Abstract
In Lovran (coastal Croatia), a unique forest/orchard of evenly mixed grafted marrons and naturally growing nongrafted sweet chestnut trees exists. This old chestnut population has been devastated by chestnut blight, caused by an aggressive introduced pathogenic fungus, Cryphonectria parasitica. However, initial observations indicated recovery of naturally growing chestnut trees in that area, mediated by Cryphonectria-associated hypovirus (Cryphonectria hypovirus 1 (CHV-1)). Such recovery was not observed on grafted trees. Genotyping both, we confirmed the clonal origin of the grafted ones—marrons. No significant difference was observed between fungal strains isolated from naturally growing trees and the ones from marrons regarding fungal vegetative compatibility types or the prevalence of CHV-1. A strong correlation was observed between the types of canker: active/deep-expanding versus healing callus or superficial necrosis and the absence or presence of CHV-1 in the fungal isolates, sampled from naturally growing trees (Spearman rho 0.686, p value 7.81 × 10−5, Kendall tau 0.686, p value 5.18 × 10−7). Such correlation was not observed on marrons (Spearman rho 0.236, p value 0.235, Kendall tau 0.236, p value 0.084), because, unexpectedly, active/deep-expanding cankers were often associated with hypovirulent fungal isolates. These data indicate that the lack or unequal distribution of naturally occurring hypovirulence were not the cause of substantial marron decay in Lovran. Ecological and age-dependant differences were ruled out because all sampled trees are growing in close proximity and are of similar age. The results imply that the marron genotype is especially vulnerable and its ability to recover is limited even when the hypovirulent strain of the fungus is present in the canker.
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References
Agapow PM, Burt A (2001) Indices of multilocus linkage disequilibrium. Mol Ecol Notes 1:101–102
Allemann C, Hoegger P, Heiniger U, Rigling D (1999) Genetic variation of Cryphonectria hypoviruses (CHV1) in Europe, assessed using restriction fragment length polymorphism (RFLP) markers. Mol Ecol 8:843–854
Anagnostakis SL (1987) Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79:23–37
Anagnostakis SL (1988) Cryphonectria parasitica, cause of chestnut blight. Adv Plant Pathol 6:123–136
Anagnostakis SL (1992) Measuring resistance of chestnut trees to chestnut blight. Can J Forest Res 22:567–571
Anagnostakis SL, Day PR (1979) Hypovirulence conversion in Endothia parasitica. Phytopathology 69:1226–1229
Anagnostakis SL, Hau B, Kranz J (1986) Diversity of vegetative compatibility groups of Cryphonectria parasitica in Connecticut and Europe. Plant Dis 70:536–538
Bazzigher G, Miller GA (1991) Blight-resistant chestnut selections of Switzerland: a valuable germplasm resource. Plant Dis 75:5–9
Biraghi A (1946) Il cancro del castagno causato da Endothia parasitica. L'Italia Agricola 7:406
Biraghi A (1953) Possible active resistance of Endothia parasitica in Castanea sativa. 11th Rep Congr Int Union For Res Org, Rome, pp 643–645.
Bissegger M, Rigling D, Heiniger U (1997) Population structure and disease development of Cryphonectria parasitica in European chestnut forests in the presence of natural hypovirulence. Phytopathology 87:50–59
Breuillin F, Dutech C, Robin C (2006) Genetic diversity of the chestnut blight fungus Cryphonectria parasitica in four French population assessed by microsatellite markers. Mycol Res 110:288–296
Buck EJ, Hadonou M, James CJ, Blakesley D, Russell K (2003) Isolation and characterization of polymorphic microsatellites in European chestnut (Castanea sativa Mill.). Mol Ecol Notes 3:239–241
Choi GH, Nuss DL (1992) Hypovirulence of chestnut blight fungus conferred by an infectious viral cDNA. Science 257:800–803
Cortesi P, Milgroom MG, Bisiach M (1996) Distribution and diversity of vegetative compatibility types in subpopulations of Cryphonectria parasitica in Italy. Mycol Res 100:1087–1093
Cortesi P, Rigling D, Heiniger U (1998) Comparison of vegetative compatibility types in Italian and Swiss subpopulations of Cryphonectria parasitica. Europ J Forest Pathol 28:167–176
Cortesi P, McCulloh CE, Song H, Lin H, Milgroom MG (2001) Genetic control of horizontal virus transmission in the chestnut blight fungus, Cryphonectria parasitica. Genetics 159:107–118
Diskin M, Steiner KC, Hebard FV (2006) Recovery of American chestnut characteristics following hybridization and backcross breeding to restore blight-ravaged Castanea dentata. Forest Ecol Manag 223:439–447
Elliston JE (1985) Characteristics of dsRNA-free and dsRNA-containing strains of Endothia parasitica in relation to hypovirulence. Phytopathology 75:151–158
Gobbin D, Hohl L, Conza L, Jermini M, Gessler C, Conedera M (2007) Microsatellite-based characterization of the Castanea sativa cultivar heritage of southern Switzerland. Genome 50:1089–1103
Goudet J (1995) FSTAT, version 1.2, a computer program to calculate F-statistics. J Heredity 86:485–486
Graves AH (1950) Relative blight resistance in species and hybrids of Castanea. Phytopathology 49:1125–1131
Grente J (1965) Les formes Hypovirulentes d'Endothia parasitica et les espoirs de lutte contre le chancre du châtaignier. Acad Agric France 51:1033–1037
Grente J, Sauret S (1969) L'hypovirulence exclusive phenomene original en pathologie vegetale. C R Hebd Seances Acad Sci Ser D 268:2347–2350
Grünwald NJ, Stephen BG, Milgroom MG, Fry WE (2003) Analysis of genotypic diversity data for populations of microorganisms. Phytopathology 93:738–46
Halambek M (1986) Chestnut blight in Yugoslavia. EPPO Bull 16:533–535
Halambek M (1988) Istraživanje virulentnosti gljive Endothia parasitica Murr./And. uzročnika raka kore pitomog kestena (Castanea sativa Mill.). Dissertation, Faculty of Forestry, University of Zagreb.
