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Role of Root Exudates and Rhizosphere Microflora in the Arbuscular Mycorrhizal Fungi-Mediated Biocontrol of Phytophthora nicotianae in Tomato

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Symbiotic Fungi

Part of the book series: Soil Biology ((SOILBIOL,volume 18))

Abstract

This chapter focuses on the biocontrol mechanisms determined by the arbuscular mycorrhizal fungi (AMF) Glomus intraradices and Glomus mosseae against Phytophthora nicotianae in tomato. A massive attractiveness of zoospores by root exudates is crucial for an efficient host-tissue invasion by this pathogen. Defense responses were shown in mycorrhizal tomato, supporting their role in the AMF-mediated biocontrol. Exudates from transformed mature mycorrhizal tomato roots were repulsive towards zoospores in vitro, suggesting that modification in root exudation may also decrease the ability of the pathogen to infect mycorrhizal roots. Nonetheless, in soil, application of mycorrhizal root exudates on noncolonized tomato roots did not inhibit the intraradical growth ofP. nicotianae, whereas direct AMF inoculation did. By PCR-DGGE profiling, mycorrhizal colonization was shown to significantly modify the rhizosphere bacterial community, whereas the application of mycorrhizal root exudates did not. The physical presence of AMF may therefore be required for the establishment of a mycorrhiza-specific antagonistic bacterial community. Some bacteria isolated from AMF spores or mycorrhizospheres showed antagonism against various soilborne pathogens. It is likely that the biocontrol studied here would not only be orchestrated by the fungi themselves, but also depend on the relationships they maintain with other soil microorganisms.

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References

  • Addepalli MK, Fujita Y (2001) Serological detection of red rot disease initiation stages of microbial pathogen, Pythium porphyrae (Oomycota) on Porphyra yezoensis. J Appl Phycol 13:221–227

    Google Scholar 

  • Allen RN, Newhook FJ (1973) Chemotaxis of zoospores of Phytophthora cinnamomi to ethanol in capillaires of soil pore dimensions. Trans Br Mycol Soc 61:287–302

    CAS  Google Scholar 

  • Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1997) Bacteria from rhizosphere and hyphosphere soils of different arbuscular–mycorrhizal fungi. Plant Soil 192:71–79

    CAS  Google Scholar 

  • Artursson V, Jansson JK (2003) Use of bromodeoxyuridine immunocapture to identify active bacteria associated with arbuscular mycorrhizal hyphae. Appl Environ Microbiol 69:6208–6215

    CAS  PubMed  Google Scholar 

  • Azaizeh HA, Marschner H, Romheld V, Wittenmayer L (1995) Effects of a vesicular–arbuscular mycorrhizal fungus and other soil microorganisms on growth, mineral nutrient acquisition and root exudation of soil-grown maize plants. Mycorrhiza 5:321–327

    Google Scholar 

  • Azcón R, Gomez M, Tobar R (1996) Physiological and nutritional responses by Lactuca sativa to nitrogen sources and mycorrhizal fungi under drought conditions. Biol Fertil Soil 22:156–161

    Google Scholar 

  • Bååth E, Hayman DS (1983) Plant growth responses to vesicular–arbuscular mycorrhizae XIV. Interactions with Verticillium wilt on tomato plants. New Phytol 95:419–426

    Google Scholar 

  • Bansal M, Mukerji KG (1994) Positive correlation between VAM-induced changes in root exudation and mycorrhizosphere mycoflora. Mycorrhiza 5:39–44

    Google Scholar 

  • Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192

    CAS  Google Scholar 

  • Bianciotto V, Bonfante P (2002) Arbuscular mycorrhizal fungi: a specialised niche for rhizospheric and endocellular bacteria. Anton Leeuw Int J G 81:365–371

    CAS  Google Scholar 

  • Bianciotto V, Minerdi D, Perotto S, Bonfante P (1996a) Cellular interactions between arbuscular mycorrhizal fungi and rhizosphere bacteria. Protoplasma 193:123–131

    Google Scholar 

  • Bianciotto V, Bandi C, Minerdi D, Sironi M, Tichy HV, Bonfante P (1996b) An obligately endosymbiotic mycorrhizal fungus itself harbors obligately intracellular bacteria. Appl Environ Microbiol 62:3005–3010

