Pacific Northwest Fungi Volume 1, Number 11, Pages 1-11 Published October 16, 2006 First Report of Erysiphe (Uncinuliella) flexuosa in western North America Dean A. Glawe 1 and Frank M. Dugan 2 1Department of Plant Pathology, Washington State University, and College of Forest Resources, Box 352100, University of Washington, Seattle, WA 98195. 2USDA-ARS Western Regional Plant Introduction Station, 59 Johnson Hall, Washington State University, Pullman WA 99164- 6402 USA. Glawe, D. A., and F. M. Dugan. 2006. First Report of Erysiphe (Uncinuliella) flexuosa in western North America. Pacific Northwest Fungi 1(11): 1-11. DOI: 10.2509/pnwf.2006.001.011 Corresponding author: Dean A. Glawe, [email protected] Accepted for publication October 16, 2006. Copyright © 2006 Pacific Northwest Fungi Project. All rights reserved. Abstract: Erysiphe flexuosa, a powdery mildew parasite of Aesculus species, is believed to have originated in North America where distribution records were confined to regions east of the Rocky Mountains. The fungus recently was found in eastern Washington State and northern Idaho. The fungus can be distinguished readily from other powdery mildews attacking Aesculus species by the presence of two distinctive kinds of chasmothecial appendages. Consistent with previous reports on similar species, observations determined that subulate appendages formed first, on dorsal sides of chasmothecia. The longer, uncinate appendages formed equatorially during later chasmothecial maturation. There are no Aesculus species native to northwest North America that could have hosted an undetected population of the fungus. It appears likely that E. flexuosa became established relatively recently in the inland Pacific Northwest, possibly being introduced on infected host material, similar to the situation in Europe where several reports documented the presence of the fungus beginning in 2000. 2 Glawe and Dugan. Erysiphe flexuosa on Aesculus sp. Pacific Northwest Fungi 1(11): 1-11 Key words: Uncinula, Uncinuliella, Erysiphe, Aesculus, powdery mildew, biogeography, fungal morphology, ascocarp appendage, chasmothecia, exotic plant pathogen. Introduction: The powdery mildew fungus west of the Rocky Mountains), Erysiphe Erysiphe flexuosa (Peck) U. Braun & S. flexuosa is thought to be native to North Takam. originally was described as America (Braun, 1987; Zimmermannová- Uncinula flexuosa Peck (Braun and Pastirčáková et al., 2002). Ing and Takamatsu, 2000). Although chasmothecia Spooner (2002) also noted another (ascocarps termed perithecia or possibility—that the fungus is native to cleistothecia by some authors) of the fungus Europe but until recently was undetected. bear uncinate appendages resembling European reports of the fungus began those in species traditionally classified in appearing in 2000 and it is now known to Uncinula, it also produces shorter, subulate occur in Croatia, France, Germany, Poland, appendages (Braun, 1987). Demonstration Slovakia, Switzerland, United Kingdom that these two kinds of appendages are (Zimmermannová-Pastirčáková et al., 2002 distinctly different, and not merely and references therein), Hungary (Kiss et developmental stages of the same kind of al., 2003), Slovenia (Milevoj, 2004), Ukraine appendage, led Braun (1981) to make the (Heluta and Vojtjuk, 2004), Lithuania new combination Uncinuliella flexuosa (Grigaliūnaitėet al., 2005) as well as Serbia (Peck) U. Braun for this fungus. and Montenegro (Rankovićand Mišić, Subsequent analysis of rDNA sequence 2006). Recently the authors examined data suggested that teleomorph characters collections of the fungus from Moscow, such as chasmothecial appendages are not Idaho and Pullman, Washington. This reliable indicators of phylogenetic paper documents for the first time the relationships (Braun et al., 2002), leading occurrence of this fungus in North America Braun and Takamatsu (2000) to make the west of the Rocky Mountains. In addition, combination Erysiphe flexuosa which is information is presented on chasmothecial used herein. development, particularly on relative timing of development of the two kinds of Erysiphe flexuosa is relatively easy to chasmothecial appendages characteristic of distinguish from other powdery mildew fungi this fungus. because of the distinctive chasmothecial morphology and the host range that is Materials and Methods: Samples of restricted to species of Aesculus Aesculus sp. leaves collected from trees (Hippocastanaceae). Other species of growing in urban landscapes, and bearing Erysiphales recorded from E. flexuosa were examined and Hippocastanaceae include Phyllactinia photographed using a Leica DMR guttata (Wallr.:Fr.) Lév., distinguished on compound microscope and a Leica MZ95 the basis of acicular chasmothecial stereo