J. Crop Prot. 2020, 9 (3): 537-542______

Short paper Additions to the biotrophic fungi of Vancouver's North Shore, British Columbia

Mehrdad Abbasi

Department of Botany, Iranian Research Institute of Plant Protection, Agricultural Research Education and Extension Organization (AREEO), Tehran, Iran.

Abstract: Puccinia tanaceti in narrow sense is reported from British Columbia for the first time. Golovinomyces asterum var. solidaginis and G. macrocarpus are also new members for mycobiota of BC. New hosts are reported for rusts and powdery mildews in BC and Canada.

Keywords: Pucciniales, Erysiphales, Biodiversity, Taxonomy, Canada

Introduction12 Materials and Methods

During October and November 2018, the author All microscopic slides were made using Lactic had an opportunity to visit parks and woods in Acid in Glycerol mounting medium (Abbasi Vancouver’s north shore, mainly in the city of 2013). Microscopic study of specimens was North Vancouver. As this is the perfect time of carried out using Leica DMRB (Leitz) DIC the year to find powdery mildews, diverse microscope and BH2 Olympus compound annual and perennial plants infected by microscope and all photomicrographs taken at Erysiphales were collected. In addition, rust 400x or 1000x with a Leica DFC420 digital color infected plants from various families were also camera or Dino-Eye Eyepiece Camera using collected. The current report discusses some of DinoCapture 2.0 software (AnMo Electronics the specimens identified so far that contribute Corporation, Taiwan). In each accession 50 new information about the biotrophic fungi of fungal spores or structures were measured. Downloaded from jcp.modares.ac.ir at 12:40 IRST on Tuesday September 28th 2021 western Canada. Fernando et al. (1999) Concerning identification of powdery mildews, compiled host-fungus lists for British Columbia. species concept and taxonomy sensu Braun and The species reported here are rarely documented, Cook (2012) were followed. Host plant common and since Fernando et al.'s compilation, no new names mostly obtained from E-FLORA BC BC herbarium specimens appear among (2020). Studied materials have been deposited at MyCoPortal records (MyCoPortal. 2019). To our University of British Columbia (UBC) and knowledge there is no specific report/list dealing University of Tehran (UTFH) herbaria. with plant parasitic fungi of Vancouver’s north shore. Hopefully this paper will be the starting Puccinia tanaceti DC. s. str. (emend. Braum point to compile such a checklist for north shore 1981). plant parasitic fungi. On Tanacetum vulgare L. (Asteraceae) [common tansy], British Columbia, North Vancouver, 17 October 2018, M. Abbasi (NV3a), UTFH 1201, Handling Editor: Naser Safaie duplicate at UBC, (II) + III. ______Uredinia not seen. Urediniospores in telia, * Corresponding author: [email protected] obovoid or ellipsoid, 25-30 × 18.5-22.5 µm, Received: 10 April 2020, Accepted: 07 July 2020 Published online: 15 July 2020 wall 2 µm thick, cinnamon-brown, echinulate,

537 Additions to the biotrophic fungi______J. Crop Prot.

echinulae 2-3 µm apart, germ pores 2-3, 25-30 × 20-22.5 µm, obovoid, broadly obovoid, equatorial, covered by smooth cap. Telia ellipsoid or globoid, wall yellowish-brown to hypophyllous and on petioles, semi-compact, cinnamon-brown, 1.5-2 µm thick, finely exposed, blackish brown, teliospores 35-46.5 echinulate, with 8-11 scattered germ pores × 16-25 µm, ellipsoid or obovoid, with having a conspicuous internal ring and small rounded, conic-rounded or unequal apex, pore cap (Fig. 1B). Few covered telia were tapering towards the pedicel, constricted at present on adaxial leaf surface. Teliospores one septum, wall 1.5-2 µm at side, up to 6.5 µm at celled, 21.25-28.75 × 15-19 µm, oblong- apex, yellowish to chestnut brown, sometimes ellipsoid, oblong or angularly obovoid, with lighter part at apex, finely and densely rounded, bluntly pointed or truncate at apex, verrucose, verrucae more visible on upper mostly attenuated below, wall chestnut-brown, cell, germ pore of upper cell apical and of smooth 1-1.5 µm thick at sides and up to 3 µm lower one at the septum, pedicel colorless, at apex (Fig. 1C). Several hyaline, narrow long persistent up to 75 µm long, mesospores cylindrical structures with more or less small rarely seen (Fig. 1A). capitate heads were always present in prepared Above features fit well with the narrow microscopic slides. As mentioned by Grove species concept of P. tanaceti provided by Braun (see Wilson & Henderson 1966, p. 361), these (1981). Teliospores of BC specimen are paraphyses-like structures are pedicels of relatively small with mean spore lengths < 45 urediniospore which remain in uredinia after µm (40 µm). There are couple of reports of P. the spores have fallen off. tanaceti from BC mentioned by Fernando et al. Uromyces dactylidis has been previously (1999). These reports are all doubtful for the reported from BC on the same host by following reasons. The report of P. tanaceti on Fernando et al. (1999). They have also reported Artemisia dracunculina should be considered as two more rust species on D. glomerata P. absinthii var. dracunculina (Fahrend.) U. including Puccinia graminis and P. Braun. The report on Artemisia frigida belongs striiformoides (as P. striiformis) from BC. to P. absinthii s.lat. Reports on Artemisia When only uredinia are present, U. dactylidis luduviciana and A. tridentata may very probably can be distinguished from the two other rusts in belong to P. ludovicianae Fahrend. and P. similis having cinnamon-brown urediniospores with 8- Ellis & Everh., respectively. Fernando et al. 11 conspicuous scattered germ pores. (1999) had also reported P. tanaceti on

