Abstract
Natural sporulation of Cronartium ribicola and C. flaccidum were investigated on known and potential alternate hosts growing in three botanical gardens representing different geographic regions in Finland and in some natural habitats next to the northern botanical garden. Uredinia and telia of Cronartium were searched for from over 27,000 leaves collected or checked in the field in 66–96 species representing 16 plant families susceptible to Cronartium. Cronartium ribicola was found on 19 species or cultivars, while C. flaccidum occurred on 17 species. Uredinia and telia of Cronartium ribicola lacked in the southern botanical garden, but they occurred on 5–16 Ribes species or cultivars in the other two botanical gardens. Cronartium ribicola sporulated on one to four Ribes rubrum cultivars, one to three R. uva-crispa cultivars, three to seven R. nigrum cultivars, R. aureum and R. glandulosum in the gardens. Cronartium flaccidum sporulated on five to nine species in the botanical gardens including species of Paeonia, Melampyrum, Loasa, Pedicularis and Vincetoxicum. In natural habitats next to the northern botanical garden, C. flaccidum sporulated also on Melampyrum sylvaticum and Euphrasia stricta var. stricta. Among all the infected species, C. flaccidum sporulated most frequently on Paeonia. For the first time, C. flaccidum was found on E. stricta growing in its natural habitat. Although the frequency of infected leaves under natural inoculum was low for several infected species, the large variety of susceptible species serve as an efficient tool for Cronartium to spread. Based on the amount of natural sporulation in the gardens and their surroundings, both Cronartium rusts are widely distributed and sporulate in different geographic areas in Finland.
Similar content being viewed by others
References
Crane, P. E., Hiratsuka, Y., & Currah, R. S. (2000). Clarification of the life-cycle of Chrysomyxa woroninii on Ledum and Picea. Mycological Research, 104(5), 581–586.
Cummins, G. B., & Hiratsuka, Y. (1991). Illustrated genera of rust fungi (Revised ed.). St. Paul: APS Press.
Diamandis, S., & De Kam, M. (1986). A severe attack of scots pine by the resin top disease in N. Greece. European Journal of Forest Pathology, 16, 247–249.
Gäumann, E. (1959). Die Rostpilze Mitteleuropas. Beiträge zur Kryptogamenflora der Schweiz, 12, 85–93.
Greig, B. J. W. (1987). History of Peridermium stem rust of Scots pine (Pinus sylvestris L.) in Thetford Forest, east Anglia. Forestry, 60, 193–202.
Heikinheimo, O. (1956). Tuloksia ulkomaisten puulajien viljelystä Suomessa. Communicationes Instituti Forestalis Fenniae, 45, 1–129.
Hummer, K., & Finn, C. (1999). Three-year update on Ribes susceptibility to white pine blister rust. Acta Horticulturae, 505, 403–408.
Hylander, N., Jørstad, I., & Nannfeldt, J. A. (1953). Enumeratio Uredinearum Scandinavicarum. Opera Botanica, 1, 12–13.
Kaitera, J. (2000). Analysis of Cronartium flaccidum lesion development on pole-stage Scots pines. Silva Fennica, 34, 21–27.
Kaitera, J., & Hantula, J. (1998). Melampyrum sylvaticum, a new alternate host for pine stem rust Cronartium flaccidum. Mycologia, 90, 1028–1030.
Kaitera, J., & Hiltunen, R. (2011). Susceptibility of Pedicularis spp. to Cronartium ribicola and C. flaccidum in Finland. Forest Pathology, 41, 237–242.
Kaitera, J., & Hiltunen, R. (2012). New alternate hosts for the rusts Cronartium ribicola and Cronartium flaccidum in Finland. Canadian Journal of Forest Research, 42, 1661–1668.
Kaitera, J., & Nuorteva, H. (2003a). Cronartium flaccidum produces uredinia and telia on Melampyrum nemorosum and on Finnish Vincetoxicum hirundinaria. Forest Pathology, 33, 205–213.
