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Geosmithia Morbida Sp. Nov., a New Phytopathogenic Species Living in Symbiosis with the Walnut Twig Beetle (Pityophthorus Juglandis)Onjuglans in USA

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Geosmithia Morbida Sp. Nov., a New Phytopathogenic Species Living in Symbiosis with the Walnut Twig Beetle (Pityophthorus Juglandis)Onjuglans in USA Mycologia, 103(2), 2011, pp. 325–332. DOI: 10.3852/10-124 # 2011 by The Mycological Society of America, Lawrence, KS 66044-8897 Geosmithia morbida sp. nov., a new phytopathogenic species living in symbiosis with the walnut twig beetle (Pityophthorus juglandis)onJuglans in USA Miroslav Kolarˇı´k1 the foliage followed by progressive branch dieback. Institute of Microbiology of the ASCR, v.v.i, Vı´denˇska´ Trees are killed within 3–4 y of initial symptoms. Tree 1083, 142 20 Praha 4, Czech Republic, and mortality is the result of aggressive feeding by the Department of Botany, Faculty of Science, Charles walnut twig beetle, Pityophthorus juglandis Blackman, University, Bena´tska´ 2, 128 01 Praha 2, Czech Republic (Coleoptera, Curculionidae, Scolytinae), and subse- quent canker development surrounding beetle gal- Emily Freeland leries in the phloem. The number of cankers formed Curtis Utley on branches and the trunk is enormous, hence the Ned Tisserat name thousand cankers to describe the disease. A Department of Bioagricultural Sciences and Pest previously undescribed species of Geosmithia (Asco- Management, Colorado State University, Plant Sciences Building 1177, Fort Collins, Colorado 80523 mycota: Hypocreales: Bionectriaceae) was consistently isolated from the canker margins, beetle galleries and adult beetles on Juglans nigra. Artificial inoculations Abstract: Widespread morbidity and mortality of of Juglans nigra demonstrated this fungus was Juglans nigra has occurred in the western USA over responsible for canker development (Tisserat et al. the past decade. Tree mortality is the result of 2009). P. juglandis and G. morbida have not been aggressive feeding by the walnut twig beetle (Pi- reported in the native range of J. nigra in eastern tyophthorus juglandis) and subsequent canker devel- North America until the recent alarming report from opment around beetle galleries caused by a filamen- eastern Tennessee. Here both the beetle and tous ascomycete in genus Geosmithia (Ascomycota: Geosmithia symbiont were found on J. nigra with Hypocreales). Thirty-seven Geosmithia strains col- TCD (Tennessee Department of Agriculture, media lected from J. californica, J. hindsii, J. major and J. release: 5 Aug 2010). nigra in seven USA states (AZ, CA, CO, ID, OR, UT, P. juglandis first was described from J. major and WA) were compared with morphological and molec- possibly is native also to other walnut species in the ular methods (ITS rDNA sequences). Strains had southwestern United States (J. californica and J. common characteristics including yellowish conidia hindsii) (Blackman 1928, Wood and Bright 1992). en masse, growth at 37 C and absence of growth on In 2008 and 2009 G. morbida was isolated from Czapek-Dox agar and belonged to a single species necrotic phloem surrounding P. juglandis galleries in described here as G. morbida. Whereas Geosmithia are J. major in native stands in AZ and NM, but the fungus common saprobes associated with bark beetles attack- was not causing branch dieback or mortality in this ing hardwoods and conifers worldwide, G. morbida is species. Both P. juglandis and G. morbida also have the first species documented as a plant pathogen. recently (2008) been associated with dieback of J. Key words: insect-associated fungi, Juglans nigra, hindsii and J. californica in their native range in CA. Juglans species, phytopathogenic fungi, thousand However pathogenicity of G. morbida to these species cankers disease has not yet been documented. Geosmithia is a genus of mitosporic filamentous fungi with a worldwide distribution containing 22 published species (Kolarˇı´k INTRODUCTION and Kirkendall 2010; Kolarˇı´k et al. 2004, 2005, 2007, Widespread branch dieback and mortality of Juglans 2008) and at least 20 more unpublished species. nigra (black walnut) has occurred in several western Certain Geosmithia species sporadically occur on states including Colorado (CO), Idaho (ID), New broad range of substrates, including plant debris, Mexico (NM), Oregon (OR), Utah (UT) and cereals and in soil (Kolarˇı´k et al. 2004, Pitt and Washington (WA) of USA since the mid-1990s. Hocking 2009), however most are exclusive associates Juglans nigra is not native to this region but has been of subcortical insects including scolytids (Coleoptera, widely planted as an ornamental and nut tree species. Curculionidae, Scolytinae) and bostrichids (Coleop- Affected trees initially exhibit yellowing and wilting of tera, Bostrichidae). Geosmithia spp. are found typical- ly in association with phloeophagous bark beetles Submitted 23 Apr 2010; accepted for publication 18 Aug 2010. (Kolarˇı´k et al. 2006, 2007, 2008) but also with wood- 1 Corresponding author. E-mail: [email protected] boring ambrosia beetles, where they can act