Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Arbuscular mycorrhisation with Glomus irregulare induces expression of potato PR homologues genes in response to infection by Fusarium sambucinum

Youssef Ismail A B and Mohamed Hijri A C
+ Author Affiliations
- Author Affiliations

A Université de Montréal, Département de sciences biologiques, Institut de recherche en biologie végétale (IRBV), 4101 rue Sherbrooke Est, Montréal, QC, H1X 2B2, Canada.

B Plant Pathology Unit, Department of Plant Protection, Desert Research Center, Cairo, Egypt.

C Corresponding author. Email: mohamed.hijri@umontreal.ca

Functional Plant Biology 39(3) 236-245 https://doi.org/10.1071/FP11218
Submitted: 28 September 2011  Accepted: 13 January 2012   Published: 21 February 2012

Abstract

Arbuscular mycorrhizal fungi (AMF) are symbiotic, root-inhabiting fungi colonising a wide range of vascular plant species. We previously showed that AMF modulate the expression of mycotoxin genes in Fusarium sambucinum. Here, we tested the hypothesis that AMF may induce defence responses in potato to protect against infection with F. sambucinum. We analysed the response of AMF-colonised potato plants to the pathogenic fungus F. sambucinum by monitoring the expression of defence-related genes ChtA3, gluB, CEVI16, OSM-8e and PR-1. In response to F. sambucinum infection, we found that the AMF treatment upregulated the expression of all defence genes except OSM-8e in potato roots at 72 and 120 h post infection (hpi). However, we found variable transcriptional regulation with gluB and CEVI16 in shoots at both times 72 and 120 hpi in AMF-colonisation and infected plants. Overall, differential regulation of defence-related genes in leaf tissues indicate that AMF are a systemic bio-inducer and their effect could extend into non-infected parts. Thus, AMF significantly suppressed disease severity of F. sambucinum on potato plants compared with those infected and non-mycorrhizal plants. Furthermore, the AMF treatment decreased the negative effects of F. sambucinum on biomass and potato tuber production.

Additional keywords: arbuscular mycorrhizal fungi, Fusarium sambucinum, gene expression, Glomus irregulare, induced resistance, mycotoxins, potatoes, PR proteins, qRT-PCR.


References

Bakker PAHM, Pieterse CMJ, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97, 239–243.
Induced systemic resistance by fluorescent Pseudomonas spp.Crossref | GoogleScholarGoogle Scholar |

Beerhues L, Kombrink E (1994) Primary structure and expression of mRNAs encoding basic chitinase and 1,3-beta-glucanase in potato. Plant Molecular Biology 24, 353–367.
Primary structure and expression of mRNAs encoding basic chitinase and 1,3-beta-glucanase in potato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktVagt7w%3D&md5=231b5e44d09330ef4d1138fc0839aabaCAS |

Blilou I, Bueno P, Ocampo JA, García-Garrido JM (2000) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae. Mycological Research 104, 722–725.
Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXls1Gnu7Y%3D&md5=7cc1068d5b6947e7a1d0e8648b063057CAS |

Chet I, Inbar J (1994) Biological control of fungal pathogens. Applied Biochemistry and Biotechnology 48, 37–43.
Biological control of fungal pathogens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M%2FntVSqtA%3D%3D&md5=b3c89275d5ca06582cce66fb78a82f54CAS |

Clarke JD, Volko SM, Ledford H, Ausubel FM, Dong X (2000) Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis. The Plant Cell 12, 2175–2190.
Roles of salicylic acid, jasmonic acid, and ethylene in cpr-induced resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1Kg&md5=705e3b8b0079a2decbdaec0eb39d0975CAS |

Desjardins AE, Hohn TM (1997) Mycotoxins in plant pathogenesis. Molecular Plant-Microbe Interactions 10, 147–152.
Mycotoxins in plant pathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhsFKiurg%3D&md5=e0edbfa77eeb83b240c0562beae8b1daCAS |

Desjardins AE, Plattner RD (1989) Trichothecene toxin production by strains of Gibberella pulicaris (Fusarium sambucinum) in liquid culture and in potato tubers. Journal of Agricultural and Food Chemistry 37, 388–392.
Trichothecene toxin production by strains of Gibberella pulicaris (Fusarium sambucinum) in liquid culture and in potato tubers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXhtlWrsLg%3D&md5=149c925e032091aeb890297b89b7b8beCAS |

