Skip to main content

Multitrophic Reciprocity of AMF with Plants and Other Soil Microbes in Relation to Biotic Stress

  • Chapter
  • First Online:
Microbial Symbionts and Plant Health: Trends and Applications for Changing Climate

Abstract

The plant roots are invariably colonized by an extent of tiny microorganisms including arbuscular mycorrhizal fungi (AMF) which support plant health in multiple ways. The symbiotic relationship with host plants is achieved through various signaling mechanisms and metabolic pathways which guide their mutual survival. Besides their plant growth-promoting activities, they communicate with other soil microbes to improve plant fitness during unfavorable circumstances. Rhizobium and mycorrhization helper bacteria (MHB) interaction with AM fungi provides us with new insight for enhanced protection of plants against abiotic factors. In addition to that, the alteration of host nutrition, modifications in root physiology and morphology, increase plant defense. Thus, remodeling of the rhizospheric microbial community by AM fungi activates their multifaceted mechanisms in host plants against phytopathogens insect pests, nematodes, and phanerogamic parasites. It modifies the host physiology which ultimately benefits plants. The current knowledge about AM fungi with their potentiality in crop production and protection is discussed in detail.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ENOD11:

Early nodulin 11 gene

IPD3:

Interacting protein of does not make infections 3

LOX:

Lipoxygenase

MDA:

Malondialdehyde

NPR1:

Non-expressor of pathogenesis-related genes

PAL:

Phenylalanine ammonia lyase

POD:

Peroxidase

SOD:

Superoxide dismutase

SYMRK:

Symbiosis receptor-like kinase

References

  • Abdel-Fattah GM, El-Dohlob SM, El-Haddad SA, Hafez EE, Rashad YM (2010) An ecological view of arbuscular mycorrhizal status in some Egyptian plants. J Environ Sci 37:123–136

    Google Scholar 

  • Abd-Elgawad MM (2020) Plant-parasitic nematodes and their biocontrol agents: current status and future vistas. In: Management of phytonematodes: recent advances and future challenges, pp 171–203

    Google Scholar 

  • Abdel-Lateif K, Bogusz D, Hocher V (2012) The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal Behav 7(6):636–641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97(6):925–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amer MA, Abou-El-Seoud II (2008) Mycorrhizal fungi and Trichoderma harzianum as biocontrol agents for suppression of Rhizoctonia solani damping-off disease of tomato. Commun Agric Appl Biol Sci 73(2):217–232

    CAS  PubMed  Google Scholar 

  • Andrade SAL, Malik S, Sawaya ACHF, Bottcher A, Mazzafera P (2013) Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants. Acta Physiol Plant 35(3):867–880

    Article  CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    Article  CAS  PubMed  Google Scholar 

  • Aseel DG, Rashad YM, Hammad SM (2019) Arbuscular mycorrhizal fungi trigger transcriptional expression of flavonoid and chlorogenic acid biosynthetic pathways genes in tomato against tomato mosaic virus. Sci Rep 9(1):1–10

    Article  CAS  Google Scholar 

  • Azcon-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens-an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Article  Google Scholar 

  • Babikova Z, Gilbert L, Bruce TJ, Birkett M, Caulfield JC, Woodcock C, Pickett JA, Johnson D (2013) Underground signals carried through common mycelial networks warn neighboring plants of aphid attacks. Ecol Lett 16(7):835–843

    Article  PubMed  Google Scholar 

  • Babikova Z, Gilbert L, Bruce T, Dewhirst SY, Pickett JA, Johnson D (2014) Arbuscular mycorrhizal fungi and aphids interact by changing host plant quality and volatile emission. Funct Ecol 28(2):375–385

    Article  Google Scholar 

  • 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 57:233–266

    Article  CAS  PubMed  Google Scholar 

  • Balestrini R, Bonfante P (2014) Cell wall remodeling in mycorrhizal symbiosis: a way towards biotrophism. Front Plant Sci 5:237

    Article  PubMed  PubMed Central  Google Scholar 

  • Barber NA (2012) Arbuscular mycorrhizal fungi are necessary for the induced response to herbivores by Cucumis sativus. J Plant Ecol 6:171–176

    Article  Google Scholar 

  • Barber NA, Kiers ET, Hazzard RV, Adler LS (2013) Context-dependency of arbuscular mycorrhizal fungi on plant-insect interactions in an agroecosystem. Front Plant Sci 4:338

    Article  PubMed  PubMed Central  Google Scholar 

  • Bauer J, Kleczewski N, Bever J, Clay K, Reynolds H (2012) Nitrogen-fixing bacteria, arbuscular mycorrhizal fungi, and the productivity and structure of prairie grassland communities. Oecologia 170:1089–1098

    Article  PubMed  Google Scholar 

  • Becard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW (1995) Flavonoids are not necessary to plant signal compounds in arbuscular mycorrhizal symbioses. Mol Plant-Microbe Interact 8(2):252–258

    Article  CAS  Google Scholar 

  • Bending GD, Poole EJ, Whipps JM, Read DJ (2002) Characterization of bacteria from Pinus sylvestris-Suillus luteus mycorrhizas and their effects on root-fungus interactions and plant growth. FEMS Microbiol Ecol 39:219–227

