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Beyond the primary host: survival of Heterodera schachtii (Nematoda, Heteroderidae) through alternative hosts

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  • Diogo AZEVEDO,
  • Eugénia DE ANDRADE,
  • Maria L. INACIO,
  • Ana Paula RAMOS,
  • Maria João CAMACHO
Diogo AZEVEDO
Instituto Superior de Agronomia (ISA), Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Portugal
Eugénia DE ANDRADE
Instituto Nacional de Investigação Agrária e Veterinária (INIAV, I.P.), Quinta do Marquês, 2780-159 Oeiras, Portugal
Maria L. INACIO
Instituto Nacional de Investigação Agrária e Veterinária (INIAV, I.P.), Quinta do Marquês, 2780-159 Oeiras, Portugal
Ana Paula RAMOS
Linking Landscape, Environment, Agriculture and Food Research Centre (LEAF), Associate Laboratory TERRA, Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017, Lisbon, Portugal
Maria João CAMACHO
Instituto Nacional de Investigação Agrária e Veterinária (INIAV, I.P.), Quinta do Marquês, 2780-159 Oeiras, Portugal
DOI: https://doi.org/10.36253/phyto-16650
Categories

Published 2026-03-16

Keywords

  • Cyst nematodes resilience,
  • population dynamics,
  • host range,
  • morphological identification,
  • molecular identification

How to Cite

[1]
D. AZEVEDO, E. DE ANDRADE, M. L. INACIO, A. P. RAMOS, and M. J. CAMACHO, “Beyond the primary host: survival of Heterodera schachtii (Nematoda, Heteroderidae) through alternative hosts”, Phytopathol. Mediterr., Mar. 2026.

Copyright (c) 2026 Diogo AZEVEDO, Eugénia DE ANDRADE, Maria L. INACIO, Ana Paula RAMOS, Maria João CAMACHO

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This work is licensed under a Creative Commons Attribution 4.0 International License.

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Abstract

Plant-parasitic nematodes are an underestimated cause of crop yield losses. Cyst nematodes, particularly Heterodera spp., are important pests of sugar beet, cereals, and soybean. Presence of these nematodes was investigated in a plot near Lisbon (Golegã), where problems with cyst nematode infestations had been detected. Heterodera cysts were extracted and isolated from soil samples, and were identified morphologically and using PCR and DNA sequencing. Morphological identifications were difficult, but molecular analyses confirmed the presence of H. schachtii, linking this with the plot’s history. This nematode had remained viable in the soil for more than 15 years, despite absence of sugar beet, the primary host.

