Table 1
Morphometrics of Xiphinema barooghii n. sp. All measurements are in μm (except L in mm), and in the form: mean ± s.d. (range).
| Female | ||||||
|---|---|---|---|---|---|---|
| Characters | J1 | J2 | J3 | J4 | Holotype | Paratypes |
| n | 3 | 1 | 5 | 5 | – | 8 |
| L | 1.15 ± 0.01 (1.14–1.16) | 1.73 | 2.19 ± 0.12 (2.01–2.31) | 3.07 ± 0.17 (2.87–3.34) | 4.10 | 4.02 ± 0.21 (3.67–4.25) |
| a | 44.0 ± 2.3 (41.0–47.0) | 41 | 55.0 ± 3.9 (51.0–62.0) | 58.0 ± 5.0 (51.0–64.0) | 55 | 59.0 ± 2.4 (53.0–63.0) |
| b | 3.7 ± 0.1 (3.6–3.8) | 5.1 | 5.1 ± 0.3 (4.7–5.6) | 6.5 ± 0.6 (5.9–7.5) | 8.2 | 7.7 ± 0.3 (7.0–8.5) |
| c | 18.0 ± 0.7 (17.0–19.0) | 29 | 44.0 ± 2.0 (42.0–47.0) | 66.0 ± 6.1 (60.0–76.0) | 132 | 117 ± 10 (103–133) |
| c′ | 3.2 ± 0.1 (3.1–3.3) | 2.3 | 1.62 ± 0.04 (1.60–1.70) | 1.1 ± 0.1 (1.0–1.3) | 0.7 | 0.80 ± 0.05 (0.70–0.90) |
| V | – | – | – | – | 47 | 47.0 ± 0.9 (46.0–48.0) |
| Lip region diam. | 10.5 ± 0.3 (10.0–11.0) | 10.6 | 12.2 ± 0.2 (12.0–13.0) | 14.0 ± 1.1 (13.0–16.0) | 15 | 14.6 ± 0.3 (14.0–15.0) |
| Odontostyle length | 58.5 ± 0.2 (58.0–59.0) | 70 | 95.0 ± 2.8 (93.0–100.0) | 113.0 ± 3.3 (109.0–117.0) | 139 | 136.0 ± 2.7 (132.0–139.0) |
| Odontophore length | 45.0 ± 1.4 (44.0–47.0) | 54 | 63.0 ± 3.0 (60.0–67.0) | 76.0 ± 6.3 (70.0–87.0) | 82 | 82.0 ± 3.2 (75.0–85.0) |
| Spear length | 104.0 ± 0.4 (103.0–105.0) | 124 | 158.0 ± 4.8 (150.0–167.0) | 189.0 ± 5.7 (181.0–196.0) | 221 | 220.0 ± 3.3 (215.0–225.0) |
| Replacement odontostyle | 72.0 ± 1.6 (71.0–74.0) | 93 | 115.0 ± 2.9 (110.0–119.0) | 137.0 ± 1.7 (135.0–139.0) | – | – |
| Oral aperture to guide ring | 51.0 ± 0.5 (50.0–52.0) | 65 | 82.0 ± 3.1 (76.0–86.0) | 101.0 ± 2.4 (98.0–104.0) | 129 | 124.0 ± 5.3 (117.0–132.0) |
| Pharynx length | 311.0 ± 3.4 (307.0–315.0) | 337 | 423 ± 27 (396–476) | 447 ± 31 (416–484) | 500 | 520 ± 19 (493–553) |
| Pharyngeal bulb length | 88.0 ± 0.7 (87.0–89.0) | 88 | 112.0 ± 8.6 (103.0–125.0) | 122.0 ± 2.5 (118.0–125.0) | 144 | 141.0 ± 9.3 (128.0–153.0) |
| Body diam. at phar. base | 24.0 ± 1.6 (23.0–26.0) | 37 | 36.0 ± 3.6 (33.0–41.0) | 45.0 ± 4.1 (41.0–51.0) | 65 | 57.0 ± 7.5 (52.0–69.0) |
| mid-body | 24.0 ± 2.1 (24.0–28.0) | 42 | 40.0 ± 3.4 (34.0–44.0) | 52.0 ± 5.0 (46.0–59.0) | 74 | 67.0 ± 6.7 (60.0–79.0) |
| anus | 18.0 ± 0.4 (17.0–19.0) | 26 | 30.0 ± 0.8 (29.0–31.0) | 40.0 ± 2.7 (36.0–43.0) | 41 | 42.0 ± 1.8 (40.0–44.0) |
| G1 | – | – | – | – | 13 | 12.3 ± 0.4 (12.0–13.0) |
| G2 | – | – | – | – | 13 | 11.0 ± 1.3 (9.0–13.0) |