Kaitera, J., & Nuorteva, H. (2003b). Relative susceptibility of four Melampyrum species to Cronartium flaccidum. Scandinavian Journal of Forest Research, 18, 499–504.
Kaitera, J., & Nuorteva, H. (2006). Susceptibility of Ribes spp. to pine stem rusts in Finland. Forest Pathology, 36, 225–246.
Kaitera, J., Nuorteva, H., & Hantula, J. (2005). Distribution and frequency of Cronartium flaccidum on Melampyrum spp. in Finland. Canadian Journal of Forest Research, 35, 229–234.
Kaitera, J., Hantula, J., & Nevalainen, S. (2011). Distribution and frequency of Cronartium flaccidum on Melampyrum spp. in permanent sample plots in Finland. Scandinavian Journal of Forest Research, 26, 413–420.
Kaitera, J., Hiltunen, R., & Samils, B. (2012). Alternate host ranges of Cronartium flaccidum and Cronartium ribicola in northern Europe. Botany, 90, 694–703.
Kaitera, J., Kauppila, T., & Hiltunen, R. (2013). Incidence of Cronartium ribicola in Finnish botanical gardens and five-needle pine plantations in northern Finland. Scandinavian Journal of Forest Research, 28, 746–751.
Kaitera, J., Hiltunen, R., & Hantula, J. (2015). Cronartium rusts sporulation on hemiparasitic plants. Plant Pathology, 64, 738–747.
Kaitera, J., Hiltunen, R., & Hantula, J. (2017). Nasa, Nemesia and Euphrasia: new alternate hosts of Cronartium spp. Forest Pathology, 47(2). doi:10.1111/efp.12306.
Kim, M. S., Klopfenstein, N. B., Ota, Y., Lee, S. K., Woo, K. S., & Kaneko, S. (2010). White pine blister rust in Korea, Japan and other regions: comparisons and implications for North America. Forest Pathology, 40, 382–401.
Kivijärvi, P., Heiskanen, L., & Dalman, P. (1999). Luomuherukan viljelytekniikka. Maatalouden Tutkimuskeskuksen Julkaisuja, 49, 1–43.
Klebahn, H. (1901). Kulturversuche mit Rostpilzen X. Zeitschrif für Pflanzenkrankheiten, 10, 136–141.
Klebahn, H. (1905). Kulturversuche mit Rostpilzen XII. Zeitschrif für Pflanzenkrankheiten, 15, 65–108.
Klebahn, H. (1914). Kulturversuche mit Rostpilzen XV. Zeitschrif für Pflanzenkrankheiten, 24, 1–32.
Kummer, V., & Klenke, F. (2015). Der Rostpilz Cronartium flaccidum und sein Wirtsspektrum in Deutschland. Schlechtendalia, 28, 59–70.
Lähde, E., Werren, M., Etholén, K., & Silander, V. (1984). Ulkomaisten havupuulajien varttuneista viljelmistä Suomessa. Communicationes Instituti Forestalis Fenniae, 125, 1–86.
Lindhard Pedersen, H. (1998). Field resistance of black currant cultivars (Ribes nigrum L.) to diseases and pests. Fruit Varieties Journal, 52, 6–10.
Liro, J. I. (1908). Uredinae Fennicae. Bidrag till Kännedom av Finlands Natur och Folk, 65, 1–567.
McDonald, G. L., Richardson, B. A., Zambino, P. J., Klopfenstein, N. B., & Kim, M. S. (2006). Pedicularis and Castilleja are natural hosts of Cronartium ribicola in North America: a first report. Forest Pathology, 36, 73–82.
Moriondo, F. (1975). Caratteristiche epidemiche della ruggine vescicolosa del Pino: Cronartium flaccidum (Alb. et Schw.) Wint in Italia. Annales Accademia Italiana di Scienze Forestali, 24, 331–406.
