Notes on Powdery Mildews (Erysiphales) in Japan: III

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Notes on powdery mildews (Erysiphales) in Japan: III. Golovinomyces and Podosphaera

Article in Mycoscience · March 2015 DOI: 10.1016/j.myc.2014.07.002

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Short communication Notes on powdery mildews (Erysiphales) in Japan: III. Golovinomyces and Podosphaera

* Jamjan Meeboon a,b, Susumu Takamatsu a, a Department of Bioresources, Graduate School, Mie University, 1577 Kurima-Machiya, Tsu 514-8507, Japan b Department of Agriculture, Ministry of Agriculture and Cooperatives, 50 Phaholyothin Rd., Ladyao, Chatuchak, Bangkok, Thailand article info abstract

Article history: Several new records of Golovinomyces and Podosphaera species (Erysiphales) in Japan are Received 22 May 2014 reported with morphological and molecular data, including the first finding of G. cynoglossi Received in revised form in Japan, the first occurrence of Euoidium sp. on Trigonotis peduncularis, G. riedlianus on 27 June 2014 Galium trifloriforme var. nipponicum and P. xanthii on Verbena brasiliensis, as well as the first Accepted 4 July 2014 morphological descriptions and molecular data for G. rubiae on Rubia hexaphylla, P. Available online 10 August 2014 curvispora on Aria alnifolia, P. tridactyla on Cerasus leveilleana, and P. xanthii on Parasenecio hastatus subsp. tanakae and V. bonariensis based on Japanese specimens. Keywords: © 2014 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved. Erysiphaceae Euoidium Molecular phylogeny Morphology New host

This is the third part of a series of studies on powdery mildews Erysiphaceae that were retrieved from DNA databases (DDBJ, in Japan. In this report, we described and illustrated four EMBL, NCBI) using MUSCLE (Edgar 2004) implemented in powdery mildew species belonging to Golovinomyces (including MEGA 5 (Tamura et al. 2011). Alignments were then manually Euoidium anamorphs) and three species belonging to reﬁned using the MEGA 5 program and were deposited in Podosphaera supplemented by molecular data. TreeBASE (http://www.treebase.org/) under the accession The nucleotide sequences of the 50-end of the 28S rRNA number S15835. Phylogenetic trees were obtained from the gene (including domains D1 and D2) and the internal tran- data using maximum parsimony (MP) method and maximum scribed spacer (ITS) regions were determined according to the likelihood (ML) method as described in Meeboon and procedure of Meeboon and Takamatsu (2015). Representative Takamatsu (2015). new sequences determined in this study were deposited in The 28S rRNA gene for three specimens of Podosphaera was DNA Data Base of Japan (DDBJ) under the accession numbers determined in this study. The three sequences were aligned AB936274eAB936277. Sequences generated from the 28S rRNA with 23 Podosphaera and Cystotheca sequences that were gene and ITS region were aligned with other sequences of the retrieved from the DNA databases. Two Cystotheca sequences

* Corresponding author. Tel.: þ81 59 231 9497; fax: þ81 59 231 9540. E-mail address: [email protected] (S. Takamatsu). http://dx.doi.org/10.1016/j.myc.2014.07.002 1340-3540/© 2014 The Mycological Society of Japan. Published by Elsevier B.V. All rights reserved. 244 mycoscience 56 (2015) 243e251

Podosphaera xanthii ex Cucurbita AB462766 28S rRNA gene 26 sequences Podosphaera xanthii ex Hibiscus AB936276 680 characters 71 steps Podosphaera xanthii ex Verbena brasiliensis AB936277 CI = 0.803 RI = 0.844 Podosphaera xanthii ex Helianthus AB462781 RC = 0.678 Podosphaera xanthii ex Zinnia AB462782