    CAS  PubMed  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001a) Extracellular polysaccharides are involved in the attachment of Azospirillum brasilense and Rhizobium leguminosarum to arbuscular mycorrhizal structures. Eur J Histochem 45:39–49

    CAS  PubMed  Google Scholar 

  • Bianciotto V, Andreotti S, Balestrini R, Bonfante P, Perotto S (2001b) Mucoid mutants of the biocontrol strain Pseudomonas fluorescens CHA0 show increased ability in biofilm formation on mycorrhizal and nonmycorrhizal carrot roots. Mol Plant Microbe Int 14:255–260

    CAS  Google Scholar 

  • Bianciotto V, Lumini E, Bonfante P, Vandamme P (2003) ‘Candidatus Glomeribacter gigasporarum’ gen. nov., sp nov., an endosymbiont of arbuscular mycorrhizal fungi. Int J Syst Evol Micr 53:121–124

    CAS  Google Scholar 

  • Bianciotto V, Genre A, Jargeat P, Lumini E, Bécard G, Bonfante P (2004) Vertical transmission of endobacteria in the arbuscular mycorrhizal fungus Gigaspora margarita through generation of vegetative spores. Appl Environ Microbiol 70:3600–3608

    CAS  PubMed  Google Scholar 

  • Bødker L, Kjøller R, Kristensen K, Rosendahl S (2002) Interactions between indigenous arbuscular mycorrhizal fungi and Aphanomyces euteiches in field-grown pea. Mycorrhiza 12:7–12

    PubMed  Google Scholar 

  • Bonfante P (2003) Plants, mycorrhizal fungi and endobacteria: a dialog among cells and genomes. Biol Bull 204:215–220

    CAS  PubMed  Google Scholar 

  • Bowen GD, Rovira AD (1999) The rhizosphere and its management to improve plant growth. Advn Agron 66:1–102

    Google Scholar 

  • Budi SW, van Tuinen D, Martinotti G, Gianinazzi S (1999) Isolation from the Sorghum bicolor mycorrhizosphere of a bacterium compatible with arbuscular mycorrhiza development and antagonistic towards soilborne fungal pathogens. Appl Environ Microbiol 65:5148–5150

    CAS  PubMed  Google Scholar 

  • Budi SW, van Tuinen D, Arnould C, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S (2000) Hydrolytic enzyme activity of Paenibacillus sp. strain B2 and effects of the antagonistic bacterium on cell integrity of two soil-borne pathogenic fungi. Appl Soil Ecol 15:191–199

    Google Scholar 

  • Calvo-Bado LA, Petch G, Parsons NR, Morgan JAW, Pettitt TR, Whipps JM (2006) Microbial community responses associated with the development of oomycete plant pathogens on tomato roots in soilless growing systems. J Appl Microbiol 100:1194–1207

    CAS  PubMed  Google Scholar 

  • Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225

    CAS  Google Scholar 

  • Chin A, Woeng TFC, Bloemberg GV, Mulders IHM, Dekkers LC, Lugtenberg BJJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant Microbe Int 13:1340–1345

    Google Scholar 

  • Christensen H, Jakobsen I (1993) Reduction of bacterial growth by a vesicular–arbuscular mycorrhizal fungus in the rhizosphere of cucumber (Cucumis sativus L). Biol Fertil Soil 15:253–258

    Google Scholar 

  • Connolly MS, Williams N, Heckman CA, Morris PF (1999) Soybean isoflavones trigger a calcium influx in Phytophthora sojae. Fungal Genet Biol 28:6–11

    CAS  PubMed  Google Scholar 

  • Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonisation patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232

    CAS  Google Scholar 

  • 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 Int 11:1017–1028

    CAS  Google Scholar 

  • Davis RM, Menge JA (1980) Influence of Glomus fasciculatus and soil phosphorus on Phytophthora root rot of Citrus. Phytopathology 70:447–452

    CAS  Google Scholar 

  • Deacon JW (1996) Ecological implications of recognition events in the pre-infection stages of root pathogens. New Phytol 133:135–145

    Google Scholar 

  • Deacon JW, Donaldson SP (1993) Molecular recognition in the homing responses of zoosporic fungi, with special reference to Pythium and Phytophthora. Mycol Res 97:1153–1171

