New Hosts and Records in Portugal for the Root-Knot Nematode Meloidogyne luci

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New Hosts and Records in Portugal for the Root-Knot Nematode Meloidogyne luci

Duarte Santos / António Correia / Isabel Abrantes / Carla Maleita *

Keywords : Cordyline australis , Esterase phenotype, Molecular biology, Oxalis corniculata , Plant-parasitic nematodes

Citation Information : Journal of Nematology. Volume 51, Pages 1-4, DOI: https://doi.org/10.21307/jofnem-2019-003

License : (CC-BY-4.0)

Received Date : 25-January-2019 / Published Online: 04-June-2019

ARTICLE

ABSTRACT

Graphical ABSTRACT

Several species of the genus Meloidogyne (root-knot nematodes, RKN) have been reported in Portugal: M. arenaria (Neal, 1889) Chitwood, 1949; M. chitwoodi Golden et al., 1980; M. hapla Chitwood, 1949; M. hispanica Hirschmann, 1986; M. incognita (Kofoid and White, 1919) Chitwood, 1949; M. javanica (Treub, 1885) Chitwood, 1949; and M. lusitanica Abrantes and Santos, 1991 (Abrantes et al., 2008; Conceição et al., 2009). In 2013, the tropical RKN, M. luci Carneiro et al., 2014, was detected in a potato field near Coimbra, Portugal (Maleita et al., 2018). Meloidogyne luci, added to the European Plant Protection Organization Alert List in 2017, was also found parasitizing maize (Zea mays L.) and kiwi (Actinidia spp.) in Greece; and tomato (Solanum lycopersicum L.) in Italy and Slovenia (Širca et al., 2004; Conceição et al., 2012; Maleita et al., 2012). In Brazil, Iran, Chile, Guatemala, and Turkey, M. luci has been found associated with several important vegetable plants and fruit tree species (Aydınlı et al., 2013; Carneiro et al., 2014; Bellé et al., 2016; Janssen et al., 2016; Machado et al., 2016). Currently, there are about 26 different plant species recognized as hosts for M. luci (EPPO, 2017). Because of its morphological resemblance to M. ethiopica Whitehead, 1968 and similar esterase phenotype, M. luci might have been misidentified as M. ethiopica in a number of surveys. Therefore, it is highly probable that this RKN has an even broader host range and distribution than is currently known. In December 2017, root galls with egg masses caused by a RKN were observed on the ornamental plant Cordyline australis (Forst f.) Hook. F (Ca) in Figueira da Foz, and the weed Oxalis corniculata L. (Oc), and tomato (Sl) in Montemor-o-Velho, all in Coimbra district. Egg masses were handpicked from infected roots of each plant and used to establish cultures of each isolate (Ca, Oc, and Sl) on tomato cv. Coração-de-Boi. Females were used to assess the esterase isoenzyme phenotype of each isolate to identify the species. The esterase phenotype from young egg-laying females protein extracts of the three isolates exhibited three bands of esterase activity (Rm: 0.38; 0.43; 0.48) (Fig. 1) corresponding to the M. luci L3 phenotype (Maleita et al., 2018). A M. javanica isolate (J3, Rm: 0.38; 0.45; 0.49) was used as reference isolate to determine the relative position of M. luci esterase bands (Fig. 1). Molecular identification was performed by amplification and sequencing of the cytochrome oxidase subunit I (COI) of mitochondrial DNA (mtDNA) region of one isolate of each location (Ca and Oc) using the primers JB3 (5′-TTTTTTGGGCATCCTGAGGTTTAT-3′) and 2R5 (5′-YTRWYCTTAAATCTAAATKMGTATG-3′) (Kiewnick et al., 2014). As no differences were observed between the sequences, the mtDNA region between cytochrome oxidase subunit II and 16S rRNA (mtDNA COII/16S rRNA) genes was only amplified and sequenced for Ca isolate using primers C2F3 (5′-GGTCAATGTTCAGAAATTTGTGG-3′) and MRH106 (5′-AATTTCTAAAGACTTTTCTTAGT-3′) (Maleita et al., 2018). DNA sequences were compared with available Meloidogyne species sequences in databases (Fig. 2). The length of all sequences of Meloidogyne spp. was set to 358 and 1,532 bp to mtDNA COI and mtDNA COII/16S rRNA regions, respectively, by removing several nucleotides to obtain a common start and end point. Phylogenetic analysis of mtDNA COI region was not very robust in differentiating M. luci from M. ethiopica (Fig. 2A), as also stated by Powers et al. (2018) for the most common RKN species (M. arenaria, M. incognita, and M. javanica). The Portuguese Oc and Ca sequences differed by only one nucleotide position from M. ethiopica, considering the 358 bp. Meloidogyne luci mtDNA COI sequence from Guatemala (KU372171.1) is similar to M. ethiopica (KU372162.1). On the other hand, the mtDNA COII/16S rRNA region differentiate these two closely related RKN species and proved to be useful for analyzing their relationship (Stare et al., 2017). Phylogenetic analysis revealed that mtDNA COII/16S rRNA sequences determined here formed a single cluster with all M. luci isolates (89% bootstrap), confirming the presence of M. luci (Fig. 2B). The mtDNA COII/16S rRNA sequence of Ca isolate and the other M. luci sequences were similar, with four to seven differences in alignment, while Ca M. luci sequence differed by 11 to 12 positions from M. ethiopica sequences. Sequences were submitted to GenBank database under the accession numbers MK190952 (isolate Ca) and MK190953 (isolate Oc) for mtDNA COI and MK190954 (isolate Ca) for mtDNA COII/16S rRNA genes. To our knowledge, this is the first report of M. luci infecting C. australis and O. corniculata. The detection of M. luci in two new locations (Figueira da Foz and Montemor-o-Velho) can be an indication that this nematode species could already be established and widespread in Portugal. Furthermore, these results draw attention to the importance of governmental inspections and the use of clean soil in nurseries. If ornamental plants, such as C. australis, were grown in infested soil, this will aid the transfer of plant-parasitic nematodes to new regions and/or other suitable hosts, with potential impact on economically important crops. Therefore, a survey for evaluation of M. luci distribution in Portugal is needed to decrease the risk of spread and to determine its potential economic impact.

