni Botryosphaeria dothidea’nın tanılanması ve bazı fungisitlerin hastalık etmenine karşı in vitro antifungal etkinliklerinin belirlenmesi. Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi 25 (1), 46-56. https://doi.org/10.37908/mkutbd.686111
• Lodha, S. (2003). Influence of pinnae position, leaf age and some fungicides on the development of Graphiola leaf spot on date palm. Arab Journal of Plant Protection, 21, 162-165. https://asplantprotection.org/wp-content/uploads/2018/07/V21-2_162-165.pdf
• Manu, D.G., Pramoda S.S., Ramanathan A., Ramchander, S., Manonmani S., Jeyaprakash, P., & Robin, S. (2017). Isolation, characterization and pathogenesis of Ustilaginoidea virens causing false smut disease in rice (Oryza sativa L.). International Journal of Current Microbiology and Applied Sciences, 6, 632-64. https://www.ijcmas.com/6-7-2017/D.G.%20Manu,%20et%20al.pdf
• Martinez, A.P. (1966). False smut of palms. Circular Plant Pathology, 43, 1. https://ccmedia.fdacs.gov/content/download/11049/file/pp43.pdf
• Mehta. N., Gupta, P.C., Tharija, R.K., & Dang, J.K. (1989). Varietal behavior and efficacy of different fungicides for the control of date palm leaf spot caused by Graphiola phoenicis. Tropical Pest Management, 35, 117-119. http://dx.doi.org/10.1080/09670878909371336
• Nixon, R.W. (1957). Differences among varieties of the date palm in tolerance to Graphiola leaf spot. Plant Disease Reporter, 41, 1026-1028
• O’Donnell, K. (1993). Fusarium and its near relatives. DR Reynolds and JW & Taylor (Eds), The Fungal holomorph: Mitotic, meiotic and pleomorphic speciation in fungal systematics (p. 225–233). CABI, Wallingford, UK. https://www.researchgate.net/publication/224900762_Fusarium_and_its_near_relatives
• Oğuz, M., Soylu, S., Üremiş, İ., Uysal, A., Soylu, E.M., Kurt, Ş., & Sertkaya, E. (2024). Determination of fungal and bacterial microbiota of broomrape species found in their major host plants grown in Hatay province of Türkiye. Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi, 29 (3), 896-911. https://doi.org/10.37908/mkutbd.1516441
• Pal, A.K. (2019). Graphiola phoenicis (Mong.) Poit. : An enigmatic parasitic fungus from mangrove palm of Indian Sundarbans. Journal of Mycopathological Research, 57, 89-93. https://imskolkata.org/pdf/july_19/asis%20pal.pdf
• Piepenbring, M., Nold, F., Trampe, T., & Kirschner, R. (2012). Revision of the genus Graphiola (Exobasidiales, Basidiomycota). New Hedwigia, 94, 67-96.
• Sattar, A.M.H., Aulaqi, W.A., & Ibrahim, R.Y. (2013). Occurrence of false smut on date palm (Phoenix dacyilifera L.). Southern Coastal Plain of Yemen Journal of Agricultural Science, 5, 22-25.
• Sepúlveda, G., Arismendi, M., Huanca-Mamani, W., Cárdenas-Ninasivincha, S., Salvatierra, R., & Latorre, B. (2017). Presence of false smut (Graphiola phoenicis (Moug. ex Fr.) Poit.) on Canary date palm (Phoenix canariensis) on Easter Island, Chile. Cıencıa E Investigación Agraria, 44, 307-311. https://doi.org/10.7764/rcia.v44i3.1787
• Simone, G.W. (2004). Graphiola leaf spot (false smut). M.L. Elliot, T.K. Broschat, J.Y. Uchida, and G.W. Simone (Eds.), Conpendium of ornamental palm diseases and disorders (p. 26-27). American Phytopathological Society, St. Paul.MN.
• Singh, D., Kumar, K., Sivalingam, P.N., Ram, C., Patil, G.B., & Subhash, N. (2023). A functional decision support system for management of Graphiola leaf spot (Graphiola phoenicis) disease during hardening of date palm tissue cultured plants in a greenhouse. Journal of Agriculture and Ecology, 17, 66-70.
• Sinha, M.oK.,Singh, R., & Jeyarajan, R. (1970). Graphiola leaf spot on date palm (Phoenix dactylifera L.) susceptibility of date varieties effect on chlorophyll content. Plant Disease Reports, 54, 617-619.
• Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
• Tubaki, K., & Yokoyama, T. (1971). Cultural aspects of Graphiola phoenicis. Mycopathologia et Mycologia applicata, 43, 49-60.
• Uysal, A., Kurt, Ş., Soylu, S., Kara, M., & Soylu, E.M. (2022). Hatay ilinde yer alan turunçgil paketleme tesislerinde meyve ve hava kökenli mikrobiyata içerisindeki fungal ve bakteriyel türler ile yoğunluklarının belirlenmesi. Mustafa Kemal Üniversitesi Tarım Bilimleri Dergisi, 27 (2), 340-351. https://doi.org/10.37908/mkutbd.1095692
• Vánky, K. (1987). Illustrated genera of smut fungi. Gustav Fischer Verlag, Stuttgart and New York.
• White, T.J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. MA Innis, DH Gelfand, JJ and White Sninsky TJ (Eds). PCR Protocols: A guide to methods and applications (p. 315-322). Academic Press.
• Zaid, A., de Wet, P.F., Djerbi, M., & Oihabi, A.C. (2002). Chapter XII: Diseases and pests of date palm. Zaid,. A and E. Arias-Jimenez, (Eds.), Date palm cultivation (p.227-281). FAO plant production and protection paper 156. https://cdn.ksu.edu.sa/ksu-subsites/iinpd.ksu.edu.sa/books/pdf/0006.pdf