    CAS  Google Scholar 

  • Diouf D, Duponnois R, Ba AT, Neyra M, Lesueur D (2005) Symbiosis of Acacia auriculiformis and Acacia mangium with mycorrhizal fungi and Bradyrhizobium spp. improves salt tolerance in greenhouse conditions. Funct Plant Biol 32:1143–1152

    CAS  Google Scholar 

  • Donaldson SP, Deacon JW (1993a) Effects of amino acids and sugars on zoospore taxis, encystment and cyst germination in Pythium aphanidermatum (Edson) Fitzp., P. catenulatum Matthews and P. dissotocum Drechs. New Phytol 123:289–295

    CAS  Google Scholar 

  • Donaldson SP, Deacon JW (1993b) Differential encystment of zoospores of Pythium species by saccharides in relation to establishment on roots. Physiol Mol Plant P 42:177–184

    CAS  Google Scholar 

  • Dukes PD, Apple JL (1961) Chemotaxis of zoospores of Phytophthora parasitica var. nicotianae by plant roots and certain chemical solutions. Phytopathol Note 51:195–197

    CAS  Google Scholar 

  • Edwards SG, Young JPW, Fitter AH (1998) Interactions between Pseudomonas fluorescens biocontrol agents and Glomus mosseae, an arbuscular mycorrhizal fungus, within the rhizosphere. FEMS Microbiol Lett 166:297–303

    CAS  Google Scholar 

  • Erwin C, Ribeiro OK (1996) Phytophthora diseases worldwide. The American Phytopathological Society Press, St Paul, MN

    Google Scholar 

  • Estrada-Garcia MT, Ray TC, Green JR, Callow JA, Kennedy JF (1990) Encystment of Pythium aphanidermatum zoospores is induced by root mucilage polysaccharides, pectin and a monoclonal antibody to a surface antigen. J Expt Bot 41:693–699

    CAS  Google Scholar 

  • Fester T, Maier W, Strack D (1999) Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 8:241–246

    CAS  Google Scholar 

  • Fester T, Hause B, Schmidt D, Halfmann K, Schmidt J, Wray V, Hanse G, Strack D (2002a) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol 43:256–265

    CAS  PubMed  Google Scholar 

  • Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002b) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154

    CAS  PubMed  Google Scholar 

  • Fester T, Wray V, Nimtz M, Strack D (2005) Is stimulation of carotenoid biosynthesis in arbuscular mycorrhizal roots a general phenomenon? Phytochemistry 66:1781–1786

    CAS  PubMed  Google Scholar 

  • Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533

    Google Scholar 

  • Filippi C, Bagnoli G, Citernesi AS, Giovannetti M (1998) Ultrastructural spatial distribution of bacteria associated with sporocarps of Glomus mosseae. Symbiosis 24:1–12

    Google Scholar 

  • Fortin JA, Bécard G, Declerck S, Dalpé Y, St-Arnaud M, Coughland A, Piché Y (2002) Arbuscular mycorrhiza on root-organ cultures. Can J Bot 80:1–20

    CAS  Google Scholar 

  • Gange AC (2001) Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol 150:611–618

    Google Scholar 

  • Gange AC, Nice HE (1997) Performance of the thistle gall fly, Urophora cardui, in relation to host plant nitrogen and mycorrhizal colonization. New Phytol 137:335–343

    Google Scholar 

  • Graham JH, Leonard RT, Menge JA (1981) Membrane-mediated decrease in root exudation responsible for phosphorus inhibition of vesicular–arbuscular mycorrhiza formation. Plant Physiol 68:548–552

    CAS  PubMed  Google Scholar 

  • Griffiths BS, Ritz K, Ebblewhite N, Dobson G (1999) Soil microbial community structure: effects of substrate loading rates. Soil Biol Biochem 31:145–153

    CAS  Google Scholar 

  • Grote D, Claussen W (2001) Severity of root rot on tomato plants caused by Phytophthora nicotianae under nutrient- and light-stress conditions. Plant Pathol 50:702–707

    Google Scholar 

  • Halsall DM (1975) Zoospore chemotaxis in Australian isolates of Phytophthora. Can J Microbiol 22:409–422

