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Additional data on Pratylenchoides riparius (Andrássy, 1985) Luc, 1986 (Nematoda: Merliniidae) from Iran

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Manouchehr HosseinvandDepartment of Plant Protection, Faculty of Agriculture, University of Zanjan, 45371-38791, Zanjan, Iran

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Ali EskandariDepartment of Plant Protection, Faculty of Agriculture, University of Zanjan, 45371-38791, Zanjan, Iran

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Reza GhaderiDepartment of Plant Protection, School of Agriculture, Shiraz University, 71441-65186, Shiraz, Iran

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Summary

The second population of Pratylenchoides riparius, including females and males, is described and illustrated based upon morphological, morphometric and molecular data. The present population from Iran is characterised by some differences with the type population of the species from Hungary in stylet length (24-26 vs 21-22 μm), slightly longer body (1002-1230 vs 830-960 μm), pharynx (202-211 vs 182-190 μm) and tail (64-85 vs 48-57 μm), areolated outer bands of the lateral field (vs non-areolated), widening of the lateral field near tail terminus (vs lateral incisures connecting each other) and presence of males (vs absent). The taxonomic status of the species with regarding the data from the type and presently recovered population, as well as the closely similar species is discussed. The newly recovered population was studied based upon its molecular phylogenetic charactes using the D2-D3 of 28S rRNA and the partial 18S rRNA gene sequences and the results revealed that it forms a clade with P. magnicauda in 28S, but occupies a distant placement from it in 18S phylogeny.

Summary

The second population of Pratylenchoides riparius, including females and males, is described and illustrated based upon morphological, morphometric and molecular data. The present population from Iran is characterised by some differences with the type population of the species from Hungary in stylet length (24-26 vs 21-22 μm), slightly longer body (1002-1230 vs 830-960 μm), pharynx (202-211 vs 182-190 μm) and tail (64-85 vs 48-57 μm), areolated outer bands of the lateral field (vs non-areolated), widening of the lateral field near tail terminus (vs lateral incisures connecting each other) and presence of males (vs absent). The taxonomic status of the species with regarding the data from the type and presently recovered population, as well as the closely similar species is discussed. The newly recovered population was studied based upon its molecular phylogenetic charactes using the D2-D3 of 28S rRNA and the partial 18S rRNA gene sequences and the results revealed that it forms a clade with P. magnicauda in 28S, but occupies a distant placement from it in 18S phylogeny.

Andrássy (1985) described the monotypic genus Hoplorhynchus Andrássy, 1985 with H. riparius Andrássy, 1985 as the type species based on a monosexual population (only females were recovered) from Hungary. He noted that this genus mostly resembles Hoplolaimidae Filipjev, 1934 members, but differs from them by having six incisures in the lateral field (vs four), comparatively long and cylindrical tail, and phasmids in the posterior half of the tail. Luc (1986) argued this genus is congeneric with Pratylenchoides Winslow, 1958, and consequently considered Hoplorhynchus as a junior synonym of Pratylenchoides. This action has met with general acceptance (Brzeski, 1998; Siddiqi, 2000; Andrássy, 2007; Ryss, 2007; Geraert, 2013; Ghaderi & Karegar, 2014). Currently, P. riparius (Andrássy, 1985) Luc, 1986 is only known from its type locality and there are no molecular data for it in the GenBank database. The present study aims to redescribe a population of the species that includes both females and males and to reconstruct its phylogenetic relationships with other species of the genus as inferred using partial sequences of the D2-D3 expansion segments of 28S rRNA and the 18S rRNA genes.

Materials and methods

Sampling, nematode extrction and morphological characterisation

Specimens of P. riparius were recovered from the rhizosphere of a forest tree in the city of Astara, northern Iran. Nematodes were extracted by using the tray method (Whitehead & Hemming, 1965), fixed by adding hot FPG (4:1:1, formaldehyde:propionic acid:glycerin) solution, processed to anhydrous glycerin (De Grisse, 1969), mounted in glycerin on permanent slides using paraffin wax and studied using a light microscope, equipped with a Dino-eye microscope eye-piece camera in conjunction with Dino Capture version 2.0 software. Specimens were identified at species level using available identification keys (Loof, 1991; Geraert, 2013; Ghaderi & Karegar, 2014).