as 325 326 MYCOLOGIA FIG. 1. Haplotype network of G. morbida ITS rDNA from 37 strains. The circles refer to haplotypes detected in the samples and their size is proportional to the sampled haplotype frequency. Isolates were collected in the states of of Arizona (AZ), California (CA), Colorado (CO), Idaho (ID), Oregon (OR), Utah (UT) and Washington (WA). Hosts of the isolates were: 1227, 1228, 1249, 1261–1264, 1266–1270 and 1272 from J. californica; 1233 and U170 from J. hindsii, 1234 from J. major and 1258–1260 from undetermined Juglans species or hybrids; all other isolates were recovered from J. nigra. The line between the haplotypes represents one base change and the small circles represent haplotypes not present in the sample. GenBank accession numbers representing each haplotype are given below the circles. (See article online for color figure.) primary or auxiliary ambrosia fungi (Kolarˇı´k and throughout western USA that were unique from Kirkendall 2010). While ambrosial Geosmthia spp. published and unnamed Geosmithia species in the provide the main nutritional source for their vectors collection of the first author. The species from Juglans and represent an extreme example of nutritional is described here as Geosmithia morbida sp. nov. mutualism, little is known about interactions of other symbiotic Geosmithia species or their vectors and host plants. Several attempts to evaluate phytopathogeni- MATERIALS AND METHODS city of Geosmithia have been conducted. A Geosmithia Fungal cultures and fungal morphology.—Thirty-seven fun- sp. associated with Cryphalus piceae (Col., Curculioni- gal isolates from Juglans spp. throughout western USA (AZ, dae, Scolytinae) was non-pathogenic to Abies alba CA, CO, NM, ID, OR UT, WA) were isolated on one-half seedlings (Jankowiak and Kolarˇı´k 2010). Cˇ´zıˇkova´ strength PDA (K PDA, Difco Corp., Sparks, Maryland) (2005) reported that the Quercus inhabiting G. containing 100 mg/L chloramphenicol and streptomycin langdonii and G. pallida inhibited the growth of sulfate from Juglans spp. exhibiting disease symptoms Lepidium sativum but were non-pathogenic to Quer- (Tisserat et al. 2009). These single-spore strains were cus seedlings. Scala et al. (2007) found that the strain characterized with ITS rDNA sequences (FIG. 1) and a of Geosmithia pallida obtained from wilting Ulmus in subset of 12 strains representing main ITS rDNA haplo- Italy possessed a cerato-ulmin toxin, the protein types, and places of origin were selected for the morpho- involved in Dutch elm disease (DED). This strain logical characterization (TABLE I). The ex-type and other was unable to cause DED symptoms on inoculated U. representatives of Geosmithia from walnut were deposited in the Culture Collection of Fungi, Prague, Czech Republic, glabra trees. Nevertheless Geosmithia spp. co-occur and Centraalbureau voor Schimmelcultures (CBS), Utrecht, regularly with phytopathogenic Ophiostoma species on the Netherlands. A dried herbarium specimen of the elms and their contribution to DED complex is little holotype was deposited in the herbarium of the Mycological explored and deserves further study. Department, National Museum in Prague (PRM). All We identified a set of morphological and molecular measurements and observations were done on fungal genetic characteristics of Geosmithia isolates collected structures grown 7–14 d on malt extract agar (MEA, malt from J. nigra, J. major, J. californica and J. hindsii extract Oxoid 20 g L-1, glucose 20 g L-1, peptone 1 g L-1, KOLARˇI´KETAL.: GEOSMITHIA MORBIDA SP. NOV. 327 TABLE I. Characterization of strains used in the description of Geosmithia morbida. Only characters showing intraspecies variability are presented Diameter growth GenBank Origin, host, collection date, after 14 days (mm) Conidium accession Source collector on MEA, 25 C size (mm) number 1268 CA, J. californica, 2008, Seybold 30 (4.5–)5.3(–6) 3 2 FN434076 1260 OR, Juglans sp., 2008, Pscheidt 30 (4.5–)5.3(–8) 3 2 FN434075 CCF 4010 (1271, PRM 859765, PRM 859767) CO, J. nigra, 2008, Utley 38 (4.3–)5.0(–5.5) 3 2 FN434077 1223 UT, J. nigra, 2007, Funk 50–55 (4.3–)5.0(–5.5) 3 2 FN434080 1276 CO, J. nigra, 2008, Utley 30 (4.6–)5.6(–7) 3 2.3 FN436020 CCF 3880 (1234, PRM 859763-4) AZ, J. major, 2008, Cranshaw 50 (4–)4.7(–5.2) 3 2.2 FN434072 CBS 124663 (CCF 3881, 1217, PRM 915943, 859766) CO, J. nigra, 2007, Tisserat 30–45 (4–)4.7(–6) 3 2.2 FN434082 1256 OR, J. nigra, 2008, Pscheidt 30 (4.2–)4.9(–5.8) 3 2 FN434073 1272 CA, J. californica, 2008, Seybold 37 (4.3–)5.0(–5.5) 3 2 FN434078 U170 CA, J. hindsii, 2009, Graves & Kolarˇı´k 35 (4.3–)5.0(–5.5) 3 2 FN434079 1259 OR, Juglans sp., 2008, Pscheidt 30 (4.3–)5.0(–5.5) 3 2 FN434074 CBS 124664 (CCF 3879, 1218, PRM 915940-2) CO, J. nigra, 2007, Tisserat 40–50 (3.9–)4.8(–5.5) 3 2 FN434081 agar 20 g L-1) and incubated in the dark or in incidental Terminator 3.1 sequencing chemistry. A genotype network light at 25 C. Other media used for colony descriptions were of the strains from Juglans was constructed with statistical Czapek yeast agar (CYA), Czapek-Dox agar (CDA) (Pitt parsimony in TCS 1.21 (Clement et al.
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