    Article  Google Scholar 

  • Hardham AR, Cahill DM, Cope M, Gabor BK, Gubler F, Hyde GJ (1994) Cell surface antigens of Phytophthora spores — biological and taxonomic characterization. Protoplasma 181:213–232

    Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220

    CAS  PubMed  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110

    CAS  PubMed  Google Scholar 

  • Hickman CJ (1970) Biology of Phytophthora zoospores. Phytopathology 60:1128–1135

    Article  Google Scholar 

  • Ho HH, Hickman CJ (1967a) Asexual reproduction and behavior of zoospores of Phytophthora megasperma var. sojae. Can J Bot 45:1963–1981

    Google Scholar 

  • Ho HH, Hickman CJ (1967b) Factors governing zoospore responses of Phytophthora megasperma var. sojae to plant roots. Can J Bot 45:1983–1994

    Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allene oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410

    CAS  PubMed  Google Scholar 

  • Jargeat P, Cosseau C, Ola'h B, Jauneau A, Bonfante P, Batut J, Bécard G (2004) Isolation, free-living capacities, and genome structure of “Candidatus glomeribacter gigasporarum,” the endocellular bacterium of the mycorrhizal fungus Gigaspora margarita. J Bacteriol 186:6876–6884

    CAS  PubMed  Google Scholar 

  • Jones SW, Donaldson SP, Deacon JW (1991) Behaviour of zoospores and zoospore cysts in relation to root infection by Pythium aphannidermatum. New Phytol 117:289–301

    Google Scholar 

  • Kapoor R, Kaur M, Mukerji KG (2000) VAM and phosphorus induced changes in the rhizosphere ecology of Anethum graveolens L. J Expt Biol 21:185–191

    Google Scholar 

  • Khew KL, Zentmyer GA (1973) Chemotactic response of zoospores of five species of Phytophthora. Phytopathology 63:1511–1517

    CAS  Google Scholar 

  • Kishor PBK, Sangam S, Amrutha RN, Laxmi PS, Naidu KR, Rao K, Rao S, Reddy KJ, Theriappan P, Sreenivaslu N (2005) Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Curr Sci 88:424–438

    CAS  Google Scholar 

  • Kozdrój J, van Elsas JD (2000) Response of the bacterial community to root exudates in soil polluted with heavy metals assessed by molecular and cultural approaches. Soil Biol Biochem 32:1405–1417

    Google Scholar 

  • Krishna KR, Bagyaraj DJ (1983) Interaction between Glomus fasciculatum and Sclerotium rolfsii in peanut. Can J Bot 61:2349–2351

    CAS  Google Scholar 

  • Kuznetsov VV, Shevyakova NI (1999) Proline under stress: biological role, metabolism, and regulation. Russ J Plant Physiol 46:274–287

    CAS  Google Scholar 

  • Labour K, Jolicoeur M, St-Arnaud M (2003) Arbuscular mycorrhizal responsiveness of in vitro tomato root lines is not related to growth and nutrient uptake rates. Can J Bot 81:645–656

    CAS  Google Scholar 

  • Larsen J, Bødker L (2001) Interactions between pea root-inhabiting fungi examined using signature fatty acids. New Phytol 149:487–493

    CAS  Google Scholar 

  • Leaño EM, Vrijmoed LLP, Jones EBG (1998) Zoospore chemotaxis of two mangrove strains of Halophytophthora vesicula from Mai Po, Hong Kong. Mycologia 90:1001–1008

    Google Scholar 

  • Levy A, Chang BJ, Abbott LK, Kuo J, Harnett G, Inglis TJJ (2003) Invasion of spores of the arbuscular mycorrhizal fungus Gigaspora decipiens by Burkholderia spp. Appl Environ Microbiol 69:6250–6256

    CAS  PubMed  Google Scholar 

  • Lioussanne L, Jolicoeur M, St-Arnaud M (2006a) The inhibition of Phytophthora nicotianae induced by AMF is not related to tomato root exudation transformation. In: Abstracts of the 5th International Conference on Mycorrhiza, Granada, Spain, 20–29 July, p 249

    Google Scholar 

  • Lioussanne L, Keough A, Jolicoeur M, St-Arnaud M (2006b) Diversity of Glomus mosseae spore-associated bacteria and their antagonism over soil-borne pathogens in vitro. In: Abstracts of the 5th International Conference on Mycorrhiza, Granada, Spain, 20–29 July, p 203