Podosphaera xanthii ex Zehneria AB462792

Podosphaera balsaminae ex Impatiens AB462788

Podosphaera sp. ex Solanum AB462769

Podosphaera euphorbiae-hirtae ex Acalypha AB462770

Podosphaera sp. ex Vigna AB462784

-/72 Podosphaera xanthii ex Lactuca AB462773

Podosphaera sp. ex Verbena AB462780

Podosphaera xanthii ex Parasenecio AB936274

Podosphaera xanthii ex Gerbera AB462763

-/71 Podosphaera xanthii ex Cosmos AB462797

Podosphaera balsaminae ex Impatiens AB462787

Podosphaera elsholtziae ex Ajuga AB462794

91/94 Podosphaera erigerontis-canadensis ex Conyza AB462772

Podosphaera intermedia ex Clerodendrum AB462777

-/80 Podosphaera astericola ex Aster AB462779

Podosphaera astericola ex Aster AB462760 100/100 Podosphaera tridactyla ex Cerasus leveilleana AB936275

Podosphaera longiseta ex Padus AB022423 92/97 Podosphaera tridactyla ex Microcerasus AB022393

Cystotheca wrightii ex Quercus AB022355

Cystotheca lanestris ex Quercus AB022353 1 change

Fig. 1 e Phylogenetic analysis of the divergent domains D1 and D2 sequences of the 28S rRNA gene for 26 sequences from the genus Podosphaera and Cystotheca. This tree is a phylogram of one of the 26 most parsimonious trees with 71 steps, which was found using a heuristic search. Horizontal branch lengths are proportional to the number of substitutions that were inferred to have occurred along a particular branch of the tree. BS (>70%) values by the maximum parsimony (MP) and maximum likelihood (ML) methods were shown on the respective branch. Sequences from the collections reported in this study are shown in boldface.

were used as outgroup taxa according to Mori et al. (2000). The sequences that were retrieved from the DNA databases. Two alignment data matrix consisted of 26 sequences and 680 Cystotheca sequences were used as outgroup taxa according to characters, of which 53 (7.8%) characters were variable and 37 Mori et al. (2000). The alignment data matrix consisted of 51 (5.4%) characters were informative for parsimony analysis. A sequences and 496 characters, of which 143 (28.8%) characters total of 26 equally parsimonious trees with 71 steps were were variable and 117 (23.6%) characters were informative for constructed by the MP analysis. One of the 26 trees with the parsimony analysis. A total of six equally parsimonious trees highest log likelihood value is shown in Fig. 1. For the ITS with 285 steps were constructed by the MP analysis. One of the analysis, the ﬁve sequences derived from the fungi reported in six trees with the highest log likelihood value is shown in this study were aligned with 46 Podosphaera and Cystotheca Fig. 2. Phylogenetic trees generated from ML analysis were mycoscience 56 (2015) 243e251 245

Podosphaera xanthii ex Gynostemma D84378 ITS Podosphaera xanthii ex Verbena AB046985 51 sequences Podosphaera xanthii ex Vigna AB040297 496 characters Podosphaera xanthii ex Cucurbita AB040315 285 steps Podosphaera xanthii ex Cucumis AB040323 CI = 0.712 Podosphaera sp. ex Saintpaulia AB040338 RI = 0.879 Podosphaera xanthii ex Zinnia AB040354 RC = 0.626 Podosphaera euphorbiae-hirtae ex Acalypha AB040306 Podosphaera xanthii ex Hibiscus AB936276 Podosphaera sp. ex Dunbaria AB040334 Podosphaera xanthii ex Rudbeckia AB040296 Podosphaera xanthii ex Petasites AB040307 Podosphaera xanthii ex Physalis AB040336 Podosphaera xanthii ex Verbena bonariensis AB462804 Podosphaera xanthii ex Verbena brasiliensis AB936277 Podosphaera sp. ex Cayratia AB026151 Podosphaera xanthii ex Lactuca AB040294 Podosphaera pseudofusca ex Fatoua AB040320 Podosphaera sp. ex Verbena AB040347 Podosphaera xanthii ex Lactuca AB040352 75/80 Podosphaera xanthii ex Cosmos AB040300 Podosphaera xanthii ex Carthamus AB040298 Podosphaera xanthii ex Parasenecio AB936274 Podosphaera xanthii ex Euryops DQ205330 Podosphaera xanthii ex Coreopsis EF442023 Podosphaera xanthii ex Calendula AB040317 Podosphaera xanthii ex Farfugium AB040346 94/98 Podosphaera sp. ex Peristrophe AB026135 Podosphaera astericola ex Aster AB040335 Podosphaera astericola ex Aster AB040353 100/100 Podosphaera erigerontis-canadensis ex Taraxacum AB046987 Podosphaera elsholtziae ex Ajuga AB026142 Podosphaera phtheirospermi ex Melampyrum AB040332 Podosphaera intermedia ex Clerodendrum AB026145 Podosphaera tridactyla ex Prunus sp. AY833659 98/98 Podosphaera tridactyla ex Cerasus leveilleana AB936275 Podosphaera Cerasus 75/- sp. ex AB026138 100/100 Podosphaera tridactyla ex Armeniaca AY833657 Podosphaera tridactyla ex Prunus AY833658 Podosphaera tridactyla ex Padus AY833652 Podosphaera tridactyla ex Microcerasus AB000943 Podosphaera longiseta ex Padus AB000945 Podosphaera leucotricha ex Malus AF073353 100/100 Podosphaera leucotricha ex Malus AB027231 76/72 Podosphaera sp. ex Photinia AB525934 Podosphaera curvispora ex Aria AB525928 76/95 100/100 Podosphaera clandestina ex Crataegus AB525931 Podosphaera clandestina ex Crataegus AB525930 Podosphaera photiniae ex Photinia AB026147 100/100 Cystotheca wrightii ex Quercus AB000932 Cystotheca lanestris ex Quercus AB000933 5 changes

