Gymnosporangium Species – An Important Issue of Plant Protection

  • 1 Institute of Horticulture, Latvia University of Agriculture, Graudu iela 1, Krimūnu pag., Dobeles nov., LV-3701, , Latvia

Abstract

Rusts (Fungi, Basidiomycota, Pucciniomycotina, Pucciniomycetes, Pucciniales) are one of the most important causal agents of diseases and they are infecting many plants including cereals and field crops, vegetables, trees and many ornamentals. They have been studied for a long time and have economic importance among the plant diseases caused by agents of different species of fungi. In Europe, thirteen rust genera have been reported, of which the genus Gymnosporangium is the second largest after genus Phragmidium. The most significant fruit tree rust pathogen is the genus Gymnosporangium. The literature review shows quite limited scientific information about this genus and its species. Studies have mainly focused on some stages of the pathogen development cycle, which are significant for the spread of diseases - uredo and teleito stages. Special attention of the review was paid to European pear rust (caused by G. sabinae (Dicks.) G. Winter), the distribution of which has increased during the last ten years, especially in organic pear orchards. Currently there is a limited number of scientific publications about European pear rust, and they are mainly based only on observations in vitro without trials in the field, despite the fact that it has become one of the most devastating diseases. Therefore, the presented review analyses the rust exploration history, diversity and distribution of species, life cycle, development biology and plant protection issues.

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  • Agrios, G. N. (1997). Plant Pathology. Fourth edition. Academic Press, San Diego. 637 pp.

  • Aime, M. C. (2006). Toward resolving family-level relationships in rust fungi (Uredinales). Mycoscience, 47 (3), 112-122.

  • Ainsworth, G. C. (1981). Introduction to the History of Plant Pathology. Cambridge University Press, Cambridge, West Nyack, New York, U.S.A. 332 pp.

  • Aldwinckle, H. S., Pearson, R. C., Seem, R. C. (1980). Infection periods of Gymnosporangium juniperi-virginianae on apple. Phytopathology, 70, 1070-1073.

  • Arthur, J. C. (1916). A gymnosporangium with repeating spores. Amer. J. Bot., 3, 40-45.

  • Bahēecioğlu, Z. (2001). New records of Pucciniaceae from Turkey. Plant Dis. Res., 16, 17-22.

  • Bartkowska, A. (2007). Ultrastructural examinations of the parasitic contact of Tuberculina persicina with Puccinia caricina and Puccinia graminis. Phytopathol. Polon., 43, 69-76.

  • Belomesyatseva, D. B. (2004). World survey of juniper-associated fungi. Mycena, 4, 127.

  • Bennett, M., Gallagher, M., Fagg, J., Bestwick, C., Paul, T., Beale, M., Mansfield, J., (1996). The hypersensitive reaction, membrane damage and accumulation of autofluorescent phenolics in lettuce cells challenged by Bremia lactucae. Plant J., 9, 851-865.

  • Börner, H. (2009). Pflanzenkrankheiten und Pflanzenschutz. Springer-Verlag, Berlin (Heidelberg). 708 S.

  • Boyd, L. A., Ridout C., O’Sullivan, D. M., Leach, J. E., Leung, H. (2013). Plant-pathogen interactions: Disease resistance in modern agriculture. Trends Gen., 29, 233-240.

  • Boyle, J. S., Fergus, C. L., Schein, R. D. (1974). Frank D. Kern. Phytopathology, 6, 766.

  • Cummins, G. B., Hiratsuka, Y. (1984). Families of Uredinales. Rep. Tottori Mycol. Inst., 22, 191-208.

  • Cummins, G. B., Hiratsuka, Y. (2003). Illustrated Genera of Rust Fungi. American Phytopathological Society, St. Paul, MN. 240 pp.

  • Dangl, J. L., Dietrich, R. A., Richberg, M. H. (1996). Death don’t have no mercy: Cell death programs in plant-microbe interactions. Plant Cell, 8, 1793-1807.

