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G. Monticola and G. Unicorne Mycologia, 101 (6), 2009, pp. 790-809. DOl: 10.3852/08-221 2009 by The Mycological Society of America, Lawrence. KS 66044-8897 The rust fungus Gymnosporangium in Korea including two new species, G. monticola and G. unicorne Hye Young Yunt molecular as well as morphological characteristics. Department of Forest Sciences, College of Agri culture Analyses of phenotypic characters mapped onto the and I,j?' Sciences, .Seou1 National University, 56-1 Sin/i, tn-doug, Kwanak-gu, Seoul 151-921, phylogenetic tree show that teliospore length followed Republic of Korea by telia shape and telia length are conserved; these are morphological characters useful in differentiating Honga Soon Gyu species of G'vmno.c/.sorartgiurn. Each of the nine species Biolog-icai Resource Center, Korea Institute of Bioscience of Cymnosporar glum in Korea is described and illus- and Biotechnology, 52 Own-dong, Yusong-kn, Daejeon 305-806, Republic '?f Korea trated, and keys based on aecia and telia stages are provided. l.ectotype specimens for several names Amy Y. Rossman described iii Gymnosporangium are designated. Systematic Mycology and Microbiology Laboratory, Key words: aecia stage, forest pathogens, LSU Agricultural Research Service, Department of Agriculture, Beltsville, Ma?yland 20705 rDNA, Piiccinialcs, systematics, lelia stage Seung Kyu Lee INTRODUCTION Southern. Forest Research Center, Korea Forest Research Institute, 719-1 Gazwa-dong, Jinju City The rust fungi (Pucciniales) are important plant Kyungsangnam-Do, 660-300, Republic of Korea pathogens affecting a variety of angiosperins and Kvung Joori Lee gymnosperms, potentially causing severe damage to Department of Forest Sciences, College of Agriculture agricultural crops and forest trees (Scott and Chakra- and Life Sciences, Seoul Vational University, 564 vorty 1982, Swann ci. al 2001). Most rust fungi are Shillim-dong, Kwanah-gu, Seou 1151-921, specialized parasites that attack only certain genera or Republic of Korea Species of host plants. Species of Gymnosporang-lum are Kyung Sook Bae3 heteroecious, producing the aecia stage on leaves and Biological Resource Center, Korea Research Institute of fruits of pomaceous hosts (Rosaceae) and the telia stage Bioscience and Biotechnology, 52 (Jo n-dong, Yusong- on needles, green stems and branches of cedar ku, Daeyeon 305-806, Republic of Korea (Cupressu.c) and juniper (Juni/)rru.c) (Cupressaceae; Kern 1973, Sinclair and Lyon 2005). Common diseases caused by Cymnosporangium include cedar apple rust Abstract: A survey was conducted of the rust fungus (G. juniperi-virg-inianae Schwein.), European pear rust (;yrnnosporangiuni in Korea. We recollected previously (C. saliinae [Dicks.] C. Winter) and Japanese pear rust known species, namely Gymnosporangium asiaticwin, (C. asiaticurn Miyahe ex U. Yamacla). C. clavarii/ortne, G. globosum, C. japonicurn Gymnosporangiurn and C. is distributed mainly in the northern hemisphere with yarnadae. Gymnosporangi urn nidus-avis and G. sahinae about 60 species of Gmnosporanglurn are reported for the first time from Korea, and two and 15 species of Roesteija, the aecia anamorph of Gymnosporarigiurn new species, C. mon.ticoia sp. nov. and C. unicorne sp. (Hiratsuka 1936a—f, 1942; Parmelee 1965, 1971; Hir- nov., are recognized. Previous single reports of C. rniyabri and C. shiraianurn could not he confirmed. atsuka 1971; Kern 1973; Hiratsuka and 1-liratsuka 1980; The LSU rDNA was sequenced from freshly collected Peterson 1982; Sato and Sato 1982; Wang and Lin 1985; specimens. Phylogenetic analyses show that species of Lohsoinhoon et al 1990; Hiratsuka et al 1992; Lee and Gymnosporang-ium form a monophyletic group with Kakishima 1999a, b; Lee et al 1999c). strong bootstrap Support within the rust fungi. The In Korea diseases caused by Gymnosporangiurn are two new species are unique based on both A and B increasingly damaging because previously separated alternate hosts are being planted close to each other Accepted for publication 9 May 2009 as landscape trees (Kim and Kim 1980). A number of Current address: Systematic Mycology and Microbiolog y Labora- species attack economically important plants such as tor y, Agricultural Research Service. Uniwrl States Department of apples. Species of Gymnosporangiurn, especially C. Agncult tire, Beltsville, Ml) 20705. yaniadae, are known to delay harvest of fruits by (uncut address: Polar BioCenter, Korea Polar Research Institute, KORDI, 7-50 Songdu-ilung. '6.onsti-gii. Incheon 406-840. Republic inhibiting photosynthesis and increasing respiration of Korea. rate (Kim and Kim 1980). Some species of Gymno- 'Corresponding author. E-mail: ksbaet4krihb.re.k sporangium that attack economically important crops 790 Vt 'N FT AL: GYMNOSPORAiVGJUM IN KORFA 791 are not widely distributed; thus they are considered to and size of peridirmmn and 1)emidial cells, shape, SI/C and color be of importance in the quarantine of plants (Smith of aeciospores and thickness of cell walls of aeciospores and et al 1992). teliospores. Spores were measured from Specimens i'ehy- drated and mounted in distilled water with a compound little molecular sequence data exist for rust Relatively light microscope (Axiopluot, Zeiss, Germany) at 400X. In fungi worldwide, and essentially nothing exists for general 30 spores were measured for each specimen species of Gyrnnosporan.gium from Asia. In one study (Parmasto and Parmasto 1987). Damaged, immature and analyzing the nuclear large subunit (LSU) or 28S rI)NA irregular teliospores and peridial cells were not measured. sequences of 52 rust fungi, the three species of of/ella morphological characters.