Skip to main content

Advertisement

Log in

Identification and characterization of a virulent population of Meloidogyne graminicola

  • Original Research Article
  • Published:
Australasian Plant Pathology Aims and scope Submit manuscript

Abstract

Resistant rice varieties are considered to be a potential alternative for controlling the plant-parasitic nematode Meloidogyne graminicola in the field due to their joint economic and environmental sustainability features. However, the emergence of virulent pathogen forms threatens natural resistance durability. In this study, we isolated a virulent M. graminicola population from a naturally infested field in Cambodia that overcomes the resistance of the Oryza sativa Zhonghua 11 rice variety. We used molecular (internal transcribed spacer of rDNA and mitochondrial markers) and morphological approaches to unequivocally identify and confirm the species identification. Few intraspecific variabilities in traits between the virulent pathotype and several avirulent pathotypes were found. Remarkably, histological analysis showed the absence of a hypersensitive response (HR) on root cells surrounding the nematode in the "virulent pathotype–Zhonghua 11" interaction. In addition, the virulent pathotype reproduced to a significant extent in two other Oryza sativa varieties known to be resistant to M. graminicola. However, this virulent population was unable to overcome the previously described resistance in three Oryza glaberrima varieties. We concluded that the virulent M. graminicola pathotype isolated in this study could compromise rice breeding programs based on the sole use of known resistant O. sativa gene pools. The identification of this virulent pathotype should provide the genetic resources needed to study the molecular mechanisms that may enable M. graminicola to bypass HR resistance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Abad P, Favery B, Rosso MN, Castagnone-Sereno P (2003) Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol Plant Pathol 4:217–224

    Article  PubMed  CAS  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2

    Article  PubMed  CAS  Google Scholar 

  • Anthony F, Topart P, Martinez A, Silva M, Nicole M (2005) Hypersensitive-like reaction conferred by the Mex-1 resistance gene against Meloidogyne exigua in coffee. Plant Pathol 54:476–482

    Article  CAS  Google Scholar 

  • Bellafiore S, Jougla C, Chapuis É, Besnard G, Suong M, Vu PN et al (2015) Intraspecific variability of the facultative meiotic parthenogenetic root-knot nematode (Meloidogyne graminicola) from rice fields in Vietnam. CR Biol 338:471–483. https://doi.org/10.1016/j.crvi.2015.04.002

    Article  Google Scholar 

  • Bleve-Zacheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P (1998) The pepper resistance genes Me1 and Me3 induce differential penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection. Plant Sci 133:79–90

    Article  CAS  Google Scholar 

  • Bybd DW Jr, Kirkpatrick T, Barker K (1983) An improved technique for clearing and staining plant tissues for detection of nematodes. J Nematol 15:142–143

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cabasan MTN, Kumar A, Bellafiore S, De Waele D (2014) Histopathology of the rice root-knot nematode, Meloidogyne graminicola, on Oryza sativa and O. glaberrima. Nematology 16:73–81. https://doi.org/10.1163/15685411-00002746

    Article  Google Scholar 

  • Cabasan MTN, Kumar A, De Waele D (2012) Comparison of migration, penetration, development and reproduction of Meloidogyne graminicola on susceptible and resistant rice genotypes. Nematol 14:405–415

    Article  Google Scholar 

  • Carvalho F (2017) Pesticides, environment and food safety. Food Ener Sec 6:48–60

    Article  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Dalmasso A (1993) Stable virulence against the tomato resistance Mi gene in the parthenogenetic root-knot nematode Meloidogyne incognita. Phytopathology 83:803–812

    Article  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Dalmasso A (1994) Reproduction of virulent isolates of Meloidogyne incognita on susceptible and Mi-resistant tomato. J Nematol 26:324–328

    PubMed  PubMed Central  CAS  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Djian-Caporalino C (2001) New data on the specificity of the root-knot nematode resistance genes Me1 and Me3 in pepper. Plant Breeding 120:429–433

