Abstract
Dutch elm disease (DED) is a vascular wilt disease of elms caused by ascomycetous fungi of the genus Ophiostoma. The initial DED pandemic was caused by Ophiostoma ulmi, a relatively weak pathogen when compared to Ophiostoma novo-ulmi, the causal agent of the current pandemic. The latter has been spreading as two distinct subspecies: O. novo-ulmi ssp. novo-ulmi and O. novo-ulmi ssp. americana. Weak prezygotic barriers to hybridization have resulted in the emergence of ssp. novo-ulmi × ssp. americana hybrids in subspecies overlap zones. In this study, samples of host species Ulmus laevis, Ulmus minor and Ulmus glabra from across Croatia were analysed for DED prevalence and pathogen distribution and characterization. Dutch elm disease was confirmed in all three elm species, but the prevalence of the infection was approximately four times higher in U. minor and U. glabra than in U. laevis. Ophiostoma novo-ulmi was identified as the only cause of DED, while O. ulmi was not detected, indicating complete replacement of O. ulmi by O. novo-ulmi in Croatia. PCR–RFLP analysis and sequencing of the cu and col1 genes indicate the presence of both O. novo-ulmi subspecies as well as their hybrids at investigated sites, often in high frequency. The results provide insight into distribution and population structure of Dutch elm disease pathogen in Croatia, as well as an assessment of virulence for selected isolates, which could be utilized for making informed management decisions regarding DED and elm conservation in Croatian forests.
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References
Brasier CM (1981) Laboratory investigation of Ceratocystis ulmi. In: Stipes RJ, Campana RJ (eds) Compendium of elm diseases. The American Phytopathological Society, Minnesota, pp 76–79
Brasier CM (1986) Comparison of pathogencity and cultural characteristics in the EAN and NAN aggressive subgroups of Ophiostoma ulmi. Trans Br Mycol Soc 87:1–13. https://doi.org/10.1016/S0007-1536(86)80001-8
Brasier CM (2000) Intercontinental spread and continuing evolution of the Dutch Elm Disease pathogens. In: Dunn CP (ed) The elms: breeding, conservation, and disease management. Springer, New York, pp 61–72
Brasier CM, Buck KW (2001) Rapid evolutionary changes in a globally invading fungal pathogen (Dutch elm disease). Biol Invasions 3:223–233. https://doi.org/10.1023/A:1015248819864
Brasier CM, Kirk SA (2001) Designation of the EAN and NAN races of Ophiostoma novo-ulmi as subspecies. Mycol Res 105:547–554. https://doi.org/10.1017/S0953756201004087
Brasier CM, Kirk SA (2010) Rapid emergence of hybrids between the two subspecies of Ophiostoma novo-ulmi with a high level of pathogenic fitness. Plant Pathol 59:186–199. https://doi.org/10.1111/j.1365-3059.2009.02157.x
Brasier CM, Webber JF (1987) Positive correlations between in vitro growth rate and pathogenesis in Ophiostoma ulmi. Plant Pathol 36:462–466. https://doi.org/10.1111/j.1365-3059.1987.tb02263.x
Brasier CM, Webber JF (2019) Is there evidence for post-epidemic attenuation in the Dutch elm disease pathogen Ophiostoma novo-ulmi? Plant Pathol 68:921–929. https://doi.org/10.1111/ppa.13022
Brasier CM, Buck K, Paoletti M, Crawford L, Kirk S (2004) Molecular analysis of evolutionary changes in populations of Ophiostma novo-ulmi. Invest Agrar Sist Recur For 13:93–103
Collin E (2002) Strategies and guidelines for the conservation of the genetic resources of Ulmus spp. In: Turok J, Eriksson G, Russel K (eds) Noble hardwoods network: report of the fourth meeting, 4–6 September 1999, Gmunden, Austria and the fifth meeting, 17–19 May 2001, Blessington, Ireland. International Plant Genetic Resources Institute, Rome, pp 50–67
Collin E, Bilger I, Eriksson G, Turok J (2000) The conservation of elm genetic resources in Europe. In: Dunn CP (ed) The elms: breeding, conservation, and disease management. Springer, New York, pp 281–293
Dvořák M, Tomšovský M, Jankovský L, Novotný D (2007) Contribution to identify the causal agents of Dutch elm disease in the Czech Republic. Plant Prot Sci 43:142–145
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259
Hoegger PJ, Binz T, Heiniger U (1996) Detection of genetic variation between Ophiostoma ulmi and the NAN and EAN races of O. novo-ulmi in Switzerland using RAPD markers. Eur J For Pathol 26:57–68. https://doi.org/10.1111/j.1439-0329.1996.tb007
Jacobi WR, Koski RD, Negron JF (2013) Dutch elm disease pathogen transmission by the banded elm bark beetle Scolytus schevyrewi. For Pathol 43:232–237. https://doi.org/10.1111/efp.12023
Kätzel R (2010) Conservation of forest genetic resources: the basis for adaptability in managed forests. In: Spathelf P (ed) Sustainable forest management in a Changing World. Springer, Dordrecht, pp 93–114
Kirisits T (2013) Dutch elm disease and other Ophiostoma diseases. In: Gonthier P, Nicolotti G (eds) Infectious forest diseases. CAB International, Wallingford, pp 256–282