Mulvey, R. L., & Hansen, E. M. (2011). Castilleja and Pedicularis confirmed as telial hosts for Cronartium ribicola in whitebark pine ecosystems of Oregon and Washington. Forest Pathology, 41, 453–463.
Munck, I. A., Tanguay, P., Weimer, J., Lombard, K., Villani, S., & Cox, K. (2014). Impact of white pine blister rust on resistant and previously immune cultivated Ribes and neighboring ezstern white pine in New Hampshire. In: Proceedings of the IUFRO Joint Conference: Genetics of five-needle pines, rusts of forest trees, & Strobusphere. June 15–20, Ft. Collins, Colorado, USA. Abstract Book. p. 48.
Pluta, S., & Broniarek-Niemiec, A. (2000). Field evaluation of resistance to white pine blister rust of selected blackcurrant genotypes in Poland. HortTechnology, 10, 567–569.
Ragazzi, A., & Dellavalle Fedi, I. (1991) The epidemic course of Cronartium flaccidum on the intermediate host Vincetoxicum hirundinaria. IUFRO Proceedings on Rusts on Pine Working Party Conference, Banff, Alberta, Canada, 18–23 September 1989, 170–177.
Roll-Hansen, F. (1973). Resistance of Paeonia cultivars to Cronartium flaccidum in Norway. European Journal of Forest Pathology, 3, 142–145.
Samils, B., Ihrmark, K., Kaitera, J., Hansson, P., & Barklund, P. (2010). Genetic structure of scots pine blister rust (Cronartium flaccidum and Peridermium pini). Phytopathologia Mediterranea, 49, 428.
Stephan, B. R. (2004). Studies of genetic variation with five-needle pines in Germany. In: Proceedings of the IUFRO five-needle pines WP conference. Breeding and genetic resources of five-needle pines: Growth, adaptability, and Pest ResistanceUSDA Forest Service, Medford, USA. p. 98–102.
Velmala, S. M., Rajala, T., Haapanen, M., Taylor, A. F. S., & Pennanen, T. (2013). Genetic host-tree effects on the ectomycorrhizal community and root characteristics of Norway spruce. Mycorrhiza, 23, 21–33.
Wulff, S., Liendelow, A., Lundin, L., Hansson, P., Axelsson, A.-L., Barklund, P., Wijk, S., & Stahl, G. (2012). Adapting forest health assessments to changing perspectives on threats – a case example from Sweden. Environmental Monitoring Assessment, 184, 2453–2464.
Zambino, P. J. (2000). Evaluating white pine blister rust resistance in Ribes after artificial inoculation. HortTechnology, 10, 544–545.
Zambino, P. J. (2010). Biology and pathology of Ribes and their implications for management of white pine blister rust. Forest Pathology, 40, 264–291.
Zhang, X. Y., Lu, Q., Sniezko, R. A., Song, R. Q., & Man, G. (2010). Blister rusts in China: Hosts, pathogens, and management. Forest Pathology, 40, 369–381.
Ziller, W. G. (1974). The tree rusts of western Canada. Canadian Forest Service Publications, 1329, 1–272.
Acknowledgements
We thank the personnel of the botanical gardens of Oulu, Turku and Helsinki, especially of Ms. Paula Havas-Matilainen and Intern Emeritus Matti Ylirekola, for supporting our survey and helping in collecting the sample material. Ms. Marja-Leena Santanen provided support during the molecular identification protocol and laboratory work, and Ms. Irene Murtovaara prepared the figures.
Author information
Authors and Affiliations
Corresponding author
Additional information
Ritva Hiltunen retired
Rights and permissions
About this article
Cite this article
Kaitera, J., Hiltunen, R., Kauppila, T. et al. Five plant families support natural sporulation of Cronartium ribicola and C. flaccidum in Finland. Eur J Plant Pathol 149, 367–383 (2017). https://doi.org/10.1007/s10658-017-1188-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-017-1188-7