    Google Scholar 

  • 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 zoospores of the pathogen Phytophthora nicotianae. Soil Biol Biochem 40:2217–2224

    CAS  Google Scholar 

  • Ludwig-Müller J, Bennett RN, García-Garrido JM, Piché Y, Vierheilig H (2002) Reduced arbuscular mycorrhizal root colonization in Tropaeolum majus and Carica papaya after jasmonic acid application can not be attributed to increased glucosinolate levels. J Plant Physiol 159:517–523

    Google Scholar 

  • Lugtenberg BJJ, Kravchenko LV, Simons M (1999) Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ Microbiol 1:439–446

    CAS  PubMed  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    CAS  Google Scholar 

  • MacDonald RM, Chandler MR, Mosse B (1982) The occurrence of bacterium-like organelles in vesicular–arbuscular mycorrhizal fungi. New Phytol 90:659–663

    Google Scholar 

  • Mansfeld-Giese K, Larsen J, Bødker L (2002) Bacterial populations associated with mycelium of the arbuscular mycorrhizal fungus Glomus intraradices. FEMS Microbiol Ecol 41:133–140

    CAS  PubMed  Google Scholar 

  • Marschner P, Timonen S (2005) Interactions between plant species and mycorrhizal colonization on the bacterial community composition in the rhizosphere. Appl Soil Ecol 28:23–36

    Google Scholar 

  • Marschner P, Crowley DE, Higashi RM (1997) Root exudation and physiological status of a root-colonizing fluorescent pseudomonad in mycorrhizal and non-mycorrhizal pepper (Capsicum annuum L). Plant Soil 189:11–20

    CAS  Google Scholar 

  • Marschner P, Crowley DE, Lieberei R (2001) Arbuscular mycorrhizal infection changes the bacterial 16S rDNA community composition in the rhizosphere of maize. Mycorrhiza 11:297–302

    CAS  Google Scholar 

  • Mayo K, Davis RE, Motta J (1986) Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78:426–431

    Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    CAS  PubMed  Google Scholar 

  • Morris PF, Ward EWB (1992) Chemoattraction of zoospores of the soybean pathogen, Phytophthora sojae, by isoflavones. Physiol Mol Plant Pathol 40:17–22

    CAS  Google Scholar 

  • Morris BM, Reid B, Gow NAR (1995) Tactic response of zoospores of the fungus Phytophthora palmivora to solutions of different pH in relation to plant infection. Microbiology 141:1231–1237

    CAS  Google Scholar 

  • Norman JR, Atkinson D, Hooker JE (1996) Arbuscular mycorrhizal fungal-induced alteration to root architecture in strawberry and induced resistance to the root pathogen Phytophthora fragariae. Plant Soil 185:191–198

    CAS  Google Scholar 

  • Norman JR, Hooker JE (2000) Sporulation of Phytophthora fragariae shows greater stimulation by exudates of non-mycorrhizal than by mycorrhizal strawberry roots. Mycol Res 104:1069–1073

    Google Scholar 

  • Omokolo ND, Nankeu DJ, Niemenak N, Djocgoue PF (2002) Analysis of amino acids and carbohydrates in the cortex of nine clones of Theobroma cacao L. in relation to their susceptibility to Phytophthora megakarya Bra. and Grif. Crop Protect 21:395–402

    CAS  Google Scholar 

  • Park S, Takano Y, Matsuura H, Yoshihara T (2004) Antifungal compounds from the root and root exudate of Zea mays. Biosci Biotech Biochem 68:1366–1368

    CAS  Google Scholar 

  • Pennanen T, Caul S, Daniell TJ, Griffiths BS, Ritz K, Wheatley RE (2004) Community-level responses of metabolically-active soil microorganisms to the quantity and quality of substrate inputs. Soil Biol Biochem 36:841–848

    CAS  Google Scholar 

  • 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 77:891–897

    Google Scholar 

  • Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398.