    Article  CAS  Google Scholar 

  • Cliff GM, Hirschmann H (1985) Evaluation of morphological variability in Meloidogyne arenaria. J Nematol 17:445–459

    PubMed  PubMed Central  CAS  Google Scholar 

  • Courtney WD, Polley D, Miller VL (1955) TAF, an improved fixative in nematode technique. Plant Disease Reporter 39:570–571

    CAS  Google Scholar 

  • Davies LJ, Elling AA (2015) Resistance genes against plant-parasitic nematodes: a durable control strategy? Nematology 17:249–263

    Article  Google Scholar 

  • De Ley IT, De Ley P, Vierstraete A, Karssen G, Moens M, Vanfleteren J (2002) Phylogenetic analyses of Meloidogyne small subunit rDNA. J Nematol 34:319–327

    PubMed  PubMed Central  Google Scholar 

  • Dimkpa SO, Lahari Z, Shrestha R, Douglas A, Gheysen G, Price AHA (2016) Genome-wide association study of a global rice panel reveals resistance in Oryza sativa to root-knot nematodes. J Exp Bot 67:1191–1200. https://doi.org/10.1093/jxb/erv470

    Article  PubMed  CAS  Google Scholar 

  • Djedatin G, Ndjiondjop MN, Mathieu T, Cruz CMV, Sanni A, Ghesquière A et al (2011) Evaluation of african cultivated rice Oryza glaberrima for resistance to bacterial blight. Plant Dis 95:441–447

    Article  PubMed  Google Scholar 

  • Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, VandeCasteele C, Faure I et al (2007) Root-knot nematode (Meloidogyne spp.) me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 114:473–486. https://doi.org/10.1007/s00122-006-0447-3

    Article  PubMed  CAS  Google Scholar 

  • Dufey I, Draye X, Lutts S, Lorieux M, Martinez C, Bertin P (2015) Novel QTLs in an interspecific backcross Oryza sativa × Oryza glaberrima for resistance to iron toxicity in rice. Euphytica 204:609–625

    Article  CAS  Google Scholar 

  • Eisenback JD, Triantaphyllou HH (2020) Root-knot nematodes: Meloidogyne species and races. Manual Agricul Nematol 1:191–274 CRC Press

  • El-Sappah AH, M M I H, El-Awady H, Yan S, Qi S, Liu J, Cheng GT, Liang Y (2019) Tomato natural resistance genes in controlling the Root-Knot Nematode. Genes (Basel) 10:925. https://doi.org/10.3390/genes10110925

    Article  PubMed  CAS  Google Scholar 

  • EPPO global database (2022) Meloidogyne graminicola (MELGGC). https://gd.eppo.int/taxon/MELGGC/hosts. Accessed 24 June 2022

  • Fanelli E, Cotroneo A, Carisio L, Troccoli A, Grosso S, Boero C et al (2017) Detection and molecular characterization of the rice root-knot nematode Meloidogyne graminicola in Italy. Eur J Plant Pathol 149:467–476

    Article  CAS  Google Scholar 

  • Golden AM, Birchfield W (1965) Meloidogyne graminicola (Heteroderidae), a new species of root-knot nematode from grass. In ‘Proceedings of the Helminthological Society of Washington 32:228 – 31

  • Hada A, Dutta TK, Singh N, Singh B, Rai V, Singh NK, Rao U (2020) A genome-wide association study in indian wild rice accessions for resistance to the root-knot nematode Meloidogyne graminicola. PLoS ONE 15:e0239085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hartman KM, Sasser J (1985) Identification of Meloidogyne species on the basis of differential host test and perineal-pattern morphology. Dept. of Plant Pathology. North Carolina State Univ

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular Calif agricultural Exp Stn 347:32

    Google Scholar 

  • Humphreys-Pereira DA, Elling AA (2013) Intraspecific variability and genetic structure in Meloidogyne chitwoodi from the USA. Nematology 15:315–327