| Prerectum length | 265 ± 16 (246–284) | 305 | 412 ± 28 (319–444) | 572 ± 40 (525–625) | 603 | 595 ± 74 (503–700) |
| Rectum length | 14.0 ± 0.6 (13.0–15.0) | 19 | 26.0 ± 1.4 (22.0–28.0) | 33.0 ± 1.5 (31.0–35.0) | 49 | 43.0 ± 5.4 (35.0–51.0) |
| Tail length | 61.0 ± 1.3 (59.0–63.0) | 60 | 49.0 ± 1.1 (48.0–51.0) | 46.0 ± 1.5 (44.0–48.0) | 30 | 33.0 ± 2.6 (30.0–38.0) |
| Hyaline part of tail | 8.4 ± 0.3 (8.0–10.0) | 13 | 13.0 ± 1.3 (12.0–15.0) | 14.2 ± 0.5 (13.0–15.0) | 13 | 13.0 ± 0.8 (11.0–16.0) |
Table 2
Specific α-numeric code of each Xiphinema spp. belonging to X. non-americanum morphospecies Group 6 according to Loof and Luc (1990) .
| Xiphinema spp. | A | B | C | D | E | F | G | H | I | J | K | L | References |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| spinuterus | 4 | 3 | 1 | 1 | 4 | 3 | 3 | 2 | 12 | – | – | 2 | 1 |
| mluci | 4 | 3 | 2 | 123 | 45 | (3)45 | 23 | 2 | 34 | 2 | – | 1 | 1 |
| xenovariabile | 4 | 3 | 23 | 34 | 56 | 23 | 1 | 2 | 3(4) | 2 | – | 2 | 1 |
| diannae | 4 | 3 | 3 | 4 | 45 | 3 | 12 | 2 | 23 | 3 | – | 2 | 1 |
| coomansi | 4 | 3 | 3 | 45 | 456 | 3 | 2 | 2 | 3 | 3 | – | 2 | 1 |
| lacrimaspinae | 4 | 3 | 4 | 4 | 4 | 3 | 2 | 2 | 3 | 34 | 2 | 1 | 1 |
| barbercheckae | 4 | 3 | 4 | 5 | 56 | 3 | 2 | 2 | 23 | 3 | – | 1 | 1 |
| mammatum | 4 | 3 | 5a | 4 | 4 | 3 | 2 | 2 | 3 | 5 | 2 | 2 | 1 |
| aequum | 4 | 3 | 5a | 5 | 5 | 45 | 3 | 2 | 3 | 5 | 2 | 2 | 1 |
| aceri | 4 | 3 | 6a | 56 | 5 | 4 | 23 | 3 | 3 | 6 | – | 1 | 1 |
| robbinsi | 4 | 3 | 5a | 65 | 56 | 3(4) | 2 | 2 | 3(4) | 5a | 2 | 2 | 2 |
| iranicum | 4 | 3 | 5a, b | 6 | 6 | 4 | 3(4) | 2 | 3 | 5 | 4 | 1 | 3 |
| nuragicum | 4 | 3 | 7 | 6 | 56 | 345 | 3 | 2 | 3 | 7 | 2 | 1 | 4 |
| pyrenaicum | 4 | 3 | 6 | 6 | 56 | 345 | 3 | 2 | 3 | 6 | 2 | 1 | 4 |
| adenohystherum | 4 | 3 | 7 | 6 | 56 | 45 | 3 | 2 | 3 | 7 | – | 1 | 4 |
| sphaerocephalum | 4 | 3 | 5 | 6 | 56 | 34 | 3 | 2 | 3 | 5 | 2 | 1 | 4 |
| mazandaranense | 4 | 3 | 7b | 6 | 456 | 45 | 2 | 2 | 23 | 7b | 2 | 1 | 5 |
| zagrosense | 4 | 3 | 6 | 6 | 456 | 45 | 34 | 2 | 3 | 5 | 2 | 1 | 6 |
| vuittenezi | 4 | 3 | 5(7b) | 56 | 56 | 34 | 23 | 2 | 3 | 45 | 2 | 1 | 7 |
| barooghii n. sp. | 4 | 3 | 5a | 6 | 5 | 4 | 3 | 2 | 3 | 4 | 2 | 1 | 8 |
1 Notes: Referenses: 1- Loof and Luc (1990). 2- Pedram et al. (2008). 3- Pedram et al. (2009). 4- Gutiérrez-Gutiérrez et al. (2010). 5- Pedram, Pourjam, Robbins, Ye, Atighi and Decramer (2012). 6- Ghaemi et al. (2012). 7- Barsi et al. (2000). 8- Present paper.