Figure 1:

Esterase phenotypes of protein homogenates from five egg-laying females of Meloidogyne species isolates. C – M. luci (positive control); 1 – M. ethiopica isolate from Brazil; J3 – M. javanica (reference isolate); 2 – M. luci (Cordyline australis); 3 – M. luci (Solanum lycopersicum) and 4 – M. luci (Oxalis corniculata).

10.21307_jofnem-2019-003-f001.jpg
Figure 2:

Phylogenetic relationship of Meloidogyne spp. sequences based on the alignment of sequences of cytochrome oxidase subunit I (A) and cytochrome oxidase subunit II (B) of mitochondrial DNA with available sequences of other Meloidogyne species. The phylogenetic tree was generated in MEGA7 using the Neighbour-Joining method. The percentage of replicate trees in which the associated Meloidogyne spp. clustered together in the bootstrap test (500 replicates) is shown next to the branches. The evolutionary distances were computed using the Jukes-Cantor method. All positions with less than 95% site coverage were eliminated. That is, fewer than 5% alignment gaps, missing data, and ambiguous bases were allowed at any position. *Recently, reclassified as M. luci, according to Stare et al. (2017).

10.21307_jofnem-2019-003-f002.jpg

Acknowledgements

This research was supported by CFE, “Instituto do Ambiente, Tecnologia e Vida,” Chemical Process Engineering and Forest Products Research Centre, Department of Chemical Engineering, UC and FEDER funds through the Portugal 2020 (PT 2020) “Programa Operacional Factores de Competitividade 2020 (COMPETE 2020)” and by “Fundação para a Ciência e a Tecnologia (FCT, Portugal),” under contracts UID/BIA/04004/2013, PEst-C/EQB/UI0102/2013, POCI-01-0145-FEDER-031946 (Ref. PTDC/ASP-PLA/31946/2017), POCI-01-0145-FEDER-029392 (Ref. PTDC/ASP-PLA/29392/2017) and Project ReNATURE – Valorization of the Natural Endogenous Resources of the Centro Region (Centro2020, Centro-01-0145-FEDER-000007). Carla Maleita (SFRH/BPD/85736/2012) acknowledges FCT for granted fellowships, financed by “Ministério da Educação e Ciência” national funding and by the European Social Funds through “Programa Operacional Capital Humano.”

