First report of powdery mildew caused by Oidium cassiae-siameae on Cassia corymbosa

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1 Mycosystema 菌物学报 15 November 2010, 29(6): ISSN CN Q 2010 Institute of Microbiology, CAS, all rights reserved. First report of powdery mildew caused by Oidium cassiae-siameae on Cassia corymbosa ZHAO Gui-Hua 1* LI De-Wei 2 XI Gang-Jun 1 1 Jiangsu Polytechnic College of Agriculture and Forestry, Jurong , China 2 The Connecticut Agricultural Experiment Station, Valley Laboratory, Windsor 06095, USA Abstract: Cassia corymbosa is an introduced ornamental shrub in the Yangtze River Delta area. Severe powdery mildew occurred on C. corymbosa from late August to mid-november. It caused early defoliation and some infected plants failed to survive in the following year. The powdery mildew is caused by Oidium cassiae-siameae. The pathogen did not develop teleomorph under field observation in the last three years. This is the first report of C. corymbosa, as a new host of powdery mildew caused by Oidium cassiae-siameae. This fungus is a newly reported species in mainland China. Key words: anamorph, new host, ornamental plant, Pseudoidium, teleomorph 伞房决明白粉病的初次报道 赵桂华 1* 李德伟 2 席刚俊 1 1 江苏农林职业技术学院句容 美国康涅狄克州农业研究所美国康涅狄克州温莎镇 摘要 : 伞房决明是长江三角洲地区的园林绿化木本植物, 在每年 8 月下旬至 11 月中旬会发生严重的白粉病, 造成提前落叶, 导致次年部分植株死亡 该病由 Oidium cassiae-siameae 引起 经过 3 年多的野外观察, 未发现有性世代 初次报道伞房决明为 Oidium cassiae-siameae 白粉菌的新寄主 此真菌为中国大陆的初次记载 关键词 : 无性世代, 新寄主, 园林植物, 假粉孢亚属, 有性世代 INTRODUCTION Cassia corymbosa Lam., Argentine senna [Syn.: Senna corymbosa (Lam.) Irwin & Barneby] is a shrub native to South America (northern Argentina, Uruguay, and Brazil) and has been introduced to the southern USA and Massachusetts area (USDA 2009). It was introduced to Wuxi and Shanghai in China in the early 1990 s (Wu 2001; Wang 2002). Its cultivation has been expanded to eastern, central, and southern China. It has become a popular ornamental plant for landscaping of urban areas, Supported by China Administration of Forestry, 948 Program (No ); Jiangsu Natural Science Foundation (No. BK ) * Corresponding author. zhaoguihua2006@yahoo.com.cn Received: , accepted:

2 870 Mycosystema freeways, and reservoirs in the Yangtze River Delta. A number of powdery mildew pathogens have been reported on Cassia spp. Erysiphe polygoni DC. was found on Cassia mimosoides L. in China (Tai 1979). Oidium cassiae-siameae J.M. Yen causes powdery mildew on C. siamea Lam. and C. fistula L., and anamorphic Ovulariopsis of Phyllactinia bauhiniae var. cassiae Y.S. Paul & V.K. Thakur on C. fistula in Taiwan I. of China (Braun 1987; Kirschner & Chen 2008). Microsphaera diffusa Cooke & Peck [=Erysiphe diffusa (Cooke & Peck) U. Braun & S. Takam.] and Sphaerotheca cassiae Pandotra & Gangulyon were reported on C. occidentalis L., while Phyllactinia dalbergiae Pirozynski has been recorded on C. obtusifolia L. in India (Braun 1987). Phyllactinia guttata (Wallr.) Lév. was reported on C. fistula in Poland (Harsh et al. 1992). P. cassiae G.J.M. Gorter & Eicker infects C. abbreviata subsp. beareana (Holmes) Brenan in South Africa (Gorter & Eicker 1987). Oidium cassiae-leschenaultianae N. Ahmad, A.K. Sarbhoy, Kamal & D.K. Agarwal and O. cassiae-torae N. Ahmad, A.K. Sarbhoy, Kamal & D.K. Agarwal occur on C. lechenaultiana DC. and C. tora L. in India respectively (Ahmad et al. 2005). Oidium cassiae-hirsutae J.M. Yen was found on C. hirsuta L. in Malaysia (Braun 1987). Ovulariopsis sp. caused powdery mildew on C. siamea and Erysiphe polygoni on C. moschata Kunth in Venezuela (Sanabria de Albarracin 1988). Oidium sp. was reported on 22 species of Cassia, except C. corymbosa (Ishii 1973; Amano 1986; Teotia et al. 1988; Farr et al. 1989). C. corymbosa in bloom is beautiful and attractive with good ornamental properties but is susceptible to powdery mildew. The disease causes early defoliation and some infected plants fail to survive in the following year. Powdery mildew has not been previously reported on C. corymbosa in China. This paper reports the occurrence of the powdery mildew in China and identification of its pathogen. 