Desjardins AE, Hohn TM, McCormick SP (1992) Effect of gene disruption of trichodiene synthase on the virulence of Gibberella pulicaris. Molecular Plant-Microbe Interactions 5, 214–222.
Effect of gene disruption of trichodiene synthase on the virulence of Gibberella pulicaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XksVCnsLc%3D&md5=902eeae688d908a8bdb5cc270e6bd6ecCAS |

Dumas-Gaudot E, Asselin A, Gianinazzi-Pearson V, Gollette A, Gianinazzi S (1994) Chitinase isoforms in roots of various pea genotypes infected with arbuscular mycorrhizal fungi. Plant Science 99, 27–37.
Chitinase isoforms in roots of various pea genotypes infected with arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXkslymtLw%3D&md5=c573e47f96500ef6f066a67066c6b53dCAS |

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261, 754–756.
Requirement of salicylic acid for the induction of systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsFKntr8%3D&md5=ad75d1ca6f1a79ad5dd46b37c6363f6eCAS |

Gao L-L, Knogge W, Delp G, Smith FA, Smith SE (2004) Expression patterns of defence-related genes in different types of arbuscular mycorrhizal development in wild-type and mycorrhiza-defective mutant tomato. Molecular Plant-Microbe Interactions 17, 1103–1113.
Expression patterns of defence-related genes in different types of arbuscular mycorrhizal development in wild-type and mycorrhiza-defective mutant tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvVarurc%3D&md5=acb3f30bffe12192bb65caa42a5faa35CAS |

Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. Journal of Experimental Botany 53, 1377–1386.
Regulation of the plant defence response in arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XktlWjtLo%3D&md5=18d8a47f456bdba96d563e930226f35fCAS |

Gavito ME, Schweiger P, Jakobsen I (2003) P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment. Global Change Biology 9, 106–116.
P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment.Crossref | GoogleScholarGoogle Scholar |

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 Phytologist 133, 45–57.
Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |

Haneef Khan M, Meghvansi MK, Panwar V, Gogoi HK, Singh L (2010) Arbuscular mycorrhizal fungi-induced signalling in plant defence against phytopathogens. Journal of Phycology 2, 53–69.

Hijri M, Sanders IR (2004) The arbuscular mycorrhizal fungus Glomus intraradices is haploid and has a small genome size in the lower limit of eukaryotes. Fungal Genetics and Biology 41, 253–261.
The arbuscular mycorrhizal fungus Glomus intraradices is haploid and has a small genome size in the lower limit of eukaryotes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtVequg%3D%3D&md5=f42f3d74051271ddcbf40cc0c6263762CAS |

Hijri M, Niculita H, Sanders IR (2007) Molecular characterization of chromosome termini of the arbuscular mycorrhizal fungus Glomus intraradices (Glomeromycota). Fungal Genetics and Biology 44, 1380–1386.
Molecular characterization of chromosome termini of the arbuscular mycorrhizal fungus Glomus intraradices (Glomeromycota).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ylsLnJ&md5=095bc81ce06cc188a3190aefb37bb9caCAS |

Hiraga S, Sasaki K, Ito H, Ohashi Y, Matsui H (2001) A large family of class III plant peroxidases. Plant & Cell Physiology 42, 462–468.
A large family of class III plant peroxidases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVWntrY%3D&md5=5c104bccfa530545f3780b752025e530CAS |

Ismail Y, McCormick S, Hijri M (2011) A fungal symbiont of plant-roots modulates mycotoxin gene expression in the pathogen Fusarium sambucinum. PLoS ONE 6, e17990
A fungal symbiont of plant-roots modulates mycotoxin gene expression in the pathogen Fusarium sambucinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksVOqu74%3D&md5=65b4ba8da85864fdefd3da2fabd4b3edCAS |

James JD (1998) Mycorrhizal symbiosis. S.E. Smith and D.J. Read. Plant Growth Regulation 25, 71
Mycorrhizal symbiosis. S.E. Smith and D.J. Read.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXis1Gju7c%3D&md5=030f830abcecc4781cc0988d29ed555dCAS |