  • De, Ryck, A. (2001). Will pear rust (Gymnosporangium fuscum = G. sabinae) become important? Fruitteelt Nieuws, 14, (11), 6-7.

  • Deacon, J. (2006). Fungal Biology. Wiley-Blackwel, Hoboken, NJ. 371 pp.

  • Dervis, S., Dixon, L., Doğanlar, M., Rossman, A. (2010). Gall production on hawthorns caused by Gymnosporangium spp. in Hatay province, Turkey. Phytoparasitica, 38, 391-400.

  • Dinē, N., Yilmaz, M. A. (1978). Investigation on Gymnosporangium spp. in eastern and southern areas of Turkey. J. Turkish Phytopathol., 7, 99-104.

  • Ditmar, F. (1817). Die Pilze Deutschlands: Tuberculina persicina. In: Sturm, J. (Ed.). Deutschlands Flora in Abbildungen nach Natur mit Beschreibungen. Lange, Nurnberg, S. 98-100. Available at: http://www.indexfungorum.org/names/NamesRecord.asp?RecordID=153382 (accessed 10 March 2016).

  • Dodge, B. O. (1915). The effect of the host on the morphology of certain species of Gymnosporangium. Bull. Torrey Bot. Club, 42, 519-544.

  • Dolińska, T., Schollenberger, M. (2011). Relationship between Gymnosporangium sabinae (pear rust) and Cladosporium herbarum. Progr. Plant Protect., 51 (2), 644-647.

  • Dong, X.-L., Li, B.-H., Zhang, Z.-F., Li, B.-D., Xu, X.-M. (2006). Effect of environmental conditions on germination and survival of teliospores and basidiospores of the pear rust fungus (Gymnosporangium asiaticum). Eur. J. Plant Pathol., 115, 341-350.

  • Eglitis, M. (1938). Plant Diseases [Augu slimîbas.] Zemnieka Domas, Rîga. 455 pp. (in Latvian).

  • Eihe, M. (2004). New disease in pear orchards [Bumbieru stādîjumus apdraud jauna slimîba]. Agrotops, 1, 38-39 (in Latvian).

  • Enescu, C. M., Houston Durrant T., Caudullo G., de Rigo, D. (2016). Juniperus communis in Europe: Distribution, habitat, usage and threats. In: San-Miguel-Ayanz, J., de Rigo, D., Caudullo, G., Houston Durrant, T., Mauri, A. (eds.), European Atlas of Forest Tree Species. Publication Office of the European Union, European Commission, Luxembourg, p. 104.

  • Erdošdu, M., Hüseyin, E., Suludere, Z. (2010). Description of the rusts from Kemaliye (Erzincan, Turkey). Phytoparasitica, 38, 81-93.

  • Farr, D. F., Bills, G. F., Chamuris, G. P., Rossman, A. Y. (1995). Fungi on Plants and Plant Products in the United States. The American Phytopathological Society, APS Press, St. Paul, Minnesota, USA. 1225 pp.

  • Figueiredo, M. B. (2000). The plasticity of rust life cycles. O Biologico, 62 (1), 107-111.

  • Filipp, M., Spornberger, A., Schildberger, B. (2012). Monitoring of pear rust (Gymnosporangium sabinae) in Austria and implications for possible control strategies. In: The 15th International Conference on Organic Fruit- Growing, February 20-22, 2012. Foerdergemeinschaft Oekologischer Obstbau e.V., Hohenheim, pp. 65-73.

  • Fischer, M., Weber, H. J. (2005). Birnenanbau Integriert und Biologisch. Eugen Ulmer, Stuttgart, Hohenheim. 164 S.

  • Fitzner, S., Fischer, M. (2005). Bewertung von Pyrus-arten auf Befall mit Birnengitterrost (Gymnosorangium sabinae Dicks.). Erwebs - Obstbau, 47, 37-39.