Fig. 2 e Phylogenetic analysis of the ITS region for 51 sequences from the genus Podosphaera and Cystotheca. This tree is a phylogram of one of the six most parsimonious trees with 285 steps, which was found using a heuristic search. Horizontal branch lengths are proportional to the number of substitutions that were inferred to have occurred along a particular branch of the tree. BS (>70%) values by the maximum parsimony (MP) and maximum likelihood (ML) methods were shown on the respective branch. Sequences from the collections reported in this study are shown in boldface.

almost identical to the MP trees in both 28S rRNA gene and ITS Golovinomyces cynoglossi (Wallr.) Heluta, Ukrayins'k. Bot. analyses, and thus only the bootstrap values were shown on Zhurn. 45(5): 62, 1988. Fig. 3. the MP trees. Phylogenetic trees of Golovinomyces spp. Description: Mycelium amphigenous, mainly epiphyllous, described in this study were already reported in Takamatsu effuse or in irregular patches, thin to moderately thick, et al. (2013), and thus not shown in this report. sometimes covering the entire leaf surface, evanescent to 246 mycoscience 56 (2015) 243e251

(2012), as far as we know there is no formal record of this species in Japan. The ITS sequence (AB769454) of this collection is 97.4% similar to G. cynoglossi on Pulmonaria obscura Dumort. (AB077684) collected in Lithuania and formed a clade together (Takamatsu et al. 2013). Based on these molecular data and anamorphic characters, this collection was identiﬁed as G. cynoglossi.

