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An integrative approach to the study of Helicotylenchus (Nematoda: Hoplolaimidae) Colombian and Brazilian populations associated with Musa crops

Donald Riascos-Ortiz
Donald Riascos-Ortiz
, 
Ana Teresa Mosquera-Espinosa
Ana Teresa Mosquera-Espinosa
, 
Francia Varón De Agudelo
Francia Varón De Agudelo
, 
Claudio Marcelo Gonçalves de Oliveira
Claudio Marcelo Gonçalves de Oliveira
 und 
Jaime Eduardo Muñoz-Florez
Jaime Eduardo Muñoz-Florez
   | 06. Juli 2020
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Online veröffentlicht: 06. Juli 2020
Seitenbereich: 1 - 19
Eingereicht: 31. März 2020
DOI: https://doi.org/10.21307/jofnem-2020-054
Schlüsselwörter
© 2020 Donald Riascos-Ortiz et al., published by Sciendo.
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Figure 1:

Helicotylenchus multicinctus. A: Habitus post-mortem of a female, B and C: Anterior region of female body, D and E: Posterior region of female body, F: Medium region of female body, G: Posterior region of male body. vu = Vulva, dgo = Dorsal esophageal Gland Orifice, an = Anus, lf = Lateral field, sptc = Spermatheca, spc = Spicule.
Helicotylenchus multicinctus. A: Habitus post-mortem of a female, B and C: Anterior region of female body, D and E: Posterior region of female body, F: Medium region of female body, G: Posterior region of male body. vu = Vulva, dgo = Dorsal esophageal Gland Orifice, an = Anus, lf = Lateral field, sptc = Spermatheca, spc = Spicule.

Figure 2:

Helicotylenchus dihystera, H. erythrinae, and H. californicus. A: Habitus post mortis of a female in H. dihystera, B: Anterior region of female body in H. dihystera, C: Posterior region of female body in H. dihystera, D: Habitus post mortis of a female in H. erythrinae, E: Anterior region of female body in H. erythrinae, F: Posterior region of female body in H. erythrinae, G: Spermatheca of female in H. erythrinae, H: Habitus post mortis of female in H. californicus, I and J: Anterior region of female body in H. californicus, K: Posterior region of female body in H. californicus with short ventral projection and sharply pointed tail, L: Posterior region of female body in H. californicus with short ventral projection and blunt tail, M: Posterior region of male body in H. californicus.
Helicotylenchus dihystera, H. erythrinae, and H. californicus. A: Habitus post mortis of a female in H. dihystera, B: Anterior region of female body in H. dihystera, C: Posterior region of female body in H. dihystera, D: Habitus post mortis of a female in H. erythrinae, E: Anterior region of female body in H. erythrinae, F: Posterior region of female body in H. erythrinae, G: Spermatheca of female in H. erythrinae, H: Habitus post mortis of female in H. californicus, I and J: Anterior region of female body in H. californicus, K: Posterior region of female body in H. californicus with short ventral projection and sharply pointed tail, L: Posterior region of female body in H. californicus with short ventral projection and blunt tail, M: Posterior region of male body in H. californicus.

Figure 3:

Populations of H. multicinctus (HM), H. dihystera (HD), H. erythrinae (HE), and H. californicus (HC) from Colombia and Brazil can be assigned to its corresponding species based on morphometric data. The two first axes of a principal components analysis (PCA) are shown. HM1 to HM2 from Colombia and HM3 to HM4 from Brazil; HD1 to HD3 from Colombia; HE1 to HE3 from Colombia; and HC1 from Colombia and HC2 from Brazil.
Populations of H. multicinctus (HM), H. dihystera (HD), H. erythrinae (HE), and H. californicus (HC) from Colombia and Brazil can be assigned to its corresponding species based on morphometric data. The two first axes of a principal components analysis (PCA) are shown. HM1 to HM2 from Colombia and HM3 to HM4 from Brazil; HD1 to HD3 from Colombia; HE1 to HE3 from Colombia; and HC1 from Colombia and HC2 from Brazil.