  • Gebauer, J., Ebert, G., Buttner, C. (2001). Birnengitterrost - eine zunehmende Gefahf in unseren Kleingarten. Gesunde Pflanzen, 53, 44-47.

  • Gjærum, H. B., Gauslaa, Y., Talg¸, V. (2008). Gymnosporangium sabinae found in Norway. Plant Pathol., 57, 376.

  • Gold, R. E., Mendgen, K. (1991). Rust basidiospore germlings and disease initiation. In: Cole, G. T., Hoch, C. (eds.). The Fungal Spore and Disease Initiation in Plants and Animals. Plenum, New York, pp. 67-99.

  • Govrin, E. M., Levine, A. (2000). The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol., 10, 751-757.

  • Hau, B., De Vallavieille-Pope, C. (2006). Wind-dispersed diseases. In: Cooke, B. M., Jones, G. D., Kaye, B. The Epidemiology of Plant Diseases. Springer, Netherlands, pp. 387-416.

  • Heath, M. C. (2000). Hypersensitive response-related death. In: Lam, E., Fukuda, H., Greenberg, J. (eds.), Programmed Cell Death in Higher Plants. Springer Science+Business media, LLC, pp. 77-90.

  • Helfer, S. (2005). Overview of the rust fungi (Uredinales) occurring on Rosaceae in Europe. Nova Hedwigia, 81, 325-370.

  • Hilber, U., Schüepp, H., Schwinn, F. J. (1990). Studies on infection biology of Gymnosporangium fuscum DC. J. Plant Dis. Protect., 97 (3), 299-305.

  • Hilber, U., Schüepp, H., Schwinn, F. J., (1990a). Untersuchungen zur Entwicklung des Birnengitterrostes. Schweizer Zeitschrift für Obst und Weinbau, 126, 486-494.

  • Hilber, W., Siegfried, W. (1989). Gitterrost auf Birnbaum und Wacholder-Sanierungsmassnahmnen bei starkem Befall. Schweizer Garten, 8, 23-28.

  • Hiratsuka, Y., Hiratsuka, N. (1980). Morphology of spermogonia and taxonomy of rust fungi. Rep. Tottori Mycol. Inst., 18, 257-68.

  • Hiratsuka, Y., Sato, S. (1982). Morphology and taxonomy of rust fungi. In: Scot, K. J., Chakravory, A. K. (eds.). The Rust Fungi. Academic Press, London, New York, pp. 1-36.

  • Holb, I. J. (2013). Apple scab management in organic fruit orchards: Epidemiology, forecasting and disease control strategies. Acta Horticult., 1001, 223-234.

  • Horst, R. K. (2013). Rusts. In: Horst, R. K. Westcott's Plant Disease Handbook. Springer, Netherlands, pp. 341-362.

  • Hunt, R. S., O'Reilly, H. J. (1978). Overwintering of pear trellis rust in pear. Plant Dis. Rep., 62, (8), 659 -660.

  • Hüseyinov, E. (2000). New records of microfungi for Turkey. Israel J. Plant Sci., 48, 75-78.

  • Hüseyinov, E., Selēuk, F. (2001). Contribution to study of mycoflora of Turkey. II. Ascomycetous and basidiomycetous microfungi of forest trees and shrubs in the Black Sea coast (Rize Province). Mikologiya i Fitopatologiya, 35, 13-15.

  • Iakimova, E. T., Michalczuk, L., Woltering, E. J. (2005). Hypersensitive cell death in plants - its mechnisms and role in plant defence against pathogens. J. Fruit Ornamental Plant Res., 13, 135-158.

  • Ivarsson, K. (2011). Studies of environmental factors (temperature and relative humidity) effecting the development of pear rust (Gymnosporangium fuscum) and studies of control methods: Horticulture and Agricultural Science Department of Plant Protection Biology, Faculty of Landscape Planning, Sveriges lantbruksuniversitet, Alnarp. 30 pp.

