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Characterization of Meloidogyne indica (Nematoda: Meloidogynidae) Parasitizing Neem in India, with a Molecular Phylogeny of the Species

Victor Phani
Victor Phani
, 
Satyapal Bishnoi
Satyapal Bishnoi
, 
Amita Sharma
Amita Sharma
, 
Keith G. Davies
Keith G. Davies
 oraz 
Uma Rao
Uma Rao
   | 17 paź 2018
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Data publikacji: 17 paź 2018
Zakres stron: 387 - 398
DOI: https://doi.org/10.21307/jofnem-2018-015
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© 2018 Victor Phani et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

Fig. 1

Plant symptoms (A–C) and morphology (D–K) of Meloidogyne indica infecting neem. A, Healthy neem seedlings; B, Infected neem seedlings devoid of lateral roots; C, Root gall with eggmass; D, Adult females; E, Anterior region of adult female; F and G, Perineal pattern morphology; H, Anterior region of male; I, Male tail; J, Anterior end of second-stage juvenile (J2); K, Second-stage juvenile tail (scale bar = D: 550 µm; E: 100 µm; H,I: 10 µm; J,K: 20 µm).
Plant symptoms (A–C) and morphology (D–K) of Meloidogyne indica infecting neem. A, Healthy neem seedlings; B, Infected neem seedlings devoid of lateral roots; C, Root gall with eggmass; D, Adult females; E, Anterior region of adult female; F and G, Perineal pattern morphology; H, Anterior region of male; I, Male tail; J, Anterior end of second-stage juvenile (J2); K, Second-stage juvenile tail (scale bar = D: 550 µm; E: 100 µm; H,I: 10 µm; J,K: 20 µm).

Fig. 2

Scanning electron microscopy photomicrographs of Meloidogyne indica. A, Female lip region; B, Male lip region; C, Male tail; D, Lateral field with lateral lines; E, Second-stage juvenile tail (scale bar in µm).
Scanning electron microscopy photomicrographs of Meloidogyne indica. A, Female lip region; B, Male lip region; C, Male tail; D, Lateral field with lateral lines; E, Second-stage juvenile tail (scale bar in µm).

Fig. 3

Citrus roots showing development of galls and eggmasses upon inoculation with the neem population of Meloidogyne indica. A, Citrus plant inoculated with neem population of M. indica; B, Healthy roots of citrus; C, Infected roots of citrus with galls and eggmasses.
Citrus roots showing development of galls and eggmasses upon inoculation with the neem population of Meloidogyne indica. A, Citrus plant inoculated with neem population of M. indica; B, Healthy roots of citrus; C, Infected roots of citrus with galls and eggmasses.

Fig. 4

Evolutionary relationship of Meloidogyne indica using ITS rRNA sequence. The evolutionary history was inferred by using the maximum likelihood method based on Kimura 2-parameter model. The bootstrap consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the analyzed taxa. Branches corresponding to partitions reproduced in less than 30% bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying neighbour-joining and BioNJ algorithms to a matrix of pairwise distances estimated using the maximum composite likelihood approach and then selecting the topology with superior log likelihood value (–1869.0466). A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories [+G, parameter = 1.0929]). The analysis involved 29 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 170 positions in the final dataset. Evolutionary analyses were conducted in MEGA6.
Evolutionary relationship of Meloidogyne indica using ITS rRNA sequence. The evolutionary history was inferred by using the maximum likelihood method based on Kimura 2-parameter model. The bootstrap consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the analyzed taxa. Branches corresponding to partitions reproduced in less than 30% bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying neighbour-joining and BioNJ algorithms to a matrix of pairwise distances estimated using the maximum composite likelihood approach and then selecting the topology with superior log likelihood value (–1869.0466). A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories [+G, parameter = 1.0929]). The analysis involved 29 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 170 positions in the final dataset. Evolutionary analyses were conducted in MEGA6.