    Article  CAS  Google Scholar 

  • Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057

    Article  PubMed  PubMed Central  Google Scholar 

  • Kaloshian I, Williamson V, Miyao G, Lawn D, Westerdahl B (1996) Resistance-breaking” nematodes identified in California tomatoes. Calif Agric 50:18–19

    Article  Google Scholar 

  • Lahari Z, Nkurunziza R, Bauters L, Gheysen G (2020) Analysis of asian rice (Oryza sativa) reveals a new source of resistance to the Root-knot nematode Meloidogyne javanica and the root-lesion nematode Pratylenchus zeae. Phytopathology 110:1572–1577

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H et al (2007) Clustal W and Clustal X version 2.0. Bioinform 23:2947–2948

  • Mantelin S, Bellafiore S, Kyndt T (2017) Meloidogyne graminicola: a major threat to rice agriculture. Mol Plant Pathol 18:3–15

    Article  PubMed  Google Scholar 

  • McClure MA, Kruk TH, Misaghi I (1973) A method for obtaining quantities of clean Meloidogyne eggs. J Nematology 5:230

    CAS  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nguyen HT, Mantelin S, Ha CV, Lorieux M, Jones J, Mai CD, Bellafiore S (2022) Insights into the genetics of the Zhonghua 11 resistance to Meloidogyne graminicola and its molecular determinism in rice. Front Plant Sci 13:854961. https://doi.org/10.3389/fpls.2022.854961

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen PV, Tran TB, Nguyen PT, Nguyen LNT, Bien TLT, Ton LB, Le TTH, Ton AT, Nguyen QB, Huynh BV, Le DD, Bellafiore S (2021) The response of rice varieties to Meloidogyne graminicola from the Mekong Delta. Vietnam Nematology 1:1–18

    Google Scholar 

  • Pandit BT, Mondal P, Mondal S, Khan MR (2021) Morphology and morphometric variations in Indian populations of Meloidogyne graminicola Golden and Birchfield, 1965. Arch Phytopathol Plant Protect 1–20

  • Pegard A, Brizzard G, Fazari A, Soucaze O, Abad P, Djian-Caporalino C (2005) Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum. Phytopathology 95:158–165. https://doi.org/10.1094/PHYTO-95-0158

    Article  PubMed  CAS  Google Scholar 

  • Petitot AS, Kyndt T, Haidar R, Dereeper A, Collin M, de Almeida Engler J, Gheysen G, Fernandez D (2017) Transcriptomic and histological responses of african rice (Oryza glaberrima) to Meloidogyne graminicola provide new insights into root-knot nematode resistance in monocots. Ann Bot 119:885–899. https://doi.org/10.1093/aob/mcw256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Phan NT, De Waele D, Lorieux M, Xiong L, Bellafiore S (2018) A hypersensitivity-like response to Meloidogyne graminicola in rice (Oryza sativa). Phytopathology 108:521–528

    Article  PubMed  Google Scholar 

  • Phan NT, Orjuela J, Danchin EGJ, Klopp C, Perfus-Barbeoch L, Kozlowski DK, Koutsovoulos GD, Lopez-Roques C, Bouchez O, Zahm M, Besnard G, Bellafiore S (2020) Genome structure and content of the rice root-knot nematode (Meloidogyne graminicola). Ecol Evol 10:11006–11021

  • Plowright RA, Coyne DL, Nash P, Jones MP (1999) Resistance to the rice nematodes Heterodera sacchari, Meloidogyne graminicola and M. incognita in Oryza glaberrima and O. glaberrima x O. sativa interspecific hybrids. Nematology 1:745–751. https://doi.org/10.1163/156854199508775

    Article  Google Scholar 

  • Pokharel RR, Abawi GS, Zhang N, Duxbury JM, Smart CD (2007) Characterization of isolates of Meloidogyne from rice-wheat production fields in Nepal. J Nematol 39:221–230

    PubMed  PubMed Central  CAS  Google Scholar 

  • Rashid MH, Al-Mamun M, Uddin MN (2017) How durable is root knot nematode resistance in tomato? Plant Breed Biotechnol 5:143–162