Golovinomyces rubiae (H.D. Shin & Y.J. La) U. Braun, Schlech- tendalia 3: 51, 1999. Fig. 4. Description: Mycelium amphigenous, also on stems and pe- duncles, thin, effuse, white, evanescent to persistent. Hyphae straight to sinuous, occasionally almost geniculate, thin- walled, smooth, hyaline, 4e8 mm wide. Hyphal appressoria poorly developed to nipple-shaped, solitary, 3e7 mm diam. Conidiophores arising from upper surface of hyphal mother cells, centrally to somewhat towards one end of the cell, (76e) 111e128(e162) mm long. Foot cells straight, cylindrical, about (39e)44e51(e85) (7.5e)8e10(e12) mm, followed by 3e6 shorter cells, with a basal septum at the branching point of the mycelium, 2.5e4 mm elevated, forming catenescent conidia. Conidia ellipsoideovoid, (23e)26e30.5(e31.5) (12.5e) 13.5e15.5(e17) mm. Germ tubes not observed. Collection examined: on Rubia hexaphylla Makino (Rubia- ceae), Japan, Niigata Pref., Mt. Myojo, 19 Oct 1996, S. Taka- Fig. 3 e Golovinomyces cynoglossi on Cynoglossum matsu (MUMH181, 292), GenBank accession number: asperrimum (MUMH3196). A: Conidia. B: Conidiophores. AB077635 (ITS), AB077634 (28S rRNA gene). Bar:20mm. usually persistent. Hyphae straight to ﬂexuous, hyphal appressoria variable, nipple-shaped, with somewhat crenu- late surface or slightly to moderately lobed, solitary per cell, occasionally several in a series or rarely in opposite pairs, 5e8 mm diam. Conidiophores arising from upper surface to somewhat laterally from the hyphal mother cell, erect, (72e) 88e157(e198) mm long. Foot cells straight or with a curved basal part, occasionally somewhat ﬂexuousesinuous, cylindrical, (40e)58e60(e64) (7e)9e12 mm, sometimes slightly constricted at the basal septum that is occasionally raised somewhat above the junction with the mother cell, followed by 3e7 shorter cells, with a basal septum at the branching point of the mycelium (3e)8e12 mm elevated, forming catenescent conidia. Conidia ellipsoideovoid to doliformecylindrical, (25.5e)27.5e31(e35) 13e17(e20) mm. Germ tubes not observed. Collection examined: on Cynoglossum asperrimum Nakai (Boraginaceae), Japan, Mie Pref., Mie University Forest Station, 26 Aug 2004, T. Inuma, MUMH3196, GenBank accession number: AB769454 (ITS). Remarks: Boraginaceae is one of the most important host families of Golovinomyces, containing 192 host species world- wide (Matsuda and Takamatsu 2003), which is the second largest host number following the Asteraceae. Most records have been reported from Europe, West/Central Asia and North America. There are only two hosts of Golovinomyces on Bor- aginaceae recorded from Japan as “Erysiphe cichoracearum”, viz. Cy. asperrimum and Trigonotis peduncularis Steven ex Palib., but without any morphological data (Wada and Hirata 1977; Takamatsu et al. 2013; Sato and Eto 2014). Although Japan is Fig. 4 e Golovinomyces rubiae on Rubia hexaphylla included in the distribution of G. cynoglossi in Braun and Cook (MUMH292). A: Conidia. B: Conidiophores. Bar:15mm. mycoscience 56 (2015) 243e251 247

Fig. 5 e Golovinomyces riedlianus on Galium triﬂoriforme var. nipponicum (MUMH414).A: Chasmothecia. B: Asci and ascospores. Bars:A50mm; B 30 mm.

Remarks: Matsuda and Takamatsu (2003) first reported Euoidium sp. on Trigonotis peduncularis Steven ex Palib. Fig. 6. rRNA gene sequences of this collection. These sequences Description: Mycelium amphigenous. Hyphal appressoria belonged to the “G. orontii group 1” clade with “G. orontii” on nipple-shaped. Conidiophores arising from upper surface of Galium spp. in Fig. 1 of Takamatsu et al. (2013), but the authors mother cell, erect, (74e)77.5e87(e98) mm long. Foot cells did not describe morphological characteristics of this collec- straight or with a curved basal part, occasionally somewhat tion. This is the first morphological record of this collection. flexuousesinuous, cylindrical, 40e60 (5e)8e10.5(e12) mm, The consistently straight conidiophore foot cells agree well followed by 1e2(e3) shorter cells, with a basal septum at the with G. rubiae, i.e. they are not in favor of G. orontii s. str. “G. branching point of the mycelium, forming catenescent con- orontii group 1” in Takamatsu et al. (2013) is thus tentatively idia. Conidia ellipsoideovoid to doliformecylindrical, (20.5e) identified as G. rubiae. Molecular data of G. rubiae from 26e28(e30.5) (11e)13e15(e17) mm. Germ tubes not observed. authentic material and taxonomic re-examination are required.