    CAS  PubMed  Google Scholar 

  • Bernaola L, Stout MJ (2021) The effect of mycorrhizal seed treatments on rice growth, yield, and tolerance to insect herbivores. J Pest Sci 94(2):375–392

    Article  CAS  Google Scholar 

  • Bernaola L, Cosme M, Schneider RW, Stout M (2018) Belowground inoculation with arbuscular mycorrhizal fungi increases the local and systemic susceptibility of rice plants to different pest organisms. Front Plant Sci 9:747

    Article  PubMed  PubMed Central  Google Scholar 

  • Bernard GC, Egnin M, Bonsi C (2017) The impact of plant-parasitic nematodes on agriculture and methods of control. Nematology 10:121–151

    Google Scholar 

  • Bharadwaj DP, Lundquist PO, Persson P, Alstrom S (2008) Evidence for specificity of cultivable bacteria associated with arbuscular mycorrhizal fungal spores. FEMS Microbiol Ecol 65:310–322

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bodker L, Kjoller R, Rosendahl S (1998) Effect of phosphate and the arbuscular mycorrhizal fungus Glomus intraradices on disease severity of root rot of peas (Pisum sativum) caused by Aphanomyces euteiches. Mycorrhiza 8(3):169–174

    Article  CAS  Google Scholar 

  • Bora M, Lokhandwala A (2016) Mycorrhizal association: a safeguard for plant pathogen. In: Plant, soil and microbes, pp 253–275

    Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Becard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12(5):224–230

    Article  CAS  PubMed  Google Scholar 

  • Bruisson S, Maillot P, Schellenbaum P, Walter B, Gindro K, Deglene-Benbrahim L (2016) Arbuscular mycorrhizal symbiosis stimulates key genes of the phenylpropanoid biosynthesis and stilbenoid production in grapevine leaves in response to downy mildew and grey mold infection. Phytochemistry 131:92–99

    Article  CAS  PubMed  Google Scholar 

  • Brunetti C, Saleem AR, Della Rocca G, Emiliani G, De Carlo A, Balestrini R, Centritto M (2021) Effects of plant growth-promoting rhizobacteria strain to produce ACC deaminase on photosynthesis, isoprene emission, ethylene formation, and growth of Mucuna pruriens (L.) DC. in response to water deficit. J Biotechnol 331:53–62

    Article  CAS  PubMed  Google Scholar 

  • Calvet C, Pinochet J, Hernandez-Dorrego A, Estaun V, Camprubí A (2001) Field microplot performance of the peach-almond hybrid GF-677 after inoculation with arbuscular mycorrhizal fungi in a replant soil infested with root-knot nematodes. Mycorrhiza 10(6):295–300

    Article  Google Scholar 

  • Cameron DD, Neal AL, Van Wees SC, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18(10):539–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campo S, Martín-Cardoso H, Olive M, Pla E, Catala-Forner M, Martínez-Eixarch M, San Segundo B (2020) Effect of root colonization by arbuscular mycorrhizal fungi on growth, productivity and blast resistance in rice. Rice 13(1):1–14

    Article  Google Scholar 

  • Campos P, Borie F, Cornejo P, Lopez-Raez JA, Lopez-García A, Seguel A (2018) Phosphorus acquisition efficiency related to root traits: is mycorrhizal symbiosis a key factor to wheat and barley cropping? Front Plant Sci 9:752

    Article  PubMed  PubMed Central  Google Scholar 

  • Campos-Soriano LIDIA, Garcia-Martinez J, Segundo BS (2012) The arbuscular mycorrhizal symbiosis promotes the systemic induction of regulatory defense-related genes in rice leaves and confers resistance to pathogen infection. Mol Plant Pathol 13(6):579–592

    Article  CAS  PubMed  Google Scholar 

  • Castellanos-Morales V, Cardenas-Navarro R, Garcia-Garrido JM, Illana A, Ocampo JA, Steinkellner S, Vierheilig H (2012) Bioprotection against Gaeumannomyces graminis in barley a comparison between arbuscular mycorrhizal fungi. Plant Soil Environ 58(6):256–261

    Article  Google Scholar 

  • Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Bonfante P (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol 189(1):347–355

    Article  CAS  PubMed  Google Scholar 

  • Chandanie WA, Kubota M, Hyakumachi M (2006) Interactions between plant growth promoting fungi and arbuscular mycorrhizal fungus Glomus mosseae and induction of systemic resistance to anthracnose disease in cucumber. Plant Soil 286(1):209–217

    Article  CAS  Google Scholar 

  • Comby M, Gacoin M, Robineau M, Rabenoelina F, Ptas S, Dupont J, Baillieul F (2017) Screening of wheat endophytes as biological control agents against Fusarium head blight using two different in vitro tests. Microbiol Res 202:11–20

    Article  PubMed  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 Interact 11(10):1017–1028

    Article  CAS  Google Scholar 

  • Cullimore J, Denarie J (2003) How legumes select their sweet talking symbionts. Sci 302(5645):575–578