Downloaded from jcp.modares.ac.ir at 12:40 IRST on Tuesday September 28th 2021 Chrysanthemum sp. It will be difficult to confirm Erysiphe adunca (Wallr.) Fr. this report as Chrysanthemum species are mainly On Populus trichocarpa Torr. & A. Gray infected by Asiatic rust species P. chrysanthemi (Salicaceae) [Black cottonwood], British Roze, across the globe. Columbia, North Vancouver, November 2018, To my knowledge the current report is the M. Abbasi (NV7), UTFH 1203. first authentic finding of P. tanaceti s.str. from Mycelium mostly epiphyllous, effuse or in BC and T. vulgare is a new host for the rust in patches, on some leaves covering the entire leaf Canada. upper surface. Chasmothecia mostly gregarious on upper side of the leaves, rarely Uromyces dactylidis G. H. Otth hypophyllous, 124-196 µm diam., with up to 65 On ornamental Dactylis glomerata L. (Poaceae) stiff to flexuous appendages, up to 2 times as [orchard-grass], British Columbia, North long as chasmothecial diam., circinate to Vancouver, 17 October 2018, M. Abbasi subhelicoid at apex (Fig. 1F). This powdery (NV8), UTFH 1202, II + III. mildew has been previously reported on P. Uredinia amphigenous, small, elliptic or trichocarpa, P. tremuloides Michx. and Salix oblong, cinnamon-brown, mostly surrounded or spp. from BC. under the name Uncinula adunca covered by ruptured epidermis. Urediniospores (Fernando et al. 1999).

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Figure 1 Puccinia tanaceti, urediniospores and teliospores, bar = 10 µm (A); Uromyces dactylidis, urediniospores (B) and teliospores (C), bar = 10 µm; Phyllactinia corni, chasmothecium (D), bar = 50 µm; Sawadaea bicornis, chasmothecium (E), bar = 15 µm; Erysiphe adunca, chasmothecia (F), bar = 60 µm; Golovinomyces asterum var. solidaginis, chasmothecium (G), bar = 30 µm.