Figure 4:

Dendrogram obtained by a conglomerates analysis to classify the Colombian and Brazilian populations of H. multicinctus (HM), H. dihystera (HD), H. erythrinae (HE), and H. californicus (HC). HM1 to HM2 from Colombia and HM3 to HM4 from Brazil; HD1 to HD3 from Colombia; HE1 to HE3 from Colombia; and HC1 from Colombia and HC2 from Brazil.
Dendrogram obtained by a conglomerates analysis to classify the Colombian and Brazilian populations of H. multicinctus (HM), H. dihystera (HD), H. erythrinae (HE), and H. californicus (HC). HM1 to HM2 from Colombia and HM3 to HM4 from Brazil; HD1 to HD3 from Colombia; HE1 to HE3 from Colombia; and HC1 from Colombia and HC2 from Brazil.

Figure 5:

Maximum likelihood phylogeny of Helicotylenchus. The tree was estimated using the D2 to D3 expansion segment of 28S RNAr and 250 bootstraps under GTR + Γ model. The outgroup (Rotylenchus magnus) is shown in gray font; the sequences that were obtained in this study appear in bold typeface. Values at the nodes represent the bootstrap support. Were provided bootstrap support for nodes with values > 80. The scale represents the number of substitutions per site.
Maximum likelihood phylogeny of Helicotylenchus. The tree was estimated using the D2 to D3 expansion segment of 28S RNAr and 250 bootstraps under GTR + Γ model. The outgroup (Rotylenchus magnus) is shown in gray font; the sequences that were obtained in this study appear in bold typeface. Values at the nodes represent the bootstrap support. Were provided bootstrap support for nodes with values > 80. The scale represents the number of substitutions per site.

Figure 6:

Bayesian phylogeny of Helicotylenchus based on D2 to D3 expansion segment of 28S RNAr. The phylogeny is a consensus tree from a posterior distribution of 1,600 trees that were inferred under GTR + Γ model in MrBayes. The outgroup (Rotylenchus magnus) is shown in gray font; the sequences that were obtained in this study appear in bold typeface. Values at the nodes represent the posterior probability. Were provided posterior probabilities for nodes with values > 0.5. The scale represents the number of substitutions per site.
Bayesian phylogeny of Helicotylenchus based on D2 to D3 expansion segment of 28S RNAr. The phylogeny is a consensus tree from a posterior distribution of 1,600 trees that were inferred under GTR + Γ model in MrBayes. The outgroup (Rotylenchus magnus) is shown in gray font; the sequences that were obtained in this study appear in bold typeface. Values at the nodes represent the posterior probability. Were provided posterior probabilities for nodes with values > 0.5. The scale represents the number of substitutions per site.

Information of sequences D2 to D3 of ribosomal DNA downloaded from GenBank and obtained in the present study for Helicotylenchus.

