The Phylogenetic Position of an Armillaria Species from Amami-Oshima, a Subtropical Island of Japan, Based on Elongation Factor and ITS Sequences

Mycoscience (2011) 52:53–58 DOI 10.1007/s10267-010-0066-3

SHORT COMMUNICATION

The phylogenetic position of an Armillaria species from Amami-Oshima, a subtropical island of Japan, based on elongation factor and ITS sequences

Yuko Ota • Mee-Sook Kim • Hitoshi Neda • Ned B. Klopfenstein • Eri Hasegawa

Received: 21 May 2010 / Accepted: 30 July 2010 / Published online: 21 August 2010 Ó The Mycological Society of Japan and Springer 2010

Abstract An undetermined Armillaria species was col- Approximately 40 Armillaria species (Physalacriaceae, lected on Amami-Oshima, a subtropical island of Japan. Agaricales, Basidiomycota) are distributed worldwide The phylogenetic position of the Armillaria sp. was (Volk and Burdsall 1995), and some of these species cause determined using sequences of the elongation factor-1a root disease to plant species (Hood et al. 1991; Dai et al. (EF-1a) gene and the internal transcribed spacer (ITS) 2007). More than 600 species of woody and nonwoody region (ITS1-5.8S-ITS2) of ribosomal DNA (rDNA). The plants are hosts of Armillaria spp. (Shaw and Kile 1991; phylogenetic analyses based on EF-1a and ITS sequences Fox 2000). In Japan, nine annulate species [A. cepistipes showed that this species differs from known Japanese taxa Velen., A. gallica Marxm. & Romagn., A. jezoensis J.Y. of Armillaria. The sequences of this species and A. novae- Cha & Igarashi, A. mellea subsp. nipponica J.Y. Cha & zelandiae from Southeast Asia were contained in a strongly Igarashi, A. nabsnona T.J. Volk & Burds., A. ostoyae supported clade, which was adjacent to a well-supported (Romagn) Herink (reported to be a synonym of A. solidipes sister clade containing A. novae-zelandiae from Australia Peck by Burdsall and Volk 2008), A. sinapina Be´rube´ & and New Zealand. Dessur., A. singula J.Y. Cha & Igarashi, and one un- described species (Nag. E)] and two exannulate species Keywords Armillaria fuscipes Armillaria novae- [A. ectypa (Fr.) Lamoure and A. tabescens (Scop.) Emel] zelandiae have been reported (Nagasawa 1991; Cha et al. 1992, 1994; Cha and Igarashi 1997; Ota et al. 1998, 2009; Kudo and Nagasawa 2003). These 11 species occur in warm-temperate to boreal areas in Japan (Ota et al. 1998, 2009). However, little information is available on Armillaria in subtropical Japan. Amami-Oshima (28°170N 129°220E) is a subtropical Y. Ota (&) H. Neda Forestry and Forest Products Research Institute, island in the Ryukyu Archipelago (Nansei Islands) located Matsunosato 1, Tsukuba, Ibaraki 305-8687, Japan approximately 300 km north of Okinawa Island and e-mail: [email protected] 380 km south of Kyushu. The vegetation is typical for evergreen forests of this region, dominated by Castanopsis M.-S. Kim Department of Forestry, Environment, and Systems, sieboldii (Makino) Hatus, Quercus miyagi Koidz, and Kookmin University, Seoul 136-702, Republic of Korea Distylium racemosum Sieb. et Maxim., along with a sec- ondary planted forest composed of Pinus luchuensis Mayr. N. B. Klopfenstein In 1998, an Armillaria sp. was collected on Amami-Oshima. USDA Forest Service, RMRS, 1221 South Main Street, Moscow, ID 83843, USA The morphological characteristics of the basidiocarp were distinct from all previously reported species from the E. Hasegawa warm-temperate to boreal regions of Japan. Recently, Kansai Research Center, sequences of elongation factor-1 alpha (EF-1a) gene and Forestry and Forest Products Research Institute, 68 Nagai-Kyutaro, Momoyama, Fushimi, ribosomal DNA (rDNA regions) [internal transcribed Kyoto 612-0855, Japan spacer (ITS) and intergenic spacer-1 (IGS-1)] have been 123 54 Mycoscience (2011) 52:53–58 used for phylogenetic studies of Armillaria spp. (Maphosa of each primer, 2–2.5 mM of each deoxyribonucleotide et al. 2006; Antonıń et al. 2009). More recently, Hasegawa