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Aphelenchoidid Nematodes Associated with Two Dominant Ficus

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Aphelenchoidid Nematodes Associated with Two Dominant Ficus Nematology 19 (2017) 323-331 brill.com/nemy Aphelenchoidid nematodes associated with two dominant Ficus species in Aceh, Indonesia ∗ Rina SRIWATI 1,YukoTAKEUCHI-KANEKO 2,J.JAUHARLINA 1 and Natsumi KANZAKI 3, 1 Department of Plant Protection, Faculty of Agriculture, Syiah Kuala University, Darussalam Banda Aceh 23111, Indonesia 2 Laboratory of Terrestrial Microbial Ecology, Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwake-cho, Sakyo-ku, Kyoto, 606-8502, Japan 3 Forestry and Forest Products Research Institute, 1 Matsunosato, Tsukuba, Ibaraki, 305-8687, Japan Received: 20 November 2016; revised: 18 January 2017 Accepted for publication: 18 January 2017; available online: 22 February 2017 Summary – Aphelenchoidid nematodes associated with the syconia of two dominant fig species, Ficus hispida and F. racemosa,were surveyed in Banda Aceh, Indonesia. Nematodes were isolated from sycones and pollinating wasps of these two fig species from four localities in the area, and identified based on the molecular sequences of two genetic loci, D2-D3 expansion segments of large subunit ribosomal RNA (D2-D3 LSU) and mitochondrial cytochrome oxidase subunit I (mtCOI). Molecular sequences of D2-D3 LSU and mtCOI were successfully determined for 44 and 19 individual nematodes, respectively, and these sequences were separated into four clades, i.e., types A-D of D2-D3 LSU and types I-IV of mtCOI. Phylogenetic analysis of the DNA sequences deposited in the GenBank database showed that the DNA sequences corresponded to three species, namely, Martininema baculum (type B/II), Ficophagus fleckeri (types A/I, D/IV) and F .cf.centerae (type C/III). Within these species, F. fl e cke r i was separated into two clades as suggested in previous studies and thus it may possibly reflect the existence of two different taxa, F. fl e cke r i and a cryptic species. The Indonesian F .cf.centerae was monophyletic with, but clearly separated from, the Chinese population of F. centerae and thus the Indonesian population is potentially an undescribed species. Overall, the species composition of fig-associated aphelenchoidids in the Aceh region seemed intermediate between continental Chinese and Australian species. However, further material collections followed by detailed morphological analyses are necessary to characterise or describe these fig-associated aphelenchoidids in Indonesia. Keywords – Aphelenchoididae, biogeography, diversity, Ficophagus cf. centerae, Ficophagus fleckeri, Ficus hispida, Ficus racemosa, figs, Martininema baculum, molecular, plant-parasitic nematode, syconia. Nematodes associated with figs (syconia of Ficus spp.) + Teratodiplogaster Kanzaki, Giblin-Davis, Davies, Ye, are now becoming an interesting model system for evolu- Center & Thomas, 2009, Pristionchus Kreis, 1932, Acros- tionary biology of parasitism/pathogenicity (Herre, 1993), tichus Rahm, 1928 and Rhabditolaimus Fuchs, 1914, de- phenotypic plasticity (e.g., Susoy et al., 2016), feeding rived from diplogastrid bacterial feeders (e.g., Kanzaki et habit (e.g., Giblin-Davis et al., 2003; Kanzaki et al., al., 2016; Susoy et al., 2016), and Caenorhabditis Osche, 2014a) and other topics. So far, at least ten lineages 1952 derived from a rhabditid bacterial feeder (Kanzaki of nematodes are known to be associated with figs and et al., 2014b). In addition, several genera have been re- fig wasps: namely, Bursaphelenchus Fuchs, 1937, Schis- ported from India (e.g., Lingaiah et al., 2012). However, tonchus Cobb, 1927, Martininema Davies & Bartholo- we cannot discuss the Indian species in detail due to a lack maeus in Davies et al., 2015 and Ficophagus Davies of detailed description, molecular barcoding information & Bartholomaeus in Davies et al., 2015, derived from and type material. aphelenchoidid fungal feeders (Kanzaki et al., 2014a; In the Asia-Oceania (West Pacific) region, fig- Davies et al., 2015), Ficotylus Davies, Ye, Giblin-Davis associated nematode surveys and species descriptions & Thomas, 2009 derived from a tylenchid plant parasite have been conducted in Australia (Bartholomaeus et al., (Davies et al., 2009), Parasitodiplogaster Poinar, 1979 2009, 2012; Davies et al., 2009, 2010, 2013a, b, 2015; ∗ Corresponding author, e-mail: [email protected] © Koninklijke Brill NV, Leiden, 2017 DOI 10.1163/15685411-00003051 R. Sriwati et al. Kanzaki et al., 2009), New Zealand (Zhao et al., 2015), according to the methods of Kanzaki & Futai (2002) and Vietnam (Susoy et al., 2016), China (Zeng et al., 2007, Ye et al. (2007). 