References


  1. Abrantes, I. M. de O. and Santos, M. S. N. de A. . 1991. Meloidogyne lusitanica n. sp. (Nematoda:Meloidogynidae), a root-knot nematode parasitizing olive tree (Olea europaea L.). Journal of Nematology 23: 210–224.
  2. Abrantes, I. M. de O. , Santos, M. C. V. dos , Conceição, I. L. P. M. da , Santos, M. S. N. de A. and Vovlas, N. . 2008. Root-knot and other plant-parasitic nematodes associated with fig trees in Portugal. Nematologia Mediterranea 36: 131–136.
  3. Aydınlı, G. , Mennan, S. , Devran, Z. , Širca, S. and Urek, G. . 2013. First report of the root-knot nematode Meloidogyne ethiopica on tomato and cucumber in Turkey. Plant Disease 97: 1262.
  4. Bellé, C. , Brum, D. , Groth, M. Z. , Barros, D. R. , Kaspary, T. E. , Schafer, J. T. and Gomes, C. B. . 2016. First report of Meloidogyne luci parasitizing Glycine max in Brazil. Plant Disease 100: 2174.
  5. Carneiro, R. M. D. G. , Correa, V. R. , Almeida, M. R. A. , Gomes, A. C. M. M. , Deimi, A. M. , Castagnone-Sereno, P. and Karssen, G. . 2014. Meloidogyne luci n. sp. (Nematoda: Meloidogynidae), a root-knot nematode parasitising different crops in Brazil, Chile and Iran. Nematology 16: 289–301, available at: https://doi.org/10.1163/15685411-00002765.
  6. Chitwood, B. G. . 1949. Root-knot nematodes - part I. A revision of the genus Meloidogyne Göldi, 1887. Proceedings of the Helminthological Society of Washington 16: 90–104.
  7. Conceição, I. L. P. M. da , Cunha, M. J. M. da , Feio, G. , Correia, M. , Santos, M. C. V. dos , Abrantes, I. M. de O. and Santos, M. S. N. Dde A. . 2009. Root-knot nematodes, Meloidogyne spp., on potato in Portugal. Nematology 11: 311–313, available at: https://doi.org/10.1163/156854109X415515.
  8. Conceição, I. L. , Tzortzakakis, E. A. , Gomes, P. , Abrantes, I. and da Cunha, M. J. . 2012. Detection of the root-knot nematode Meloidogyne ethiopica in Greece. European Journal of Plant Pathology 134: 451–457, available at: https://doi.org/10.1007/s10658-012-0027-0.
  9. EPPO . 2017. EPPO Alert List: addition of Meloidogyne luci together with M. ethiopica . EPPO Reporting Service, 2017/218, accessed from: https://gd.eppo.int/reporting/article-6186 (December 2018).
  10. Golden, A. M. , O'Bannon, J. H. , Santo, G. S. and Finley, A. M. . 1980. Description and SEM observations of Meloidogyne chitwoodi n. sp. (Meloidogynidae), a root-knot nematode on potato in the Pacific Northwest. Journal of Nematology 12: 319–27.
  11. Hirschmann, H. . 1986. Meloidogyne hispanica n. sp. (Nematoda: Meloidogynidae), the ‘Seville root-knotnematode’. Journal of Nematology 18: 520–32.
  12. Janssen, T. , Karssen, G. , Verhaeven, M. , Coyne, D. and Bert, W. . 2016. Mitochondrial coding genome analysis of tropical root-knot nematodes (Meloidogyne) supports haplotype based diagnostics and reveals evidence of recent reticulate evolution. Scientific Reports 6: 22591.
  13. Kiewnick, S. H. M. , van den Elsen, S. , van Megen, H. , Frey, J. E. and Helder, J. . 2014. Comparison of two short DNA barcoding loci (COI and COII) and two longer ribosomal DNA genes (SSU & LSU rRNA) for specimen identification among quarantine root-knot nematodes (Meloidogyne spp.) and their close relatives. European Journal of Plant Pathology 140: 97–110.
  14. Kofoid, C. A. , and White, W. A. . 1919. A new nematode infection of man. Journal of the American Medical Association 72: 567–69.
  15. Machado, A. C. Z. , Dorigo, O. F. , Carneiro, R. M. D. G. and De Araújo Filho, J. V. . 2016. Meloidogyne luci, a new infecting nematode species on common bean fields at Paraná State, Brazil. Helminthologia 53: 207–210, avalable at: https://doi.org/10.1515/helmin-2016-0014.
  16. Maleita, C. M. , Simões, M. J. , Egas, C. , Curtis, R. H. C. and Abrantes, I. M. D. O. . 2012. Biometrical, biochemical, and molecular diagnosis of Portuguese Meloidogyne hispanica isolates. Plant Disease 96: 865–874, available at: https://doi.org/10.1094/PDIS-09-11-0769-RE.
  17. Maleita, C. , Esteves, I. , Cardoso, J. M. S. , Cunha, M. J. , Carneiro, R. M. D. G. and Abrantes, I. . 2018. Meloidogyne luci, a new root-knot nematode parasitizing potato in Portugal. Plant Pathology 67: 366–376, available at: https://doi.org/10.1111/ppa.12755.
  18. Neal, J. C. . 1889. The root-knot disease of the peach, orange and other plants in Florida, due to the work of Anguillula. Bulletin 20, Division of Entomology, US Department of Agriculture.
  19. Powers, T. , Harris, T. , Higgins, R. , Mullin, P. and Powers, K. . 2018. Discovery and identification of Meloidogyne species using COI DNA barcoding. Journal of Nematology 50: 399–412, available at: https://doi.org/10.21307/jofnem-2018-029.
  20. Širca, S. , Urek, G. and Karssen, G. . 2004. First report of the root-knot nematode Meloidogyne ethiopica on tomato in Slovenia. Plant Disease 88: 680.
  21. Stare, B. G. , Strajnar, P. , Susič, N. , Urek, G. and Širca, S. . 2017. Reported populations of Meloidogyne ethiopica in Europe identified as Meloidogyne luci . Plant Disease 101: 1627–1632.
  22. Treub, M. . 1885. Onderzoekingen over Sereh-Ziek Suikkeriet gedaan in s Lands Plantentium te Buitenzorg. Mededeelingen uit's Lands Plantentium, Batavia 2: 1–39.
  23. Whitehead, A. G. . 1968. Taxonomy of Meloidogyne (Nematoda: Heteroderidae) with descriptions of four new species. Transactions of the Zoological Society of London 31: 263–401.
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FIGURES & TABLES

