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A New Phytoplasma Taxon Associated with Japanese Hydrangea Phyllody

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A New Phytoplasma Taxon Associated with Japanese Hydrangea Phyllody international Journal of Systematic Bacteriology (1 999), 49, 1275-1 285 Printed in Great Britain 'Candidatus Phytoplasma japonicum', a new phytoplasma taxon associated with Japanese Hydrangea phyllody Toshimi Sawayanagi,' Norio Horikoshi12Tsutomu Kanehira12 Masayuki Shinohara,2 Assunta Berta~cini,~M.-T. C~usin,~Chuji Hiruki5 and Shigetou Nambal Author for correspondence: Shigetou Namba. Tel: +81 424 69 3125. Fax: + 81 424 69 8786. e-mail : snamba(3ims.u-tokyo.ac.jp Laboratory of Bioresource A phytoplasma was discovered in diseased specimens of f ield-grown hortensia Technology, The University (Hydrangea spp.) exhibiting typical phyllody symptoms. PCR amplification of of Tokyo, 1-1-1 Yayoi, Bunkyo-ku 113-8657, DNA using phytoplasma specific primers detected phytoplasma DNA in all of Japan the diseased plants examined. No phytoplasma DNA was found in healthy College of Bioresource hortensia seedlings. RFLP patterns of amplified 165 rDNA differed from the Sciences, Nihon University, patterns previously described for other phytoplasmas including six isolates of Fujisawa, Kanagawa 252- foreign hortensia phytoplasmas. Based on the RFLP, the Japanese Hydrangea 0813, Japan phyllody (JHP) phytoplasma was classified as a representative of a new sub- 3 lstituto di Patologia group in the phytoplasma 165 rRNA group I (aster yellows, onion yellows, all vegetale, U niversita degli Studi, Bologna 40126, Italy of the previously reported hortensia phytoplasmas, and related phytoplasmas). A phylogenetic analysis of 16s rRNA gene sequences from this 4 Unite de Pathologie Vegetale, Centre de and other group Iphytoplasmas identified the JHP phytoplasma as a member Versa iI les, Inst it ut Nat iona I of a distinct sub-group (sub-group Id) in the phytoplasma clade of the class de la Recherche Mollicutes. The phylogenetic tree constructed from 165 rRNA gene sequences Agronomique, F78026 Versailles Cedex, France was consistent with the hypothesis that the JHP phytoplasma and its closest known relatives, the Australian grapevine yellows (AUSGY), Phormium yellow 5 Department of Agricultural, Food, and leaf (PYL), Stolbur of Capsicum annuum (STOL) and Vergilbungskrankheit of Nutritional Science, grapevine (VK) share a common ancestor. The unique properties of the DNA University of Alberta, from the JHP phytoplasma clearly establish that it represents a new taxon, Edmonton, Alberta, Canada T6G 2P5 Candidatus Phytoplasma japonicum '. Keywords : Japanese Hydrangea phyllody, ' Candidatus Phytoplasma japonicum ' INTRODUCTION genicity of phytoplasmas has been elusive because of the inability to culture these cell-wall-less prokaryotes The hortensia plant (Hydrangea spp.) is native to in a cell-free medium, indirect evidence from electron Japan. It was exported to Europe more than 200 years microscopy, and use of molecular probes support the ago and now is distributed all over the world. Recently, hypothesis of a phytoplasmal aetiology for these Kanehira et al. (1996) reported a Japanese Hydrangea diseases (Kanehira et al., 1996). JHP was such a case as phyllody (JHP) disease, documented that it is a serious described above (Kanehira et al., 1996). disease and spread wherever hortensia is grown in Japan, and determined that the causal agent was likely We used molecular biological methods to classify the a phytoplasma. Although rigorous proof of the patho- phytoplasma associated with JHP disease in Japan. This paper reports the results of an extended study involving the PCR amplification of phytoplasma- Abbreviations: AUSGY, Australian grapevine yellows; JHP, Japanese Hydrangea phyllody; OY, onion yellows; PYL, fhormium yellow leaf; RYD, specific DNA from JHP phytoplasma templates and rice yellow dwarf; STOL, Stolbur of Capsicum annuum; TWB, tsuwabuki the analysis of the amplified DNA. We report the witches' broom; VK, Vergilbungskrankheit of grapevine. nucleotide sequence of a segment of the JHP phyto- The EMBUDDBJ/GenBank accession number for the 165 rDNA sequence plasma 16s rDNA for the first time, present the results of Japanese Hydrangea phyllody phytoplasma is A601 0425. of a phylogenetic analysis of the sequences, and 00861 0 1999 IUMS 1275 T. Sawayanagi and others describe sequences that are unique to JHP phyto- Primer pairs and conditions for PCR. A pair of previously plasma 16s rDNA. Our data led us to propose that the designed oligonucleotide primers (SN9 10601 and JHP phytoplasma is a taxonomically distinct phyto- SN910502) (Namba et al., 1993a) was used in the PCR to plasma. amplify the 16s rDNA in each sample tested. Three DNA samples isolated from three different places described above were used to amplify the 16s rDNA. METHODS For the direct