Table 3
Xiphinema species, locality, associated host and sequences used in this study.
| Species | Locality | Host-plant | Accession number |
|---|---|---|---|
| X. abrantinum | – | – | AY601625 |
| X. adenohystherum | Bollullos par del Condado, Huelva province, Spain | Vitis vinifera L. | GU725075 |
| X. adenohystherum | Arévalo de la Sierra, Soria province, Spain | Holly tree | KC567164 |
| X. andalusiense | Belmez, Cordoba province, Spain | Wild olive | KX244884 |
| X. baetica | Manzanilla, Huelva province, Spain | Grapevine | KC567167 |
| X. bakeri | – | – | AY601623 |
| X. barense | Apulian region, Torre pozzella, Brindisi province, southern Italy | Wild olive (Olea europaea sylvestris L.) | KM199690 |
| X. barense | Apulian region, Torre Pozzella, Brindisi Province, southern Italy | Wild olive (Olea europaea sylvestris L.) | KM199691 |
| X. barense | Apulian region, Torre Pozzella, Brindisi Province, southern Italy | Wild olive (Olea europaea sylvestris L.) | KM199692 |
| X. barooghii n. sp. | Roodghat area, Sufiyan, East-Azarbaijan province, northwest of Iran | Common wheat (Triticum aestivum L.) | MH884067 |
| X. basiri | – | – | AY601630 |
| X. belmontense | Merza, Coruña province, Spain | Pedunculate oak | KC567172 |
| X. brasiliense | Shenzhen, China | – | KP793050 |
| X. brasiliense | – | – | AY601616 |
| X. castilloi | Sefid Rud River near Rasht, Gilan province, Iran | Ash tree | KF446655 |
| X. cadavalense | Espiel ,Cordoba province, Spain | Cultivated olive | KX244900 |
| X. celtiense | Peñafor, Sevilla province, Spain | Wild olive | KX244889 |
| X. chambersi | Florida, USA | – | DQ299512 |
| X. chambersi | – | – | AY601617 |
| X. citricolum | Florida, USA | – | DQ285668 |
| X. cohni | El Puerto de Santa María, Cádiz province, Spain | Stone pine | KC567173 |
| X. conurum | Uleila del Campo, Almeria province, Spain | cultivated olive | KX244902 |
| X. cretense | Hersonisos, Heraklion province, Crete, Greece | Olive (Olea europaea L. subsp. europaea) | KJ802878 |
| X. costaricense | Pacayitas, La Suiza de Turrialba, Cartago, Costa Rica | Sugarcane | KX931059 |
| X. coxi | Hinojos, Huelva province, Spain | Carob tree | KC567175 |
| X. dentatum | Czech Republic | Carpinus betulus and Acer platanoides | EU781538 |
| X. diversicaudatum | – | – | EF538755 |
| X. diversicaudatum | Marchegg, Austria | – | JQ780366 |
| X. elongatum | China | – | EF140790 |
| X. floridae | Florida, USA | – | DQ299507 |
| X. gersoni | Almonte, Huelva province, Spain | Eucalyptus | KC567180 |
| X. georgianum | Florida, USA | – | DQ299497 |
| X. globosum | Valdeinfierno in the Los Alcornocales Regional Park, Alcalá de los Gazules, Cádiz province, southern Spain | Black alder, Alnus glutinosa L. Gaertn., and river bank grapevine, Vitis riparia | GU549474 |
| X. granatum | Saveh, Markazi province, Iran | Pomegranate trees (Punica granatum L.) | JQ240273 |
| X. hangzhouense | Hangzhou, Zhejiang Province, China | Magnolia grandiflora L. | MF538772 |
