, Volume 66, Issue 2, pp 55–64 | Cite as

Mycorrhiza-induced protection against pathogens is both genotype-specific and graft-transmissible

  • G. A. Mora-Romero
  • R. G. Cervantes-Gámez
  • H. Galindo-Flores
  • M. A. González-Ortíz
  • R. Félix-Gastélum
  • I. E. Maldonado-Mendoza
  • R. Salinas Pérez
  • J. León-Félix
  • M. C. Martínez-Valenzuela
  • M. López-MeyerEmail author


In addition to the nutrient exchange that is promoted by the arbuscular mycorrhiza symbiosis (AMS) between plants and fungi, AMS triggers mycorrhiza-induced protection against plant pathogens. Although the induction of this protection against diverse plant pathogens has been described for several plant species, it is not clear if its onset differs among genotypes within a species. To address this, we have examined if and how this defense response is triggered by AMS in common bean and tomato. Leaflets from three different genotypes of mycorrhizal common beans and two genotypes of tomato were challenged with the pathogens Sclerotinia sclerotiorum and Xanthomonas campestris pv. vesicatoria, respectively, to determine if disease protection induced by mycorrhiza is genotype-specific. We have found that one tomato and two common bean genotypes display this type of protection, although this was not observed in Az Hig common bean and Micro-Tom tomato. These findings indicate that mycorrhiza-induced disease protection is genotype-specific for the species and genotypes included in this study. Previous work has shown that defense induced by mycorrhiza colonization is effective against foliar pathogens, suggesting the existence of a signal that must move from colonized roots to shoots. We examined the possibility that this defense response can be triggered in scions from non-mycorrhizal plants when they were grafted onto mycorrhizal rootstock. Pathogen infection assays were then performed on leaflets of both scions and rootstock, and infection damage was compared to non-grafted plants. Our results indicate that in genotypes displaying mycorrhiza-induced disease protection, scions originating from non-mycorrhizal plants acquired the ability to decrease disease symptoms when grafted onto mycorrhizal rootstocks, indicating that they are responsive to the putative signal that moves from mycorrhizal roots to the upper part of the plant to trigger disease protection. This grafting experimental system may be useful in elucidating the molecular mechanisms involved in the systemic signaling of mycorrhiza-induced defense response.


Mycorrhiza Rhizophagus irregularis Sclerotinia sclerotiorum Phaseolus vulgaris Solanum lycopersicum Xanthomonas campestris pv. vesicatoria 



MLM acknowledges support from the Red de Biotecnología from the Instituto Politécnico Nacional (IPN), the Secretaría de Investigación y Posgrado-IPN (project nos. 20090463 and 20131537), and the Consejo Estatal de Ciencia y Tecnología-Sinaloa grants. MRGA, CGRG and GOMA acknowledge the Consejo Nacional de Ciencia yTecnología of México and the Programa Institucional de Formación de Investigadores (PIFI)-IPN graduate fellowships. GFH acknowledges the Institutional (IPN) and PIFI-IPN graduate fellowships. We thank Brandon Loveall of Improvence for English proofreading of the manuscript.

Conflict of interest

The authors declare no conflicts of interest.