PCR, the template consisted of the total nucleic acids extracted from tissues of hortensia, periwinkle, Plant samples and reference phytoplasma strains. Samples garland chrysanthemum and rice plants using previously from naturally occurring diseased Hydrangea macrophylla described methods (Namba et al., 1993a). Each PCR mixture (Thunb. ex J. Murr.) Ser. f. macrophylla, H. macrophylla (total volume, 50 p1) contained 20 ng (for hortensia) or (Thunb. ex J. Murr.) Ser. f. normalis (E. H. Wils.) Hara, and 50-1 00 ng (for periwinkle, garland chrysanthemum or rice Hydrangea serrata (Thunb.) Ser.f. exhibiting symptoms of plants) of total nucleic acids extracted from healthy or JHP, which include phyllody and proliferation of the flower diseased plant tissue. The PCR conditions were : each primer organs as well as stunting and dieback, were collected in the 0.5 pM, 1.5 mM MgCl,, 10 mM Tris/HCl (pH 8.3), 50 mM field from Tochigi [isolate number (No.) 950951, Shizuoka KCl, 0.001 YOgelatin, 1.25 U Taq DNA polymerase (Takara (No. 95227) and Oita (No. 95094) Prefectures in Japan, Taq; Takara Shuzo), and 200 pM each dNTP. The reaction during 1994 and 1995 (Kanehira et al., 1996). The causal mixtures were overlaid with mineral oil, and the PCR was agent was transmitted to periwinkle [Catharanthus roseus performed in a thermal cycler (Perkin-Elmer Cetus). An (L.) G. Don] by graft inoculation and the infected peri- initial 2min denaturation at 94°C was followed by 40 winkles were used as samples. Hydrangea phyllody phyto- cycles, each consisting of 2 min denaturation at 94 "C, 2 min plasma isolates other than JHP phytoplasma used for RFLP annealing at 60 "C, and 3 min extension at 72 "C. In the last analyses were an Italian isolate (HyPhl) (Lee et al., 1993), cycle, the extension step at 72 "C was 7 min. A 2 p1 aliquot of Belgium isolate (HYDP) (Schneider et al., 1993), French each PCR product was analysed by electrophoresis in a & isolate (HF) (Cousin Sharma, 1986), and three Canadian 1.0 % agarose gel, which was stained with ethidium bromide isolates (HC) (Hiruki et al., 1994). Additional samples were (0-5 pg ml-l) and visualized with a UV transilluminator. taken from healthy, greenhouse-grown hortensia and peri- winkle seedlings. The reference phytoplasmas used included RFLP analysis of PCR-amplified DNA. The PCR products were onion yellows (OY) in periwinkle or garland chrysanthemum digested individually with each of the restriction enzymes (Chrysanthemum coronarium L.) tissues, tsuwabuki witches ' DraI, EcoRI, EcoRII, HaeIII, HindIII, Hinfl, KpnI, Sau3AI broom (TWB) in periwinkle or garland chrysanthemum (Nippon Gene), AluI, HhaI, HpaII, RsaI, TaqI(Toyobo), tissues, and rice yellow dwarf (RYD) in rice (Oryza sativa AccII, HpaI (Takara Shuzo) and Tru9I (Boehringer L.) tissues. Mannheim) according to the manufacturers' instructions. Table 1. Strains of the phytoplasmas and acholeplasma used in this study, associated diseases, and accession numbers of their 165 rDNA sequences Ph ytoplasma Associated disease GenBank no. Ashy Ash yellows X68339 ACLR Apricot chlorotic leafroll X68338 AT Apple proliferation X68375 AUSGY Australian grapevine yellows L76865 BB Tomato big bud L33760 BVK Leafhopper Psamrnotettix cephalotes X76429 CP Clover proliferation L33761 CPh Clover phyllody L33762 FD Flavescence dorke X76560 JHP Japanese Hydrangea phyllody ABO 10425 LfWB Loofah witches' broom L33764 LY Coconut lethal yellowing U18747 OY Onion yellows D 12569 PPWB Pigeon pea witches' broom U18763 PYL Phormium yellow leaf U43569 RYD Rice yellow dwarf D12571 SAY Western aster yellows M86340 STOL Stolbur of Capsicum annuurn X76427 TWB Tsuwabuki witches ' broom D 12570 VK Vergilbungskrankheit of grapevine X76428 WBDL Witches'-broom disease of lime U 15442 Acholeplasma luidlawii M23932 ~~~~~ ~~~ ~ ~~ 1276 International journal of Systematic Bacteriology 49 ' Candidatus Phytoplasma japonicum ' The digested DNA was analysed by electrophoresis in a identical to those from corresponding RFLP profiles and to 2.5% agarose gel, followed by staining with ethidium compare with putative RFLP profiles of the STOL/VK bromide and visualization of the DNA bands with a UV phytoplasmas and AUSGY/PYL phytoplasmas of which transilluminator. The RFLP patterns of JHP phytoplasma DNA samples were not used in this experiments, each DNA were compared with those of amplified DNA from the putative restriction site was predicted with DNASIS. reference strains and previously published data (Ahrens & Seemiiller, 1992; Lee et al., 1993; Prince et al., 1993; Nucleotide sequence accession numbers. The GenBank Schneider et al., 1993). The group names 'I'-'V' were accession numbers of the 16s rDNA sequences of JHP followed from the previous report (Seemiiller et al., 1994). phytoplasma, other phytoplasmas and Acholeplasma However, the classification of sub-groups was basically
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