1 MATERIALS AND METHODS 1.1 Disease investigation Powdery mildew on C. corymbosa was investigated on the campus at Jiangsu Polytechnic College of Agriculture and Forestry (JPCAF), Jurong, Jiangsu, and along the road sides of the demonstration area of Science of Technology of JPCAF from the end of August to late November in 2007 and The survey was conducted in different habitats, ecological niches, and locations in the affected areas. Disease occurrence and symptom development were observed periodically at the two plots on a monthly basis. Specimens were collected for observation of the morphology and development of the pathogen under the microscope. 1.2 Observation of teleomorph of the pathogen To observe the teleomorph of the powdery mildew, 80 infected leaves were collected during early November from 2007 to 2009, placed in one mesh bag, and hung on a plant branch of C. corymbosa on campus. The bag was 3cm off ground. The winter temperature in the area dropped down to -8. Half of the leaves collected in early November 2008 were placed in a freezer at -10 ± 0.5 for 10 days and then transferred to glass Petri dishes in a refrigerator (3±0.5 ). The plant materials in the Petri dish were observed microscopically for the development of chasmothecia every 2-3 weeks until January Observation of morphology of the pathogen White fungal structures were picked up from the upper surface of the leaves with a needle and mounted in 0.5% cotton blue on a slide and observed microscopically for morphological characters of mycelia, hyphae, conidiophores, conidia and appressoria. Microphotographs of the fungus were taken with a digital image system with DIC optics (ZEISS Imager A1). 2 RESULTS 2.1 Pathogen and its morphological characters Pathogen: Oidium cassiae-siameae J.M. Yen, Cahiers Pacifiques, 11: 88, Colonies developing on the upper surfaces of leaves; mycelia effuse, epiphytic, subpersistent, white at early stages of infection, turning to light gray with age, becoming powdery in 7 days with irregular edges, spreading and covering the entire upper surface of leaves by a single colony or coalescing multiple colonies (Fig. 1). Hyphae septate, hyaline, branched, µm (mean = 6.6 ± 1.3µm, n = 11) wide. Conidiophores erect, arising singly or in groups, often at a right angle from superficial hyphae, 1-3 septa, unbranched, hyaline, smooth,

3 Vol.29 No (mean = 79.0 ± 29.4, n = 30) (mean = 9.9 ± 1.1, n = 30)µm; foot cell straight or flexuous, cylindric, (mean = 47.0 ± 3.7, n = 15) (mean = 9.7 ± 0.9, n = 15)µm, followed by 1-2 shorter cells (Fig. 2-A, B); conidia developing singly, unicellular, thin-walled, vacuolate, ellipsoid and smooth when young, doliiform or cylindrical with polygonally wrinkled surfaces when mature, hyaline, occasionally in two-conidial short chains, (mean = 45.2 ± 5.9, n = 30) (mean = 19.0 ± 2.2, n = 30)µm, L/W ratio 2.4 ± 0.5 (Fig. 2-C). Germ tubes at an end and occasionally on both ends, terminal or subterminal, short to long, some dichotomously branched, terminating in a simple apex to slightly lobed or multilobed appressorium (Fig. 2-D, E). Appressoria on hyphae multilobed, often opposite in pairs, occasionally in groups, hyaline, (mean = 8.7 ± 1.4, n = 30) (mean = 6.6 ± 1.0, n = 30)µm (Fig. 2-F). 2.2 Symptoms and occurrence According to observation from 2007 to 2009, the powdery mildew caused by Oidium cassiae-siameae on C. corymbosa occurred from late August to mid- November in Jurong, Jiangsu. The disease only infected the upper surfaces of the leaves and does not infect the lower surfaces and young branches. Mycelial mats started from the lower-central or basal part of the upper surfaces of leaves as pale yellow ellipsoid or irregular shaped spots of 1-2mm diam. with irregular edge (Fig. 1). It spread out gradually to leaf tips and could cover the entire upper surface. Its color turned from white to whitish gray. The infected area became powdery in 7 days. When severe infection occurred, the entire leaves Fig. 1 Symptoms of powdery mildew caused by Oidium cassiae-siameae on Cassia corymbosa. Fig. 2 Morphology of Oidium cassiae-siameae on Cassia corymbosa. A-B: Conidiophore and immature conidia (bars=20µm); C: Conidia (bar=10µm); D-E: Germinating conidiua (bars=10µm); F: Appressoria (bar=20µm). 菌物学报