Species name Location Plant-host GenBank accession number Reference or source
H. dihystera Colombia, Córdoba, Quindío Musa AAA (Banana) MT321729; MT321730 Present study
H. dihystera USA, Florida, Ft Lauderdale Schefflera arboricola HM014245 Subbotin et al. (2011)
H. dihystera USA, Florida, Goulds Bromeliads HM014246 Subbotin et al. (2011)
H. dihystera USA, Florida, Ft Pierce Ficus HM014247 Subbotin et al. (2011)
H. dihystera USA, Hawaii, Kawai Grasses HM014248 Subbotin et al. (2011)
H. dihystera USA, Georgia – HM014249 Subbotin et al. (2011)
H. dihystera USA, Hawaii, Kawai Grasses HM014250 Subbotin et al. (2011)
H. dihystera USA, Georgia – HM014251 Subbotin et al. (2011)
H. dihystera USA, California, Kern county Vitis vinifera KM506834 Subbotin et al. (2015)
H. dihystera USA, Texas (plant shipment) – KM506835 Subbotin et al. (2015)
H. dihystera USA, California, Merced Grasses KM506836 Subbotin et al. (2015)
H. dihystera China, Fujian Province Musa sp. KF486503 Xiao et al. (2014)
H. leiocephalus USA, Nebraska, Lincoln, Nine mile Prairie Amorpha canescens HM014268; HM014269 Subbotin et al. (2011)
H. pseudorobustus USA, Kansas, Konza Prairie, Manhattan Koeleria pyramidata HM014266; HM014267 Subbotin et al. (2011)
H. pseudorobustus New Zealand, MAF farm, Kaitoke Lolium perenne, Trifolium repens HM014278 Subbotin et al. (2011)
H. pseudorobustus New Zealand, Rotorua Lolium perenne HM014279; HM014280 Subbotin et al. (2011)
H. pseudorobustus China, Beijing – DQ328747 Subbotin et al. (2011)
H. pseudorobustus USA, California, Fresno – DQ328748 Subbotin et al. (2011)
H. pseudorobustus Italy, Ancona – DQ328750 Subbotin et al. (2011)
H. pseudorobustus Germany, Münster, BBA glasshouse – DQ328751 Subbotin et al. (2011)
Helicotylenchus spIV-2 USA, Florida, Gainesville, Winter garden Calathea sp. KM506844 Subbotin et al. (2015)
H. multicinctus Colombia, Calarcá, Quindío Musa AAA (Banana) MT321731 Present study
H. multicinctus Colombia, Rozo, Palmira, Valle del Cauca Musa AAB (Plantain) MT321732; MT321733; MT321734 Present study
H. multicinctus South Africa, Lambani Musa sp. HM014290; HM014291 Subbotin et al. (2011)
H. multicinctus USA, Florida, Ft. Pierce Ficus benjamina HM014292 Subbotin et al. (2011)
H. multicinctus Sudan Musa sp. DQ328745; DQ328746 Subbotin et al. (2011)
H. multicinctus China, Fujian Province Musa sp. KF443214 Xiao et al. (2014)
H. californicus Colombia, La Delfina, Buenaventura, Valle del Cauca Musa AAB (Plantain) MT321735; MT321736; MT321737; MT321738 Present study
H. erythrinae Colombia, La Celia, Risaralda Musa AAB (Plantain) MT321739 Present study
H. labiodiscinus USA, Kansas, Manhattan Poa pratensis HM014293 Subbotin et al. (2011)
H. labiodiscinus USA, Kansas, Manhattan Andropogon gerardii HM014294 Subbotin et al. (2011)
H. labiodiscinus USA, Kansas, Manhattan Schizachyrium scoparium HM014295 Subbotin et al. (2011)
H. martini South Africa, Lambani Grasses HM014304; HM014305 Subbotin et al. (2011)
H. brevis South Africa, North West Province Solanum mauritianum HM014299; HM014300 Subbotin et al. (2011)
H. vulgaris Italy, Ancona – DQ328759; DQ328760; DQ328761 Subbotin et al. (2011)
H. vulgaris USA, Kansas, University of Arkansas – FJ485650 Subbotin et al. (2011)

Morphometric data of H. dihystera and reference populations.