Kirisits T, Konrad H (2004) Dutch elm disease in Austria. Invest Agrar Sist Recur For 13:81–92
Konrad H, Kirisits T, Riegler M, Halmschlager E, Stauffer C (2002) Genetic evidence for natural hybridization between the Dutch elm disease pathogens Ophiostoma novo-ulmi ssp. novo-ulmi and O. novo-ulmi ssp. americana. Plant Pathol 51:78–84. https://doi.org/10.1046/j.0032-0862.2001.00653.x
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Martín JA, Sobrino-Plata J, Rodríguez-Calcerrada J, Collada C, Gil L (2019) Breeding and scientific advances in the fight against Dutch elm disease: will they allow the use of elms in forest restoration? New For 50:183–215. https://doi.org/10.1007/s11056-018-9640-x
Menkis A, Östbrant IL, Davydenko K, Bakys R, Balalaikins M, Vasaitis R (2016) Scolytus multistriatus associated with Dutch elm disease on the island of Gotland: phenology and communities of vectored fungi. Mycol Prog 15:55. https://doi.org/10.1007/s11557-016-1199-3
Naruzawa ES, Bernier L (2014) Control of yeast-mycelium dimorphism in vitro in Dutch elm disease fungi by manipulation of specific external stimuli. Fungal Biol 118:872–884. https://doi.org/10.1016/j.funbio.2014.07.006
Pajares JA (2004) Elm breeding for resistance against bark beetles. Invest Agrar Sist Recur For 13:207–215
Pipe ND, Buck KW, Brasier CM (1997) Comparison of the cerato-ulmin (cu) gene sequences of the Himalayan Dutch elm disease fungus Ophiostoma himal-ulmi with those of O. ulmi and O. novo-ulmi suggests that the cu gene of O. novo-ulmi is unlikely to have been acquired recently from O. himal-ulmi. Mycol Res 101:415–421. https://doi.org/10.1017/s0953756296002754
Plourde KV, Bernier L (2014) A rapid virulence assay for the Dutch elm disease fungus Ophiostoma novo-ulmi by inoculation of apple (Malus × domestica ‘Golden Delicious’) fruits. Plant Pathol 63:1078–1085. https://doi.org/10.1111/ppa.12177
Santini A, Montaghi A, Vendramin GG, Capretti P (2005) Analysis of the Italian Dutch elm disease fungal population. J Phytopathol 153:73–79. https://doi.org/10.1111/j.1439-0434.2004.00931.x
Škorić V (1943) Holandska bolest briestova. Šumarski List 67:65–73
Solheim H, Eriksen R, Hietala AM (2011) Dutch elm disease has currently a low incidence on wych elm in Norway. For Pathol 41:182–188. https://doi.org/10.1111/j.1439-0329.2010.00650.x
Solla A, Dacasa MC, Nasmith C, Hubbes M, Gil L (2008) Analysis of Spanish populations of Ophiostoma ulmi and O novo-ulmi using phenotypic characteristics and RAPD markers. Plant Pathol 57:33–44. https://doi.org/10.1111/j.1365-3059.2007.01692.x
Spaić I (1955) Problematika zaštite šuma u NR Hrvatskoj. Šumarski List 79:440–468
Stipes RJ, Campana RJ (1981) Compendium of elm diseases. The American Phytopathological Society, Minnesota
Tziros GT, Nakopoulou ZG, Perlerou C, Diamandis S (2017) Current status of the Dutch elm disease pathogen populations affecting Ulmus minor in Greece. For Pathol 47:e12323. https://doi.org/10.1111/efp.12323
Webber JF (1990) Relative effectiveness of Scolytus scolytus, S. multistriatus and S. kirschi as vectors of Dutch elm disease. Eur J For Pathol 20:184–192. https://doi.org/10.1111/j.1439-0329.1990.tb01129.x
Webber JF (2004) Experimental studies on factors influencing the transmission of Dutch elm disease. Invest Agrar Sist Recur For 13:197–205
Zebec M, Idžojtić M, Poljak I, Mihaldinec I (2010) The variability of field elm (Ulmus minor Mill. sensu latissimo) in Croatian Drava river valley according to the leaf morphology. Šumarski List 134:569–579 (in Croatian with English summary)
Zebec M, Idžojtić M, Poljak I (2014) Morphological variability of the field elm (Ulmus minor Mill. sensu latissimo) in continental Croatia. Šumarski List 138:563–572 (in Croatian with English summary)
Zebec M, Idžojtić M, Poljak I, Modrić I (2015) Population variability of wych elm (Ulmus glabra Huds.) in the mountainous region of Croatia according to the leaf morphology. Šumarski List 139:429–439 (in Croatian with English summary)
Zebec M, Idžojtić M, Šatović Z, Poljak I, Liber Z (2016) Alive and kicking, or, living on borrowed time? Microsatellite diversity in natural populations of the endangered Ulmus minor Mill. sensu latissimo from Croatia. Acta Bot Croat 75:53–59. https://doi.org/10.1515/botcro-2016-0007
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This research was supported by grants from University of Zagreb.
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Communicated by Claus Bässler.
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Marko Zebec was formerly at University of Zagreb, Zagreb, Croatia.
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Katanić, Z., Krstin, L., Ježić, M. et al. Identification and characterization of the causal agent of Dutch elm disease in Croatia. Eur J Forest Res 139, 805–815 (2020). https://doi.org/10.1007/s10342-020-01286-4
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DOI: https://doi.org/10.1007/s10342-020-01286-4