Plant and Soil

, Volume 354, Issue 1–2, pp 335–345 | Cite as

Arbuscular mycorrhizal fungi reduce root-knot nematode penetration through altered root exudation of their host

  • Christine Vos
  • Sofie Claerhout
  • Rachel Mkandawire
  • Bart Panis
  • Dirk De Waele
  • Annemie Elsen
Regular Article
First Online:
Received:
Accepted:

Abstract

Aims

Arbuscular mycorrhizal fungi (AMF) can control root-knot nematode infection, but the mode of action is still unknown. We investigated the effects of AMF and mycorrhizal root exudates on the initial steps of Meloidogyne incognita infection, namely movement towards and penetration of tomato roots.

Methods

M. incognita soil migration and root penetration were evaluated in a twin-chamber set-up consisting of a control and mycorrhizal (Glomus mosseae) plant compartment (Solanum lycopersicum cv. Marmande) connected by a bridge. Penetration into control and mycorrhizal roots was also assessed when non-mycorrhizal or mycorrhizal root exudates were applied and nematode motility in the presence of the root exudates was tested in vitro.

Results

M. incognita penetration was significantly reduced in mycorrhizal roots compared to control roots. In the twin-chamber set-up, equal numbers of nematodes moved to both compartments, but the majority accumulated in the soil of the mycorrhizal plant compartment, while for the control plants the majority penetrated the roots. Application of mycorrhizal root exudates further reduced nematode penetration in mycorrhizal plants and temporarily paralyzed nematodes, compared with application of water or non-mycorrhizal root exudates.

Conclusions

Nematode penetration was reduced in mycorrhizal tomato roots and mycorrhizal root exudates probably contributed at least partially by affecting nematode motility.

Keywords

Glomus mosseae Meloidogyne incognita Motility test Mycorrhiza-induced resistance Nematode penetration Root exudates 