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References

  1. Camacho M.J., Nóbrega F., Lima A., Mota M., Inácio M.L., 2017. Morphological and molecular identification of potato nematodes (Globodera rostochiensis and G. pallida) in Portuguese potato fields. Nematology 19: 883–889. https://doi.org/10.1163/15685411-23000003094 DOI: https://doi.org/10.1163/15685411-00003094
  2. Camacho M.J., Andrade E., Mota M., Nóbrega F., Vicente C., … Inácio M.L., 2020. Potato cyst nematodes: geographical distribution, phylogenetic relationships and integrated pest management outcomes in Portugal. Frontiers in Plant Science 11. https://doi.org/10.3389/fpls.2020.606178 DOI: https://doi.org/10.3389/fpls.2020.606178
  3. Camacho M. J., Inácio M. L., Andrade E. d., 2025. Multi-Marker Approach for the Identification of Different Heterodera Species (Nematoda: Heteroderidae). Pathogens 14: 1052. https://doi.org/10.3390/pathogens14101052 DOI: https://doi.org/10.3390/pathogens14101052
  4. Decraemer W., Hunt D.J., 2013. Structure and classification. In: Plant Nematology, 2nd ed. (Perry R.N., Moens M. ed.). CAB International, Wallingford, UK. pp. 3–39. DOI: https://doi.org/10.1079/9781780641515.0003
  5. Eberlein C., Heuer H., Westphal A., 2020. Biological suppression of populations of Heterodera schachtii adapted to different host genotypes of sugar beet. Frontiers in Plant Science 11: 812. https://doi.org/10.3389/fpls.2020.00812 DOI: https://doi.org/10.3389/fpls.2020.00812
  6. European and Mediterranean Plant Protection Organization. 2013a. Nematode extraction PM 7/119 (1). EPPO Bulletin 43: 471–495. https://doi.org/10.1111/epp.12077 DOI: https://doi.org/10.1111/epp.12077
  7. European and Mediterranean Plant Protection Organization. 2013b. Globodera rostochiensis and Globodera pallida PM 7/40 (3). EPPO Bulletin 39: 354–368. https://doi.org/10.1111/epp.12025 DOI: https://doi.org/10.1111/epp.12025
  8. Fenwick D., 1940. Methods for the recovery and counting of cysts of Heterodera schachtii from soil. Journal Helminthology 18: 155–172. http://dx.doi.org/10.1017/S0022149X00031485 DOI: https://doi.org/10.1017/S0022149X00031485
  9. Golden A.M., 1986. Morphology and identification of cyst nematodes. In Cyst Nematodes. (Lamberti F., Taylor C.E. ed.). Springer, Boston, MA., USA, Volume 121. pp. 23–45. https://doi.org/10.1007/978-1-4613-2251-1_2 DOI: https://doi.org/10.1007/978-1-4613-2251-1_2
  10. Goodey J.B., Franklin M.T., Hooper D.J., 1965. The Nematode Parasites of Plants Catalogued under their Hosts. 3rd ed. Commonwealth Agricultural Bureaux, Farnham Royal, UK. 214 pp.
  11. Holterman M., van der Wurff A., Van den Elsen S., Van Megen H., Bongers T., … Helder J., 2006. Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23: 1792–1800. https://doi.org/10.1093/molbev/msl044 DOI: https://doi.org/10.1093/molbev/msl044
  12. Hu M., Höglund J., Chilton N.B., Zhu X.Q., Gasser R.B., 2002. Mutation scanning analysis of mitochondria cytochrome c oxidase subunit 1 reveals limited gene flow among bovine lungworm subpopulations in Sweden. Electrophoresis 23: 3357–3363. https://doi.org/10.1002/1522-2683(200210)23:19<3357::AID-ELPS3357>3.0.CO;2-B DOI: https://doi.org/10.1002/1522-2683(200210)23:19<3357::AID-ELPS3357>3.0.CO;2-B
  13. Hunt D., 2008. Heterodera glycines (soybean cyst nematode). CABI Compendium. https://doi.org/10.1079/cabicompendium.27027 DOI: https://doi.org/10.1079/cabicompendium.27027
  14. Huston D.C., Khudhir M., Hodda M., 2022. Reliability and utility of standard gene sequence barcodes for the identification and differentiation of cyst nematodes of the genus Heterodera. Journal of Nematology 54: e2022-0024. https://doi.org/10.2478/jofnem-2022-0024 DOI: https://doi.org/10.2478/jofnem-2022-0024
  15. Inagaki H., Tsutsumi M., 1971. Survival of the soybean cyst nematode, Heterodera glycines Ichinohe (Tylenchida: Heteroderidae) under certain storing conditions. Applied Entomology and Zoology 6: 156–162. https://doi.org/10.1303/aez.6.156 DOI: https://doi.org/10.1303/aez.6.156
  16. Khan M.F.R., Arabiat S., Chanda A.K., Yan G., 2021. Sugarbeet Cyst Nematode. In: Plant Disease Management (NDSU Extension), PP1788.