    Article  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (https://www.R-project.org/)

  • Reversat G, Boyer J, Sannier C, Pando-Bahuon A (1999) Use of a mixture of sand and water-absorbent synthetic polymer as substrate for the xenic culturing of plant-parasitic nematodes in the laboratory. Nematology 1:209–212

    Article  Google Scholar 

  • Reversat G, Fernandez L (2004) Effect of inoculations with single and multiple juveniles on release of progeny of Meloidogyne graminicola from susceptible rice. Nematology 6:1–6

    Article  Google Scholar 

  • Salalia R, Walia RK, Somvanshi VS, Kumar P, Kumar A (2017) Morphological, morphometric, and molecular characterization of intraspecific variations within indian populations of Meloidogyne graminicola. J Nematology 49:254–267

    Article  Google Scholar 

  • Santos D, Martins da Silva P, Abrantes I, Maleita C (2020) Tomato Mi-1.2 gene confers resistance to Meloidogyne luci and M. ethiopica. Eur J Plant Pathol 156:571–580

    Article  CAS  Google Scholar 

  • Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4:67–69. https://doi.org/10.1163/187529259X00381

    Article  Google Scholar 

  • Soriano IR, Schmit V, Brar DS, Prot JC, Reversat G (1999) Resistance to rice root-knot nematode Meloidogyne graminicola identified in Oryza longistaminata and O. glaberrima. Nematol 1:395–398

    Article  Google Scholar 

  • Suong M, Chapuis E, Leng V, Tivet F, Waele DD, Thi HN, Bellafiore S (2019) Impact of a conservation agriculture system on soil characteristics, rice yield, and root-parasitic nematodes in a cambodian lowland rice field. J Nematol 51

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tian Z, Maria M, Barsalote EM, Castillo P, Zheng J (2018) Morphological and molecular characterization of the rice root-knot nematode, Meloidogyne graminicola, Golden and Birchfield, 1965 occurring in Zhejiang, China. J Integr Agric 17:2724–2733. https://doi.org/10.1016/S2095-3119(18)61971-9

  • Torrini G, Roversi PF, Cesaroni CF, Marianelli L (2020) Pest risk analysis of rice root-knot nematode (Meloidogyne graminicola) for the italian territory. EPPO Bull 50:330–339

    Article  Google Scholar 

  • Williamson VM (1999) Plant nematode resistance genes. Curr Opin Plant Biol 2:327–331

    Article  PubMed  CAS  Google Scholar 

  • Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends Genet 22:396–403

    Article  PubMed  CAS  Google Scholar 

  • Williamson VM, Roberts PA (2009) Mechanisms and genetics of resistance. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CAB International, Wallingford, UK, pp 301–325

    Chapter  Google Scholar 

  • Zhan LP, Zhong D, Peng DL, Huan P, Kong LA, Liu SM, Ying L, Zhong-cai L, Huag WK (2018) Evaluation of chinese rice varieties resistant to the root-knot nematode Meloidogyne graminicola. J Integr Agric 17:621–630

    Article  Google Scholar 

Download references

Acknowledgments

The authors thank the Department of Nematology; the Institute of Ecology and Biological Resources (Vietnam Academy of Science and Technology), under the FWO.106.2020.02 project, for providing access to the facilities for conducting morphology analysis of virulent M. graminicola (Mg). This research was financially supported by the French National Research Institute for Sustainable Development (IRD) for the Ph.D. research of student Nguyen Thi Hue.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stéphane Bellafiore.

Ethics declarations

Conflict of interest

The authors declare that they have no confict of interest.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, H.T., Vang, S., Phan, N.T. et al. Identification and characterization of a virulent population of Meloidogyne graminicola. Australasian Plant Pathol. 52, 391–405 (2023). https://doi.org/10.1007/s13313-023-00926-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13313-023-00926-8

Keywords

Navigation