References

  1. Akhtar MS, Siddiqui ZA (2008) Arbuscular mycorrhizal fungi as potential bioprotectants against plant pathogens. In: Siddiqui ZA, Akhtar MS, Futai K (eds) Mycorrhizae: sustainable agriculture and forestry. Springer Science + Business Media, pp 61–97Google Scholar
  2. Azcon-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens—an overview of the mechanisms involved. Mycorrhiza 6:457–464CrossRefGoogle Scholar
  3. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681PubMedCrossRefGoogle Scholar
  4. Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32PubMedCrossRefGoogle Scholar
  5. Bais HP, Prithiviraj B, Jha AK, Ausubel FM, Vivanco JM (2005) Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature 434:217–221PubMedCrossRefGoogle Scholar
  6. Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266PubMedCrossRefGoogle Scholar
  7. Bird AF (1960) Additional notes on the attractiveness of roots to plant parasitic nematodes. Nematologica 5:217CrossRefGoogle Scholar
  8. Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe Interact 11:1017–1028CrossRefGoogle Scholar
  9. Curtis RHC, Robinson AF, Perry RN (2009) Hatch and host location. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CAB International, Wallingford, pp 139–162CrossRefGoogle Scholar
  10. Dababat A, Sikora RA (2007) Influence of the mutualistic endophyte Fusarium oxysporum 162 on Meloidogyne incognita attraction and invasion. Nematology 9:771–776CrossRefGoogle Scholar
  11. Declerck S, Laloux S, Sarah JL, Delvaux B (1998) Application of a flowing solution culture technique to study the parasitic fitness of the nematode Radopholus similis on banana plantlets under two different nitrogen nutrient regimes. Plant Pathol 47:580–585CrossRefGoogle Scholar
  12. Dong LQ, Zhang KQ (2006) Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288:31–45CrossRefGoogle Scholar
  13. Edens RM, Anand SC, Bolla RI (1995) Enzymes of the phenylpropanoid pathway in soybean infected with Meloidogyne incognita or Heterodera glycines. J Nematol 27:292–303PubMedGoogle Scholar
  14. Elsen A, Gervacio D, Swennen R, De Waele D (2008) AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256PubMedCrossRefGoogle Scholar
  15. Fillion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533CrossRefGoogle Scholar
  16. Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530PubMedCrossRefGoogle Scholar
  17. Gianinazzi-Pearson V, Dumas-Gaudot E, Gollotte A, Tahiri-Alaoui A, Gianinazzi S (1996) Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol 133:45–57CrossRefGoogle Scholar
  18. Harrier LA, Watson CA (2004) The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soil-borne pathogens in organic and/or other sustainable farming systems. Pest Manag Sci 60:149–157PubMedCrossRefGoogle Scholar
  19. Hodge A (2000) Microbial ecology of the arbuscular mycorrhiza. FEMS Micobiol Ecol 32:91–96CrossRefGoogle Scholar
  20. Hol WHG, Cook R (2005) An overview of arbuscular mycorrhizal fungi-nematode interactions. Basic Appl Ecol 6:489–503CrossRefGoogle Scholar
  21. Hooper DJ, Hallman J, Subbotin S (2005) Methods for extraction, processing and detection of plant and soil nematodes. In: Luc M, Sikora R, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CABI, Wallingford, pp 53–86CrossRefGoogle Scholar
  22. Hubbard JE, Flores-Lara Y, Schmitt M, McClure MA, Stock SP, Hawes MC (2005) Increased penetration of host roots by nematodes after recovery from quiescence induced by root cap exudates. Nematology 7:321–331CrossRefGoogle Scholar
  23. Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480CrossRefGoogle Scholar
  24. Koltai H, Sharon E, Spiegel Y (2002) Root-nematode interactions: recognition and pathogenicity. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots, the hidden half, 3rd edn. Marcel Dekker, New York, pp 933–947Google Scholar
  25. Li HY, Yang GD, Shu HR, Yang YT, Ye BX, Nishida I, Zheng CC (2006) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant Cell Physiol 47:154–163PubMedCrossRefGoogle Scholar
  26. Lioussanne L, Jolicoeur M, St-Arnaud M (2008) Mycorrhizal colonization with Glomus intraradices and development stage of transformed tomato roots significantly modify the chemotactic response of the pathogen Phytophthora nicotianae. Soil Biol Biochem 40:2217–2224CrossRefGoogle Scholar
  27. Lioussanne L, Jolicoeur M, St-Arnaud M (2009) Role of the modification in root exudation induced by arbuscular mycorrhizal colonization on the intraradical growth of Phytophthora nicotianae in tomato. Mycorrhiza 19:443–448PubMedCrossRefGoogle Scholar
  28. Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonization in split-root maize. Plant Soil 251:279–289CrossRefGoogle Scholar
  29. McArthur DAJ, Knowles NR (1992) Resistance responses of potato to vesicular-arbuscular mycorrhizal fungi under varying abiotic phosphorus levels. Plant Physiol 100:341–351PubMedCrossRefGoogle Scholar
  30. Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions and their potential role in biological control. Plant Soil 185:241–251CrossRefGoogle Scholar
  31. Norman JR, Hooker JE (2000) Sporulation of Phytophthora fragariae shows greater stimulation by exudates of non-mycorrhizal than by mycorrhizal strawberry roots. Mycol Res 104:1069–1073CrossRefGoogle Scholar