DNA extraction, PCR and sequencing

DNA was extracted from single individuals according to Tanha Maafi et al. (2003) and stored at −20°C until used as a PCR template. The D2-D3 expansion segments of 28S rRNA gene were amplified using the forward D2A (5′-ACAAGTACCGTGAGGGAAAGT-3′) and reverse D3B (5′-TCGGAAGGAACCAGCTACTA-3′) primers (Subbotin et al., 2006). The partial 18S rRNA gene was amplified using the forward primer 1096F (5′-GGTAATTCTGGAGCTAATAC-3′) and reverse primer 1912R (5′-TTTACGGTYAGAACTAGGG-3′), and forward primer 1813F (5′-CKGCGYKAGAGGTGAAAT-3′) and reverse primer 2646R (5′-GCTACCTTGTTACGACTTTT-3′) for the second fragment (Holterman et al., 2008). The 30 μl PCR mixture contained 15 μl 2× Taq DNA polymerase mix. (Ampliqon), 1 μl (10 pmol μl−1) each of forward and reverse primers, 2 μl of DNA template and 11 μl distilled water. The thermal cycling program was as follows: denaturation at 95°C for 4 min, followed by 33 cycles of denaturation at 94°C for 30 s, annealing at 54°C for 30 s (18S rRNA) and 57°C for 30 s (28S rRNA) and extension at 72°C for 90 s. A final extension was performed at 72°C for 10 min. The quality of amplification and the size of amplicons were checked by electrophoresis of 4 μl of the PCR products in 1% agarose gel containing ethidium bromide, and subsequent visualisation under UV light. The PCR products were purified and directly sequenced using the same primers with an ABI 3730XL sequencer (Bioneer, Seoul, South Korea). The newly obtained sequences were submitted to the GenBank database under accession numbers MK089267 for the D2-D3 28S and MK089266 for the 18S sequences.

Phylogenetic analyses

The newly obtained sequences were edited using BioEdit and compared with other available sequences in GenBank using the BLAST homogeneity search program. The previously available sequences (van Megen et al., 2009; Majd Taheri et al., 2013; Ghaderi et al., 2014; Panahandeh et al., 2014; Azizi et al., 2016) of the genus were retrieved from the database, updated based upon the results of the BLAST search and aligned using Clustal W implemented in MEGA7 (Kumar et al., 2016) after including the newly generated sequences. The ambiguously aligned parts and divergent regions were eliminated using the online version of Gblocks 0.91b (Castresana, 2000; http://molevol.cmima.csic.es/castresana/Gblocks_server.html). The best-fit model of nucleotide substitution used for the phylogenetic analysis was statistically selected using jModelTest 2.1.10 (Darriba et al., 2012). The phylogenetic tree was generated with Bayesian inference method using MrBayes 3.2.6 (Ronquist et al., 2012) using Psilenchus hilarulus de Man, 1921 as outgroup for both the 28S and 18S trees based on the basal placement of the genus Psilenchus de Man, 1921 in previous studies (Ghaderi et al., 2014; Panahandeh et al., 2014; Azizi et al., 2016). The analysis was initiated with a random starting tree, running the chains for 1 × 106 generations. The Markov chain Monte Carlo (MCMC) method within a Bayesian framework was used to estimate the posterior probabilities of the phylogenetic trees (Larget & Simon, 1999) using the 50% majority rule. The tree was visualised and saved with FigTree 1.4.3 (Rambaut, 2014) and redrawn with Adobe® Acrobat® XI Pro 11.0.1.

Fig. 1.
Fig. 1.

