Geosmithia species associated with fir-infesting beetles in Poland

Robert Jankowiak, Piotr Bilański

Abstract


Geosmithia species (Ascomycota: Hypocreales) are common ectosymbionts of scolytine bark and ambrosia beetles that feed on coniferous and deciduous trees in different forest ecosystems. Geosmithia morbida is the canker pathogen that causes extensive mortality of Juglans nigra. Because little is known regarding the Geosmithia species on European silver fir (Abies alba), we have investigated the diversity and abundance of these fungi associated with insects infesting European silver fir in Poland. Samples associated with eight beetle species were collected from three fir forests. Fungi were isolated from beetles and galleries. Isolates were identified based on morphological characteristics, DNA sequence comparison for three gene regions (ITS, ßT, TEF1-α), and phylogenetic analyses. Geosmithia was detected in 33% of the total 531 beetle samples obtained from A. alba. Two undescribed species of Geosmithia were distinguished, Geosmithia sp. 9 and Geosmithia sp. 16. Associations of Pityokteines spp. with Geosmithia fungi were recorded for the first time. Pityokteines vorontzowi and Pityophthorus pityographus appear to be regular vectors for Geosmithia sp. 9 and Geosmithia sp. 16, respectively. Pityokteines curvidens and Cryphalus piceae were associated with Geosmitha sp. 9 at lower frequencies.

Keywords


Abies alba; ambrosia beetles; bark beetles; Geosmithia, weevil

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References


Wingfield MJ, Barnes I, de Beer ZW, Roux J, Wingfield BD, Taerum SJ. Novel associations between ophiostomatoid fungi, insects and tree hosts: current status – future prospects. Biol Invasions. 2017;19:3215–3228. https://doi.org/10.1007/s10530-017-1468-3

Kolařik M, Kubátová A, Hulcr J, Pažoutová S. Geosmithia fungi are highly diverse and consistent bark beetle associates: evidence from their community structure in temperate Europe. Microb Ecol. 2008;55:65–80. https://doi.org/10.1007/s00248-007-9251-0

Rossman AY, Samuels GJ, Rogerson CT, Lowen R. Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud Mycol. 1999;42:1–248. https://doi.org/10.5598/imafungus.2013.04.01.05

Kolařík M, Kubátová A, Pazoutova S, Šrutka P. Morphological and molecular characterisation of Geosmithia putterillii, G. pallida comb. nov. and G. flava sp. nov., associated with subcorticolous insects. Mycol Res. 2004;108:1053–1069. https://doi.org/10.1017/S0953756204000796

Kolařík M, Kubátová A, Cepicka I, Pazoutova S, Šrutka P. A complex of three new white-spored, sympatric, and host range limited Geosmithia species. Mycol Res. 2005;109:1323–1336. https://doi.org/10.1017/S0953756205003965

Kolařík M, Kostovčík M, Pazoutova S. Host range and diversity of the genus Geosmithia (Ascomycota: Hypocreales) living in association with bark beetles in the Mediterranean area. Mycol Res. 2007;111:1298–1310. https://doi.org/10.1016/j.mycres.2007.06.010

Kolařík M, Freeland E, Utley C, Tisserat N. Geosmithia morbida sp. nov., a new phytopathogenic species living in symbiosis with the walnut twig beetle (Pityophthorus juglandis) on Juglans in USA. Mycologia. 2011;103:325–332. https://doi.org/10.3852/10-124

Kolařík M, Kirkendall LR. Evidence for a new lineage of primary ambrosia fungi in Geosmithia Pitt (Ascomycota: Hypocreales). Fungal Biol. 2010;114:676–689. https://doi.org/10.1016/j.funbio.2010.06.005

Kolařík M, Jankowiak R. Vector affinity and diversity of Geosmithia fungi living on subcortical insects inhabiting Pinaceae species in Central and Northeastern Europe. Microb Ecol. 2013;66:682–700. https://doi.org/10.1007/s00248-013-0228-x

Kolařík M, Hulcr J, Kirkendall LR. New species of Geosmithia and Graphium associated with ambrosia beetles in Costa Rica. Czech Mycol. 2015;67:29–35.

Kolařík M, Hulcr J, Tisserat N, De Beer W, Kostovčík M, Kolaříková Z, et al. Geosmithia associated with bark beetles and woodborers in the Western USA: taxonomic diversity and vector specificity. Mycologia. 2017;109:185–199. https://doi.org/10.1080/00275514.2017.1303861

Jankowiak R, Kolaŕík M, Bilański P. Association of Geosmithia fungi (Ascomycota: Hypocreales) with pine- and spruce-infesting bark beetles in Poland. Fungal Ecol. 2014;11:71–79. https://doi.org/10.1016/j.funeco.2014.04.002

Dori-Bachash M, Avrahami-Moyal L, Protasov A, Mendel Z, Freeman S. The occurrence and pathogenicity of Geosmithia spp. and common blue-stain fungi associated with pine bark beetles in planted forests in Israel. Eur J Plant Pathol. 2015;143:627–639. https://doi.org/10.1007/s10658-015-0713-9

Machingambi NM, Roux J, Dreyer LL, Roets F. Bark beetles (Curculionidae: Scolytinae), their phoretic mites (Acari) and associated Geosmithia species (Ascomycota: Hypocreales) from Virgilia trees in South Africa. Fungal Biol. 2014;118:472–483. https://doi.org/10.1016/j.funbio.2014.03.006