    Article  CAS  Google Scholar 

  • Devi NO, Tombisana Devi RK, Debbarma M, Hajong M, Thokchom S (2022) Effect of endophytic Bacillus and arbuscular mycorrhiza fungi (AMF) against Fusarium wilt of tomato caused by Fusarium oxysporum f. sp. lycopersici. Egypt J Biol. Pest Control 32(1):1–14

    Google Scholar 

  • Dotzler N, Krings M, Taylor TN, Agerer R (2006) Germination shields in Scutellospora (Glomeromycota: Diversisporales, Gigasporaceae) from the 400 million-year-old Rhynie chert. Mycol Prog 5:178–184

    Article  Google Scholar 

  • Dowarah B, Gill SS, Agarwala N (2021) Arbuscular mycorrhizal fungi in conferring tolerance to biotic stresses in plants. J Plant Growth Regul 1–16

    Google Scholar 

  • Duponnois R, Garbaye J (1991) Mycorrhization helper bacteria associated with the Douglas fir-Laccaria laccata symbiosis: effects in aseptic and in glasshouse conditions. Ann Sci For 48(3):239–251

    Article  Google Scholar 

  • Ebrahimi S, Eini O, Koolivand D (2020) Arbuscular mycorrhizal symbiosis enhances virus accumulation and attenuates resistance-related gene expression in tomato plants infected with beet curly top Iran virus. J Plant Dis Prot 127(3):341–348

    Article  Google Scholar 

  • Elsen A, Declerck S, De Waele D (2001) Effects of Glomus intraradices on the reproduction of the burrowing nematode (Radopholus similis) in dixenic culture. Mycorrhiza 11(1):49–51

    Article  Google Scholar 

  • Elsharkawy MM, Shimizu M, Takahash H, Hyakumachi M (2012) The plant growth-promoting fungus Fusarium equiseti and the arbuscular mycorrhizal fungus Glomus mosseae induce systemic resistance against cucumber mosaic virus in cucumber plants. Plant Soil 361(1):397–409

    Article  CAS  Google Scholar 

  • Erdogan P (2022) Parasitic plants in agriculture and management. Parasitic Plants 1

    Google Scholar 

  • FAO (2019). https://www.fao.org/news/story/en/item/1187738/icode/

  • Felten J, Legue V, Ditengou FA (2010) Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor: is fungal auxin the trigger? Plant Signal Behav 7:864–867

    Article  Google Scholar 

  • Ferlian O, Biere A, Bonfante P, Buscot F, Eisenhauer N, Fernandez I, Martinez-Medina A (2018) Growing research networks on mycorrhizae for mutual benefits. Trends Plant Sci 23(11):975–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Aparicio M, Garcia-Garrido JM, Ocampo JA, Rubiales D (2010) Colonization of field pea roots by arbuscular mycorrhizal fungi reduces Orobanche and Phelipanche species seed germination. Weed Res 50(3):262–268

    Article  Google Scholar 

  • Fernandez-Aparicio M, Delavault P, Timko MP (2020) Management of infection by parasitic weeds: a review. Plan Theory 9(9):1184

    CAS  Google Scholar 

  • Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling DJ, Cameron DD, Duckett JG, Leake JR, Pressel S (2019) Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. New Phytol 223:908–921

    Article  CAS  PubMed  Google Scholar 

  • Fiorilli V, Vannini C, Ortolani F, Garcia-Seco D, Chiapello M, Novero M, Domingo G, Terzi V, Morcia C, Bagnaresi P, Moulin L, Bracale M, Bonfante P (2018) Omics approaches revealed how arbuscular mycorrhizal symbiosis enhances yield and resistance to leaf pathogens in wheat. Sci Rep 8(1):1–18

    Article  CAS  Google Scholar 

  • Formenti L, Rasmann S (2019) Mycorrhizal fungi enhance resistance to herbivores in tomato plants with reduced jasmonic acid production. Agronomy 9(3):131

    Article  CAS  Google Scholar 

  • Frew A, Wilson BA (2021) Different mycorrhizal fungal communities differentially affect plant phenolic-based resistance to insect herbivory. Rhizosphere 19:100365

    Article  Google Scholar 

  • Frew A, Powell JR, Allsopp PG, Sallam N, Johnson SN (2017) Arbuscular mycorrhizal fungi promote silicon accumulation in plant roots, reducing the impacts of root herbivory. Plant Soil 419(1):423–433

    Article  CAS  Google Scholar 

  • Frew A, Powell JR, Johnson SN (2020) Aboveground resource allocation in response to root herbivory as affected by the arbuscular mycorrhizal symbiosis. Plant Soil 447(1):463–473

    Article  CAS  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  CAS  PubMed  Google Scholar 

  • Fritz M, Jakobsen I, Lyngkjaer MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhiza reduces the susceptibility of tomatoes to Alternaria solani. Mycorrhiza 16(6):413–419