Species H. dihystera H. dihystera H. dihystera H. dihystera H. dihystera
Locality/publication Banana, Córdoba–Quindío–HD1 Plantain, Córdoba–Quindío–HD2 Sher (1961) Uzma et al. (2015) Wount and Yates
n = 10 n = 15 n = 12 n = not defined n = 10 n = 10
L 0.62 ± 0.08 (0.53-0.77) 0.61 ± 0.06 (0.48-0.69) 0.67 (0.61-0.86) 0.59-0.79 0.67 ± 0.05 (0.57-0.73) 0.71 ± 0.04 (0.61-0.75)
a 25.5 ± 1.94 (22.93-29.69) 24.0 ± 1.83 (20.50-28.13) 29.5 (26.0-34.0) 27-35 29.3 ± 2.21 (26.0-33.0) 29.5 ± 1.35 (27.0-32.0)
c 43.8 ± 8.36 (25.12-55.45) 45.3 ± 4.49 (39.0-56.3) 48.0 (40.0-65.0) 35- 49 46.0 ± 4.69 (37.0-53.0) 43.0 ± 4.67 (35.0-50.0)
c′ 1.0 ± 0.17 (0.80-1.31) 0.9 ± 0.07 (0.71-0.94) 1.0-1.3 0.8-1.2 1.11 ± 0.11 (1.0-1.3) 1.09 ± 0.11 (0.9-1.3)
V% 64.6 ± 1.19 (62.24-66.35) 64.5 ± 1.24 (61.94-66.12) 63.0 (60.0-66.0) 60-65 65 ± 1.32 (63.0-67.0) 63.0 ± 0.84 (61.0-64.0)
DGO 14.7 ± 1.38 (13.0-16.0) 14.9 ± 1.57 (13.0-17.0) – – 11.5 ± 1.63 (8.5-13.5) 10.0 ± 1.25 (7.0-11.0)
Stylet length 24.4 ± 0.97 (23.0-26.0) 23.8 ± 0.77 (23.0-25.0) 26.0 (24.5-27.5) 24-29 27.9 ± 1.08 (25.5-29.0) 26.1 ± 0.74 (25.0-27.0)
Number of head annuli 4.0 ± 0.0 (4.0-4.0) 4.0 ± 0.26 (4.0-5.0) 3.0-4.0 4-5 – –
Tail length 14.5 ± 3.06 (11.0-21.0) 13.5 ± 1.51 (12.0-16.0) – – 14.5 ± 1.48 (12.0-17.0) 16.7 ± 2.50 (12.0-21.0)
Number of tail annuli 8.0 ± 1.88 (5.0-12.0) 8.0 ± 0.68 (7.0-10.0) 8-12 6-12 – –
Position of phasmid 8.0 ± 0.99 (7.0-10.0) 9.0 ± 1.91 (6.0-11.0) 6-12 5-11 – –

Correlations between the first four component principals and the morphometric parameters of females in Helicotylenchus spp.

Vector Diagnostic character 1 2 3 4
1 L –0.25 0.21 0.02 0.66
2 a 0.09 –0.01 –0.57 0.35
3 c –0.34 –0.33 –0.01 0.02
4 c′ 0.36 0.28 –0.12 –0.11
5 V % –0.06 –0.48 –0.13 0.01
6 DGO –0.22 0.35 –0.25 –0.27
7 Stylet length –0.31 –0.05 –0.39 –0.03
8 Number of head annuli 0.01 0.05 0.61 0.07
9 Number of tail annuli 0.37 0.07 –0.09 0.33
10 Position of phasmid –0.29 0.31 –0.09 –0.40
11 Maximum body diameter –0.39 0.22 0.02 0.15
12 Tail length 0.32 0.35 –0.10 –0.05
13 Anal body diameter –0.24 0.37 0.17 0.22

Morphometric data of H. californicus and reference populations.

Species H. californicus H. californicus H. californicus H. californicus H. californicus
Locality/publication Plantain, Delfina–Buenaventura–HC1 n = 12 Banana, Brazil HC2 n = 19 Van Den Berg and Heyns (1975) n = 25 Uzma et al. (2015) n = not defined Sher (1966) n = 16
L 0.6 ± 0.05 (0.5-0.6) 0.6 ± 0.1 (0.5-0.7) 0.7 (0.6-0.8) 0.58-0.78 0.6 (0.5-0.7)
a 23.5 ± 1.0 (22.0-25.2) 24.6 ± 1.4 (21.5-26.6) 28.8 (23.4-35.0) 27-32 24.1 (21.1-26.2)
c 35.5 ± 4.7 (27.2-45.8) 34.9 ± 3.0 (30.3-40.2) 39.0 (30.8-53.0) 32.0-50.0 38.7 (31.2-48.1)
c′ 1.0 ± 0.1 (0.8-1.1) 1.1 ± 0.1 (1.0-1.3) 1.1 (0.7-1.5) 0.8-1.3 1.2 (0.9-2.1)
V% 62.1 ± 1.7 (59.3-64.8) 65.6 ± 3.0 (61.3-75.5) 63.0 (60.0-64) 59-64 64 (60-67)
DGO 11.4 ± 1.2 (10.0-14.0) 11.4 ± 2.4 (8.0-14.0) – – 10 (8-14)
Stylet length 22.4 ± 0.9 (20.0-23.0) 23.5 ± 1.0 (21.0-25.0) 24.1 (22.8-27.2) 24-27 27 (26-29)
Number of head annuli 4.7 ± 0.7 (4.0-6.0) 4.2 ± 0.5 (4.0-6.0) 3.0-5.0 4 5-7
Tail length 15.9 ± 1.0 (13.0-19.0) 16.5 ± 1.5 (14.0-20.0) 17.9 (15.1-25.0) – 16 (13-21)
Number of tail annuli 7.8 ± 1.1 (6.0-9.0) 7.8 ± 0.9 (6.0-9.0) 10.0-17.0 8 9 (6-12)
Position of phasmid 6.8 ± 1.3 (5.0-8.0) 6.0 ± 2.7 (2.0-8.0) 3.0-14.0 2 1-11