—Host relation- G'mnosorangmiu, C. clavaru/arme, C. cornulu m and Evaluation ships and morphological characters were numerically now regarded as C. sa/ilnar, formed a C. /icscnm, coded. Seven macroscopic and microscopic characters were monophyletic group (Maier et al 2003). In another analyzed. Characters with their character states are provided study with 18S and 28S rDNA sequences (Aime 2006) and nnumericall y coded (TABLE 111). The eolutionv ol each two species of Cyinrwspora.ngium., C. cla.vipes and C. phenotypic character was reconstructed onto the consensus pim/ri-virginianac, formed a unique lineage in the tree of most parsimonious trees based on I SU rDNA Pucciniales distinct from the Pucciniaceae. sequences of the Korean species of G'vmn o.cpora ngwm. Fit of This paper reports the results of a Survey fir each character to the tree was evaluated by a consistency Gymnosporangium in Korea, including a key, descrip- index (c) calculated with an algorithm in PAUP 4.0. tions and illustrations for the nine species encoun- nnsistencv index was defined as c = outs, where rn represents minimum amount of change that the character tered. Two new species ase described that are unique may show on any conceivable Lice and s represents number in both morphological and molecular characteristics. of steps requited by the character on the tree being A phylogcny of the species from Korea is presented evaluated (Swofford 1993). based on 1.StJ rDNA sequence data and nmrpholog- ical characteristics evaluated based on this pitylogeny. I)j\nil u'xliy ction, PCI? and sequencing.— total DNA was isolated from mature telia by protocols modified horn those of Lecellier and Silar (1991). Dried and crushed telia were \IATERI\1 .S ANt) M1:lHODS suspended in 500 tl - lvsis buffer (50 mM Tris-l--h(l [pH 8.0], 50 mM EDTA, 3% SDS). Telia suspensions were fis)/en in Sa?npinig ad morphological examination and identification.— liqund nitrogen I mm, incubated at 70 C For 2 inin and One hundred thirteen te]ia and 78 accia specimens of vortexed at high speed I ruin. This process was repeated thiee collected by the first author in Korea Gvmnosporangium times. RNA was removed by 0.5 Ml RNase A (20 mg/nil,) 2001-2006 were identified according to Parinclee (1965. treatment at 37 C for 30 inn. DNA was purified by phenol, 1971). Kern (1973). Wang and Lin (1985), Hiratsuka ci al phenol: chloroform and chloroform extractions. Purified (1992) and Lee and Kakishima (1999a, b). The specimens DNA was precipitated with I volume isopropanol and are deposited at the I herbarium of Korea Forest Research collected by centrifugation at 12000 rpm 10 min at room Institute, Seoul, Korea (l-IKF'Rl) ..Also many specimens temperature. The pellet was washed with 70% ethanol, air- outside Korea were examined from the National Mvcolog- dried, and suspended in 50 tit. sterile distilled water. ical Herbarium, Agriculture and Agri-Food C.anada, Ontario The D1/D2 douriain of the 28S rDNA was amplified with (1)AOM), Canada Mvcological Herbariunn. Institute of the primer pair, forward printer No. 4 (5-AC- Microbiology, Academia Sinica, China (HMAS); Hokkaido CCGC1c;AAYFTAAG('ATAT-3') and reverse primer University Museum, Sapporo, Hokkaido, Japan (SAPA); No. II (5-CI(:CTTGGTC(GTG1TrCAA(;ACG(;-3') (van Herbarium of Forest Mycology and Pathology, Forest and (Icr Auuwera et al 1994). I'CR proceeded as follows: initial Forest Products Research Institute, Ibaraki, Japan (TFM); denaturation at 94 C for 3 mm; 30 c ycles, each consisting of and U.S. National Fungus Collections, Beltsville, Maryland denaturation at 94 C for 30 s, annealing at 55 C for 30 s, (BPI), abbreviated according to Index Jlerhariorurn. extension at 72 C for 1 miii: final extension at 72 C for Identifications were made based on the host plant as well as 10 min. PCR products were purified with Wizard PCR prep morphological characteristics of the peridia, telia and kit (l'momcga, Madison, Wisconsin) following the mannulac- teliospores. Each species is described with the specimens tum-er's instructions. Nucleotide sequences were determined examined listed. Terminology for shapes and ornamentation with BigDye terminator cycle sequencing kits (Applied of aecia and tclia follows Kern (1973) and Cummins and Riosystems, Foster City, California) with the same primers as I lirat.suka (1983). Names of colors arc based on Kornerup used in PCR amplification. Sequences were proofread, and Wanschcr (1978). Terminology for telia shapes follows edited and merged into composite sequences with the the definitions in Kern (1973).
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