Heiniger U, Rigling D (1994) Biological control of chestnut blight in Europe. Annu Rev Phytopathol 32:581–599
Hillman BI, Shapira R, Nuss DL (1990) Hypovirulence-associated suppression of host functions in Cryphonectria parasitica can be partially relieved by high light intensity. Phytopathology 80:950–956
Hogan EP, Griffin GJ (2002) Incomplete movement of Cryphonectria hypovirus 1 within a vegetative compatibility type of Cryphonectria parasitica in natural cankers on grafted American chestnut trees. Forest Pathol 6:331–344
Huang H, Dane F, Kubisiak TL (1998) Allozyme and RAPD analysis of the genetic diversity and geographic variation in wild populations of the American chestnut (Fagaceae). Am J Bot 85:1013–1021
Idžojtić M, Zebec M, Poljak I, Liber Z, Šatović Z, Vahčić N (2010) Očuvanje genofonda maruna. In: Jasprica N, Pandža M, Milović M (eds) Treći hrvatski botanički kongres, knjiga sažetaka, Murter, 24–26 September 2010, pp 92–93.
Ježić M, Krstin L, Rigling D, Ćurković-Perica M (2012) High diversity in populations of the introduced plant pathogen, Cryphonectria parasitica, due to encounters between genetically divergent genotypes. Mol Ecol 21:87–99
Jurc D (2002) An overview of the history of chestnut blight epidemic in Slovenia. Zbornik gozdarstva in lesarstva 68:33–59
Kišpatić J (1956) Rak kestenove kore (Endothia parasitica Anders.). Zavod za zaštitu bilja, Zagreb. Uputstva iz zaštite bilja 19:1–12
Krstin L, Novak-Agbaba S, Rigling D, Ćurković-Perica M (2011) Diversity of vegetative compatibility types and mating types of Cryphonectria parasitica in Slovenia and occurrence of associated Cryphonectria hypovirus 1. Plant Pathol 60:752–761
Krstin L, Novak-Agbaba S, Rigling D, Krajačić M, Ćurković-Perica M (2008) Chestnut blight fungus in Croatia: diversity of vegetative compatibility types, mating types and genetic variability of associated Cryphonectria hypovirus 1. Plant Pathol 57:1086–1096
Kubisiak TL, Hebard FV, Nelson CD, Zhang J, Bernatzky R, Huang H, Anagnostakis SL, Doudrick RL (1997) Molecular mapping of resistance to blight in an interspecific cross in the genus Castanea. Phytopathology 87:751–759
Marinoni D, Akkak A, Bounous G, Edwards KJ, Botta R (2003) Development and characterization of microsatellite markers in Castanea sativa (Mill.). Mol Breed 11:127–136
Martin MA, Alvarez JB, Mattioni C, Cherubini M, Villani F, Martin LM (2009) Identification and characterization of traditional chestnut varieties of southern Spain using morphological and simple sequence repeats SSR markers. Ann Appl Biol 154:389–398
Martin MA, Mattion C, Cherubini M, Taurchini D, Villani F (2010a) Genetic characterization of traditional chestnut varieties in Italy using microsatellites (simple sequence repeats) markers. Ann Appl Biol 157:37–44
Martin MA, Mattioni C, Cherubini M, Taurchini D, Villani F (2010b) Genetic diversity in European chestnut populations by means of genomic and genic microsatellite markers. Tree Genet Genomes 6:735–744
Martin MA, Mattioni C, Molina JR, Alvarez JB, Cherubini M, Herrera MA, Villani F, Martin LM (2011) Landscape genetic structure of chestnut (Castanea sativa Mill). in Spain. Tree Genet Genomes 8:127–136
McManus PS, Ewers FW, Fulbright DW (1989) Characterization of the chestnut blight canker and the localization and isolation of the pathogen Cryphonectria parasitica. Can J Bot 67:3600–3607
Medak J, Perić S (2007) Šume pitomog kestena u Hrvatskoj-fitocenološke, ekološke i gospodarske karakteristike. In: Britvec M, Škvorc, Ž (eds), Zbornik sažetaka 2. botaničkog kongresa. Zagreb, 20–22 September 2007, pp 89–90.