Golovinomyces riedlianus (Speer) Heluta, Ukrayins'k. Bot. Zhurn. 45(5): 63, 1988. Fig. 5. Description: Mycelium amphigenous, forming irregular patches, pale to white, thin, evanescent to persistent. Chas- mothecia (87e)95e105(e116) mm diam., dark, scattered to gregarious. Peridium composed of dark brown, irregularly polygonal cells. Appendages numerous, equatorial and in the lower half of the ascomata, sometimes also in the upper half, mycelioid, simple, rarely irregularly branched, septate, thin- walled, smooth or somewhat rough, yellowish to deep brown throughout, interlaced with each other and with the mycelium. Asci (39e)41e51(e64) (22e)25e33(e35) mm, 8e12 per chasmothecium, 2-spored, clavate to saccate, with a thickened ascal wall. Ascospores (14e) 15.5e21 9e13(e15.5) mm, ellipsoid to ovoid, hyaline. Collection examined: on Galium triﬂoriforme Kom. var. nipponicum Nakai (Rubiaceae), Japan, Shiga Pref., Taga-cho, Kawachi Cave, 13 Sep 1997, S. Takamatsu, MUMH414. Remarks: Four powdery mildew species with catenate conidia have been recorded on Galium, viz. Neo€erysiphe galii (S. Blumer) U. Braun, G. calceolariae Havryl., S. Takam. & Heluta, G. orontii, and G. riedlianus (Takamatsu et al. 2009). This collection differs from N. galii by usually containing mature ascospores in asci. Golovinomyces orontii is distinguished from G. riedlianus in length/width (l/w) ratio of ascospores (l/w ¼ 1.22e1.45 in G. orontii and 1.44e1.89 in G. riedlianus; Takamatsu et al. 2009). l/w ratio of this collection was about 1.5, which is consistent with Fig. 6 e Euoidium sp. on Trigonotis peduncularis that of G. riedlianus. rRNA gene sequencing of this collection (MUMH1562). A: Conidia. B: Conidiophores. C: Appressoria. failed. Bar:20mm. 248 mycoscience 56 (2015) 243e251

Fig. 7 e Podosphaera curvispora on Aria alnifolia (MUMH3266). A: Chasmothecium and ascus. B: Appendages. C: Asci and ascospores. Bars:A50mm; B 10 mm; C 40 mm. Composite ﬁgure made from separate original photos.