    Article  PubMed  Google Scholar 

  • Fujita M, Kusajima M, Fukagawa M, Okumura Y, Nakajima M, Akiyama K, Nakashita H (2022) Response of tomatoes primed by mycorrhizal colonization to virulent and avirulent bacterial pathogens. Sci Rep 12(1):1–12

    Article  Google Scholar 

  • Gallou A, Mosquera HPL, Cranenbrouck S, Suarez JP, Declerck S (2011) Mycorrhiza-induced resistance in potato plantlets challenged by Phytophthora infestans. Physiol Mol Plant Pathol 76(1):20–26

    Article  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(3):611–618

    Article  Google Scholar 

  • Gange AC, Brown VK, Sinclair GS (1994) Reduction of black vine weevil larval growth by vesicular-arbuscular mycorrhizal infection. Entomol Exp Appl 70(2):115–119

    Article  Google Scholar 

  • Gao XX, Lu M, Wu H, Zhang R, Pan J, Tian S, Li H, Liao (2012) Co-inoculation with rhizobia and AMF inhibited soybean red crown rot: from field study to plant defense-related gene expression analysis. PLoS One 7(3):e33977

    Google Scholar 

  • Gao WQ, Lu LH, Srivastava AK, Wu QS, Kuca K (2020) Effects of mycorrhizae on physiological responses and relevant gene expression of peach affected by replant disease. Agronomy 10(2):186

    Article  CAS  Google Scholar 

  • Garbaye J, Duponnois R, Wahl JL (1990) The bacteria associated with Laccaria laccata ectomycorrhizas or sporocarps: effect on symbiosis establishment on Douglas Fir. Symbiosis 9:267–273

    Google Scholar 

  • Garcia-Garrido JM, Ocampo JA (1989) Effect of VA mycorrhizal infection of tomato on damage caused by Pseudomonas syringae. Soil Biol Biochem 21(1):165–167

    Article  Google Scholar 

  • García-Garrido JM, Garcia-Romera I, Ocampo JA (1992) Cellulase production by the vesicular–arbuscular mycorrhizal fungus Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe. New Phytol 121(2):221–226

    Article  Google Scholar 

  • Garmendia I, Goicoechea N, Aguirreolea J (2004) Antioxidant metabolism in asymptomatic leaves of verticillium-infected pepper associated with an arbuscular mycorrhizal fungus. J Phytopathol 152(11–12):593–599

    Article  CAS  Google Scholar 

  • Garzo E, Rizzo E, Fereres A, Gomez SK (2020) High levels of arbuscular mycorrhizal fungus colonization on Medicago truncatula reduces plant suitability as a host for pea aphids (Acyrthosiphon pisum). Insect Sci 27(1):99–112

    Article  CAS  PubMed  Google Scholar 

  • Gehring C, Bennett A (2009) Mycorrhizal fungal–plant–insect interactions: the importance of a community approach. Environ Entomol 38(1):93–102

    Article  PubMed  Google Scholar 

  • Goddard ML, Belval L, Martin IR, Roth L, Laloue H, Deglene-Benbrahim L, Chong J (2021) Arbuscular mycorrhizal symbiosis triggers major changes in primary metabolism together with modification of defense responses and signaling in both roots and leaves of Vitis vinifera. Front Plant Sci 1675

    Google Scholar 

  • Gull A, Lone AA, Wani NUI (2019) Biotic and abiotic stresses in plants. In: Abiotic and biotic stress in plants, pp 1–19

    Google Scholar 

  • Hao Z, Tuinen D, Fayolle L, Chatagnier O, Li X, Chen B, Gianinazzi S, Gianinazzi-Pearson V (2018) Arbuscular mycorrhiza affects grapevine fanleaf virus transmission by the nematode vector Xiphinema index. Appl Soil Ecol 129:107–111

    Article  Google Scholar 

  • Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Biol 50(1):361–389

    Article  CAS  Google Scholar 

  • Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54(1):323–342

    Article  CAS  PubMed  Google Scholar 

  • Hashem A, Akhter A, Alqarawi AA, Singh G, Almutairi KF, AbdAllah EF (2021) Mycorrhizal fungi induced activation of tomato defense system mitigates Fusarium wilt stress. Saudi J Biol Sci 28(10):5442–5450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hayek S, Grosch R, Gianinazzi-Pearson V, Franken P (2012) Bioprotection and alternative fertilisation of petunia using mycorrhiza in a soilless production system. Agron Sustain Dev 32(3):765–771

    Article  Google Scholar 

  • Hol WG, Cook R (2005) An overview of arbuscular mycorrhizal fungi–nematode interactions. Basic Appl Ecol 6(6):489–503

    Article  Google Scholar 

  • Ho-Plagaro T, García-Garrido JM (2022) Multifarious and interactive roles of GRAS transcription factors during arbuscular mycorrhiza development. Front Plant Sci 13

    Google Scholar 

  • Huang J, Luo S, Zeng R (2003) Mechanisms of plant disease resistance induced by arbuscular mycorrhizal fungi. J Appl Ecol 14(5):819–822