Kasiamdari RS, Smith SE, Smith FA, Scott ES (2002) Influence of the mycorrhizal fungus, Glomus coronatum and soil phosphorus on infection and disease caused by binucleate Rhizoctonia Rhizoctonia solani on mung bean (Vigna radiata). Plant and Soil 238, 235–244.
Influence of the mycorrhizal fungus, Glomus coronatum and soil phosphorus on infection and disease caused by binucleate Rhizoctonia Rhizoctonia solani on mung bean (Vigna radiata).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xitl2qsLc%3D&md5=a73eb7906c5fae5ee80211c3e8b525a6CAS |

Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Reports 21, 829–837.

Lahlali R, Hijri M (2010) Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants. FEMS Microbiology Letters 311, 152–159.
Screening, identification and evaluation of potential biocontrol fungal endophytes against Rhizoctonia solani AG3 on potato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtleqsLvM&md5=e1da4e8e77de05261564f4ff47e2ac0fCAS |

Lecomte J, St-Arnaud M, Hijri M (2011) Isolation and identification of soil bacteria growing at the expense of arbuscular mycorrhizal fungi. FEMS Microbiology Letters 317, 43–51.
Isolation and identification of soil bacteria growing at the expense of arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvFamsrk%3D&md5=e03fcb996a4d0cfd836386586111a505CAS |

Lehtonen MJ, Somervuo P, Valkonen JPT (2008) Infection with Rhizoctonia solani induces defense genes and systemic resistance in potato sprouts grown without light. Phytopathology 98, 1190–1198.
Infection with Rhizoctonia solani induces defense genes and systemic resistance in potato sprouts grown without light.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlamsbnN&md5=397e1cc60de47798de7aea88b39e0df2CAS |

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, 443–448.
Role of the modification in root exudation induced by arbuscular mycorrhizal colonization on the intraradical growth of Phytophthora nicotianae in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVGjtLw%3D&md5=81bb74a167a3bc67e3defe5b524fae62CAS |

Liu D, Raghothama KG, Hasegawa PM, Bressan RA (1994) Osmotin overexpression in potato delays development of disease symptoms. Proceedings of the National Academy of Sciences of the United States of America 91, 1888–1892.
Osmotin overexpression in potato delays development of disease symptoms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFaktbk%3D&md5=aac9d0b413502e898c31f2d7b1ebae92CAS |

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. The Plant Journal 50, 529–544.
Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsVWms7Y%3D&md5=27ee7a86c840917cd6aba615e1ee28faCAS |

Loon L (1997) Induced resistance in plants and the role of pathogenesis-related proteins. European Journal of Plant Pathology/European Foundation for Plant Pathology 103, 753–765.

Niemira B, Hammerschmidt R, Safir G (1996) Postharvest suppression of potato dry rot (Fusarium sambucinum) in prenuclear minitubers by arbuscular mycorrhizal fungal inoculum. American Journal of Potato Research 73, 509–515.
Postharvest suppression of potato dry rot (Fusarium sambucinum) in prenuclear minitubers by arbuscular mycorrhizal fungal inoculum.Crossref | GoogleScholarGoogle Scholar |

Norman J, Atkinson D, Hooker J (1996) Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae. Plant and Soil 185, 191–198.
Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXntlyksQ%3D%3D&md5=f4e6f9ec6f254624b4a474c63a99258bCAS |

Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36
Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.Crossref | GoogleScholarGoogle Scholar |

Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1998) Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophthora parasitica. Journal of Experimental Botany 49, 1729–1739.
Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophthora parasitica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmslagtrc%3D&md5=4186e1239d326342ad71c8b7a1cc9e8bCAS |

Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1999) β-1,3-Glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Science 141, 149–157.
β-1,3-Glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsVWlu7c%3D&md5=9f325ff7ec4cc7d6d92093298a0ee9adCAS |

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 responses to Phytophthora infection in tomato plants. Journal of Experimental Botany 53, 525–534.
Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVegtL4%3D&md5=3c6f19e7b753458394420f9f93ac637bCAS |

Pozo MJ, Van Loon LC, Pieterse CMJ (2004) Jasmonates – signals in plant-microbe interactions. Journal of Plant Growth Regulation 23, 211–222.

Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In ‘Mycorrhizas – functional processes and ecological impact’. (Eds C Azcòn-Aguilar, JM Barea, S Gianinazzi, V Gianinazzi-Pearson) pp. 123–136. (Springer-Verlag: Berlin)

Ruiz R, Herrera C, Ghislain M, Gebhardt C (2005) Organization of phenylalanine ammonia lyase (PAL), acidic PR-5 and osmotin-like (OSM) defence-response gene families in the potato genome. Molecular Genetics and Genomics 274, 168–179.
Organization of phenylalanine ammonia lyase (PAL), acidic PR-5 and osmotin-like (OSM) defence-response gene families in the potato genome.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFChsLnJ&md5=038c2eb9029913ddf16037f2681354e3CAS |

Ruiz-Lozano JM, Roussel H, Gianinazzi S, Gianinazzi-Pearson V (1999) Defense genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes. Molecular Plant-Microbe Interactions 12, 976–984.
Defense genes are differentially induced by a mycorrhizal fungus and Rhizobium sp. in wild-type and symbiosis-defective pea genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVWksr4%3D&md5=ea0fc374eab5c83477cf2e42a518778dCAS |

Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiology 133, 16–20.
Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlait7o%3D&md5=00e3f15f66680c4262c160fc18cfcea5CAS |

St-Arnaud M, Vujanovic V (2007) ‘Effects of the arbuscular mycorrhizal symbiosis on plant diseases and pests In ‘Mycorrhiza in crop production’. (Eds C Hamel, C Plaenchette) pp. 67–122. (Haworth’s Food Production Press: New York)

Stein E, Molitor A, Kogel K-H, Waller F (2008) Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1. Plant & Cell Physiology 49, 1747–1751.
Systemic resistance in Arabidopsis conferred by the mycorrhizal fungus Piriformospora indica requires jasmonic acid signaling and the cytoplasmic function of NPR1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFSnsb%2FL&md5=4637bd8fc01c12125cfc737aa8cf2ac0CAS |

Suttle JC (1998) Involvement of ethylene in potato microtuber dormancy. Plant Physiology 118, 843–848.
Involvement of ethylene in potato microtuber dormancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnsFekt70%3D&md5=0022fdec43fe901fcb6a5873b4a7840aCAS |

van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annual Review of Phytopathology 44, 135–162.
Significance of inducible defense-related proteins in infected plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVylsLnK&md5=7b7403ae998d900bde53c0ea3fc5aea8CAS |

Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Current Opinion in Plant Biology 11, 443–448.
Plant immune responses triggered by beneficial microbes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVamurw%3D&md5=889aaca2641992a55e70c2d28332802cCAS |

Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Applied and Environmental Microbiology 64, 5004–5007.

Walters D, Walsh D, Newton A, Lyon G (2005) Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology 95, 1368–1373.
Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCjtL%2FK&md5=57211e029f4b3e4b4d8d58874e6dd042CAS |

Wharton PS, Tumbalam P, Kirk WW (2006) First report of potato tuber sprout rot caused by Fusarium sambucinum in Michigan. Plant Disease 90, 1460
First report of potato tuber sprout rot caused by Fusarium sambucinum in Michigan.Crossref | GoogleScholarGoogle Scholar |

Yao M, Tweddell R, Désilets H (2002) Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micropropagated potato plantlets and on the extent of disease caused by Rhizoctonia solani. Mycorrhiza 12, 235–242.
Effect of two vesicular-arbuscular mycorrhizal fungi on the growth of micropropagated potato plantlets and on the extent of disease caused by Rhizoctonia solani.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38nhslKktw%3D%3D&md5=590246815e991239f1d0190bd7560744CAS |

Zhu B, Chen THH, Li PH (1995) Activation of two osmotin-like protein genes by abiotic stimuli and fungal pathogen in transgenic potato plants. Plant Physiology 108, 929–937.
Activation of two osmotin-like protein genes by abiotic stimuli and fungal pathogen in transgenic potato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvFGmt7s%3D&md5=092da198dcb6b7c1b3bb33d15fdfd811CAS |