539 Additions to the biotrophic fungi______J. Crop Prot.

Golovinomyces asterum var. solidaginis U. Golovinomyces macrocarpus (Speer) U. Braun Braun On Tanacetum vulgare L. (Asteraceae) On Solidago sp. (Asteraceae) [goldenrod], British [common tansy], British Columbia, North Columbia, North Vancouver, November 2018, M. Vancouver, 17 October 2018, M. Abbasi Abbasi (NV5) UTFH 1204-Solidago ‘Crown of (NV3b), UTFH 1206, duplicate at UBC. Rays’, North Vancouver, October 2018, M. Abbasi Only anamorph observed. Mycelium in dense (NV1) UTFH 1205, duplicate at UBC. white persistent patches on both sides of the leaf Mycelium white, amphigenous, effused or and on stem; conidiophores erect and straight with in patches. Conidiophores mostly arising mostly cylindrical or rarely slightly curved foot laterally from the hyphal mother cell, foot- cells with 50-80 µm length followed by 1-3 shorter cells often curved in the basal part, 50-82.5 cells; conidia mostly doliiform to ellipsoid-ovoid µm in length. Conidia in chains, doliiform, 26-36 × 15-17.5 µm; conidial germination with cylindrical, doliiform-subcylindrical or clavate, relatively short germ tubes arising from an ellipsoid, 27.5-42.5 × 15-18.75 µm, germ end. These features fit the morphological tubes mostly terminal, long up to three times characteristics of G. macrocarpus provided by as long as the conidial length, filiform, with Braun and Cook (2012). This is the first report of one septum and swollen appressorium at G. macrocarpus from BC on T. vulgare. apex, sometimes with two germ tubes. The studied material (UTFH 1206) was also Chasmothecia amphigenous, mostly in large infected by Puccinia tanaceti. Thus, Tanacetum groups, 117.5-150 µm diam. Appendages vulgare is reported here as a contemporaneous numerous mostly in the lower part of host of two biotrophic fungi viz. G. chasmothecia, mycelium like, at first hyaline macrocarpus and P. tanaceti. later brown, simple, septate, of variable length up to 2 times as long as chasmothecial Phyllactinia corni H. D. Shin & M. J. Park diameter (Fig. 1G). Asci 6-8, clavate or On Cornus occidentalis (Torr. & A. Gray) broadly clavate with 2 ascospores. Coville (Cornaceae) [red-osier dogwood], Erysiphe cichoracearum is the only North Vancouver, Oct. 2018, M. Abbasi (NV6), reported powdery mildew on Solidago sp. UTFH 1207, duplicate at UBC. from BC (Fernando et al. 1999). This species Chasmothecia were present on both sides of is now recognized as Golovinomyces the leaf, mainly hypophyllous, scattered or cichoracearum, which is confined to hosts of gregarious, up to 225 µm diam. Appendages 9-17,

Downloaded from jcp.modares.ac.ir at 12:40 IRST on Tuesday September 28th 2021 subfamily Cichorioideae in strict sense in equatorial part, acicular, rarely forked at apex, (Braun & Cook 2012). The above specimens with basal swelling up to 40 µm diam (Fig. 1D). on Solidago (subfamily Asteroideae) from Penicillate cells mostly bifurcated or branched North Vancouver fit well with the description into several branchlets, having numerous of G. asterum var. solidaginis provided by mucilaginous appendages at apex. Braun and Cook (2012). The entire plant of Above powdery mildew was formerly an ornamental Solidago ‘Crown of Rays’ was reported as Ph. guttata on Cornus spp. from BC heavily infected by the powdery mildew. (Fernando et al. 1999). However, C. Heavy infection by hyperparasite species occidentalis is a new host for Ph. corni in BC. Ampelomyces quisqualis was also observed on this specimen. This is the first report of G. Sawadaea bicornis (Wallr.) Homma asterum var. solidaginis on this cultivated On Acer pseudosieboldianum (Pax) Kom. plant from BC. The Fernando et al.'s report of (Sapindaceae) [Korean Maple], North E. cichoracearum on Solidago sp. is based on Vancouver, Oct. 2018, M. Abbasi (NV2), an old report from literature (Barr 1953) and UTFH 1208, duplicate at UBC. very probably belongs to G. asterum var. Mycelium on leaves mainly epiphyllous, in solidaginis. patches, often vein-limited. Chasmothecia

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mostly hypophyllous, 150-200 µm diam., Braun, U. 1981. Vorarbeiten zu einer scattered with numerous (up to 45) simple or Rostpilzflora der DDR. Feddes Repertorium 1-3 times branched appendages arising from Specierum Novarum Regni Vegetabilis. upper half of ascocarp. Apices of appendages 92(1-2): 95-123. were uncinated or circinate (Fig. 1E). Braun, U. and Cook, R. T. A. 2012: Parmelee (1977) first reported this powdery Taxonomic Manual of the Erysiphales mildew from BC, as Uncinula bicornis (Powdery Mildews). CBS Biodiversity (Wallr.) Lév. on Acer macrophyllum. The Series. 11. 707 p. second record belongs to Mel’nik (1995) who E-FLORA BC. 2020. Electronic Atlas of the reported the fungus from Chilliwack, around Flora of British Colombia. Last updated Agassiz on the same host. Acer June 14, 2020, Available on: http://ibis.geog. pseudosieboldianum is a new host for S. ubc.ca/biodiversity/eflora. bicornis in North America. Fernando, A., Ring, F., Lowe, D., and Callan, B. 1999. Index of plant pathogens, plant- Acknowledgements associated microorganisms and forest fungi of British Columbia. Canadian Forest I would like to thank Prof. M. Berbee, Dept. of Service, Pacific Forestry Centre Information Botany, University of British Columbia for Report BC-X-385. permitting me to use his lab instruments and Mel’nik, V. A. 1995. Materials to the equipment generously. Prof. Berbee is also micromycetes studies of British Columbia acknowledged for proofreading this manuscript (CANADA). Mikologia i Fitopatologia, and for valuable comments and corrections. 29(2): 14-19. MyCoPortal. 2019. The Mycology Collections References data Portal. http://mycoportal.org/portal/index. php. (Accessed on Sept. 01). Abbasi, M. 2013. New reports of rust fungi for Parmelee, J. A. 1977. The fungi of Ontario. II. mycobiota of Iran. Iranian Journal of Plant Erysiphaceae (mildews). Canadian Journal Pathology, 49(3): 351-356. of Botany, 55(14): 1940-1983. Barr, M. E. 1953. Pyrenomycetes of British Wilson, M. and Henderson, D. M. 1966. British Columbia. Canadian Journal of Botany, 31: Rust Fungi. Cambridge University Press, 810-830. Cambridge, UK. Downloaded from jcp.modares.ac.ir at 12:40 IRST on Tuesday September 28th 2021