  32. 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. Phytopathol 95:158–165CrossRefGoogle Scholar
  33. Perry RN (2005) An evaluation of types of attractants enabling plant-parasitic nematodes to locate plant roots. Russ J Nematol 13:83–88Google Scholar
  34. Pinior A, Wyss U, Piché Y, Vierheilig H (1999) Plants colonized by AM fungi regulate further root colonization by AM fungi through altered root exudation. Can J Bot 77:891–897Google Scholar
  35. Pinochet J, Calvet C, Camprubi A, Fernandez C (1996) Interactions between migratory endoparasitic nematodes and arbuscular mycorrhizal fungi in perennial crops: a review. Plant Soil 185:183–190CrossRefGoogle Scholar
  36. Plenchette C, Morel C (1996) External phosphorus requirements of mycorrhizal and non-mycorrhizal barley and soybean plants. Biol Fertil Soils 21:303–308CrossRefGoogle Scholar
  37. Pozo MJ, Azcon-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398PubMedCrossRefGoogle Scholar
  38. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534PubMedCrossRefGoogle Scholar
  39. Ryan NA, Duffy EM, Cassells AC, Jones PW (2000) The effect of mycorrhizal fungi on the hatch of potato cyst nematodes. Appl Soil Ecol 15:233–240CrossRefGoogle Scholar
  40. Scheffknecht S, Mammerler R, Steinkellner S, Vierheilig H (2006) Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants. Mycorrhiza 16:365–370PubMedCrossRefGoogle Scholar
  41. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill Book Co, New YorkGoogle Scholar
  42. Sikora RA, Pocasangre L, zum Felde A, Niere B, Vu TT, Dababat AA (2008) Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes. Biol Control 46:15–23CrossRefGoogle Scholar
  43. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  44. Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol Ecol 45:219–227CrossRefGoogle Scholar
  45. Speijer PR, De Waele D (1997) Screening of Musa germplasm for resistance and tolerance to nematodes. INIBAP Technical guidelines, nr. 1. INIBAP, MontpellierGoogle Scholar
  46. Spence KO, Lewis EE, Perry RN (2008) Host-finding and invasion by entomopathogenic and plant-parasitic nematodes: evaluating the ability of laboratory bioassays to predict field results. J Nematol 40:93–98PubMedGoogle Scholar
  47. St-Arnaud M, Vujanovic V (2007) Effect of the arbuscular mycorrhizal symbiosis on plant diseases and pests. In: Hamel C, Plenchette C (eds) Mycorrhizae in crop production: applying knowledge. Haworth, New York, pp 67–122Google Scholar
  48. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306PubMedCrossRefGoogle Scholar
  49. Vierheilig H, Piché Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. Adv Exp Med Biol 505:23–29PubMedGoogle Scholar
  50. Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedGoogle Scholar
  51. Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170PubMedCrossRefGoogle Scholar
  52. Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido GM (2008) The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of AM symbiosis: one mechanism, two effects? In: Varma A (ed) Mycorrhiza: genetics and molecular biology—Eco-function—Biotechnology—Eco-physiology—Structure and systematics. Springer, Berlin, pp 307–320Google Scholar
  53. Vivanco JM, Guimaraes RL, Flores HE (2002) Underground plant metabolism: the biosynthetic potential of roots. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots, the hidden half, 3rd edn. Marcel Dekker, New York, pp 1045–1070Google Scholar
  54. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedCrossRefGoogle Scholar
  55. Wamberg C, Christensen S, Jakobsen I, Muller AK, Sørensen SJ (2003) The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem 35:1349–1357CrossRefGoogle Scholar
  56. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227CrossRefGoogle Scholar
  57. Wuyts N, Lognay G, Swennen R, De Waele D (2006a) Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. J Exp Bot 57:2825–2835PubMedCrossRefGoogle Scholar
  58. Wuyts N, Swennen R, De Waele D (2006b) Effects of plant phenylpropanoid pathway products and selected terpenoids and alkaloids on the behaviour of the plant-parasitic nematodes Radopholus similis, Pratylenchus penetrans and Meloidogyne incognita. Nematology 8:89–101CrossRefGoogle Scholar
  59. Wuyts N, Zin Thu Zar M, Swennen R, De Waele D (2006c) Banana rhizodeposition: characterization of root border cell production and effects on chemotaxis and motility of the parasitic nematode Radopholus similis. Plant Soil 283:217–228CrossRefGoogle Scholar
  60. Zhao X, Schmitt M, Hawes MC (2000) Species-dependent effects of border cell and root tip exudates on nematode behavior. Plant Pathol 90:1239–1245Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Christine Vos
    • 1
  • Sofie Claerhout
    • 1
  • Rachel Mkandawire
    • 1
    • 3
  • Bart Panis
    • 1
  • Dirk De Waele
    • 1
    • 3
  • Annemie Elsen
    • 2
    • 3
  1. 1.Laboratory of Tropical Crop Improvement, Department of Biosystems, Faculty of Bioscience EngineeringUniversity of Leuven (K.U.Leuven)LeuvenBelgium
  2. 2.Bodemkundige Dienst van BelgiëHeverleeBelgium
  3. 3.Department of Biology, Faculty of SciencesGhent UniversityGhentBelgium

Personalised recommendations