    Google Scholar 

  • Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7(8):1267–1287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iqbal SH, Nasim G, Niaz M (1988) Role of vesicular-arbuscular mycorrhiza as a deterrent to damping off caused by Rhizoctonia solani in Brassica oleracea. Biologia

    Google Scholar 

  • Ito S, Yamagami D, Umehara M, Hanada A, Yoshida S, Sasaki Y, Asami T (2017) Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol 174(2):1250–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacott CN, Murray JD, Ridout CJ (2017) Trade-offs in arbuscular mycorrhizal symbiosis: disease resistance, growth responses and perspectives for crop breeding. Agronomy 7(4):75

    Article  Google Scholar 

  • Jain RK, Sethi C (1988) Influence of endomycorrhizal fungi Glomus fasciculatum and G. eplgaeus on penetration and development of Heterodera cajani on cowpea. Indian J Nematol 18(1):89–93

    Google Scholar 

  • Jain RK, Hasan N, Singh RK, Pandey PN (1998) Interaction between plant parasitic nematodes, Meloidogyne incognita, Tylenchorhynchus vulgaris and VAM fungi, Glomus fasciculatum on lucerne. Ann Plant Protect Sci 6(1):37–40

    Google Scholar 

  • Jaiti F, Kassami M, Meddich A, El Hadrami I (2008) Effect of arbuscular mycorrhization on the accumulation of hydroxycinnamic acid derivatives in date palm seedlings challenged with Fusarium oxysporum f. sp. albedinis. J Phytopathol 156(11–12):641–646

    Article  CAS  Google Scholar 

  • Jayaraman J, Kumar D (1995) Influence of mungbean yellow mosaic virus on mycorrhizal fungi associated with Vigna radiata var. PS16. Indian Phytopathol 48(1):108–110

    Google Scholar 

  • Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea JM (2003) The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils 37(1):1–16

    Article  Google Scholar 

  • Jia Y, Gray VM (2008) Growth yield of Vicia faba L in response to microbial symbiotic associations. S Afr J Bot 74:25–32

    Article  Google Scholar 

  • Jia Y, Gray VM, Straker CJ (2004) The influence of rhizobium and arbuscular mycorrhizal fungi on nitrogen and phosphorus accumulation by Vicia faba. Ann Bot 94:251–258

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang D, Tan M, Wu S, Zheng L, Wang Q, Wang G, Yan S (2021) Defense responses of arbuscular mycorrhizal fungus-colonized poplar seedlings against gypsy moth larvae: a multiomics study. Hortic Res 8

    Google Scholar 

  • Jiang D, Lin R, Tan M, Yan J, Yan S (2022) The mycorrhizal-induced growth promotion and insect resistance reduction in Populus alba× P. berolinensis seedlings: a multi-omics study. Tree Physiol 42(5):1059–1069

    Article  CAS  PubMed  Google Scholar 

  • Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48(1):1–13

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  CAS  PubMed  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defences. J Chem Ecol 38(6):651–664

    Article  CAS  PubMed  Google Scholar 

  • Kadam SB, Pable AA, Barvkar VT (2020) Mycorrhiza induced resistance (MIR): a defence developed through synergistic engagement of phytohormones, metabolites and rhizosphere. Funct Plant Biol 47(10):880–890

    Article  PubMed  Google Scholar 

  • Kapoor R (2008) Induced resistance in mycorrhizal tomato is correlated to concentration of jasmonic acid. J Biol Sci 8(3):49–56

    CAS  Google Scholar 

  • Kassab AS, Taha AHY (1990) Aspects of the host-parasite relationships of nematodes and sweet potato 1. Population dynamics and interaction of Criconemella spp., Rotylenchulus reniformis, Tylenchorhynchus spp. and endomycorrhiza. Ann Agric Sci (Cairo) 35(1):497–508

    Google Scholar 

  • Kaur J, Chavana J, Soti P, Racelis A, Kariyat R (2020) Arbuscular mycorrhizal fungi (AMF) influences growth and insect community dynamics in Sorghum-sudangrass (Sorghum x drummondii). Arthropod Plant Interact 14(3):301–315

    Article  Google Scholar 

  • Khaosaad T, Garcia-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biol Biochem 39(3):727–734

    Article  CAS  Google Scholar 

  • Khoshkhatti N, Eini O, Koolivand D (2020a) Effect of Rhizoglomus irregulare symbiosis on reducing disease severity in tomato plants infected with tomato bushy stunt virus with emphasis on the expression of methylation-related genes. Crop Biotech 10(30):43–55

    Google Scholar 

  • Khoshkhatti N, Eini O, Koolivand D, Pogiatzis A, Klironomos JN, Pakpour S (2020b) Differential response of mycorrhizal plants to tomato bushy stunt virus and tomato mosaic virus infection. Microorganisms 8(12):2038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirk PM (2001) Ainsworth and Bisby’s dictionary of the fungi, 9th edn. C.A.B International, Oxon

    Google Scholar 

  • Kobra N, Jalil K, Youbert G (2009) Effects of three Glomus species as biocontrol agents against Verticillium-induced wilt in cotton. J Plant Prot Res