Fig. 5

Evolutionary relationship of Meloidogyne indica using D2D3 expansion segment of 28S rRNA sequence. The evolutionary history was inferred by using the maximum likelihood method based on General Time Reversible model. The bootstrap consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the analyzed taxa. Branches corresponding to partitions reproduced in less than 30% bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying neighbour-joining and BioNJ algorithms to a matrix of pairwise distances estimated using the Maximum Composite Likelihood approach and then selecting the topology with superior log likelihood value (−4112.4125). A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories [+G, parameter = 0.4693]). The analysis involved 34 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 525 positions in the final dataset. Evolutionary analyses were conducted in MEGA6.
Evolutionary relationship of Meloidogyne indica using D2D3 expansion segment of 28S rRNA sequence. The evolutionary history was inferred by using the maximum likelihood method based on General Time Reversible model. The bootstrap consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the analyzed taxa. Branches corresponding to partitions reproduced in less than 30% bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying neighbour-joining and BioNJ algorithms to a matrix of pairwise distances estimated using the Maximum Composite Likelihood approach and then selecting the topology with superior log likelihood value (−4112.4125). A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories [+G, parameter = 0.4693]). The analysis involved 34 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 525 positions in the final dataset. Evolutionary analyses were conducted in MEGA6.

Fig. 6

Evolutionary relationship of Meloidogyne indica using mitochondrial COI sequences. The evolutionary history was inferred by using the maximum likelihood method based on General Time Reversible model. The bootstrap consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the analyzed taxa. Branches corresponding to partitions reproduced in less than 30% bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying neighbour-joining and BioNJ algorithms to a matrix of pairwise distances estimated using the maximum composite likelihood approach and then selecting the topology with superior log likelihood value (−2471.1920). A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories [+G, parameter = 0.5728]). The analysis involved 21 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 309 positions in the final dataset. Evolutionary analyses were conducted in MEGA6.
Evolutionary relationship of Meloidogyne indica using mitochondrial COI sequences. The evolutionary history was inferred by using the maximum likelihood method based on General Time Reversible model. The bootstrap consensus tree inferred from 1,000 replicates is taken to represent the evolutionary history of the analyzed taxa. Branches corresponding to partitions reproduced in less than 30% bootstrap replicates are collapsed. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1,000 replicates) is shown next to the branches. Initial tree(s) for the heuristic search were obtained automatically by applying neighbour-joining and BioNJ algorithms to a matrix of pairwise distances estimated using the maximum composite likelihood approach and then selecting the topology with superior log likelihood value (−2471.1920). A discrete Gamma distribution was used to model evolutionary rate differences among sites (five categories [+G, parameter = 0.5728]). The analysis involved 21 nucleotide sequences. All positions containing gaps and missing data were eliminated. There were a total of 309 positions in the final dataset. Evolutionary analyses were conducted in MEGA6.

Morphometrics for Meloidogyne indica infecting neem and citrus. All linear measurements are in micrometer and in the form of mean ± SD.

Neem population Citrus population (After Whitehead, 1968)
Character J2 Male Female J2 Female
n 20 15 30 25 8
L 484 ± 31.5 (430–520) 1253 ± 80 (1180–1380) 653 ± 92.2 (450–790) 414 ± 4.5 (381–448) –
Body width 18 ± 1.5 (16.77–21.15) 28 ± 4 (24.55–34.66) 408 ± 75 (325–550) – –
A 26.68 ± 1.9 (24.20–29.87) 44.89 ± 3.5 (39.81–48.06) 1.60 ± 0.3 (1.38–2.10) – –
Stylet length 13.8 ± 0.1 (13.57–14.21) 16.3 ± 0.4 (15.90–17.08) 13.7 ± 0.4 (13.32–14.18) 12 ± 0.9 (10–14) 14 (12–16)
DGO 2.8 ± 0.2 (2.45–3.25) 3.1 ± 0.1 (2.92–3.30) 2.9 ± 0.3 (2.49–3.67) – 3 (2–4)
Head-metacorpus 50 ± 2.3 (46.45–53.02) 73 ± 4.1 (68.70–78.14) – – –
Head-oesophageal gland 138 ± 4.8 (129.97–144.65) – – – –
b′ 3.5 ± 0.1 (3.10–3.65) – – – –
c 26.2 ± 1.2 (24.15–27.65) – – 24.9 ± 1.36 (21.2–31) –
c′ 1.6 ± 0.1 (1.52–1.91) – – 1.57 ± 0.012 (1.06–1.78) –
Tail length 18 ± 0.6 (17.50–19.50) – – 16.8 ± 1.88 (13–20.1) –
Anal body width 11.1 ± 1.0 (9.85–12.45) – – – –
Spicule – 26 ± 0.6 (25.90–27.50) – – –

List of primers used for polymerase chain reaction amplification in this study.