Diagnostic characters of Pratylenchoides riparius (Andrássy, 1985) Luc, 1986 from Iran: female (A, C, F-L, N-P) and male (B, D, E, M). A, B: Entire body; C, D: Head and stylet; E, F, H: Anterior end and pharyngeal region; G: Reproductive system; I-M: Posterior end; N-P: Pharyngeal basal bulb and gland nuclei.

Citation: Nematology 21, 8 (2019) ; 10.1163/15685411-00003257

Fig. 2.
Fig. 2.

Light photomicrographs of Pratylenchoides riparius (Andrássy, 1985) Luc, 1986 from Iran: female (A, C-E, I-L) and male (A, B, F-H). A: Entire body; B, C: Anterior end and pharyngeal region; D-H: Head and stylet; I, J: Pharyngeal basal bulb and gland nuclei; K: Vulva and part of reproductive system; L: Lateral field at mid-body showing six incisures (arrows). (Abbreviations: c = pharyngo-intestinal valve or cardium; n = pharyngeal gland nuclei; s = spermatheca.) (Scale-bars: A = 200 μm; B, C = 20 μm; D-L = 10 μm.)

Citation: Nematology 21, 8 (2019) ; 10.1163/15685411-00003257

Fig. 3.
Fig. 3.

Light photomicrographs of posterior end of Pratylenchoides riparius (Andrássy, 1985) Luc, 1986 from Iran: male (A, B) and female (C-K). (Abbreviations: a = anus; p = phasmid.) Arrows in G indicate the six lateral lines.) (Scale-bars: A, D-K = 10 μm; B, C = 20 μm.)

Citation: Nematology 21, 8 (2019) ; 10.1163/15685411-00003257

Results

Redescription of Pratylenchoides riparius (Andrássy, 1985) Luc, 1986 = Hoplorhynchus riparius Andrássy, 1985 (Figs 1-3)

Measurements

See Table 1.

Description

Female

Body almost straight or with slight ventral curvature. Cuticle annuli 2.0-2.3 μm wide at mid-body. Lateral field 8-18 μm wide or 28-43% of body diam., with six incisures near mid-body, at deirid level and on entire tail region. Lateral field widening near tail tip, all six incisures reaching to tail terminus and connecting to terminal striae of tail. Outer or sometimes inner bands areolated on some parts of body and typically on tail. Cephalic region bluntly rounded, anteriorly flattened or slightly dome-shaped, narrower than body and slightly offset, 4-5 μm high and 10-11 μm wide at base, with four or five distinct annuli anterior to basal plate. Cephalic framework moderately developed, outer margins extending for over two annuli into body. Anterior cephalids immediately posterior to proximal extensions of cephalic framework, posterior cephalids 5-7 annuli posterior to anterior cephalids. Stylet robust, 2.4-2.6 times as long as cephalic region diam. at base, conus ca 13 μm and forming nearly half of total stylet, basal knobs 6-7 μm wide, directed laterally and slightly concave anteriorly. Dorsal pharyngeal gland orifice located 3-4 μm from stylet base. Pharyngeal median bulb oval, 12-16 μm diam., located 84-89 μm from anterior end. Nerve ring situated nearly at mid-isthmus, 113-123 μm from anterior end. Hemizonid two annuli wide, located two annuli anterior to secretory-excretory pore. Pharyngeal glands 35-61 μm long and 15-18 μm wide, overlapping intestine dorsally for 6-14 μm or 0.2-0.6 corresponding body diam. Pharyngo-intestinal valve (cardium) pyriform, situated in centre of body. Dorsal pharyngeal gland nucleus and both subventral gland nuclei located anterior to pharyngo-intestinal valve. Intestinal fasciculi indistinct. Reproductive system didelphic-amphidelphic, vulval lips slightly raised, vagina 8-12 μm long or 28-35% of corresponding body diam. Spermatheca round, axial, with numerous fine spheroid sperm. Phasmids 34-48 μm posterior to anus, usually in posterior half of tail. Tail cylindrical with coarsely and irregularly annulated hemispherical terminus, most annuli on tail terminus distinctly wider than adjoining tail annuli. Hyaline region 8-12 μm long.