  • Jones, J. D. G., Dangl, J. L. (2006). The plant immune system. Nature, 444, 323-329.

  • Juhasova, G., Praslieka, J. (2002). Occurrence and harmful effects of Gymnosporangium sabinae (Dicks.) in Slovak Republic. Plant Protection Sci., 38, 89-93.

  • Karlsson, K. (2008). The distribution of Gymnosporangium fuscum and its implication on pear cultivation in Sweden. Bachelor Project, Sveriges Lantbruksuniversitet, Alnarp, Sweden. Available at: http://ex-epsilon.slu.se/2199/1/pear_rust_bachelor.pdf.

  • Kellerhals, M., Szalatnay, D., Hunziker, K., Duffy, B., Nybom, H., Ahmadi-Afzadi, M., Höfer, M., Richter, K., Lateur, M. (2012). European pome fruit genetic resources evaluated for disease resistance. Trees, 26, 179-189.

  • Kemp, H., van Dieren, M. C. A. (2000). Screening of pear cultivars for resistance to fungal diseases (Venturia pirina, Nectria galligena). Acta Horticulturae, 538, 95-101.

  • Kern, F. D. (1908). Studies in the genus Gymnosporangium. Bull. Torrey Bot. Club, 35, 499-511.

  • Kern, F. D. (1911). A biologic and taxonomic study of the genus Gymnosporangium. Bull. New York Bot. Garden, 7, 391-483.

  • Kern, F. D. (1973). A host survey of Gymnosporangium. Mycopathol. Mycol. Appl., 51 (1), 99-101.

  • Kolmer, J. A., Ordonez, M. E., Groth, J. V. (2009). The rust fungi. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd Chichester, pp.1-8.

  • Lāce, B., Bankina, B. (2013). Evaluation of European pear rust severity depending on agro-ecological factors. In: Research for Rural Development 2013: Annual 19th International Scientific Conference Proceedings, 15-17 May 2013. Latvia University of Agriculture, Jelgava, pp. 6-12

  • Lāce, B., Lācis, G. (2015). Evaluation of pear (Pyrus communis L.) cultivars in Latvia. Horticult. Sci., 42, 107-113.

  • Linnaeus, C. (1753). Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Berolini: impensis G.C. Nauk, 2, 561-1200.

  • Lutz, M., Bauer, R., Begerow, D., Oberwinkler, F. (2004a). Tuberculina-Helicobasidium: Host specificity of the Tuberculina-stage reveals unexpected diversity within the group. Mycologia, 96, 1316-1329.

  • Lutz, M., Bauer, R., Begerow, D., Oberwinkler, F. (2004b). Tuberculina Thanatophytum/rhizoctonia crocorum - Helicobasidium: A unique mycoparasitic-phytoparasitic life strategy. Mycol. Res., 108, 227-238.

  • Meier, U. (2001). Growth stages of mono and dicotyledonous plants. BBCH Monograph. Federal Biological Research Centre for Agriculture and Forestry, Bonn. 622 pp.

  • Mitrofanova, O. V. (1970). Pear Rust and Control Posibilities [Ìèòğîôàíîāà, Î. ā. ğæàā÷èíà ãğóøè è ìåğû áîğüáû ń íåé]. Izdatelstvo Krim, Simferopol. 46 pp. (in Russian).

  • Naton, B., Hahlbrock, K., Schmelzer, E. (1996). Correlation of rapid cell death with metabolic changes in fungus-infected, cultured parsley cells. Plant Physiol., 112, 433-444.

  • Ormrod, D. J., O'Reilly, H. J., van der Kamp, B. J., Borno, C. (1984). Epidemiology, cultivar susceptibility, and chemical control of Gymnosporangium fuscum in British Columbia. Canadian J. Plant Pathol., 6, 63-7.

  • Pearson, R. C., Seem, R. C., Meyer, F. W. (1980). Environmental factors influencing the discharge of basidiospores of Gymnosporangium juniperivirginianae. Phytopathology, 70, 262-266.