| X. herakliense | Vathy Rema, Heraklion province, Crete, Greece | Olive tree (Olea europaea subsp. sylvestris) | KM586345 |
| X. herakliense | Vathy Rema, Heraklion province, Crete, Greece | Olive tree (Olea europaea subsp. sylvestris) | KM586346 |
| X. herakliense | Agiofarago, south west Heraklion province, Crete, Greece | Olive | KM586347 |
| X. herakliense | Agiofarago, south west Heraklion province, Crete, Greece | Olive | KM586348 |
| X. herakliense | Agiofarago, south west Heraklion province, Crete, Greece | Olive | KM586349 |
| X. herakliense | Agiofarago, south west Heraklion province, Crete, Greece | Olive | KM586350 |
| X. herakliense | Hersonisos, northeast Heraklion province, Crete, Greece | Olive (Olea europaea subsp. europaea L.) | KM586351 |
| X. herakliense | Hersonisos, northeast Heraklion province, Crete, Greece | Olive (Olea europaea subsp. europaea L.) | KM586352 |
| X. hispanum | Andujar, Jaen province, Spain | Cistus albidus L. | GU725074 |
| X. hispidum | Bollullos par del Condado, Huelva province, Spain | Grapevine (Vitis vinifera L.) | HM921346 |
| X. hunaniense | Shenzhen, China | – | KP793046 |
| X. hunaniense | Shenzhen, China | – | KP793048 |
| X. index | Córdoba province, Spain | Grapevine | HM921398 |
| X. index | Kentri, Greece | Olive | KJ802882 |
| X. index | Córdoba province, Spain | Grapevine | HM921399 |
| X. index | Córdoba province, Spain | Grapevine | HM921400 |
| X. index | Córdoba province, Spain | Grapevine | HM921401 |
| X. index | Cádiz province, Spain | Grapevine | HM921402 |
| X. index | Roodghat area, Sufiyan, East-Azarbaijan province, northwest of Iran | Apple (Malus domestica L.) variety Red delicious | MH879782 |
| X. ingens | Chogha Kaboud village, Harsin, Kermanshah province, Iran | Astragalus sp. | KJ956388 |
| X. insigne | – | – | AY601619 |
| X. israeliae | Roufas, Greece | Olive | KJ802883 |
| X. israeliae | Agiofarago, Greece | Wild olive | KJ802884 |
| X. italiae | Cabra, Córdoba province, Spain | Grapevine | KC567182 |
| X. italiae | AY601613 | ||
| X. iznajarense | Iznaajar, Cordoba province, Spain | Cultivated olive | KX244892 |
| X. japonicum | Japan | Podocarpus macrophyllus L. | KY131240 |
| X. laevistriatum | Florida, USA | – | DQ299505 |
| X. lambertii | India | – | HM163211 |
| X. lupini | Bollullos par del Condado, Huelva province, Spain | Grapevine (Vitis vinifera L.) | HM921352 |
| X. lupini | Hinojos, Huelva province, Spain | Grapevine | KC567183 |
| X. macroacanthum | Southern Italy | Olive orchards | HF546080 |
| X. macrodora | La Granjuela, Córdoba province, Spain | Cultivated olive | KU171040 |
| X. mengibarense | Mengibar, Jaen province, Spain | Cultivated olive | KX244894 |
| X. meridianum | Sbitla, Kasserine, Tunisia | Cultivated olive | KX062679 |
| X. naturale | Florida, USA | – | DQ299515 |
| X. nuragicum | Marchena, Seville province, Spain | Olea europaea sp. europaea L. | GU725071 |
| X. nuragicum | Puente Genil, Cordoba province, Spain | Vitis vinifera L. | GU725067 |
| X. oleae | Tarifa, Cádiz province, Spain | Wild olive | KU171037 |