Male

Frequent. Body straight to ventrally curved especially in posterior half. Cuticle annuli 1.0-1.8 μm wide at mid-body. Lateral field 5-9 μm wide, occupying 30-47% of body diam., with six distinct incisures on most of body length, oblique striae in middle band and incomplete areolation of outer bands may be seen in some specimens. Cephalic region bluntly rounded to nearly hemispherical, offset from body contour, with five or six fine annuli. Stylet generally as long as in female or slightly shorter, with smaller basal knobs. Median bulb and pharyngeal glands usually slightly reduced, with obscure or smaller nuclei. Intestinal fasciculi usually present and distributed over entire intestine. Caudal alae with crenate margins, arising at level of spicule heads and extending to tail terminus. Spicules slightly curved ventrad, 44-61% of tail length long, gubernaculum simple. Tail curved dorsally, tapering gradually to a conical terminus.

Habitat and locality

This species was recovered from soil around roots of a deciduous tree native to Iran, and commonly called the Persian ironwood (Hamamelidaceae: Parrotia persica (DC) C.A. Meyer), in Astara, Gilan province, northern Iran (GPS coordinates 38°19′16″N, 48°43′43″E).

Voucher specimens

Three females and 11 males deposited in the collection of the Department of Plant Protection, College of Agriculture, University of Zanjan, Zanjan, Iran. One female and two males deposited in the collection of the Department of Plant Protection, School of Agriculture, Shiraz University, Shiraz, Iran.

Morphological remarks

Females of the present population from Iran are characterised by having a flattened or slightly dome-shaped cephalic region, slightly offset and narrower than the body contour and bearing four or five annuli, stylet 24-26 μm long, pharyngeal glands abutting or slightly overlapping intestine dorsally, all three gland nuclei located anterior to pharyngo-intestinal valve, small globular sperm, six distinct lateral incisures at mid-body, deirid and on tail, and tail cylindrical with rounded and coarsely striated terminus. Males of the present population are characterised by having a similar cephalic region and comparable stylet length to those of the female, 27-33 μm long spicules and a conical tail.

The present population differs from the females of the type population of P. riparius (Andrássy, 1985) by having a longer stylet (25 (24-26) vs 21-22 μm), slightly larger body (1100 (1002-1230) vs 830-960 μm), pharynx (205 (202-211) vs 182-190 μm) and tail (69 (64-85) vs 48-57 μm), areolated outer bands of the lateral field (vs non-areolated), widened lateral field near tail terminus (vs lateral incisures connecting with each other at distal end) and presence of males (vs absent). However, some clarifications are necessary concerning the two populations.

Table 1.
Table 1.

Morphometric characters of Pratylenchoides riparius (Andrássy, 1985) Luc, 1986 from Iran and comparison with the original description. All measurements are in μm and in the form: mean ± s.d. (range). The coefficient of variation (CV) value is given for the male only as female n ⩽ 10.

Citation: Nematology 21, 8 (2019) ; 10.1163/15685411-00003257

In the original description, the stylet length was measured at 21-22 μm long, this representing a discontinuous variation with that of our population. However, taking 21-22 μm as the stylet length of the Hungarian population and 24-26 μm for the Iranian population, the maximum/minimum ratio for P. riparius is 1.24, which is comparable with that of P. batatae Zhang & Zhang, 2003 (1.33), P. camachoi Gómez-Barcina, Castillo & Gonzalez Pais, 1990 (1.19), P. crenicauda Winslow, 1958 (1.26), P. heathi Baldwin, Luc & Bell, 1983 (1.17), P. hispaniensis Troccoli, Vovlas & Castillo, 1997 (1.20), P. laticauda Braun & Loof, 1966 (1.20), P. magnicauda (Thorne, 1935) Baldwin, Luc & Bell, 1983 (1.36), P. nevadensis Talavera & Tobar, 1996 (1.18) and P. ritteri Sher, 1970 (1.42) (see Brzeski, 1998 and Geraert, 2013). Ranges in the stylet length ratio in certain species of Pratylenchoides may reach 1.45 (Ghaderi et al., 2017). Furthermore, a similar range (21-25 μm) can be found among the male individuals of the present population.