microscope, both equipped with appendages and fusiform-clavate conidia, Leica DC300 digital cameras. The following and species of Sawadaea, distinguished on material was characterized in this study: the basis of dichotomously or Glawe 03-383, from Aesculus sp., trichotomously branched chasmothecial University of Idaho campus, Moscow, Latah appendages and synanamorphs producing Co., Idaho, coll. September 4, 2002 by both microconidia and macroconidia with Jennifer Fallacy; Glawe 02-90, from fibrosin bodies (Braun, 1987). Aesculus sp., Pullman, Whitman Co. Washington, coll. Autumn, 2005 by Wayne Although the fungus has remained Shull; Glawe 06-609, from Aesculus sp., unreported from the western USA (regions University of Idaho Arboretum, Latah Co., Glawe and Dugan. Erysiphe flexuosa on Aesculus sp. Pacific Northwest Fungi 1(11): 1-11 3 Idaho, coll. September 13, 2006 by F. M. and Phyllactinia coryli (Pers.) P. Dugan; Glawe 06-610 from Aesculus sp., Karst.(regarded by Braun [1987] as Pullman, Whitman Co., Washington, synonymous with P. guttata), both of which collected September 4, 2006 by F. M. were from California (Farr et al., n. d.). Dugan. Voucher material was deposited Phyllactinia guttata is easily differentiable with the Mycology Herbarium in the from E. flexuosa on the basis of its acicular Department of Plant Pathology, Washington chasmothecial appendages (Braun, 1987). State University (WSP). The current study appears to be the first to Results: Morphological features of the document formally the presence of E. fungus were as follows: mycelia on leaves flexuosa in North American west of the amphigenous, sparse to whitish. Rocky Mountains. Collections made by Chasmothecia initially whitish to pale yellow students and retained in the teaching to amber-colored (Figs. 1-3), becoming herbarium of Lori Carris at the Department black at maturity (Figs. 4-5), (135-)140- of Plant Pathology, Washington State 160(-180) µm, dehiscence appearing to University, indicate that the fungus also was result from separation of basal hyphae from collected by students in 2002 and 2004 (L. vegetative mycelium (Figs. 6-8). Carris, personal communication). A Appressoria on vegetative hyphae were photograph of a chasmothecium from the lobed (Fig. 9). Chasmothecia with two forms former collection was published (Callan and of appendages: subulate appendages Carris 2004) but without reference to (Figs. 10, 11) formed primarily on dorsal geographic origin of the specimen or surfaces of chasmothecia, tapering toward geographic distribution of the species. apices, walls displaying encrustation-like Interestingly, the fungus has not been found ornamentations, (20-)22.5-39(-41) x (3-)3.5- in the Pacific Northwest west of the cascade 7(-8) µm; uncinate appendages (Fig. 10) mountains. The fungus is not listed in primarily equatorial, rather narrow at base records of the Oregon State University Plant and widening toward middle, distal portions Disease Diagnostic Clinic covering the last geniculate to helically-twisted, strongly 50 years of samples submitted to the clinic recurved at apices, (110-)135-165(-225) x (J. Pscheidt, personal communication). Nor 7-10(-10.5) µm. Asci (Fig. 12) clavate, was the fungus encountered in western short-stipitate, (52.5-)54-66.5(-67) x (24- Washington despite several years of active )36.5-40 µm, containing 5-8 ascospores. collecting of Erysiphales in the region Ascospores (Fig. 13) hyaline, ellipsoid- (Glawe, 2004). Preston (1976) included ovoid, (16-)17.5-24.5(-27.5) x (7-)9-11(-13) information on geographical distributions for µm. Anamorph scarce, conidia short- seven species of Aesculus native to the cylindrical to ovoid (Fig. 14), (22-)22.5-27.5 USA, of which only A. californica (Spach) x (10.5-)11-14.5 µm, germ tube originating Nutt. was native to the western USA. On at site near end of conidium (Fig. 15). the basis of existing information it is reasonable to hypothesize that E. flexuosa Discussion: Based on morphological arose on one of the native North American features of chasmothecia and conidia, the Aesculus species somewhere in the eastern powdery mildew fungus on Aesculus sp. USA. The fungus most likely was was determined to be E. flexuosa. Previous introduced on infected plant material into reports of the fungus, on several species of the inland Pacific Northwest. Perhaps the Aesculus, included Georgia, Indiana, Iowa, use of appropriate molecular markers would Mississippi, New York, North Carolina, allow testing this hypothesis by assessing Pennsylvania, and Vermont (Farr et al., n. genetic variation of populations of this d.). The only powdery mildew fungus fungus on native Aesculus species in the reports on Aesculus from a western state eastern USA and comparing them with were Phyllactinia guttata