| X. poasense | Toro Amarillo, Valverde Vega, San Carlos Alajuela, Costa Rica | Eucalyptus, cypress and fountain grass | MF461347 |
| X. pseudocoxi | Alcaracejos, Cordoba province, Spain | Wild olive | KX244915 |
| X. pyrenaicum | Cahors, Midi-Pyrenees province, France | Vitis vinifera L. | GU725073 |
| X. rivesi | Bollullos par del Condado, Huelva province, Spain | Grapevine (Vitis vinifera L.) | HM921358 |
| X. robbinsi | Sbitla, Kasserine, Tunisia | Cultivated olive | KX062683 |
| X. robbinsi | Abida, Kairouan, Tunisia | Cultivated olive | KX062685 |
| X. santos | – | – | AY601587 |
| X. savanicola | – | – | AY601620 |
| X. setariae | – | – | AY601621 |
| X. sphaerocephalum | Coto Rios, Jaen province, Spain | Quercus faginea L. | GU725076 |
| X. tarjanense | DQ299511 | ||
| X. tica | Chirraca, San Ignacio de Acosta, San José, Costa Rica | Grapevine | KY623485 |
| X. turcicum | Sanlúcar de Barrameda, Cádiz province, Spain | Grapevine | KC567185 |
| X. turdetanensis | Sanlúcar de Barrameda, Cádiz province, Spain | Stone pine | KC567186 |
| X. vuittenezi | Czech Republic | – | EF614266 |
| X. vuittenezi | – | – | AY601614 |
| X. vulgare | Florida, USA | – | DQ299514 |
| X. zagrosense | Madavan village, Kohgiluyeh and Boyer-Ahmad province, Iran | Grasses | JN153101 |
Figure 1
Xiphinema barooghii n. sp. (A) Amphidial pouch; (B) Entire body; (C) Neck region; (D) Female tail; (E) Anterior end; (F) Posterior genital branch; (G–J) Tail of juveniles from J1–J4, respectively.
Figure 2
Xiphinema barooghii n. sp. Female (A, B) anterior end; (C, G) uterine differentiation spines; (D) entire body; (E) reproductive system; (F) vagina; (H) tail; (I) caudal pores in lateral optical view; (J) amphidial pouch; (K) pharyngeal expansion. (Scale bars: A–K = 10 μm, D = 70 μm).
Figure 3
Juvenile stages of Xiphinema barooghii n. sp. Anterior region and tail shape of (A, B) first; (C, D) second; (E, F) third and (G, H) fourth juvenile stages, respectively (Scale bars = 10 μm).
Figure 4
Xiphinema barooghii n. sp. Graph of correlation of functional and replacement odontostyle to body length in all developmental stages from Jl to mature females.
Figure 5
Bayesian tree inferred under the GTR + I + G model from 28S rDNA D2–D3 expansion domains of X. barooghii n. sp. and X. index (−lnL = 9,085.8555; AIC = 18,191.7109; freqA = 0.2402; freqC = 0.2341; freqG = 0.2885; freqT = 0.2373; R(a) = 1.0503; R(b) = 2.8325; R(c) = 2.6784; R(d) = 0.5047; R(e) = 4.0878; R(f) = 1.0000). Posterior probabilities are given for appropriate clades. Newly obtained sequences are indicated by bold letters.
Figure 6
(A–E) Xiphinema index Thorne and Allen, 1950, (A) Anterior end; (B) Tubular part of uterus; (C) Vagina; (D) Pars dilatata oviductus; (E) Tail, (F–H) X. pachtaicum (Thlaganov, 1938) Kirjanova, 1951, (F) Anterior end; (G) Anterior genital branch; (H) Tail, (I–N) X. vuittenezi Luc, Lima, Weischer and Flegg, 1964, (I) Anterior end; (J, L) Uterine differentiation spines; (K) Vagina; (M, N) Tail. (Scale bars = 10 Μm).