Figure 1:

Esterase phenotypes of protein homogenates from five egg-laying females of Meloidogyne species isolates. C – M. luci (positive control); 1 – M. ethiopica isolate from Brazil; J3 – M. javanica (reference isolate); 2 – M. luci (Cordyline australis); 3 – M. luci (Solanum lycopersicum) and 4 – M. luci (Oxalis corniculata).

Full Size   |   Slide (.pptx)

Figure 2:

Phylogenetic relationship of Meloidogyne spp. sequences based on the alignment of sequences of cytochrome oxidase subunit I (A) and cytochrome oxidase subunit II (B) of mitochondrial DNA with available sequences of other Meloidogyne species. The phylogenetic tree was generated in MEGA7 using the Neighbour-Joining method. The percentage of replicate trees in which the associated Meloidogyne spp. clustered together in the bootstrap test (500 replicates) is shown next to the branches. The evolutionary distances were computed using the Jukes-Cantor method. All positions with less than 95% site coverage were eliminated. That is, fewer than 5% alignment gaps, missing data, and ambiguous bases were allowed at any position. *Recently, reclassified as M. luci, according to Stare et al. (2017).

Full Size   |   Slide (.pptx)

REFERENCES

  1. Abrantes, I. M. de O. and Santos, M. S. N. de A. . 1991. Meloidogyne lusitanica n. sp. (Nematoda:Meloidogynidae), a root-knot nematode parasitizing olive tree (Olea europaea L.). Journal of Nematology 23: 210–224.
  2. Abrantes, I. M. de O. , Santos, M. C. V. dos , Conceição, I. L. P. M. da , Santos, M. S. N. de A. and Vovlas, N. . 2008. Root-knot and other plant-parasitic nematodes associated with fig trees in Portugal. Nematologia Mediterranea 36: 131–136.
  3. Aydınlı, G. , Mennan, S. , Devran, Z. , Širca, S. and Urek, G. . 2013. First report of the root-knot nematode Meloidogyne ethiopica on tomato and cucumber in Turkey. Plant Disease 97: 1262.
  4. Bellé, C. , Brum, D. , Groth, M. Z. , Barros, D. R. , Kaspary, T. E. , Schafer, J. T. and Gomes, C. B. . 2016. First report of Meloidogyne luci parasitizing Glycine max in Brazil. Plant Disease 100: 2174.
  5. Carneiro, R. M. D. G. , Correa, V. R. , Almeida, M. R. A. , Gomes, A. C. M. M. , Deimi, A. M. , Castagnone-Sereno, P. and Karssen, G. . 2014. Meloidogyne luci n. sp. (Nematoda: Meloidogynidae), a root-knot nematode parasitising different crops in Brazil, Chile and Iran. Nematology 16: 289–301, available at: https://doi.org/10.1163/15685411-00002765.
  6. Chitwood, B. G. . 1949. Root-knot nematodes - part I. A revision of the genus Meloidogyne Göldi, 1887. Proceedings of the Helminthological Society of Washington 16: 90–104.
  7. Conceição, I. L. P. M. da , Cunha, M. J. M. da , Feio, G. , Correia, M. , Santos, M. C. V. dos , Abrantes, I. M. de O. and Santos, M. S. N. Dde A. . 2009. Root-knot nematodes, Meloidogyne spp., on potato in Portugal. Nematology 11: 311–313, available at: https://doi.org/10.1163/156854109X415515.
  8. Conceição, I. L. , Tzortzakakis, E. A. , Gomes, P. , Abrantes, I. and da Cunha, M. J. . 2012. Detection of the root-knot nematode Meloidogyne ethiopica in Greece. European Journal of Plant Pathology 134: 451–457, available at: https://doi.org/10.1007/s10658-012-0027-0.
  9. EPPO . 2017. EPPO Alert List: addition of Meloidogyne luci together with M. ethiopica . EPPO Reporting Service, 2017/218, accessed from: https://gd.eppo.int/reporting/article-6186 (December 2018).