    Google Scholar 

  • Koricheva J, Gange AC, Jones T (2009) Effects of mycorrhizal fungi on insect herbivores: a meta-analysis. Ecology 90(8):2088–2097

    Article  PubMed  Google Scholar 

  • Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131(3):952–962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumari SMP, Prabina BJ (2019) Protection of tomato, Lycopersicon esculentum from wilt pathogen, Fusarium oxysporum f. sp. lycopersici by arbuscular mycorrhizal fungi, Glomus sp. Int J Curr Microbiol Appl Sci 8:1368–1378

    Article  CAS  Google Scholar 

  • Kumari SMP, Srimeena N (2019) Arbuscular mycorrhizal fungi (AMF) induced defense factors against the damping-off disease pathogen, Pythium aphanidermatum in chilli (Capsicum annum). Int J Curr Microbiol Appl Sci 8:2243–2248

    Article  CAS  Google Scholar 

  • Labbe JL, Weston DJ, Dunkirk N (2014) Newly identified helper bacteria stimulate ectomycorrhizal formation in Populus. Front Plant Sci 5:1–10

    Google Scholar 

  • Labeena P, Sreenivasa MN, Lingaraju S (2002) Interaction effects between arbuscular mycorrhizal fungi and root-knot nematode Meloidogyne incognita on tomato. Indian J Nematol 32(2):118–120

    Google Scholar 

  • Lee YJ, George E (2005) Development of a nutrient film technique culture system for arbuscular mycorrhizal plants. Hort Sci 40(2):378–380

    Google Scholar 

  • Lendzemo VW, Kuyper TW, Kropff MJ, van Ast AV (2005) Field inoculation with arbuscular mycorrhizal fungi reduces Striga hermonthica performance on cereal crops and has the potential to contribute to integrated Striga management. Field Crops Res 91(1):51–61

    Article  Google Scholar 

  • Li AR, Smith SE, Smith FA, Guan KY (2012) Inoculation with arbuscular mycorrhizal fungi suppresses initiation of haustoria in the root hemiparasite Pedicularis tricolor. Ann Bot 109(6):1075–1080

    Article  PubMed  PubMed Central  Google Scholar 

  • Lingua G, DAgostino G, Massa N, Antosiano M, Berta G (2002) Mycorrhiza-induced differential response to a yellows disease in tomato. Mycorrhiza 12(4):191–198

    Article  PubMed  Google Scholar 

  • 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(3):529–544

    Article  CAS  PubMed  Google Scholar 

  • Louarn J, Carbonne F, Delavault P, Becard G, Rochange S (2012) Reduced germination of Orobanche cumana seeds in the presence of arbuscular mycorrhizal fungi or their exudates. PLoS One 7(11):e49273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lv Y, Wang F, Chen H, Zhang T, Yan J, Hu Y (2022) Unraveling arbuscular mycorrhizal fungi-induced resistance of purple branch rose (Rosa rugosa ‘Zizhi’) to Lymantria dispar based on metabolomics. Biol Control 172:104971

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ma J, Wang W, Yang J, Qin S, Yang Y, Sun C, Huang J (2022) Mycorrhizal symbiosis promotes nutrient content accumulation and affects the root exudates in maize. BMC Plant Biol 22(1):1–13

    Article  Google Scholar 

  • Maffei G, Miozzi L, Fiorilli V, Novero M, Lanfranco L, Accotto GP (2014) The arbuscular mycorrhizal symbiosis attenuates symptom severity and reduces virus concentration in tomato infected by tomato yellow leaf curl Sardinia virus (TYLCSV). Mycorrhiza 24(3):179–186

    Article  CAS  PubMed  Google Scholar 

  • Manila R, Nelson R (2017) Nutrient uptake and promotion of growth by arbuscular mycorrhizal fungi in tomato and their role in bio-protection against the tomato wilt pathogen. J Microbiol Biotechnol 3(4):4246

    Google Scholar 

  • Manresa-Grao M, Pastor-Fernández J, Sanchez-Bel P, Jaques JA, Pastor V, Flors V (2022) Mycorrhizal symbiosis triggers local resistance in citrus plants against spider mites. Front Plant Sci 13

    Google Scholar 

  • Marquez N, Giachero ML, Gallou A, Debat HJ, Declerck S, Ducasse DA (2019) Transcriptome analysis of mycorrhizal and nonmycorrhizal soybean plantlets upon infection with Fusarium virguliforme, one causal agent of sudden death syndrome. Plant Pathol 68(3):470–480

    Article  CAS  Google Scholar 

  • Martinez-Molina E, Morales VM, Hubbell DH (1979) Hydrolytic enzyme production by Rhizobium. Appl Environ Microbiol 38(6):1186–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsubara Y, Tamura H, Harada T (1995) Growth enhancement and Verticillium wilt control by vesicular-arbuscular mycorrhizal fungus inoculation in eggplant. J Jpn Soc Hortic Sci

    Google Scholar 

  • Maurya AK, Kelly MP, Mahaney SM, Gomez SK (2018) Arbuscular mycorrhizal symbiosis alters plant gene expression and aphid weight in a tripartite interaction. J Plant Interact 13(1):294–305