Morphometric data of H. erythrinae and reference populations.

Species H. erythrinae H. erythrinae H. erythrinae H. erythrinae H. erythrinae
Locality/publication Banana, Calarcá–Quindío (La Julia)–HE1 Plantain, Calarcá –Quindío (Resta)–HE2 Van Den Berg and Heyns (1975) Uzma et al. (2015) Wount and Yates
n = 15 n = 25 n = 7 n = not defined n = 10 n = 10
L 0.53 ± 0.1 (0.4-0.7) 0.6 ± 0.1 (0.46-0.68) 0.5 (04-0.6) 0.48-0.61 0.87 ± 0.06 0.69 ± 0.05
a 25.03 ± 2.0 (22.7-29.7) 25.90 ± 2.2 (22.86-30.91) 25.1 (21.1-26.7) 23.0-26.0 29.7 ± 1.64 (27.0-32.0) 28.2 ± 1.87 (24.0-30.0)
c 25.93 ± 4.1 (19.2-31.5) 28.09 ± 3.0 (21.82-32.94) 28.9 (23.3-30.3) 27.0-34.0 43.0 ± 5.99 (31.0 -51.0) 48.0 ± 10.55 (35.0-74.0)
c′ 1.46 ± 0.2 (1.1-1.7) 1.41 ± 0.15 (1.13-1.73) 1.4 (1.3-1.4) 1.0-1.6 1.13 ± 0.106 (1.0-1.3) 1.03 ± 0.206 (0.60-1.30)
V% 63.8 ± 1.8 (60.1-67.6) 63.7 ± 2.16 (60.82-68.54) 64.0 (61.0-67.0) 60.0-65.0 62.0 ± 2.85 (58.0-68.0) 63.0 ± 2.22 (59.0-65.0)
DGO 10.36 ± 2.6 (5.0-8.0) 12 ± 1.97 (8.0-15.0) – – 9.6 ± 2.07 (75.0-13.0) 9.1 ± 0.94 (7.0-10.0)
Stylet length 22.7 ± 1.0 (21.0-25.0) 22.8 ± 0.83 (21.0-24.0) 24.6 (21.7-26.8) 23.0-26.0 28.3 ± 1.23 (26.0-30.0) 27.9 ± 0.97 (25.5-29.0)
Number of head annuli 4.0 ± 0.0 (4.0-4.0) 4.0 ± 0.32 (3.0-5.0) 4.0 4.0-5.0 – –
Tail length 20.53 ± 2.2 (17.0-25.0) 20.65 ± 2.39 (17.0-26.0) 17.9 – 20.6 ± 2.8 (16.0-24.0) 14.7 ± 2.71 (9.0-18.0)
Number of tail annuli 10.0 ± 2.8 (7.0-17) 11.0 ± 1.01 (10.0-13.0) 10.0-14.0 6.0-12.0 13.4 ± 0.97 (12.0-15.0) 10.2 ± 2.25 (7.0-15.0)
Position of phasmid 6.0 ± 0.9 (4.0-7.0) 3.0 ± 1.01 (1.0-5.0) 9 4/2 – –

Morphometric data of H. multicinctus and reference populations.