    CAS  PubMed  Google Scholar 

  • Pozo MJ, Dumas-Gaudot E, Slezack S, Cordier C, Asselin A, Gianinazzi S, Gianinazzi-Pearson V, Azcón-Aguilar C, Barea JM (1996) Induction of new chitinase isoforms in tomato roots during interactions with Glomus mosseae and/or Phytophthora nicotianae var parasitica. Agronomie 16:689–697

    Google 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. J Expt Bot 49:1729–1739

    CAS  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1999) Beta-1,3-glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141:149–157

    CAS  Google Scholar 

  • Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcón-Aguilar C (2002a) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Expt Bot 53:525–534

    CAS  Google Scholar 

  • Pozo MJ, Slezack-Deschaumes S, Dumas-Gaudot E, Gianinazzi S, Azcón-Aguilar C (2002b) Plant defense responses induced by arbuscular mycorrhizal fungi. In: Gianinazzi S, Schuepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture: from genes to bioproducts. Birkhauser Verlag Ag, Basel, Switzerland, pp 103–111

    Google Scholar 

  • Pozo MJ, Van Loon LC, Pieterse CMJ (2004) Jasmonates — Signals in plant–microbe interactions. J Plant Growth Regul 23:211–222

    CAS  Google Scholar 

  • Rai VK (2002) Role of amino acids in plant responses to stresses. Biol Plant 45:481–487

    CAS  Google Scholar 

  • Ravnskov S, Nybroe O, Jakobsen I (1999) Influence of an arbuscular mycorrhizal fungus on Pseudomonas fluorescens DF57 in rhizosphere and hyphosphere soil. New Phytol 142:113–122

    Google Scholar 

  • Reid B, Morris BM, Gow NAR (1995) Calcium-dependent, genus-specific autoaggregation of zoospores of phytopathogenic fungi. Expt Mycol 19:202–213

    CAS  Google Scholar 

  • Roesti D, Ineichen K, Braissant O, Redecker D, Wiemken A, Aragno M (2005) Bacteria associated with spores of the arbuscular mycorrhizal fungi Glomus geosporum and Glomus constrictum. Appl Environ Microbiol 71:6673–6679

    CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Azcón R, Gómez M (1995) Effects of arbuscular–mycorrhizal Glomus species on drought tolerance: physiological and nutritional plant responses. Appl Environ Microbiol 61:456–460

    CAS  PubMed  Google Scholar 

  • Satour MM, Butler EE (1967) A root and crown rot of tomato caused by Phytophthora capsici and P. parasitica. Phytopathology 57:510–515

    Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. J Plant Physiol 162:625–633

    CAS  PubMed  Google Scholar 

  • 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 16:365–370

    CAS  PubMed  Google Scholar 

  • Scheffknecht S, St-Arnaud M, Khaosaad T, Steinkellner S, Vierheilig H (2007) An altered root exudation pattern through mycorrhization affecting microconidia germination of the highly specialized tomato pathogen Fusarium oxysporum f. sp. lycopersici (Fol) is not tomato-specific but also occurs in Fol non-host plants. Can J Bot 85:347–351

    CAS  Google Scholar 

  • Secilia J, Bagyaraj DJ (1987) Bacteria and actinomycetes associated with pot cultures of vesicular–arbuscular mycorrhizas. Can J Microbiol 33:1069–1073

    Google Scholar 

  • Selim S, Negrel J, Govaerts C, Gianinazzi S, van Tuinen D (2005) Isolation and partial characterization of antagonistic peptides produced by Paenibacillus sp. strain B2 isolated from the sorghum mycorrhizosphere. Appl Environ Microbiol 71:6501–6507

    CAS  PubMed  Google Scholar 

  • Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Expt Bot 57:711–726

    CAS  Google Scholar 

  • Simons M, Permentier HP, de Weger LA, Wijffelman CA, Lugtenberg BJJ (1997) Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Int 10:102–106

    CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular–arbuscular mycorrhizal tomato plants. FEMS Microbiol Ecol 45:219–227

    Google Scholar 

  • 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. Haworth Press, Binghampton, NY, pp 67–122

    Google Scholar 

  • St-Arnaud M, Hamel C, Caron M, Fortin JA (1995a) Endomycorhizes VA et sensibilité aux maladies: synthèse de la littérature et mécanismes d'interaction potentiels. In: Fortin JA, Charest C, Piché Y (eds) La symbiose mycorhizienne — État des connaissances. Orbis Publishing, Frelighsburg, Québec, pp 51–87