Observed difference in the body length (and concomitant differences in pharynx and tail lengths) could also be explained by the intraspecific ranges common for certain species (see Brzeski (1998), Geraert (2013) and Ghaderi & Karegar (2014) for P. crenicauda, P. laticauda and P. ritteri. Also, see Ghaderi et al. (2017) for a general conclusion based on the literature data). Areolation of the lateral field cannot be considered as a stable diagnostic character, as already discussed by Ghaderi & Karegar (2014). The end of the lateral field on the tail was not drawn completely in the original description as incisures in the lateral field may connect to the cuticular striae on the tail terminus, as can be seen in the Iranian population (Figs 1J-L; 3G-K). As to the presence/absence of males, both monosexual and bisexual populations have frequently been recovered for certain species of the genus (e.g., P. crenicauda) and the spermatheca was described as “packed with very small (1 μm) globular spermatozoa” in the Hungarian population (Andrássy, 1985), indicating that males were probably present but not recovered at the time. Considering these facts, we believe that such features cannot be used as reliable diagnostic characters and may be attributed to intraspecific variations among different geographically distant populations.

Pratylenchoides riparius appears similar to P. epacris Eroshenko, 1978 in having six lateral incisures on the post-phasmid region, and to P. heathi, P. sheri Robbins, 1985 and P. magnicauda by several similar morphometric characters. It differs from P. epacris by different position of the pharyngeal gland nuclei (all three glands anterior to the pharyngo-intestinal valve vs one of the subventral gland nuceli posterior to the valve), different cephalic region shape (bluntly rounded vs hemispherical), and slightly shorter stylet (21-26 vs 28 μm). From P. heathi and P. sheri, the number of lateral incisures on the tail region remains as the only stable differential character and from P. magnicauda it differs by having six lateral incisures on most of the tail length (vs four), shape of cephalic region (bluntly rounded vs conoid), cephalic framework (moderately vs well developed), slightly shorter stylet (average under 26 vs > 28 μm) and very small-sized sperm (vs larger).

Pratylenchoides riparius also has similarities with five other species: P. acuticauda Ryss & Sturhan, 2001, P. arenicola Ryss & Sturhan, 2001, P. magnicaudoides Minagawa, 1984, P. persicus Azizi, Eskandari, Karegar, Ghaderi, van den Elsen, Holterman & Helder, 2016, and P. rivalis Ryss & Sturhan, 2001, in having the pharyngeal glands abutting or slightly overlapping the intestine and all three gland nuclei being located anterior to the pharyngo-intestinal valve. However, none of these species has six lateral incisures on the post-phasmid region of the tail. Furthermore, P. acuticauda and P. magnicaudoides have a conical female tail, P. arenicola males have a cylindrical tail, P. persicus has a shorter body, stylet and tail, and P. rivalis has a shorter body and stylet and a longer tail with more annuli on the ventral contour.

Molecular phylogenetic status

The amplification of D2-D3 expansion segments of 28S rRNA and the partial 18S rRNA genes of P. riparius yielded a single fragment of 749 and 1602 bp, respectively. The D2-D3 sequence of P. riparius matched well with the corresponding Pratylenchoides spp. sequences deposited in GenBank. The D2-D3 dataset contained 31 ingroup sequences plus Psilenchus hilarulus as the outgroup taxon and was 577 bp in length after removing ambiguously aligned regions. The 50% majority rule consensus phylogenetic tree generated using this dataset by Bayesian inference (BI) under GTR + I + G model is presented in Figure 4. Together with P. magnicauda (KF026289), it (MK419953) formed a basal clade to other Pratylenchoides species (BPP = 0.84). Both aforementioned sequences (KF026289 and MK419953) differed by 19 bp (3.3% difference).