  1. Agrios GN (2005) Plant pathology. Elsevier Academic Press, FloridaGoogle Scholar
  2. Alejo-Iturvide F, Márquez-Lucio M, Morales-Ramírez I, Vázquez-Garcidueñas MS, Olalde-Portugal V (2008) Mycorrhizal protection of chili plants challenged by Phytophthora capsici. Eur J Plant Pathol 120:13–20CrossRefGoogle Scholar
  3. Cameron DD, Neal AL, van Wees SCM, Tonemail J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545PubMedCentralCrossRefPubMedGoogle Scholar
  4. Campos-Soriano L, García-Martínez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defence-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13:579–592CrossRefPubMedGoogle Scholar
  5. Chabot S, Becard G, Piche Y (1992) Life cycle of Glomus intraradix in root organ culture. Mycology 84:315–321CrossRefGoogle Scholar
  6. 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(10):1017–1028CrossRefGoogle Scholar
  7. De Deyn G, Biere A, van der Putten W, Wagenaar R, Klironomos JN (2009) Chemical defense, mycorrhizal colonization and growth responses in Plantago lanceolata L. Oecologia 160:433–442CrossRefPubMedGoogle Scholar
  8. Elsen A, Declerck S, De Waele D (2003) Use of root organ cultures to investigate the interaction between Glomus intraradices and Pratylenchus coffeae. Appl Environ Microbiol 69:4308–4311PubMedCentralCrossRefPubMedGoogle Scholar
  9. Elsen A, Gervacio D, Swennen R, De Waele D (2008) AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18:251–256CrossRefPubMedGoogle Scholar
  10. Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kuhnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16:413–419CrossRefPubMedGoogle Scholar
  11. Gianinazzi-Pearson V, Gianinazzi S (1992) Influence of intergenic grafts between host and non-host legumes on the formation of vesicular-arbuscular mycorrhiza. New Phytol 120:505–508CrossRefGoogle Scholar
  12. Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular Mycorrhizal infection in roots. New Phytol 84:489–500CrossRefGoogle Scholar
  13. Hao Z, Fayolle L, van Tuinen D, Chatagnier O, Li X, Gianinazzi S, Gianinazzi-Pearson V (2012) Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine. J Exp Bot 63:3657–3672PubMedCentralCrossRefPubMedGoogle Scholar
  14. Harada T (2010) Grafting and RNA transport via phloem tissue in horticultural plants. Sci Hortic 125:545–550CrossRefGoogle Scholar
  15. Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, Garcia Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564CrossRefPubMedGoogle Scholar
  16. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Sta Circ 347:1–32Google Scholar
  17. Hol WHG, Cook R (2005) An overview of arbuscular mycorrhizal fungi–nematode interactions. Basic Appl Ecol 6:489–503CrossRefGoogle Scholar
  18. Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664CrossRefPubMedGoogle Scholar
  19. Khaosaad T, García-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39:727–734CrossRefGoogle Scholar
  20. King SR, Davis AR, Liu W, Levi A (2008) Grafting for disease resistance. Hortscience 43:1673–1676Google Scholar
  21. Leyns F, Cleene M, Swings J-G, Ley J (1984) The host range of the genus Xanthomonas. Bot Rev 50:308–356CrossRefGoogle Scholar
  22. 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 the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the Class III Chitinase gene VCH3. Plant Cell Physiol 47:154–163CrossRefPubMedGoogle Scholar
  23. Lingua G, D'Agostino G, Massa N, Antosiano M, Berta G (2002) Mycorrhiza-induced differential response to a yellows disease in tomato. Mycorrhiza 12:191–198CrossRefPubMedGoogle Scholar
  24. Little TM, Hills FJ (1973) Agricultural experimentation and analysis. Wiley, New YorkGoogle Scholar
  25. Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544CrossRefPubMedGoogle Scholar
  26. Lucas WJ, Yoo BC, Kragler F (2001) RNA as a long-distance information macromolecule in plants. Nat Rev Mol Cell Biol 2:849–857CrossRefPubMedGoogle Scholar
  27. Marti E, Gisbert C, Bishop GJ, Dixon MS, Garcia-Martinez JL (2006) Genetic and physiological characterization of tomato cv. Micro-Tom. J Exp Bot 57:2037–2047CrossRefPubMedGoogle Scholar
  28. Mora-Romero GA, Gonzalez-Ortiz MA, Quiroz-Figueroa F, Calderon-Vazquez CL, Medina-Godoy S, Maldonado-Mendoza I, Arroyo-Becerra A, Perez-Torres A, Alatorre-Cobos F, Sanchez F, Lopez-Meyer M (2015) PvLOX2 silencing in common bean roots impairs arbuscular mycorrhiza-induced resistance without affecting symbiosis establishment. Funct Plant Biol 42:18–30CrossRefGoogle Scholar
  29. Noval B, Pérez E, Martínez B, León O, Martínez-Gallardo N, Délano-Frier J (2007) Exogenous systemin has a contrasting effect on disease resistance in mycorrhizal tomato (Solanum lycopersicum) plants infected with necrotrophic or hemibiotrophic pathogens. Mycorrhiza 17:449–460CrossRefPubMedGoogle Scholar
