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Identification of Phytophthora Species Baited and Isolated from Forest Soil and Streams in Northwestern Yunnan Province, China

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Identification of Phytophthora Species Baited and Isolated from Forest Soil and Streams in Northwestern Yunnan Province, China For. Path. 43 (2013) 87–103 doi: 10.1111/efp.12015 © 2013 Blackwell Verlag GmbH REVIEW ARTICLE Identification of Phytophthora species baited and isolated from forest soil and streams in northwestern Yunnan province, China By W.-x. Huai1, G. Tian1, E. M. Hansen2, W.-x. Zhao1,5, E. M. Goheen3,N.J.Grunwald€ 4 and C. Cheng1 1Research Institute of Forest Ecology, Environment and Protection, The Key Laboratory of State Forestry Administration on Forest Protection, Chinese Academy of Forestry, Beijing, 100091, China; 2Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR USA; 3USDA Forest Service, Forest Health Protection, Central Point, OR USA; 4USDA Agricultural Research Service, Corvallis, OR USA; 5E-mail: [email protected] (for correspondence) Summary Phytophthora species were surveyed by collecting soil samples and placing bait leaves in selected streams during June–October in the years 2005, 2006 and 2010 at three sites in oak forests in Diqing Tibetan Autonomous Prefecture of NW Yunnan province, China. Seventy-three isolates of Phytophthora spp. were recovered from 135 baited leaf samples and 81 soil samples. Eight Phytophthora species were identified by observation of morphological features and ITS1-5.8S-ITS2 rDNA sequence analysis. The eight taxa included two well-known species P. gonapodyides and P. cryptogea, two recently described species P. gregata and P. plurivora, two named but as yet undescribed taxa, P. taxon PgChlamydo and P. taxon Salixsoil, and two previously unrecognized species, Phytophthora sp.1 and P. sp.2. The most numerous species, P. taxon PgChlamydo, and the second most abundant species, P. taxon Salixsoil, were recovered at all three sites. Phytophthora cryptogea was detected only once at site Nixi. Phytophthora gregata and P. sp.2 were isolated from a stream only at site Bitahai, while the other three species were each found at two sites. Phylogenetic analysis revealed that the isolates belonged to three ITS clades, one species including six isolates in clade 2, six species including 66 isolates in clade 6 and one species in clade 8. There was a relatively rich species and genetic diversity of Phytophthora detected in the investigated regions where the forest biotic and abiotic factors affecting the growth and evolution of Phytophthora populations were diverse. 1 Introduction Phytophthora is a genus that is mainly parasitic on various plant hosts. Some species are host specific and some have broad host ranges. It occupies a small but pathologically significant niche in Oomycota currently belonging to the kingdom Chro- mista (Dick 1995a,b). In 1983, only 43 species of Phytophthora were recognized. Later, about 60 species were described by Erwin and Ribeiro 1996; and by 2008, the number of species was approaching 100 (Gallegly and Hong 2008). The genus Phytophthora has complex life cycles with several spore stages. Chlamydospores and oospores are two kinds of resting spores that Phytophthora produces for long-term survival. Oospores are the outcome of sexual reproduction, pro- duced by mating of a female organ called oogonium, which is fertilized by a male organ called antheridium. When environ- mental conditions become suitable, the resting spores germinate by forming sporangia, which release motile, biflagellate zoospores into the soil water.(Erwin and Ribeiro 1996) Because of the morphological variation encountered in this genus, it is often difficult to identify a given isolate to species merely based on morphological and physiological traits. Advances in molecular techniques, such as DNA sequence data analysis from the internal transcribed spacer region and 5.8S gene of the rDNA operon, the mitochondrial cox1 and cox2, ras-related protein, elicitin and b-tubulin genes have permitted a more rational study of genetic distance and phylogenetic relationships within the genus Phytophthora and enhanced the efficiency and accuracy of identification of species as well as clonal lineages within species (Cooke et al. 2000; Forster et al. 2000; Elliott et al. 2009; Grunwald€ et al. 2009). Over the past decade, a number of new Phytophthora species have been described from forests around the world. Some of these new species, such as P. ramorum (Grunwald€ et al. 2008), cause dramatic tree and woody ornamental diseases. Other times, these new Phytophthora species have been found during broader surveys of soil or streams in forest stands that are not part of direct observations of forest declines (Balci et al. 2007). In China, extensive studies about morphological and molecular detection and identification of Phytophthora species as well as population genetics have been focused on pathogens of agricultural crops or ornamental plants such as soybean (P. sojae), potato and tomato (P. infestans), pepper (P. capsici), etc., and some flowers (Zheng 1997; Li et al. 1999; Wang et al. 2000, 2004; Yang et al. 2008, 2011; Guo et al. 2010). So far, there have been only a few reports investigating Phytoph- thora diseases of woody plants. Some species including P. cinnamomi, P. citricola, P. heveae, P. drechsleri, P. citrophthora and P. palmivora were recorded in association with woody plant and forest diseases (Zheng 1997; Zeng et al.2009). Of these, P. cinnamomi is of particular significance due to its broad host range and worldwide distribution, although it lacks the information on economic impacts in China. It had been identified as the cause of death of black locust, cedar and camellia, etc., (Ho et al. 1984; Shen et al. 1990; Zhou et al. 1993). Moreover, some early identified species may need to be re-examined or revised with the advent of a new taxonomic era highlighting the combination of morphological and molecu- lar classification. So far, there have not been any reports on the comprehensive investigation of Phytophthora species in the forest of the north-west region of Yunnan province, China. Therefore, the objectives of this study were to isolate and Received: 5.4.2012; accepted: 4.11.2012; editor: L. Belbahri http://wileyonlinelibrary.com/ 88 W.-x. Huai, G. Tian, E. M. Hansen et al. identify Phytophthora species by baiting techniques from streams and forest soil among or alongside oak forests and to use a combination of morphological and molecular tools to evaluate the genetic diversity of Phytophthora populations. Phytoph- thora ramorum, cause of sudden oak death disease in Europe and North America, was a particular target of the search. 2 Materials and methods 2.1 Study sites The study was carried out in Diqing Tibetan Autonomous Prefecture of NW Yunnan province, mainly in the geographic area of Zhongdian (Shangrila). There are evergreen sclerophyllous Quercus forests in this region distributed from 900 to 4800 m asl, chiefly between 2400 and 3600 m. Quercus aquifolioides Rehd. et Wils., Q. pannosa Hand.-Mazz., and Q. longispica (Hand.-Mazz) A. Camus were the most important species in the Quercus forests, accompanied by Rhododen- dron rubiginosum Franch., R. vernicosum Franch., R. oreotrephes W. W. Sm., R. decorum Franch., Larix potaninii Batalin, Picea likiangensis (Franch.) Pritz., P. armandii Franch., Pinus densata Mast., Populus szechuanica Schneid., Sorbus rehderiana Koehne and S. rufo pilosa Schneid. Based on climatological data for the cities of Zhongdian (Shangrila) (27°42′N, 99°42′E), average monthly temperatures range between À1.5°C in January and 15°C in July. The mean annual precipitation is 520.5 mm for Zhongdian. Most of it occurs during the monsoon months of June–October. Three decline sites and streams in Quercus forests were surveyed in this area (Fig. 1). Site Nixi (N) (27°58′N, 99°35′E) was about 500 m downstream of a stream in forest located in Nixi Township north of Zhongdian. Site Bitahai (B) (27°44′N, 99°58′E) was near Yakou Inspec- tion Station in the south of the Bitahai Nature Reserve. The third site, Hutiaoxia (H) (27°12′N, 100°02′E) was chosen at the edge of forest that was close to the Hutiaoxia Forest Farm. 2.2 Sampling procedure and isolation methods Surveys were conducted from June to October in the years 2005, 2006 and 2010 both by collecting soil samples at the base of declining trees and placing baiting leaves in selected streams. Nine soil samples were collected from each declining site per year. Unripe apples (variety Golden Delicious) were used as baits for isolating Phytophthora species from soil (Jeffers and Martin 1986). After 4–6 days of incubation at 24°C, the browning parts of apple flesh around holes were plated onto a selective medium (CARP+: corn meal agar [CMA] with 25 ppm hymexazol [99%], 20 ppm Delvocid [50% natamycin salt], 200 ppm ampicillin sodium salt, 10 ppm rifamycin SV sodium salt and 30 ppm Benlate [benomyl 50WP]) and incubated at 20°C in the dark. Three pieces of Rhododendron (site 2) or Quercus (site N and H) leaves were placed in each nylon mesh bag and were floated in relatively slow-moving water in streams as baits. The leaf baits were removed after 7–10 days when lesions developed. Fifteen bags of baited leaf samples were collected from each stream per sampling year. Pieces about 2-mm2 were cut from the margin of the brown spots and plated in CARP+. Colonies of suspected Phytophthora and Pythium species growing from plated baits were transferred to CARP (CARP+ without Benlate and hymexazol) to confirm purity and then to CMA for characterization and storage. 2.3 Identification of Phytophthora 2.3.1 Morphological studies Pure cultures of Phytophthora isolates were cultivated on V8-juice agar amended with 20 ppm b-sitosterol (V8S) and on carrot agar (CA) plates and were incubated in the dark at 20°C. After 5–10 days, the isolates were examined for cultural Fig. 1. The Map of Diqing Tibetan Autonomous Region in the northwestern part of Yunnan province, showing locations of the sampling and baiting sites.
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