Table 4
Morphometrics of the Iranian populations of Xiphinema species. All measurements are in μm (except L in mm), and in the form: mean ± s.d. (range).
| X. index | X. pachtaicum | X. vuittenezi | |
|---|---|---|---|
| Characters | Female | Female | Female |
| n | 5 | 5 | 6 |
| L | 2.98 ± 0.18 (2.68–3.13) | 2.04 ± 0.08 (1.95–2.17) | 3.51 ± 0.16 (3.25–3.76) |
| a | 55.0 ± 4.2 (50.0–60.0) | 61.0 ± 8.7 (52.0–74.0) | 69.0 ± 5.0 (63.0–78.0) |
| b | 6.7 ± 0.3 (6.3–7.3) | 6.7 ± 0.6 (6.3–7.8) | 7.6 ± 0.1 (7.3–7.9) |
| c | 76.0 ± 2.4 (74.0–80.0) | 69.0 ± 3.6 (64.0–73.0) | 89.0 ± 3.6 (77.0–95.0) |
| c′ | 1.04 ± 0.05 (1.00–1.10) | 1.50 ± 0.10 (1.40–1.70) | 1.10 ± 0.08 (1.00–1.20) |
| V | 37.0 ± 0.7 (36.0–38.0) | 54.0 ± 1.2 (53.0–56.0) | 49.0 ± 0.4 (47.0–50.0) |
| Lip region diam. | 13.0 ± 0.8 (12.0–14.0) | 9.4 ± 0.5 (9.0–10.0) | 13.0 ± 0.7 (12.0–14.0) |
| Odontostyle length | 121.0 ± 2.7 (118.0–125.0) | 83.0 ± 2.6 (81.0–87.0) | 122.0 ± 3.7 (118.0–128.0) |
| Odontophore length | 70.0 ± 1.7 (69.0–73.0) | 50.0 ± 3.3 (44.0–54.0) | 68.0 ± 4.1 (51.0–75.0) |
| Spear length | 192.0 ± 2.7 (189.0–195.0) | 133.0 ± 2.7 (130.0–137.0) | 191.0 ± 6.8 (175.0–200.0) |
| Oral aperture to guide ring | 114.0 ± 4.3 (106.0–119.0) | 70.0 ± 3.6 (68.0–77.0) | 108.0 ± 4.3 (100.0–113.0) |
| Pharynx length | 437 ± 11 (421–450) | 303 ± 20 (250–328) | 457 ± 11 (443–475) |
| Pharyngeal bulb length | 99.0 ± 6.4 (87.0–110.0) | 77.0 ± 4.6 (72.0–84.0) | 114 ± 10 (100–131) |
| Body diam. at phar. base | 47.0 ± 3.4 (43.0–52.0) | 29.0 ± 2.2 (26.0–32.0) | 41.0 ± 2.7 (37.0–45.0) |
| mid-body | 54.0 ± 3.8 (45.0–59.0) | 33.0 ± 2.4 (28.0–37.0) | 49.0 ± 5.3 (41.0–56.0) |
| anus | 35.0 ± 3.5 (31.0–40.0) | 19.0 ± 1.4 (17.0–21.0) | 35.0 ± 2.1 (32.0–38.0) |
| G1 | 13.2 ± 0.4 (13.0–14.0) | 12.0 ± 1.2 (11.0–14.0) | 12.6 ± 0.3 (12–13) |
| G2 | 12.0 ± 1.3 (11.0–14.0) | 12.0 ± 1.9 (10.0–14.0) | 12.0 ± 0.8 (11.0–13.0) |
| Prerectum length | 320 ± 46 (250–381) | 168 ± 17 (134–187) | 496 ± 58 (431–575) |
| Rectum length | 30.0 ± 1.9 (27.0–32.0) | 24.0 ± 3.5 (23.0–28.0) | 31.0 ± 1.2 (29.0–33.0) |
| Tail length | 39.0 ± 0.9 (36.0–41.0) | 29.0 ± 1.1 (28.0–31.0) | 39.0 ± 1.4 (38.0–41.0) |
| Hyaline part of tail | 17.0 ± 1.4 (15.0–19.0) | 10.0 ± 0.8 (9.0–11.0) | 14.0 ± 1.8 (12.0–16.0) |