  30. Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161CrossRefGoogle Scholar
  31. Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398CrossRefPubMedGoogle Scholar
  32. Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense response to phytophthora infection in tomato plants. J Exp Bot 53:525–534CrossRefPubMedGoogle Scholar
  33. Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C (2010) Impact of Arbuscular Mycorrhizal symbiosis on plant response to biotic stress: the role of plant defence mechanisms. In: Koltai H, Kapulnik Y (eds) Arbuscular Mycorrhizas: Physiology and Function. Springer, Netherlands, pp. 193–207CrossRefGoogle Scholar
  34. Rosales-Serna R, Acosta-Gallegos JA, Muruaga-Martínez JS, Hernández-Casillas JM, Esquivel-Esquivel G, Pérez-Herrera P (2004) Variedades mejoradas de frijol del Instituto Nacional de Investigaciones Forestales Agrícolas y Pecuarias. Libro Técnico no 6 SAGARPA-INIFAP, MexicoGoogle Scholar
  35. Schübler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421CrossRefGoogle Scholar
  36. Scott JW, Harbaugh BK (1989) Micro-Tom. A miniature dwarf tomato. Florida Agr Exp Sta Circ S 370:1–6Google Scholar
  37. Shi T, Reeves RH, Gilichinsky DA, Friedmann EI (1997) Characterization of viable bacteria from Siberian permafrost by 16S rDNA sequencing. Microb Ecol 33:169–179CrossRefPubMedGoogle Scholar
  38. Singh SP, Gutierrez A, Teran H (2003) Registration of indeterminate tall upright small black seeded common bean germplasmb A-55. Crop Sci 43:1887–1888CrossRefGoogle Scholar
  39. Smith S, Read D (1997) Mycorrhizal symbiosis, 2 edn. Academic Press, LondonGoogle Scholar
  40. St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1996) Enhanced hyphal growth and spore production of the arbuscular mycorrhizal fungus Glomus intraradices in an in vitro system in the absence of host roots. Mycol Res 100:328–332CrossRefGoogle Scholar
  41. Trotta A, Varese GC, Gnavi E, Fusconi A, Sampò S, Berta G (1996) Interactions between the soilborne root pathogen Phytophthora nicotianae var. parasitica and the arbuscular mycorrhizal fungus Glomus mosseae in tomato plants. Plant Soil 185:199–209CrossRefGoogle Scholar
  42. Vos C, Claerhout S, Mkandawire R, Panis B, Waele D, Elsen A (2012a) Arbuscular mycorrhizal fungi reduce root-knot nematode penetration through altered root exudation of their host. Plant Soil 354:335–345CrossRefGoogle Scholar
  43. Vos C, Geerinckx K, Mkandawire R, Panis B, De Waele D, Elsen A (2012b) Arbuscular mycorrhizal fungi affect both penetration and further life stage development of root-knot nematodes in tomato. Mycorrhiza 22:157–163CrossRefPubMedGoogle Scholar
  44. Vos C, Van Den Broucke D, Lombi FM, De Waele D, Elsen A (2012c) Mycorrhiza-induced resistance in banana acts on nematode host location and penetration. Soil Biol Biochem 47:60–66CrossRefGoogle Scholar
  45. Vos CM, Tesfahun AN, Panis B, De Waele D, Elsen A (2012d) Arbuscular mycorrhizal fungi induce local and systemic resistance in tomato against the sedentary nematode Meloidogyne incognita and the migratory nematode Pratylenchus penetrans. Appl Soil Ecol 61:1–6CrossRefGoogle Scholar
  46. Vos C et al. (2013) Mycorrhiza-induced resistance against the root–knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem 60:45–54CrossRefGoogle Scholar
  47. Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Can J Bot 82:1198–1227CrossRefGoogle Scholar
  48. White TJ, Bruns TD, Lee TD, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, pp. 315–322Google Scholar
  49. Williams B, Kabbage M, Kim H-J, Britt R, Dickman MB (2011) Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog 7:e1002107. doi: 10.1371/journal.ppat.1002107

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • G. A. Mora-Romero
    • 1
    • 2
  • R. G. Cervantes-Gámez
    • 1
  • H. Galindo-Flores
    • 1
  • M. A. González-Ortíz
    • 1
  • R. Félix-Gastélum
    • 3
  • I. E. Maldonado-Mendoza
    • 1
  • R. Salinas Pérez
    • 4
  • J. León-Félix
    • 5
  • M. C. Martínez-Valenzuela
    • 2
  • M. López-Meyer
    • 1
    Email author
  1. 1.Instituto Politécnico Nacional, CIIDIR-Sinaloa, Departamento de Biotecnología AgrícolaGuasaveMéxico
  2. 2.Universidad de Occidente, Instituto de Investigación en Ambiente y SaludLos MochisMéxico
  3. 3.Departamento de Ciencias BiológicasUniversidad de OccidenteLos MochisMéxico
  4. 4.INIFAP, Campo Experimental Valle del FuerteLos MochisMéxico
  5. 5.CIAD-Unidad Culiacán, Carretera a Culiacán-El DoradoCuliacánMéxico

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