triphosphate (dNTP), and 0.5 U Takara Taq or ExTaq et al. (2010) showed that the EF-1a gene was the most (Takara, Tokyo, Japan). The polymerase chain reaction suitable region for identifying eight species of Japanese (PCR) condition was as follows: 94°C for 1 min, 30 cycles Armillaria. Advantages of using EF-1a compared with at 94°C for 30 s, 53°C for 30 s, and 72°C for 1 min. The ITS and IGS-1 regions for phylogenetic analyses of PCR products were purified with MicroSpin Columns and Armillaria are: (1) it is easier to align the sequence data Sephacryl S-300 (GE Healthcare, Piscataway, NJ, USA) because indels are less frequent than those found in the and sequenced with an ABI PRISM 3100 Genetic Analyzer ITS and IGS regions, and (2) EF-1a contains sufficient (Applied Biosystems, Foster City, CA, USA) in both sequence variation to distinguish among closely related directions to ensure accuracy. The sequences are deposited species. in the DNA Data Bank of Japan (accession numbers: The objective of this study was to clarify the phyloge- AB558990–AB559004 and AB36893, Table 1). netic position of an Armillaria sp. collected on Amami- The sequence data reported by Hasegawa et al. (2010) Oshima, a subtropical island of Japan, using sequences of was used for eight known Japanese species (A. cepistipes, EF-1a and ITS region. Two isolates of Armillaria sp. were A. gallica, A. mellea, A. nabsnona, A. ostoyae, A. sinapina, collected from Amami-Oshima, Kagoshima Prefecture, A. tabescens) and Nagasawa’s E (Nag. E). Nag. E is a from basidiocarp tissue and multiple spores and established Japanese Armillaria species reported by Nagasawa (1991) in culture (Table 1). For comparisons, A. ectypa from without valid description. Armillaria jezoensis and A. sin- Japan was also sequenced (Table 1). Two isolates of gula were not used for DNA analysis because cultured Tricholoma matsutake and T. magnivelare (Table 1) were isolates could not be found. Some sequences from Gen- analyzed as outgroups in the preliminary analysis. The Bank, which showed the highest similarities with the examined isolates are deposited in the culture banks of the examined isolates according to a BLAST search, were also Forestry and Forest Products Research Institute (FFPRI) in used for the analyses. Sequence alignments were examined Tsukuba, Ibaraki, Japan, and the Microbial Ecology Lab of using Clustal X (Jeanmougin et al. 1998) followed by FFPRI; Japanese voucher specimens have been deposited visual editing and alignment using BioEdit (Hall 1999). in the Mycological Herbarium of FFPRI (TFM). All gaps and ambiguously aligned regions were removed Isolates were grown on liquid MYG medium [2% (w/v) for analyses. The sequence alignments were deposited in malt extract, 0.2% (w/v) yeast extract, 2% (w/v) glucose] at TreeBase as submission no. S10511. Phylogenetic analyses 25°C in the dark, and mycelia were harvested after 10 days were conducted using PAUP* ver. 4.0b10 (Swofford 2002) in culture. DNA was extracted from cultured mycelia using for the neighbor-joining (NJ) method, and PhyML (Guin- a DNeasy extraction kit (Qiagen, Valencia, CA, USA) fol- don and Gascuel 2003) was used for the maximum likeli- lowing the manufacturer’s protocol. Primers EF595F/ hood (ML) method. NJ trees were generated using p, K2P, EF1160R (Maphosa et al. 2006) and ITS1-F/ITS4-B (Gardes and HKY85 distances. The confidence for the internal and Bruns 1993) were used to amplify a portion of the EF- branches of the resulting trees were tested statistically 1a gene and the ITS region, respectively. Each 20-ll using bootstrap analysis (Felsenstein 1985), with 1,000 reaction mixture contained 10 ng of template DNA (or no bootstrap replications through a FastStep search using the DNA template for a negative control), 10 mM Tris– default settings. For ML trees, the initial tree was con- hydrochloride (HCl) (pH 8.3), 50 mM potassium chloride structed by BioNJ; the HKY85 substitution model was used