  10. Golden, A. M. , O'Bannon, J. H. , Santo, G. S. and Finley, A. M. . 1980. Description and SEM observations of Meloidogyne chitwoodi n. sp. (Meloidogynidae), a root-knot nematode on potato in the Pacific Northwest. Journal of Nematology 12: 319–27.
  11. Hirschmann, H. . 1986. Meloidogyne hispanica n. sp. (Nematoda: Meloidogynidae), the ‘Seville root-knotnematode’. Journal of Nematology 18: 520–32.
  12. Janssen, T. , Karssen, G. , Verhaeven, M. , Coyne, D. and Bert, W. . 2016. Mitochondrial coding genome analysis of tropical root-knot nematodes (Meloidogyne) supports haplotype based diagnostics and reveals evidence of recent reticulate evolution. Scientific Reports 6: 22591.
  13. Kiewnick, S. H. M. , van den Elsen, S. , van Megen, H. , Frey, J. E. and Helder, J. . 2014. Comparison of two short DNA barcoding loci (COI and COII) and two longer ribosomal DNA genes (SSU & LSU rRNA) for specimen identification among quarantine root-knot nematodes (Meloidogyne spp.) and their close relatives. European Journal of Plant Pathology 140: 97–110.
  14. Kofoid, C. A. , and White, W. A. . 1919. A new nematode infection of man. Journal of the American Medical Association 72: 567–69.
  15. Machado, A. C. Z. , Dorigo, O. F. , Carneiro, R. M. D. G. and De Araújo Filho, J. V. . 2016. Meloidogyne luci, a new infecting nematode species on common bean fields at Paraná State, Brazil. Helminthologia 53: 207–210, avalable at: https://doi.org/10.1515/helmin-2016-0014.
  16. Maleita, C. M. , Simões, M. J. , Egas, C. , Curtis, R. H. C. and Abrantes, I. M. D. O. . 2012. Biometrical, biochemical, and molecular diagnosis of Portuguese Meloidogyne hispanica isolates. Plant Disease 96: 865–874, available at: https://doi.org/10.1094/PDIS-09-11-0769-RE.
  17. Maleita, C. , Esteves, I. , Cardoso, J. M. S. , Cunha, M. J. , Carneiro, R. M. D. G. and Abrantes, I. . 2018. Meloidogyne luci, a new root-knot nematode parasitizing potato in Portugal. Plant Pathology 67: 366–376, available at: https://doi.org/10.1111/ppa.12755.
  18. Neal, J. C. . 1889. The root-knot disease of the peach, orange and other plants in Florida, due to the work of Anguillula. Bulletin 20, Division of Entomology, US Department of Agriculture.
  19. Powers, T. , Harris, T. , Higgins, R. , Mullin, P. and Powers, K. . 2018. Discovery and identification of Meloidogyne species using COI DNA barcoding. Journal of Nematology 50: 399–412, available at: https://doi.org/10.21307/jofnem-2018-029.
  20. Širca, S. , Urek, G. and Karssen, G. . 2004. First report of the root-knot nematode Meloidogyne ethiopica on tomato in Slovenia. Plant Disease 88: 680.
  21. Stare, B. G. , Strajnar, P. , Susič, N. , Urek, G. and Širca, S. . 2017. Reported populations of Meloidogyne ethiopica in Europe identified as Meloidogyne luci . Plant Disease 101: 1627–1632.
  22. Treub, M. . 1885. Onderzoekingen over Sereh-Ziek Suikkeriet gedaan in s Lands Plantentium te Buitenzorg. Mededeelingen uit's Lands Plantentium, Batavia 2: 1–39.
  23. Whitehead, A. G. . 1968. Taxonomy of Meloidogyne (Nematoda: Heteroderidae) with descriptions of four new species. Transactions of the Zoological Society of London 31: 263–401.

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