  • Prokopova, B. (2011). The severity of European pear rust depending on pear cultivars. Sodininkyste ir Darzininkyste, 30 (2), 43-50.

  • Rancane, R., Lace, B., Lacis, G. (2012). Distribution and development of European pear rust in Latvia and relationship between severity and yield. Integrated Plant Protection in Fruit Crops” Subgroup “Pome Fruit Diseases”, IOBC-WPRS Bulletin (International Organization for Biological Control, West Palearctic Regional Section), 84, 39-45.

  • Richards, H.M(1889). The uredo-stage of Gymnosporangium. Bot. Gazette, 14 (9), 211-216.

  • Saccardo, P. A. (1881). Fungi Italici Autographice Delineati. Fascs 17-28, Patavii, Italy. Tabs 641-1120.

  • Schildberger, B. (2011). Untersuchungen zur Biologie des Birnengitterrostes (Gymnosporangium sabinae) und zum Befallsverlauf an der Birne. Wissenbericht, 173-176.

  • Shamsi, S., Naher, N. (2010). Hypoparasitic fungus Tuberculina persicina (Ditm. Ex Fr.) sacc., as biocontrol agent for rusts. Dhaka Univ. J. Biol. Sci., 19, (1), 99-102.

  • Sharma, P. D. (2014). Principles of Plant Pathology. Rastogi Publications, New Delhi (India). 478 pp.

  • Shirasu, K., Schulze-Lefert, P. (2000). Regulation of cell death in disease resistance. Plant Mol. Biol., 44, 371-385.

  • Smarods, J. (1947). Retrieved from National Museum collection of Latvia (Latvijas Nacionālā Muzeja krājumi) database. Available at: http://www.nmkk.lv/Items/ItemViewForm.aspx?id=177841 (accessed 7 June 2017).

  • Smarods, J. (1951). Retrieved from National Museum collection of Latvia (Latvijas Nacionālā Muzeja krājumi) database. Available at: http://www.nmkk.lv/Items/ItemViewForm.aspx?id=177890 (accessed 7 June 2017).

  • Soriano, J. M., Joshi, S. G., van Kaauwen, M. Noordijk, Y., Groenwold, R., Henken, B., van de Weg W. E., Schouten, H. J. (2009). Identification and mapping of the novel apple scab resistance gene Vd3. Tree Genetics and Genomes, 5, 475-482.

  • Soufflet-Freslon, V., Gianfranceschi, L., Patocchi, A. Durel, C. E. (2008). Inheritance studies of apple scab resistance and identification of Rvi14, a new major gene that acts together with other broad-spectrum QTL. Genome, 51, 657-667.

  • Thaxter, R. (1886). On certain cultures of Gymnosporangium, with notes on their Roesteli¿. Proc. Amer. Acad. Arts Sci., 22, 259-269.

  • Thaxter, R. (1889). Notes on cultures of Gymnosporangium made in 1887 and 1888. Botanical Gazette, 14 (7), 163-172.

  • Thaxter, R. (1891). The Connecticut species of Gymnosporangium (cedar apples). Bull. Connecticut Agricult. Exper. Station, 107, 1-6.

  • Toome, M., Aime, M. C. (2012, January). Pucciniomycetes. Available at: http://tolweb.org/%20Pucciniomycetes/51246/2012.01.30 (accessed 11 August 2016).

  • Vilar, L., Caudullo, G., de Rigo, D. (2016). Juniperus oxycedrus in Europe: distribution, habitat, usage and threats. In: San-Miguel-Ayanz, J., de Rigo, D., Caudullo, G., Houston Durrant, T., Mauri, A. (eds.). European Atlas of Forest Tree Species. Publication Office of the European Union, European Commission, Luxembourg, p. 105.

  • Wicker, E. F. (1981). Natural control of white pine blister Rust by Tuberculina maxima. Phytopatalogy, 71, 997-1000.

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