(KCl), 1.5 mM magnesium chloride (MgCl2), 0.1–0.2 mM with an estimated proportion of invariant sites (0.515 for

Table 1 Isolates used in this study Species Isolate Original Location Host Specimen EF accession ITS accession no. no. no. (TFM) no. no.

Armillaria sp. 00-13 S841 Amami, Kagoshima, Japan Decayed wood 26911 AB558990 AB558998 Armillaria sp. 00-14 S842 Amami, Kagoshima, Japan Decayed wood AB558991 AB558999 A. ectypa Je-2 Aomori, Japan Phragmites australis 27105 AB558992 AB559001 Je-4 Aomori, Japan Phragmites australis 27109 AB558993 AB559002 Je-7 Aomori, Japan Phragmites australis 27212 AB558994 AB559003 Je-9 Aomori, Japan Phragmites australis 27213 AB558995 AB559004 Tricholoma matsutake Tmm4 Tm029 Shiga, Japan Unknown AB558996 AB559005 T. magnivelare Tmm27 Tp-C3 Canada Unknown AB558997 AB036893

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100/100 2006-20-01 (AB510807) 2002-06-03 (AB510806) 96-1-8 (AB510804) A. tabescens 96- 3- 3 (AB510805) 100/100 Je-2 Je-4 Je-7 A. ectypa Je-9 100/100 CMW4980 (DQ435648) Australia A. hinnulea 83/86 CMW4981 (DQ435649) Australia 99/97 CMW4967(DQ425651) Australia 100/99 CMW4722 (DQ435652) New Zealand A. novae-zelandiae 89/84 PNZ87.54(FJ618650) PNG CMW4143 (DQ435654) Indonesia 99/80 00-14 99/97 00-13 96-37-1 (AB510769) Armillaria sp. from Amami-Oshima 2003-71-13 (AB510767) 100/100 94-2-1 (AB510768) 94-35-01 (AB510770) 2000-23-02 (AB510773) Nag.E NE4 (AB510771) 94-43-08(AB510772) -/81 NA4 (AB510761) NA17 (AB510759) 94/91 NA13 (AB510760) A. gallica 100/100 00-4-4 (AB510762) NB3(AB510763) 75/93 00-3-1 (AB510766) NB4 (AB510764) A. nabsnona 00-16-4 (AB510765) A-12 (AB510801) 100/100 A-10 (AB510800) 94-7 (AB510799) 94-5 (AB510802) 89-07 (AB510796) A. mellea var. nipponica 97-6 (AB510797) 94-10-1 (AB510798) 94-68 (AB510803) 91-01-10 (AB510785) 100/100 NC8 (AB510782) 2002-66-3 (AB510781) 89-03B-09 (AB510780) 94-75-07 (AB510779) A. ostoyae 94-8-2 (AB510783) -/84 88-01-19 (AB510784) 96-7-1 (AB510774) 97/95 05-13-2 (AB510776) 96-8-1 (AB510777) A. sinapina 05-7-1 (AB510775) -/87 05-46-1 (AB510778) ND11 (AB510787) 94-39-04 (AB510786) 93/98 2000-07-04 (AB510788) ND1 (AB510792) 94-33-01 (AB510789) 90-10-12 (AB510790) A. cepistipes 04-16-1 (AB510795) 2000-08-14 (AB510794) 96-19-1 (AB510791) 94-46-01 (AB510793) 1

Fig. 1 Neighbor-joining tree based on elongation factor-1a gene sequences of known Japanese Armillaria species, the unknown isolates from Amami-Oshima, and other highly similar sequences from GenBank. Bootstrap values and reliability values are shown on the nodes

EF-1a gene and 0.446 for ITS region) and four gamma- 2006). EF-1a sequences from the isolates from Amami- distributed rate categories to account for rate heterogeneity Oshima showed the highest similarity (97%) to that of the across sites. The gamma shape parameter was estimated isolate from Indonesia (isolate no. CMW4143) referred to directly from the data (gamma = 1.872 for EF-1a gene as A. novae-zelandiae. The sequence similarities between and 0.613 for ITS region). The reliability value of each the isolates from Amami-Oshima and A. novae-zelandiae internal branch was assessed using the aLRT test (SH-like; from Australia, New Zealand, and Papua New Guinea, and Anisimova and Gascuel 2006). This test is based on an A. hinnulea ranged from 92 to 95%. In the preliminary approximation of the standard likelihood ratio test and is EF-1a sequence analysis, which used Tricholoma matsu- much faster to compute than the usual bootstrap procedure. take and T. magnivelare as the outgroup, A. ectypa and Similar trees were derived from both methods; branch A. tabescens formed the basal clades for the Armillaria spp. supports were generally highly correlated (Dereeper et al. (data not shown). Therefore, A. ectypa and A. tabescens 2008). were used as the outgroup for subsequent analyses. An Ampliﬁcation of the partial EF-1a gene yielded an EF-1a data set consisting of 61 sequences was analyzed. approximately 600-bp product for isolates of Japanese Topologies of the NJ and ML trees based on the EF-1a A. ectypa and isolates from Amami-Oshima, which is in the sequences showed some minor differences, but both trees expected size range (Hasegawa et al. 2010; Maphosa et al. showed generally consistent relationships among the