Primer name Gene Sequence References
V5367 ITS 5′-TTGATTACGTCCCTGCCCTTT-3′ Vrain et al. (1992)
26S ITS 5′-TTTCACTCGCCGTTACTAAGG-3′ Vrain et al. (1992)
D2A LSU 5′-ACAAGTACCGTGAGGGAAAGTTG-3′ Castillo et al. (2003)
D3B LSU 5′-TCGGAAGGAACCAGCTACTA-3′ Castillo et al. (2003)
JB3 COI 5′-TTTTTTGGGCATCCTGAGGTTTAT-3′ Bowles et al. (1992)
JB5 COI 5′-AGCACCTAAACTTAAAACATAATGAAAATG-3′ Derycke et al. (2005)

List of GenBank accession numbers used in phylogenetic analyses (** Not found in NCBI database).

Species ITS rRNA D2D3 28S rRNA COI mtDNA
Meloidogyne arabicida ** KF993624 **
Meloidogyne africana ** ** KY433441
Meloidogyne arenaria AF387092 JX987332 JX683705
Meloidogyne artiellia KC545880 AY150369 KU517173
Meloidogyne baetica AY150366 AY150367 **
Meloidogyne camelliae JX912885 KF542869 KM887148
Meloidogyne chitwoodi AY281852 AF435802 KU517168
Meloidogyne christiei KR082319 KR082317 **
Meloidogyne dunensis EF612711 EF612712 **
Meloidogyne duytsi ** ** KU517177
Meloidogyne enterolobii KM046989 KJ146862 KT936633
Meloidogyne ethiopica KF482366 KF482372 **
Meloidogyne exigua ** AF435795 **
Meloidogyne fallax AY281853 KC241969 KU517182
Meloidogyne graminicola KM111531 KJ728847 KY250093
Meloidogyne graminis JN157866 JN019326 **
Meloidogyne hapla EU908052 DQ145641 JX683719
Meloidogyne haplanaria ** ** KU174206
Meloidogyne hispanica EU443613 EU443607 JX683712
Meloidogyne ichinohei ** EF029862 KY433448
Meloidogyne incognita KJ739707 JX100425 JX683696
Meloidogyne indica KC311146 MF680038 MF662179
Meloidogyne inornata KF482368 KF482374 **
Meloidogyne izalcoensis ** KF993621 **
Meloidogyne javanica KJ739709 KC953092 JX683711
Meloidogyne konaensis ** AF435797 **
Meloidogyne lopezi ** KF993616 **
Meloidogyne luci KF482365 KF482371 **
Meloidogyne mali JX978228 KF880398 KU517175
Meloidogyne marylandi JN157854 JN019333
Meloidogyne minor KC241953 JN628436 KU517178
Meloidogyne naasi KJ934132 KC241979 KU517170
Meloidogyne panyuensis ** ** **
Meloidogyne paranaensis ** AF435799 **
Meloidogyne silvestris EU570216 EU570214 **
Meloidogyne spartelensis KP896294 KP895293 KP997301
Meloidogyne thailandica AY858795 EU364890 **
Meloidogyne trifoliophila JX465593 AF435801 **
Pratylenchus vulnus FJ713011 EU130885 KX349427
Hirschmanniella oryzae DQ309588 JX291142 **
Tylenchorhynchus leviterminalis EF030984 KJ475548 **
Heterodera glycines HM370421 GU595446 **
Radopholus similis KJ845638 JN091964 KX349430
Heterotheca mucronata ** ** KR819278
Tylenchorhynchus sp ** ** KY639376
eISSN:
2640-396X
Język:
Angielski
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