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ﮔﺰارﺷﯽ از ﻗﺎرچﻫﺎي ﺑﯿﻮﺗﺮوﻓﯿﮏ ﺳﺎﺣﻞ ﺷﻤﺎﻟﯽ وﻧﮑﻮور، ﺑﺮﯾﺘﯿﺶ ﮐﻠﻤﺒﯿﺎ

ﻣﻬﺮداد ﻋﺒﺎﺳﯽ

ﺑﺨﺶ ﺗﺤﻘﯿﻘﺎت رﺳﺘﻨﯽﻫﺎ، ﻣﺆﺳﺴﻪ ﺗﺤﻘﯿﻘﺎت ﮔﯿﺎهﭘﺰﺷﮑﯽ ﮐﺸﻮر، ﺳﺎزﻣﺎن ﺗﺤﻘﯿﻘﺎت، آﻣﻮزش و ﺗﺮوﯾﺞ ﮐﺸﺎورزي، ﺗﻬﺮان، اﯾﺮان. ﭘﺴﺖ اﻟﮑﺘﺮوﻧﯿﮑﯽ ﻧﻮﯾﺴﻨﺪه ﻣﺴﺌﻮل ﻣﮑﺎﺗﺒﻪ: [email protected] درﯾﺎﻓﺖ: 22 ﻓﺮوردﯾﻦ 1399؛ ﭘﺬﯾﺮش: 17 ﺗﯿﺮ 1399

ﭼﮑﯿﺪه: ﻗﺎرچ ﻣﻮﻟﺪ زﻧﮓ Puccinia tanaceti ﺑﺎ ﻣﻔﻬﻮم اﺧﺺ ﮔﻮﻧﻪ ﺑﺮاي اوﻟﯿﻦ ﺑﺎر از اﺳﺘﺎن ﺑﺮﯾﺘﯿﺶ ﮐﻠﻤﺒﯿﺎ ﮔﺰارش ﻣﯽﮔﺮدد. ﺗﺎﮐﺴﻮنﻫﺎي ﻣﻮﻟﺪ ﺳﻔﯿﺪك ﭘﻮدري Golovinomyces asterum var. solidaginis و G. macrocarpus ﻧﯿﺰ ﺑﻪﻋﻨﻮان اﻋﻀﺎ ﺟﺪﯾﺪ ﺑﺮاي ﻣﯿﮑﻮﺑﯿﻮﺗﺎي اﺳﺘﺎن ﮔﺰارش ﻣﯽﺷﻮﻧﺪ. ﮔﻮﻧﻪﻫﺎي ﮔﯿﺎﻫﯽ ﻣﺘﻌﺪدي ﺑﻪﻋﻨﻮان ﻣﯿﺰﺑﺎﻧﺎن ﺟﺪﯾﺪ زﻧﮓﻫﺎ و ﺳﻔﯿﺪكﻫﺎ در اﺳﺘﺎن ﺑﺮﯾﺘﯿﺶ ﮐﻠﻤﺒﯿﺎ و ﮐﺎﻧﺎدا ﻣﻌﺮﻓﯽ ﻣﯽﺷﻮﻧﺪ.

واژﮔﺎن ﮐﻠﯿﺪي: Erysiphales ،Pucciniales، ﺗﻨﻮع زﯾﺴﺘﯽ، ﺗﺎﮐﺴﻮﻧﻮﻣﯽ، ﮐﺎﻧﺎدا Downloaded from jcp.modares.ac.ir at 12:40 IRST on Tuesday September 28th 2021

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