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98/94 CMW4143(AF448421) Indonesia PNZ87.54.1 (FJ664600) PNG Armillaria sp. from 00-14 99/75 00-13 Amami -Oshima 100/100 CMW3951(AF448419) Malaysia 100/100 Arg49 (FJ660935) Argentina Arg55 (FJ711612) Argentina 94/98 RP8306(FJ660943) Argentina 82/- CMW4964(AF329924) Australia A. novae-zelandiae RP2615 (FJ660942) New Zealand RP2560 (FJ660941) New Zealand CMW4722 (AF3299926) New Zealand 100/100 Je-2 Je-4 Je-7 A. ectypa Je-9 94-7 (AB510863) 100/94 94-5 (AB510880) 94-68(AB510858) A-12 (AB510864) A. mellea var. nipponica 95/94 A-10(AB510860) 97-6 (AB510856) 94-10-1 (AB510857) 100/89 2002-06-03 (AB510892) 96-1-8 (AB510867) 96-3-3 (AB510868) A. tabescens 2006-20-1 (AB510887) 98/94 2002-66-03 (AB510896) 94-8-2 (AB510855) NC8 (AB510897) 94-75-07 (AB510854) A. ostoyae 89-03B-09 (AB510861) 88-01-19 (AB510859) 91-01-10 (AB510865) NB3 (AB510894) 99/80 00-4-4 (AB510876) 00-3-1 (AB510899) A. nabsnona 00-16-4 (AB510883) NB4 (AB510900) NE4 (AB510874) 2003-71-13 (AB510871) 99/95 2000-23-02 (AB510879) 94-43-08 (AB510895) Nag. E 96-37-1 (AB510893) 94-2-1 (AB510888) 94-35-01 (AB510891) NA17 (AB510872) 05-46-1 (AB510889) NA4 (AB510881) 96-7-1 (AB510873) 96-8-1 (AB510878) 04-16-1 (AB510877) 94-46-1 (AB510898) 05-13-2 (AB510884) A. gallica, A. cepistipes 94-39-04 (AB510853) NA13 (AB510890) 2000-07-04 (AB510870) and A. sinapina 2000-08-14 (AB510875) 90-10-12 (AB510862) 96-19-01 (AB510882) ND1 (AB510885) ND11 (AB510869) 94-33-01 (AB510866) 05-7-1 (AB510886)

Fig. 2 Neighbor-joining tree based on internal transcribed spacer sequences from GenBank. Bootstrap values and reliability values are (ITS 1-5.8S-ITS 2) sequences of known Japanese Armillaria species, shown on the nodes the unknown isolates from Amami-Oshima, and other highly similar strongly supported clades. The NJ tree based on EF-1a the isolates A. novae-zelandiae from Malaysia (isolate no. sequences is shown in Fig. 1.TheArmillaria sp. sequences CMW3951). The sequence similarity between Amami- from Amami-Oshima isolates formed a strongly supported Oshima isolates and A. novae-zelandiae isolates from Aus- clade (bootstrap and reliability values [84%) with isolates tralia, New Zealand, and Papua New Guinea ranged from 82 from Indonesia and Papua New Guinea, A. novae-zelan- to 85%. The ITS 1 of A. novae-zelandiae from Australia, diae. This Amami-Oshima isolate clade was adjacent to a New Zealand, and Papua New Guinea contained more well-supported sister clade (bootstrap and reliability values insertions than in the ITS 1 of the isolates from Amami- [97%) that comprised A. novae-zelandiae from Australia Oshima and Malaysia. Compared with known Armillaria and New Zealand. spp. in Japan, the isolates from Amami-Oshima had a Amplification of the ITS region yielded an approximately [100-bp insertion in ITS 1 and a[100-bp deletion in ITS 2. 800-bp product for the Amami-Oshima and A. ectypa iso- In the way similar to that of the EF-1a gene, A. novae- lates. ITS sequences from the Amami-Oshima isolates zelandiae was used as the outgroup for subsequent analysis showed the highest similarity ([92%) to the sequences of of ITS region. The ITS-based NJ tree that used a data set 123 Mycoscience (2011) 52:53–58 57 consisting of 63 sequences is shown in Fig. 2. The isolates grateful to Dr. Eiji Nagasawa (Tottori Mycological Institute, Tottori, from Amami-Oshima formed a strongly supported clade Japan) who provided the isolates. Thanks are also due to Dr. Norio Sahashi, Dr. Tsutomu Hattori, Dr. Taisei Kikuchi, Dr. Amy Ross- with those of A. novae-zelandiae from Malaysia, Indonesia, Davis, and Mr. John W. Hanna for their helpful suggestions on an and Papua New Guinea, with bootstrap and reliability earlier version of this manuscript and to Ms. EtsukoTsutsumi and values of 98% and 94%, respectively. In addition, the Ms. Kazuko Komaru for their technical assistance. This work was Amami-Oshima isolate clade and another clade containing supported by the Program for Supporting Activities for Female Researchers funded by the Special Coordination Fund for Promoting A. novae-zelandiae from Australia and New Zealand Science and Technology of Ministry of Education, Culture, Sports, formed a well-supported, larger clade with bootstrap and Science and Technology, Japan. reliability values of 100%. In this study, the undetermined Armillaria isolates from Amami-Oshima in subtropical Japan were shown to be References distinct from previously reported Armillaria spp. in Japan. The phylogenetic trees based on EF-1a and ITS sequences Anisimova M, Gascuel O (2006) Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. 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