Species H. multicinctus H. multicinctus H. multicinctus H. multicinctus H. multicinctus H. multicinctus
Locality/publication Plantain, Cordoba–Quindío–HM1 n = 19 Plantain, Rozo–Palmira–HM2 n = 20 Banana, Brazil HM3–* n = 24 Banana, Brazil 233–HM4 n = 21 Goodey (1940), Golden (1956) n = 2 Uzma et al. (2015) n = not defined
L 0.6 ± 0.1 (0.4–0.8) 0.6 ± 0.04 (0.5-0.7) 0.5 ± 0.05 (0.5-0.6) 0.5 ± 0.1 (0.4-0.6) 0.54 (0.46-0.68) 0.47-0.53
a 26.1 ± 2.8 (22.5-31.1) 24.4 ± 1.5 (22.1-27.4) 24.7 ± 1.9 (22.4-30.3) 24.5 ± 2.0 (21.2-27.9) 24.47 (23.8-28.5) 24.0-30.0
c 45.6 ± 5.1 (36.1-55.2) 44.6 ± 5.6 (36.5-59.8) 49.2 ± 7.0 (37.7-64.1) 50.7 ± 7.4 (39.6-69.6) 53.8 (48.0-63.0) 35.0-46.0
c′ 0.9 ± 0.1 (0.7-1.1) 0.9 ± 0.1 (0.7-1.0) 0.8 ± 0.1 (0.6-1.1) 0.8 ± 0.1 (0.4-1.0) 0.8-1.0 0.8-1.0
V% 68.4 ± 1.6 (65.9-71.7) 67.2 ± 1.7 (64.1-70.0) 68.9 ± 2.3 (65.0-73.1) 69.1 ± 1.1 (66.2-71.1) 69.0 (64.6-71.8) 65.0-69.0
DGO 8.6 ± 0.6 (8.0-10.0) 9.5 ± 0.5 (9.0-10.0) 9.1 ± 1.0 (7.0-11.0) 9.3 ± 1.1 (7.0-11.0) – –
Stylet length 23.4 ± 1.3 (21.0-26.0) 23.7 ± 0.7 (23.0-25.0) 23.5 ± 0.9 (22.0-25.0) 23.1 ± 0.8 (22.0-24.0) 20.0-24.0 22.0-24.0
Number of head annuli 4.0 ± 0.6 (3.0-5.0) 4.0 ± 0.5 (4.0-5.0) 4.0 ± 0.5 (4.0-5.0) 4.0 ± 0.0 (4.0-4.0) 3.0-5.0 3.0-4.0
Tail length 13.0 ± 1.9 (10.0-16.0) 12.9 ± 1.2 (10.0-15.0) 11.3 ± 1.7 (8.0-15.0) 10.5 ± 1.9 (7.0-15.0) – –
Number of tail annuli 9.0 ± 1.2 (7.0-12.0) 9.3 ± 1.3 (7.0-12.0) 8.0 ± 1.9 (5.0-12.0) 7.7 ± 1.5 (5.0-10.0) 6.0-13.0 6.0-12.0
Position of phasmid 3.0 ± 1.2 (2.0-6.0) 3.8 ± 1.0 (3.0-6.0) 5.0 ± 2.1 (2.0-7.0) 5.0 ± 1.2 (3.0-7.0) 1.0-6.0 2.0-6.0

Eigenvalues and percent total variance accounted for each principal component.

Principal component Eigenvalues Cumulative total % of Total variance Cum. % of total variance
1 4.92 4.92 37.88 37.88
2 3.75 8.68 28.88 66.76
3 2.16 10.84 16.63 83.39
4 1.04 11.88 7.99 91.39
5 0.35 12.23 2.70 94.09
6 0.29 12.52 2.22 96.31
7 0.22 12.74 1.68 97.99
8 0.16 12.89 1.23 99.22
9 0.06 12.95 0.43 99.65
10 0.04 12.99 0.29 99.94
11 0.01 13 0.06 100
12 1.5128E–7 13 1.16369E–6 100
13 –4.65844E–10 13 –3.58342E–9 100
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