  17. Ley P.D., Felix M., Frisse L., Nadler S., Sternberg P., Thomas W.K., 1999. Molecular and morphological characterisation of two reproductively isolated species with mirror-image anatomy (Nematoda: Cephalobiidae). Nematology 1(6): 591–612. https://doi.org/10.1163/156854199508559 DOI: https://doi.org/10.1163/156854199508559
  18. Lilley C.J., Atkinson H.J., Urwin P.E., 2005. Molecular aspects of cyst nematodes. Molecular Plant Pathology 6: 577–588. https://doi.org/10.1111/j.1364-3703.2005.00306.x DOI: https://doi.org/10.1111/j.1364-3703.2005.00306.x
  19. Moens M., Perry R.N., Jones J.T., 2018. Cyst nematodes – life cycle and economic importance. In Cyst Nematodes, 1st ed. (Perry R.N., Moens M., Jones J.T. ed.). CAB International, Wallingford, UK. pp. 1–26. https://doi.org/10.1079/9781786390837.0001 DOI: https://doi.org/10.1079/9781786390837.0001
  20. Mwamula A.O., Ko H.R., Kim Y., Kim Y.H., Lee J.K., Lee D.W., 2019. Morphological and molecular characterization of Heterodera schachtii and the newly recorded cyst nematode, H. trifolii, associated with Chinese cabbage in Korea. Plant Pathology Journal 35: 90. https://doi.org/10.5423/PPJ.ER.12.2017.0262 DOI: https://doi.org/10.5423/PPJ.ER.12.2017.0262
  21. Nisa R.U., Tantray A.Y., Shah A.A., 2022. Shift from morphological to recent advanced molecular approaches for the identification of nematodes. Genomics 114: 1–12. https://doi.org/10.1016/j.ygeno.2022.110295. DOI: https://doi.org/10.1016/j.ygeno.2022.110295
  22. Portuguese Ministry of Agriculture, 2010. Decreto-lei n.º 87/2010 de 16 de julho – Controlo dos nemátodes de quisto da batateira. Diário da República I série, nº 137. Available online: www.dre.pt (accessed September 3, 2024).
  23. Raski D.J., 1950. The life history and morphology of the sugar beet nematode, Heterodera schachtii Schmidt. Phytopathology 40: 135–151.
  24. Rivoal R., Valette S., Bekal S., Gauthier J.P., Yahyaoui A., 2003. Genetic and phenotypic diversity in the graminaceous cyst nematode complex, inferred from PCR-RFLP of ribosomal DNA and morphometric analysis. European Journal of Plant Pathology 109: 227–241. https://doi.org/10.1023/A:1022838806268 DOI: https://doi.org/10.1023/A:1022838806268
  25. Seesao Y., Gaya M., Merlinc S., Viscogliosi E., Aliouat-Denis C., Audebet C., 2016. A review of methods for nematode identification. Journal of Microbiological Methods 138: 37–49. https://doi.org/10.1016/j.mimet.2016.05.030 DOI: https://doi.org/10.1016/j.mimet.2016.05.030
  26. Sikora R.A., Helder J., Molendijk L.P.G., Desaeger J., Eves-van den Akker S., Mahlein A.K., 2023. Integrated nematode management in a world in transition: constraints, policy, processes, and technologies for the future. Annual Review of Phytopathology 61: 209–230. https://doi.org/10.1146/annurev-phyto-021622-113058 DOI: https://doi.org/10.1146/annurev-phyto-021622-113058
  27. Smiley R.W., Nicol J.M., 2009. Nematodes which challenge global wheat production. In: Wheat: Science and Trade, 1st ed.; Carver B.F. (ed). Wiley, Iowa, USA. pp. 171–187. DOI: https://doi.org/10.1002/9780813818832.ch8
  28. Subbotin S.A., Mundo-Ocampo M., Baldwin J.G., 2010. Systematics of cyst nematodes (Nematoda: Heteroderinae). In: Nematology Monographs and Perspectives 8A; Hunt D.J., Perry R.N. (eds). Brill, Leiden. 351 pp. DOI: https://doi.org/10.1163/ej.9789004162259.i-352.81
  29. Turner S.J., Subbotin S.A., 2013. Cyst nematodes. In: Plant Nematology. (Perry R.N., Moens M. ed.). CABI, UK. pp. 110–143. DOI: https://doi.org/10.1079/9781780641515.0109
  30. Westphal A., Becker J.O., 2001. Soil suppressiveness to Heterodera schachtii under different cropping sequences. Nematology 3: 551–558. https://doi.org/10.1163/156854101753389167 DOI: https://doi.org/10.1163/156854101753389167
  31. Yan G.P., Smiley R.W., 2009. Distinguishing Heterodera filipjevi and H. avenae using polymerase chain reaction–restriction fragment length polymorphism and cyst morphology. Phytopathology 100: 216–224. https://doi.org/10.1094/PHYTO-100-3-0216 DOI: https://doi.org/10.1094/PHYTO-100-3-0216
  32. Yeates G., Bongers T., de Goede R., Freckman D., Georgieva S., 1993. Feeding habits in soil nematode families and genera – an outline for soil ecologists. Journal of Nematology 25: 315–331.