Pepori AL, Kolařík M, Bettini PP, Vettraino AM, Santini A. Morphological and molecular characterisation of Geosmithia species on European elms. Fungal Biol. 2015;119:1063–1074. https://doi.org/10.1016/j.funbio.2015.08.003

Huang YT, Kolařík M, Kasson MT, Hulcr J. Two new Geosmithia species in G. pallida species complex from bark beetles in eastern USA. Mycologia. 2017;109:790–803. https://doi.org/10.1080/00275514.2017.1410422

Jankowiak R, Rossa R. Associations between Pityogenes bidentatus and fungi in young managed Scots pine stands in Poland. For Pathol. 2008;38:169–177. https://doi.org/10.1111/j.1439-0329.2007.00535.x

Montecchio L, Faccoli M. First record of Thousand cankers disease Geosmithia morbida and walnut twig beetle, Pityophthorus juglandis on Juglans nigra in Europe. Plant Dis. 2014;98:696. https://doi.org/10.1094/PDIS-10-13-1027-PDN

Jankowiak R, Kolařík M. Fungi associated with the fir bark beetle Cryphalus piceae in Poland. For Pathol. 2010;40:133–144. https://doi.org/10.1111/j.1439-0329.2009.00620.x

Jankowiak R. Fungi associated with Ips typographus on Picea abies in southern Poland and their succession into the phloem and sapwood of beetle-infested trees and logs. For Pathol. 2005;35:37–55. https://doi.org/10.1111/j.1439-0329.2004.00395.x

Jankowiak R. Fungi associated with Tomicus piniperda in Poland and assessment of their virulence using Scots pine seedlings. Ann For Sci. 2006;63:801–808. https://doi.org/10.1051/forest:2006063

Jankowiak R. Fungi associated with Tomicus minor on Pinus sylvetris in Poland and their succession into the sapwood of beetle-infested windblown trees. Can J For Res. 2008;38:2579–2588. https://doi.org/10.1139/X08-101

Jankowiak R, Kolaŕík M. Diversity and pathogenicity of ophiostomatoid fungi associated with Tetropium species colonizing Picea abies in Poland. Folia Microbiol. 2010;55:145–154. https://doi.org/10.1007/s12223-010-0022-9

Jankowiak R. Ophiostomatoid fungi associated with Ips sexdentatus on Pinus sylvestris in Poland. Dendrobiology. 2012;68:43–54.

Jankowiak R, Bilański P. Association of the pine-infesting Pissodes species with ophiostomatoid fungi in Poland. Eur J For Res. 2013;132:523–534. https://doi.org/10.1007/s10342-013-0693-2

Jankowiak R, Bilański P. Diversity of ophiostomatoid fungi associated with the large pine weevil, Hylobius abietis and infested Scots pine seedlings in Poland. Ann For Sci. 2013;70:391–402. https://doi.org/10.1007/s13595-013-0266-z

Jankowiak R, Bilański P. Ophiostomatoid fungi associated with root-feeding bark beetles in Poland. For Pathol. 2013;43:422–428. https://doi.org/10.1111/efp.12049

Jankowiak R, Strzałka B, Bilański P, Kacprzyk M, Lukášová K, Linnakoski R, et al. Diversity of Ophiostomatales species associated with conifer-infesting beetles in the Western Carpathians. Eur J For Res. 2017;136:939–956. https://doi.org/10.1007/s10342-017-1081-0

Nunberg M. Klucze do rozpoznawania owadow Polski. Część XIX. Chrząszcze – Coleoptera, Korniki – Scolytidae, Wyrynniki – Platypodidae. Zeszyt 99–100. Warszawa: PWN; 1981.

Smreczyński S. Klucze do oznaczania owadów Polski; Część XIX: Chrząszcze – Coleoptera, zeszyt 98d: Ryjkowce – Curculionidae; podrodzina Curculioninae. Warszawa: Polskie Towarzystwo Entomologiczne; 1972.

Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes: application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x

White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. San Diego, CA: Academic Press; 1990. p. 315–322.

Glass NL, Donaldson GC. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol. 1995;61:1323–1330.

O’Donnel K, Cigelnik E. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol Phylogenet Evol. 1997;7:103–116. https://doi.org/10.1006/mpev.1996.0376

Carbone I, Kohn LM. A method for designing primer sets for speciation studies filamentous ascomycetes. Mycologia. 1999;91:553–556. https://doi.org/10.2307/3761358

Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9:286–298. https://doi.org/10.1093/bib/bbn013

Jankowiak R, Stępniewska H, Szwagrzyk J, Bilański P, Gratzer G. Characterization of Cylindrocarpon-like species associated with litter in the old-growth beech forests of Central Europe. For Pathol. 2016;46:582–594. https://doi.org/10.1111/efp.12275

Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25:1253–1256. https://doi.org/10.1093/molbev/msn08

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–321. https://doi.org/10.1093/sysbio/syq010

Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

Rambaut A, Drummond AJ. Tracer v1.4. 2007 [cited 2016 Dec 28]. Available from: http://beast.bio.ed.ac.uk/Tracer

Michalski J, Mazur A. Korniki. Praktyczny przewodnik dla leśników. Warszawa: Oficyna Edytorska “Wydawnictwo Świat”; 1999.