Collection examined: on Trigonotis peduncularis (Bor- (15e)16e24(e26) (6e)8e13 mm, crescent-shaped, curved, aginaceae), Japan, Kyoto Pref., Mt. Hie, 11 Nov 2001, S. Taka- hyaline. matsu, MUMH1562. Collection examined: on Aria alnifolia (Siebold & Zucc.) Remarks: Trigonotis peduncularis is a biennial herb distrib- Decne. (Rosaceae), Japan, Toyama Pref., Asahi-machi, Shir- uted in Japan, Korea and China, and recorded as a host of G. oyama, 20 Oct 2001, Y. Sato, MUMH3266, GenBank accession cynoglossi in Braun and Cook (2012). Wada and Hirata (1977) number: AB525928 (ITS). recorded Erysiphe cichoracearum on this plant in Japan. How- Remarks: Podosphaera curvispora was first described by ever, this record is based on the inoculation test of tobacco Nomura (1984) as a powdery mildew on Sorbus commixta Hedl. powdery mildew on this plant conducted by Fukuda et al. Mimuro and Sato (2002) reported this species on A. alnifolia (1973), not based on natural occurrence. Based on the briefly in an abstract. Therefore, detailed morphological anamorphic characteristics, this collection belongs to Euoi- characteristics of this fungus are presented in this study. dium (anamorphic state of Golovinomyces), most likely to G. Phyllactinia pyri-serotinae Sawada also occurred on this cynoglossi. However, the length of conidiophores and foot cells specimen. is shorter than those of G. cynoglossi (Braun and Cook 2012). In addition, sequencing of this collection failed. Thus, this Podosphaera tridactyla (Wallr.) de Bary, Abh. Senkenberg. collection was tentatively identified as Euoidium sp. in the Naturf. Ges. 7: 390, 1870. Fig. 8. present stage. Further examinations using fresh materials are Description: Chasmothecia scattered to gregarious, (90e) required. 102e114(e122) mm diam. Peridium cells irregularly shaped. Appendages few, 2e5, in the upper half, almost fasciculate, Podosphaera curvispora Y. Nomura, Trans. Mycol. Soc. Japan rather stiff and straight or somewhat curved, apices 2e6 times 25: 199, 1984. Fig. 7. regularly dichotomously branched, branching pattern vari- Description: Mycelium amphigenous, persistent. Chasmo- able, primary and sometimes secondary branches elongated, thecia (76e)93e104 mm in diam., globose, dark brown, scat- often horizontal, rarely short primary branches cause more tered to ± gregarious. Peridium 10e13 mm thick, composed of compact branching, appendages occasionally deeply cleft, dark, irregularly polygonal cells. Appendages (23.5e) even forked in the lower half, tips of the ultimate 69e153(e175) (5e)6e8.5(e9.5) mm, 4e13 per chasmothecium, branchlets ± knob-like, rarely slightly recurved, length vari- 1e1.5 times as long as the chasmothecial diam., 3e6-septate, able and unequal in length on the same chasmothecia, (41e) equatorial, stiff, brown up to the uppermost septum, primary 72e188(e221) mm, stalk moderately thick-walled throughout, branches often somewhat elongated, tips of the ultimate sometimes very thick below but thinner above, septate branchlets knob-like or somewhat recurved, rarely branched throughout or only in the lower half, mostly with 0e4(e6) near the middle of the stalk, with 4e5 times regularly septa, smooth to faintly rough-walled, brown in the lower half branched apices. Asci (85e)96e109(e114) (62e) becoming paler to hyaline above, pigmentation sometimes 64e74(e92) mm, 8-spored, broadly ovate, sessile. Ascospores reaching the upper half, outline of the stalk sometimes mycoscience 56 (2015) 243e251 249

Fig. 8 e Podosphaera tridactyla on Cerasus leveilleana (MUMH418). A: Chasmothecia. B: Appendages. C: Asci and ascospores. Bars:A60mm; B 50 mm; C 30 mm. Composite ﬁgure made from separate original photos.

somewhat uneven. Ascus subglobose to broadly ellip- apetala (Siebold & Zucc.) Ohle ex H. Ohba var. pilosa (Koidz.) H. soideovoid, (57e)62e81(e100) (52e)55e68(e76) mm, rarely Ohba (AB026138) collected in Japan. somewhat larger, sessile, (4e)6e8-spored. Ascospores ellipsoideovoid to subglobose, (15e)17e23(e25) (8e) Podosphaera xanthii (Castagne) U. Braun & Shishkoff, 9e14(e16) mm, usually colorless. Schlechtendalia 4: 31, 2000. Collections examined: on Cerasus leveilleana (Koehne) H. 1) Host: Parasenecio hastatus (L.) H. Koyama subsp. tanakae Ohba (Rosaceae), Japan, Nara Pref., Koriyama-shi, Yata (Franch. & Sav.) H. Koyama. Fig. 9. Temple, 20 Sep 1997, S. Takamatsu, MUMH418; Niigata Pref., Description: Mycelium on leaves hypophyllous, effuse or in Mt. Yahiko, 18 Oct 1996, S. Takamatsu, MUMH274, GenBank patches, evanescent to persistent. Chasmothecia scattered to accession number: AB936275 (ITS þ 28S rRNA gene). gregarious, (78e)86e103(e113) mm in diam. Peridium Remarks: Podosphaera sp. was reported by Hirata and Wada composed of irregular, conspicuous, large, dark brown cells. (1973) as a powdery mildew on C. leveilleana without Appendages 99e266 4e6 mm, about 0.5e2 times the chas- morphological description. Based on teleomorph characters mothecial diam., about 4e14, mostly in the lower half of the and molecular data, this fungus is identiﬁed as P. tridactyla. chasmothecia, occasionally reaching the upper half, myce- Cunnington et al. (2005) reported that P. tridactyla separates lioid, simple, septate, thin-walled, smooth to rough, occa- into three phylogeny groups based on RFLP and ITS se- sionally irregularly branched, brown throughout when quences, which was conﬁrmed by Takamatsu et al. (2010) mature, long appendages often paler or hyaline in the upper later. The present collection belongs to the clade 3 of half, often forming dark patches on the leaves when com- Cunnington et al. (2005) and is identical to ITS sequences from bined with pigmented hyphae around grouped ascomata. Asci collections on Prunus sp. (AY833659) collected in Korea and C. (84e)88e114(e124) (57e)61e69(e82) mm, 8-spored, broadly 250 mycoscience 56 (2015) 243e251