Fig. 4.
Fig. 4.

The 50% majority rule consensus trees from Bayesian analysis generated from the D2-D3 expansion segments of 28S rRNA gene dataset under the GTR + I + G model. Posterior probabilities for BI analysis more than 50% are given for appropriate clades. The new sequence is indicated in bold.

Citation: Nematology 21, 8 (2019) ; 10.1163/15685411-00003257

Fig. 5.
Fig. 5.

The 50% majority rule consensus trees from Bayesian analysis generated from the the partial 18S rRNA gene dataset under the GTR + I + G model. Posterior probabilities for BI analysis more than 50% are given for appropriate clades. The new sequence is indicated in bold.

Citation: Nematology 21, 8 (2019) ; 10.1163/15685411-00003257

The partial 18S sequence of P. riparius matched well with the corresponding Pratylenchoides spp. sequences deposited in GenBank after BLAST. The partial 18S alignment contained 24 sequences, including Psilenchus hilarulus as the outgroup taxon, and was 1586 bp in length after removing ambiguously aligned regions. The 50% majority rule consensus Bayesian tree inferred under GTR + I + G model is presented in Figure 5. In this tree it occupied a distinct basal placement to the clade of other Pratylenchoides species and its sister relative in the 28S tree had a distant placement.

Discussion

During the present study, a population of Pratylenchoides was recovered from Iran that comes close to the P. riparius described from Hungary. Although the Iranian population showed differences from the type population in the structure of the lateral field, presence of males and some morphometric data, the evidence from previously published morphological and molecular data (Brzeski, 1998; Geraert, 2013; Ghaderi & Karegar, 2014; Ghaderi et al., 2017) justified assigning the Iranian population to P. riparius, this therefore being the second population of the species since its original description. This species shares almost identical morphological and morphometric characters with P. heathi and P. sheri, excluding the number of lateral incisures on the female tail. No variation of this feature has been reported among individuals or populations of a given species in the genus so far and, as a result, it would be logical to accept this feature as a diagnostic character for delimiting P. riparius from P. heathi and P. sheri.

Based on the molecular trees inferred from the 28S and 18S rRNA gene sequences, Pratylenchoides currently forms a monophyletic group, having a close phylogenetic relationship with Amplimerlinius Siddiqi, 1976 and Paramerlinius Sturhan, 2012 in both trees. The monophyletic nature of Pratylenchoides and its close relationship with genera in Merliniidae Siddiqi, 1971 has already been observed in some previously published works (Ghaderi et al., 2014; Panahandeh et al., 2014; Azizi et al., 2016). However, including more sequences of certain species having similarities to P. riparius and which share with Amplimerlinius and Paramerlinius an abutting pharyngeal basal bulb or six lateral incisures on the tail (e.g., P. heathi, P. sheri, P. arenicola, P. acuticauda, P. magnicaudoides, P. rivalis, and P. epacris) may provide new insights into the phylogeny of Pratylenchoides.

In the present phylogenies, P. riparius formed a clade with P. magnicauda in the 28S phylogeny, but was distantly related to it in 18S phylogeny. They share many morphometric characters, but can be separated by differences in the number of lateral incisures on the tail region, shape of the cephalic region, structure of the cephalic framework, and size of sperm. Currently, there are no molecular data available for the type population of P. riparius and the availability of such data, and/or data from the more closely related species P. heathi and P. sheri, may require an update to the results of the present study.

*

Corresponding author, e-mail: rghaderi@shirazu.ac.ir

Acknowledgement

The authors gratefully acknowledge Dr. Akbar Karegar (Shiraz University, Iran) for his valuable and helpful comments.

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