    Google Scholar 

  • St-Arnaud M, Hamel C, Vimard B, Caron M, Fortin JA (1995b) Altered growth of Fusarium oxysporum f. sp. chrysanthemi in an in vitro dual culture system with the vesicular arbuscular mycorrhizal fungus Glomus intraradices growing on Daucus carota transformed roots. Mycorrhiza 5:431–438

    Google Scholar 

  • Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172:22–34

    CAS  PubMed  Google Scholar 

  • Stumpe M, Carsjens JG, Stenzel I, Göbel C, Lang I, Pawlowski K, Hause B, Feussner I (2005) Lipid metabolism in arbuscular mycorrhizal roots of Medicago truncatula. Phytochemistry 66:781–791

    CAS  PubMed  Google Scholar 

  • Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254:34–40

    CAS  PubMed  Google Scholar 

  • Trotta A, Varese GC, Gnavi E, Fusconi A, Sampo 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 185:199–209

    CAS  Google Scholar 

  • van West P, Appiah AA, Gow NAR (2003) Advances in research on oomycete root pathogens. Physiol Mol Plant Pathol 62:99–113

    Google Scholar 

  • Vazquez MM, Azcón R, Barea JM (2001) Compatibility of a wild type and its genetically modified Sinorhizobium strain with two mycorrhizal fungi on Medicago species as affected by drought stress. Plant Sci 161:347–358

    CAS  PubMed  Google Scholar 

  • Vierheilig H (2004) Regulatory mechanisms during the plant–arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176

    CAS  Google Scholar 

  • Vierheilig H, Piché Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. In: Bushlig B, Manthey J (eds) Flavonoids in cell function. Kluwer, New York, pp 23–39

    Google Scholar 

  • Vierheilig H, García-Garrido JM, Wyss U, Piché Y (2000a) Systemic suppression of mycorrhizal colonisation of barley roots already colonized by AM fungi. Soil Biol Biochem 32:589–595

    CAS  Google Scholar 

  • Vierheilig H, Gagnon H, Strack D, Maier W (2000b) Accumulation of cyclohexenone derivatives in barley, wheat and maize roots in response to inoculation with different arbuscular mycorrhizal fungi. Mycorrhiza 9:291–293

    CAS  Google Scholar 

  • Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170

    CAS  PubMed  Google Scholar 

  • Vigo C, Norman JR, Hooker JE (2000) Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol 49:509–514

    Google Scholar 

  • Wamberg C, Christensen S, Jakobsen I, Müller AK, Sørensen SJ (2003) The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum). Soil Biol Biochem 35:1349–1357

    CAS  Google Scholar 

  • Wright SF, Frankesnyder M, Morton JB, Upadhyaya A (1996) Time-course study and partial characterization of a protein on hyphae of arbuscular mycorrhizal fungi during active colonization of roots. Plant Soil 181:193–203

    CAS  Google Scholar 

  • Wright SF, Starr JL, Paltineanu IC (1999) Changes in aggregate stability and concentration of glomalin during tillage management transition. Soil Sci Soc Am J 63:1825–1829

    CAS  Google Scholar 

  • Wright SF, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97–107

    CAS  Google Scholar 

  • Wu QS, Xia RX (2006) Arbuscular mycorrhizal fungi influence growth, osmotic adjustment and photosynthesis of citrus under well-watered and water stress conditions. J Plant Physiol 163:417–425

    CAS  PubMed  Google Scholar 

  • Xavier LJC, Germida JJ (2003) Bacteria associated with Glomus clarum spores influence mycorrhizal activity. Soil Biol Biochem 35:471–478

    CAS  Google Scholar 

  • Yang CH, Crowley DE, Menge JA (2001) 16S rDNA fingerprinting of rhizosphere bacterial communities associated with healthy and Phytophthora infected avocado roots. FEMS Microbiol Ecol 35:129–136

    CAS  PubMed  Google Scholar 

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Lioussanne, L., Jolicoeur, M., St-Arnaud, M. (2009). Role of Root Exudates and Rhizosphere Microflora in the Arbuscular Mycorrhizal Fungi-Mediated Biocontrol of Phytophthora nicotianae in Tomato. In: Varma, A., Kharkwal, A.C. (eds) Symbiotic Fungi. Soil Biology, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-95894-9_9

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