Fig. 9 e Podosphaera xanthii on Parasenecio hastatus var. tanakae (MUMH244). A: Chasmothecium. B: Chasmothecia and asci. C: Asci and ascospores. Bars:A50mm; B 20 mm; C 40 mm. Composite ﬁgure made from separate original photos.

ellipsoideovoid, sessile, very short-stalked. Ascospores (14e) 17e20.5(e22.5) 12e14.5(e16) mm, broadly ellipsoideovoid, hyaline. Collections examined: Japan, Niigata Pref., Mt. Myojo, 19 Oct 1996, S. Takamatsu (MUMH177, 178, 244), GenBank accession number: AB936274 (ITS þ 28S rRNA gene). Remarks: Parasenecio hastatus var. tanakae is a perennial herb distributed from Tohoku region to northern part of Kanto region of the Main Island of Japan. Oidium sp. was reported by Hirata and Wada (1973) on this plant without morphological record. Both morphological and molecular data supported that this fungus is P. xanthii.

2) Hosts: Verbena brasiliensis Vell. and V. bonariensis L. (Verbe- naceae). Fig. 10. Description: Mycelium amphigenous, in irregular patches or effuse, thin to dense, evanescent to ± persistent. Hyphae thin- walled, smooth, 3e6 mm wide. Hyphal appressoria indistinct to slightly nipple-shaped, solitary. Conidiophores arising from the upper surface of hyphal mother cells, (93e) 112e146(e170) mm long, mostly towards one end of the cell but sometimes ± centrally, erect. Foot cells (31e) 43e48(e54) 10e14 mm, cylindrical, sometimes slightly constricted at the basal septum or slightly swollen at the very base, followed by 0e2 shorter cells, with a basal septum at the branching point of the mycelium, forming conidia in chains. Conidia ellipsoideovoid to doliform, (24e)26e30(e39) (14e) 16.5e17.5(e19) mm. Germ tubes ± lateral, simple. Collections examined: on V. brasiliensis, Japan, Mie Pref., Tsu-shi, Mie University, 30 Jun 1999, S. Takamatsu, MUMH856, GenBank accession number: AB936277 (ITS þ 28S rRNA gene); Fig. 10 e Podosphaera xanthii on Verbena bonariensis on V. bonariensis, Japan, Mie Pref., Tsu-shi, Mie University, 10 (MUMH1899). A: Conidia. B: Conidiophores. Bar:20mm. mycoscience 56 (2015) 243e251 251