Medak J, Idžojtić M, Novak-Agbaba S, Ćurković-Perica M, Mujić I, Poljak I, Juretić D, Prgomet Ž (2009) Croatia. In: Avanzato D (ed) Following chestnut footprints (Castanea spp.)—cultivation and culture, folklore and history, traditions and use. Scripta Horticult 9:40–43
Meštrović Š, Fabijanić G (1995) Forest management planning manual. Republic of Croatia, Ministry of Agriculture and Forestry, Zagreb, Croatia, pp 322–323 (in Croatian)
Milgroom MG, Cortesi P (2004) Biological control of chestnut blight with hypovirulence: a critical analysis. Annu Rev Phytopathol 42:311–338
Milgroom MG, Lipari SE (1995) Spatial analysis of nuclear and mitochondrial RFLP genotypes in populations of chestnut blight fungus, Cryphonectria parasitica. Mol Ecol 4:633–642
Milgroom MG, Sotirovski K, Spica D, Davis JE, Brewer MT, Milev M, Cortesi P (2008) Clonal population structure of the chestnut blight fungus in expanding ranges in southeastern Europe. Mol Ecol 17:4446–4458
Novak-Agbaba S, Liović B, Pernek M (2000) Prikaz sastojina pitomog kestena (Castanea sativa Mill.) u Hrvatskoj i zastupljenost hipovirulentnih sojeva gljive Cryphonectria parasitica (Murr.) Barr. Radovi Šumarskog instituta Jastrebarsko 35(1):91–110
Peakall R, Smouse PE (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Perica MĆ, Šola I, Urbas L, Smrekar F, Krajačić M (2009) Separation of hypoviral double-stranded RNA on monolithic chromatographic supports. J Chromatogr A 13:2712–2716
Peever TL, Liu Y-C, Cortesi P, Milgroom MG (2000) Variation in tolerance and virulence in the chestnut blight fungus–hypovirus interaction. Appl Environ Microbio 66:4863–4869
Prospero S, Conedera M, Heiniger U, Rigling D (2006) Saprophytic activity and sporulation of Cryphonectria parasitica on dead chestnut wood in forests with naturally established hypovirulence. Phytopathology 96:1337–1344
Raymond M, Rousset (1995) GENEPOP (Version 1.2): Population genetic software for exact tests and ecumenicism. J Hered 86:248–249
Robin C, Lanz S, Soutrenon A, Rigling D (2010) Dominance of natural over released biological control agents of the chestnut blight fungus Cryphonectria parasitica in south-eastern France is associated with fitness-related traits. Biol Control 53:55–61
Robin C, Heiniger U (2001) Chestnut blight in Europe: diversity of Cryphonectria parasitica, hypovirulence and biocontrol. For Snow Land Res 76:361–367
Rousset (2008) GENEPOP 007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Sotirovski K, Milgroom MG, Rigling D, Heiniger U (2006) Occurrence of Cryphonectria hypovirus 1 in the chestnut blight fungus in Macedonia. Forest Pathol 36:136–143
Sotirovski K, Rigling D, Heiniger U, Milgroom MG (2011) Variation in virulence of Cryphonectria hypovirus 1 in Macedonia. Forest Pathol 41:59–65
Wagner HW, Sefc KM (1999) IDENTITY 1.0. Centre for Applied Genetics, University of Agricultural Sciences, Vienna
Acknowledgments
We thank Silvia Dingwall for the final English editing. This research was supported by Swiss National Science Foundation (SCOPES project IZ7370-12792/1) and the Croatian Ministry of Science Education and Sport.
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Genotypes of the chestnut trees in Lovran are given in Supplementary 847 materials. 848.
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Ježić, M., Krstin, L., Poljak, I. et al. Castanea sativa: genotype-dependent recovery from chestnut blight. Tree Genetics & Genomes 10, 101–110 (2014). https://doi.org/10.1007/s11295-013-0667-z
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DOI: https://doi.org/10.1007/s11295-013-0667-z