4 872 Mycosystema were covered by white conidial powder. Infected leaves turned yellow and started to defoliate in October. The symptom of powdery mildew was still present on the leaves in November, but the pathogen ceased its development and the white powdery symptom disappeared gradually. The infected leaves became darker. Infection on old leaves was more severe than that on the young leaves. 2.3 Teleomorph observation Oidium cassiae-siameae did not develop chasmothecia on the leaves in the mesh bags and on the hosts outdoors from 2007 to 2009, nor the ones cold-treated in a freezer and a refrigerator indoors in the winter of The infected leaves became black and decayed in the following spring. The pathogen seems to overwinter as hyphae in bud scales. Voucher specimen: China, Jiangsu, Jurong, Demonstration Garden of Science and Technology, Jiangsu Polytechnic College of Agriculture and Forestry, 31 o N, 118 o E, on leaves of Cassia corymbosa Lam., 7 September 2008, Gui-Hua Zhao and De-Wei Li, HMAS (=JSNL ). 3 DISCUSSION Oidium cassiae-siameae was reported on Cassia siamea from Taiwan I. of China and Tanzania (formerly Tanganyika) (Braun 1987; Yen 1967). Erysiphe cf. pisi reported on Cassia occidentalis in Cuba and Mexico is actually O. cassiae-siameae (Braun 1982; Braun, personal communication 2010). This is the first report of Oidium cassiae-siameae in China s mainland. Cassia corymbosa is a new host of O. cassiae-siameae. Oidium spp. have been reported from 22 species of Cassia, but C. corymbosa is not among these hosts (Amano 1986; Farr & Rossman 2009). Powdery mildew on C. corymbosa was briefly reported on the website of Backyardgardener in the USA, but no information of the pathogen was reported (Backyardgardener 2009). There is no report on powdery mildew on C. corymbosa from other areas in the world. In the last decade, C. corymbosa has become a popular ornamental plant for landscaping in eastern China but no report has been published on this disease previously. Presently, it is not clear whether this disease exists in other areas in China. Since C. corymbosa and C. siamea are introduced species, it is unknown whether O. cassiae-siameae is a hitchhiker species introduced with C. corymbosa or C. siamea to China s mainland. Studies on the origin of the pathogen are necessary in the future. Similar to Oidium cassiae-siameae on C. corymbosa, powdery mildews (Oidium spp.) on evergreen hosts, Euonymus japonicus Thunb. and Mahonia fortunei (Lindl.) Fedde do not develop teleomorphs in the Jurong area, despite the fact that the symptoms of powdery mildew are present on these hosts during the whole year. Powdery mildew on Euonymus japonicus was induced to develop chasmothecia of Microsphaera sp. (= Erysiphe sp.) in complete darkness at in Shandong (Jiang et al. 2001). Future study is necessary to determine whether failure to develop teleomorph on C. corymbosa is due to local habitat effects or permanent loss of the teleomorph. Oidium cassiae-siameae can be distinguished from other powdery mildew fungal species on Cassia spp. by morphological characters. Bigger conidia, longer foot cells and multilobed appressoria in opposite pairs of O. cassiae-siameae differentiate it from Oidium cassiae-leschenaultianae and O. cassiae-torae (Ahmad et al. 2005; Braun 1987; Farr & Rossman 2009). Oidium cassiae-hirsutae develops conidia in chains (Braun 1987) which is different from O. cassiae-siameae and the other species of Oidium developing solitary conidia. Erysiphe cichoracearum, E. communis (=E. polygoni), E. diffusa, E. pisi, E. polygoni, E. trifolii were reported from Cassia spp. (Braun 1987; Farr & Rossman 2009). Conidia of E. cichoracearum are in long chains which separate it from O. cassiae-siameae. Erysiphe diffusa, E. polygoni and E. trifolii have much shorter foot cells than O. cassiae-siameae (Braun 1987). Erysiphe pisi has long straight foot cells which distinguish it from the straight or flexuous foot cells of O. cassiae-siameae (Braun 1987). Cunnington et al. (2004) found that O. cassiae-siameae was genetically similar to E. trifolii and E. pisi. Zheng & Yu (1987) opined that identification of Erysiphe polygoni reported on Cassia sp. in China is questionable and no specimen was available for confirmation. Its determination can only be possible when a new collection is available for study. The taxonomy of the powdery mildew fungi has