    Article  CAS  Google Scholar 

  • Meena RS, Vijayakumar V, Yadav GS, Mitran T (2018) Response and interaction of Bradyrhizobium japonicum and arbuscular mycorrhizal fungi in the soybean rhizosphere. Plant Growth Regul 84(2):207–223

    Article  CAS  Google Scholar 

  • Meier AR, Hunter MD (2018) Mycorrhizae alter toxin sequestration and performance of two specialist herbivores. Front Ecol Evol 6:33

    Article  Google Scholar 

  • Miao-Miao XIE, Zhang YC, Li-Ping LIU, Ying-Ning ZOU, Qiang-Sheng WU, Kamil KUCA (2019) Mycorrhiza regulates signal substance levels and pathogen defense gene expression to resist citrus canker. Not Bot Horti Agrobot Cluj Napoca 47(4):1161–1167

    Article  Google Scholar 

  • Miller JB, Pratap A, Miyahara A, Zhou L, Bornemann S, Morris RJ, Oldroyd GE (2013) Calcium/Calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell 25(12):5053–5066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mingqin G, Yu C, Fengzhen W (2004) Resistance of the AM fungus Eucalyptus seedlings against Pseudomonas solanacearum. Forest Res 17(4):441–446

    Google Scholar 

  • Miozzi L, Catoni M, Fiorilli V, Mullineaux PM, Accotto GP, Lanfranco L (2011) Arbuscular mycorrhizal symbiosis limits foliar transcriptional responses to viral infection and favors long-term virus accumulation. Mol Plant-Microbe Interact 24(12):1562–1572

    Article  CAS  PubMed  Google Scholar 

  • Miozzi L, Vaira AM, Catoni M, Fiorilli V, Accotto GP, Lanfranco L (2019) Arbuscular mycorrhizal symbiosis: plant friend or foe in the fight against viruses? Front Microbiol 10:1238

    Article  PubMed  PubMed Central  Google Scholar 

  • Miozzi L, Vaira AM, Brilli F, Casarin V, Berti M, Ferrandino A, Nerva L, Accotto GP, Lanfranco L (2020) Arbuscular mycorrhizal symbiosis primes tolerance to cucumber mosaic virus in tomato. Viruses 12(6):675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitchell C, Brennan RM, Graham J, Karley AJ (2016) Plant defense against herbivorous pests: exploiting resistance and tolerance traits for sustainable crop protection. Front Plant Sci 7:1132

    Article  PubMed  PubMed Central  Google Scholar 

  • Mora-Romero GA, Cervantes-Gamez RG, Galindo-Flores H, González-Ortíz MA, Felix-Gastelum R, Maldonado-Mendoza IE, Lopez-Meyer M (2015) Mycorrhiza-induced protection against pathogens is both genotype-specific and graft-transmissible. Symbiosis 66(2):55–64

    Article  CAS  Google Scholar 

  • Mosse B (1973) Advances in the study of vesicular-arbuscular mycorrhiza. Annu Rev Phytopathol 11(1):171–196

    Article  Google Scholar 

  • Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015a) Role of methyl jasmonate in the expression of mycorrhizal induced resistance against Fusarium oxysporum in tomato plants. Physiol Molecul Plant Pathol 92:139–145

    Article  CAS  Google Scholar 

  • Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015b) Systemic jasmonic acid modulation in mycorrhizal tomato plants and its role in induced resistance against Alternaria alternata. Plant Biol 17(3):625–631

    Article  CAS  PubMed  Google Scholar 

  • Nemec S, Myhre D (1984) Virus-Glomus etunicatum interactions in citrus rootstocks. Plant Dis 68:311–314

    Article  Google Scholar 

  • Newman EI, Reddell P (1987) The distribution of mycorrhizas among families of vascular plants. New Phytol 106:745–751

    Article  CAS  PubMed  Google Scholar 

  • Nishad R, Ahmed T, Rahman VJ, Kareem A (2020) Modulation of plant defense system in response to microbial interactions. Front Microbiol 11:1298

    Article  PubMed  PubMed Central  Google Scholar 

  • Omomowo IO, Fadiji AE, Omomowo OI (2018) Assessment of bio-efficacy of Glomus versiforme and Trichoderma harzianum in inhibiting powdery mildew disease and enhancing the growth of cowpea. Ann Agric Sci 63:917

    Article  Google Scholar 

  • Parker C, Riches CR (1993) Parasitic weeds of the world: biology and control. CAB international

    Google Scholar 

  • Perez-de-Luque A, Tille S, Johnson L, Pascual-Pardo D, Ton J, Cameron DD (2017) The interactive effects of arbuscular mycorrhiza and plant growth-promoting rhizobacteria synergistically enhance host plant defences against pathogens. Sci Rep 7(1):1–10

    Article  CAS  Google Scholar 

  • Peterson RK, Varella AC, Higley LG (2017) Tolerance: the forgotten child of plant resistance. Peer J 5:e3934