2010, 2011, 2013a, b, c), India (Kumari & Reddy, 1984; The determined sequences were compared with the Reddy & Rao, 1986; Anand, 2002, 2005; Bajaj & Tomar, other fig-associated aphelenchoidids with maximum like- 2014) and Japan (Kanzaki et al., 2014b, c). Indonesia is lihood phylogenetic analyses. The sequences for compar- surrounded by the countries where the fig-associated ne- ison with present data were downloaded from the Gen- matode studies have been conducted and is a contact point Bank database (http://www.genome.jp/dbget-bin/www_ of the East and South Asian and Oceania regions. There- bfind?genbank-today). The phylogenetic analyses were fore, it is important to examine the fig-associated nema- performed in PhyML (Guindon et al., 2010: http://www. todes there as basic information for future biogeograph- atgc-montpellier.fr/phyml/) using the D2-D3 LSU and mt- ical studies. However, at present almost no information COI sequence data separately. Sequence alignments were about fig-associated nematodes has been reported from performed using the online version of MAFFT (Katoh et this region. al., 2002: http://mafft.cbrc.jp/alignment/server/). The nu- In the present study, nematodes associated with two cleotide substitution model was selected automatically in dominant Ficus L. species, F. racemosa L. and Ficus the online PhyML and the tree topology was evaluated hispida L., were examined at Aceh, Indonesia, based on with 1000 bootstrap pseudoreplicates. molecular barcoding focusing on aphelenchoidid plant parasites. Results Materials and methods Adults and propagative juveniles were isolated from fig syconia, while the nematodes isolated from the wasps NEMATODE COLLECTION AND MATERIAL seemed to be young adult females. However, because PREPARATION of the poor condition of the fixed material, probably because the temperature for heat-killing was not sta- Syconia were collected from Ficus racemosa and F. ble, detailed morphological analysis was not conducted hispida growing in natural forest around Banda Aceh, and the nematodes were identified using molecular se- Indonesia in July 2013 (Table 1). Collected figs were quences. Although the species-specific morphological dissected in distilled water or kept at room temperature for characters were not clearly observed, the photomicro- fig wasp development. The emerged fig wasps were then graphs of DESS-fixed materials are available upon re- dissected for nematode isolation. Collected nematodes quest. were either heat-killed at 60°C for 1 min and fixed in The D2-D3 LSU and mtCOI were successfully se- TAF (7.0% formalin, 2.0% triethanolamine, 91% distilled quenced for 44 and 19 individuals, respectively and the water) for morphological vouchers for future taxonomic sequences were divided into four genotypes for both loci. studies, or stored in DESS (Yoder et al., 2006) for Furthermore, D2-D3 LSU type B was separated into seven molecular material. subtypes, and mtCOI types I, II and III were separated into three, six and three subtypes, respectively (Fig. 1; Ta- MOLECULAR IDENTIFICATION ble 1). However, these variations could be derived from sequencing error or unclear (heterologous) bases often DESS-fixed nematodes were hand-picked from the found in those loci of fig-associated aphelenchoidids (e.g., reagent using a flame-sterilised stainless steel entomolog- Davies et al., 2015). The determined sequences were de- ical pin, washed in a drop of sterile water and observed posited in the GenBank database with the accession num- under a light microscope for casual morphotyping. Then, bers LC208749-LC208772 (Figs 1, 2). the nematodes were individually transferred to nematode Based upon phylogenetic analyses, four genotypes digestion buffer (Kikuchi et al., 2009; Tanaka et al., 2012) were tentatively identified as Martininema baculum and individually digested at 60°C for 30 min. The nema- (Davies, Bartholomaeus, Kanzaki, Ye & Giblin-Davis, tode lysate served as PCR templates, and their amplicons 2013) Davies & Bartholomaeus in Davies et al., 2015 of D2-D3 expansion segments of large subunit ribosomal (D2-D3 type B; mtCOI type II); Ficophagus cf. cen- RNA (D2-D3 LSU) and partial fragment of mitochondrial terae (D2-D3 type C; mtCOI type III) and F. fleckeri cytochrome oxidase subunit I (mtCOI) were sequenced (Davies, Bartholomaeus, Kanzaki, Ye & Giblin-Davis, 324 Nematology Vol. 19(3), 2017 Table 1. Summary of collection locality, tree species, individual tree code, source of nematode and nematode genotype. Aphelenchoidid nematodes associated with two dominant Locality (GPS) Tree species Individual Source of D2-D3 mtCOI genotype Nematode identification tree code nematode genotype Leupung 1 (5°2039N, 95°1433E) Ficus hispida H3 Syconia B3, B4, B5, C IIa, IIb, IIIa, IIIb, IIIc Martininema baculum, Ficophagus cf. centerae Fig wasp B1, B2, B6, B7 IIb, IIc Martininema baculum H4 Syconia B1, B2, B3, B4, – Martininema baculum B6, B7, C H5 Syconia B1 IIIc Martininema baculum, Ficophagus cf. centerae Ficus racemosa R4 Syconia A Ia, Ib, Ic, Id, Ie Ficophagus
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