Jun 2002, S. Takamatsu, MUMH1899, GenBank accession Hirata K, Wada K, 1973. List of the powdery mildew fungi and number: AB462804 (ITS). their host plants found up to date in Niigata Prefecture (in e Remarks: Verbena brasiliensis and V. bonariensis are intro- Japanese). Reports of the Tottori Mycological Institute 10: 485 503. Homma Y, 1976. Powdery mildew fungi and their host plants in duced perennial herbs of Verbenaceae originated in South Shikoku District (1) (in Japanese). Proceedings of the Association America. Occurrence of powdery mildews was reported in for Plant Protection of Shikoku 11: 131e139. South America and Oceania on V. bonariensis (Amano 1986). Matsuda S, Takamatsu S, 2003. Evolution of hosteparasite Oidium sp. was reported on V. bonariensis by Homma (1976) relationships of Golovinomyces (Ascomycete: Erysiphaceae) without morphological description. There is no record of inferred from nuclear rDNA sequences. Molecular Phylogenetics e powdery mildew on V. brasiliensis. Based on the morphological and Evolution 27: 314 327; http://dx.doi.org/10.1016/S1055- characteristics of anamorph and molecular data, both fungi 7903(02)00401-3. Meeboon J, Takamatsu S, 2015. Erysiphe viburni-plicati and were identified as P. xanthii. Podosphaera photiniae, two new species of Erysiphales (Ascomycota) from Japan. Mycoscience 56: 14e23; http:// dx.doi.org/10.1016/j.myc.2014.01.010. Mimuro G, Sato Y, 2002. New records of Podosphaera curvispora and Acknowledgments Phyllactinia sp. on Sorbus alnifolia in Japan (in Japanese). Japanese Journal of Phytopathology 68: 188. The authors thank Dr. Uwe Braun for critical reading the Mori Y, Sato Y, Takamatsu S, 2000. Evolutionary analysis of the manuscript and two anonymous reviewers for helpful com- powdery mildew fungi using nucleotide sequences of the nuclear ribosomal DNA. Mycologia 92: 74e93. ments. This work was financially supported in part by a Grant- Nomura Y, 1984. A new powdery mildew fungus, Podosphaera in-Aid for Scientific Research (No. 23580061) from the Japan curvispora on Sorbus commixta (in Japanese). Transactions of the Society for the Promotion of Science, a grant from the Institute Mycological Society of Japan 25: 199e203. for Fermentation, Osaka, Japan to ST, and MONBUKAGAKU Sato Y, Eto S, 2014. Powdery mildews and their host plants in SHO: MEXT (Ministry of Education, Culture, Sports, Science, Japan (in Japanese). Bulletin of Toyama Prefectural University 24: e and Technology) Scholarship of the Japanese Government 26 65. Takamatsu S, Heluta V, Havrylenko M, Divarangkoon R, 2009. awarded to JM. Four powdery mildew species with catenate conidia infect Galium: molecular and morphological evidence. Mycological Research 113: 117e129; http://dx.doi.org/10.1016/ references j.mycres.2008.09.006. Takamatsu S, Matsuda S, Grigaliunaite B, 2013. Comprehensive phylogenetic analysis of the genus Golovinomyces (Ascomycota: Erysiphales) reveals close evolutionary Amano (Hirata) K, 1986. Host range and geographical distribution of relationships with its host plants. Mycologia 105: 1135e1152; the powdery mildew fungi. Japan Scientific Societies Press, http://dx.doi.org/10.3852/13-046. Tokyo. Takamatsu S, Niinomi S, Harada M, Havrylenko M, 2010. Braun U, Cook RTA, 2012. Taxonomic manual of the Erysiphales Molecular phylogenetic analyses reveal a close evolutionary (powdery mildews). CBS Biodiversity Series No. 11. CBS-KNAW relationship between Podosphaera (Erysiphales: Erysiphaceae) Fungal Biodiversity Centre, Utrecht. and its rosaceous hosts. Persoonia 24: 38e48; http://dx.doi.org/ Cunnington JH, Lawrie AC, Pascoe IG, 2005. Genetic variation 10.3767/003158510X494596. within Podosphaera tridactyla reveals a paraphyletic species Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, complex with biological specialization towards specific Prunus 2011. MEGA5: molecular evolutionary genetics analysis using subgenera. Mycological Research 109: 357e362. maximum likelihood, evolutionary distance, and maximum Edgar RC, 2004. MUSCLE: multiple sequence alignment with high parsimony methods. Molecular Biology and Evolution 28: accuracy and high throughput. Nucleic Acids Research 32: 2731e2739; http://dx.doi.org/10.1093/molbev/msr121. 1792e1797. Wada K, Hirata K, 1977. The powdery mildew fungi and their host Fukuda N, Hayashi M, Izita Y, 1973. Host plants of the powdery plants recorded up to date in Japan (in Japanese). Bulletin of the mildew of tobacco (Erysiphe cichoracearum) (in Japanese). Faculty of Agriculture Niigata University 29: 77e114. Bulletin of the Kagoshima Tobacco Experiment Station 17: 199e216.

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