5 Vol.29 No experienced drastic changes in the last decade (Braun & Takamatsu 2000; Braun et al. 2002). For the convenience of tracking powdery mildew literature and avoiding confusion among mycologists and plant pathologists, the names of powdery mildew fungi cited in this paper are those first reported. Acknowledgments: The authors express their sincere gratitude to Prof. Zheng Ru-Yong of the Institute of Microbiology, Chinese Academy of Sciences for her inspiring discussion and providing some literature, to Dr. Uwe Braun of Martin-Luther Universität, Germany for helping in identification of the pathogen, to Dr. Tang Geng-Guo of Nanjing Forestry University for identifying the host, and to Dr. James A. LaMondia of The Connecticut Agricultural Experiment Station, USA for reviewing the pre-submission manuscript. [REFERENCES] Ahmad N, Sarbhoy AK, Kamal, Agarwal DK, Five new anamorphic powdery mildews from India. Indian Phytopathology, 58(1): Amano K, Host range and geographical distribution of the powdery mildew fungi. Japan Scientific Societies Press, Tokyo. 741 Backyardgardener, Cassia corymbosa (Senna). backyardgardener. com/plantname/pda_d83e.html, access Braun U, Morphological studies in the genus Oidium (II). Zentralblatt Fur Mikrobiologie, 137: Braun U, A monograph of the Erysiphales (powdery mildews). Beihefte zur Nova Hedwigia, 89: Braun U, Cook RTA, Inman AJ, Shin HD, The taxonomy of the powdery mildew fungi. In: Bélanger RR, Bushnell WR, Dik AJ, Carver TLW (eds.) The powdery mildews: a comprehensive treatise. APS Press, St. Paul. 292 Braun U, Takamatsu S, Phylogeny of Erysiphe, Microsphaera, Uncinula (Erysipheae) and Cystotheca, Podosphaera, Sphaerotheca (Cystotheceae) inferred from rdna ITS sequences-some taxonomic consequences. Schlechtendalia, 4: 1-33 Cunnington JH, Lawrie AC, Pascoe IG, Molecular determination of anamorphic powdery mildew fungi on the Fabaceae in Australia. Australasian Plant Pathology, 33(2): Farr DF, Bills GF, Chamuris GP, Rossman AY, Fungi on plants and plants products in the United States. APS Press, St. Paul, Minnesota Gorter GJMA, Eicker A, Additional first records of perfect stages of some powdery mildew fungi in South Africa, including a new species. South African Journal of Botany, 53(1): Harsh NSK, Tiwari CK, Nath V, Some powdery mildews from Madhya Pradesh. Journal of Tropical Forestry, 8(2): Ishii M, Control of powdery mildew of Cassia occidentalis in relation to bioassay of Cymbidium mosaic virus. Plant Disease Reporter, 57(5): Jiang SX, Jia W, Li CH, Huang GQ, Sun YW, Powdery mildew sexual stage of evergreen Euonymus first found in China. Journal of Shandong Agricultural University (Natural Science), 32(3): (in Chinese) Kirschner R, Chen CJ, The Ovulariopsis anamorph of Phyllactinia bauhiniae var. cassiae: first record outside India and morphological characterization. Sydowia, 60(1): Sanabria de Albarracin N, Fungi causing powdery mildew on ornamental plants from the central region of Venezuela. Fitopatologia Venezolana, 1(2): Tai FL, Sylloge fungorum sinicorum. Science Press, Beijing (in Chinese) Teotia RS, Lokendra S, Sadhana S, Neelima T, Effect of powdery mildew infection on phylloplane fungi of Xanthium strumarium and Cassia occidentalis. Acta Botanica Indica, 16(2): United States Department of Agriculture (USDA), USDA plants profile: Senna corymbosa. retrieved 2009-March 4. Wang B, Cultivation of Cassia corymbosa Lam. Anhui Forestry, 2002(5): 25 (in Chinese) Wu BZ, Introducing and cultivation of Cassia corymbosa Lam. Plants, 2001(5): 17 (in Chinese) Yen JM, Etude sur les champignons parasites du Sud-Est asiatique. VIII. Quelques especes d'oidium de Formose. Cahiers de Pacifique, 11: Zheng RY, Yu YN, Flora fungorum sinicorum. Vol. 1. Erysiphales. Science Press, Beijing. 552 (in Chinese) 菌物学报

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