    Article  PubMed  PubMed Central  Google Scholar 

  • Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  PubMed  Google Scholar 

  • Pirozynsky KA, Malloch DW (1975) The origin of land plants: a matter of mycotrophism. Biosystems 6:153–164

    Article  Google Scholar 

  • Poole EJ, Bending GD, Whipps JM, Read DJ (2001) Bacteria associated with Pinus sylvestris-Lactarius rufus ectomycorrhizas and their effects on mycorrhiza formation in vitro. New Phytol 151:743–751

    Article  PubMed  Google Scholar 

  • Primieri S, Magnoli SM, Koffel T, Sturmer SL, Bever JD (2022) Perennial, but not annual legumes synergistically benefit from infection with arbuscular mycorrhizal fungi and rhizobia: a meta-analysis. New Phytol 233(1):505–514

    Article  CAS  PubMed  Google Scholar 

  • Rabin LB, Pacovsky RS (1985) Reduced larva growth of two lepidoptera (Noctuidae) on excised leaves of soybean infected with a mycorrhizal fungus. J Econ Entomol 78(6):1358–1363

    Article  Google Scholar 

  • Rahou YA, Boutaj H, Boutasknit A, Douira A, Benkirane R, El Modafar Cherkaoui, Meddich A (2021) Colonization of tomato roots with arbuscular mycorrhizal fungi changes of antioxidative activity and improves tolerance to Verticillium dahliae. Plant Cell Biotechnol Molecul Biol 65–81

    Google Scholar 

  • Rao MS, Naik D, Shylaja M, Reddy PP (2003) Management of Meloidogyne incognita on eggplant by integrating endomycorrhiza, Glomus fasciculatum with bio-agent Verticillium chlamydosporium under field conditions. Indian J Nematol 33(1):29–32

    Google Scholar 

  • Ravnskov S, Cabral C, Larsen J (2020) Mycorrhiza induced tolerance in Cucumis sativus against root rot caused by Pythium ultimum depends on fungal species in the arbuscular mycorrhizal symbiosis. Biol Control 141:104133

    Article  CAS  Google Scholar 

  • Raza S, Akhter A, Wahid F, Hashem A, AbdAllah EF (2022) Rhizophagus intraradices and tomato-basil companionship affect root morphology and root exudate dynamics in tomato under fusarium wilt disease stress. Appl Ecol Environ Res 20(1):235–249

    Article  Google Scholar 

  • Real-Santillan RO, Del-Val E, Cruz-Ortega R, Contreras-Cornejo HA, Gonzalez-Esquivel CE, Larsen J (2019) Increased maize growth and P uptake promoted by arbuscular mycorrhizal fungi coincide with higher foliar herbivory and larval biomass of the fall armyworm Spodoptera frugiperda. Mycorrhiza 29(6):615–622

    Article  CAS  PubMed  Google Scholar 

  • Redman RSYO, Kim CJDA, Woodward C, Greer L, Espino SL, Doty RJ, Rodriguez (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS One 6:e14823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivero J, Lidoy J, Llopis-Gimenez A, Herrero S, Flors V, Pozo MJ (2021) Mycorrhizal symbiosis primes the accumulation of antiherbivore compounds and enhances herbivore mortality in tomato. J Exp Bot 72(13):5038–5050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Castillo G, Molina-Rodríguez M, Cambronero-Heinrichs JC, Quiros-Fournier JP, Lizano-Fallas V, Jimenez-Rojas C, Rodriguez-Rodriguez CE (2019) Simultaneous removal of neonicotinoid insecticides by a microbial degrading consortium: detoxification at reactor scale. Chemosphere 235:1097–1106

    Article  PubMed  Google Scholar 

  • Rodriguez-Kabana R, King PS (1980) Use of mixtures of urea and blackstrap molasses for control of root-knot nematodes in soil. Nematropica 38–44

    Google Scholar 

  • Rydlova J, Puschel D, Sudova R, Gryndler M, Mikanova O, Vosatka M (2011) Interaction of arbuscular mycorrhizal fungi and rhizobia: effects on flax yield in spoil-bank clay. J Plant Nutr Soil Sci 174(1):128–134

    Article  CAS  Google Scholar 

  • Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19(2):610–624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salonen V, Vestberg M, Vauhkonen M (2001) The effect of host mycorrhizal status on host plant–parasitic plant interactions. Mycorrhiza 11(2):95–100

    Article  Google Scholar 

  • Sanmartín N, Pastor V, Pastor-Fernández J, Flors V, Pozo MJ, Sanchez-Bel P (2020a) Role and mechanisms of callose priming in mycorrhiza-induced resistance. J Exp Bot 71(9):2769–2781

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanmartín N, Sanchez-Bel P, Pastor V, Pastor-Fernández J, Mateu D, Pozo MJ, Flors V (2020b) Root-to-shoot signalling in mycorrhizal tomato plants upon Botrytis cinerea infection. Plant Sci 298:110595

    Article  PubMed  Google Scholar 

  • Schausberger P, Peneder S, Jurschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26(2):441–449

    Article  Google Scholar 

  • Schoenherr AP, Rizzo E, Jackson N, Manosalva P, Gomez SK (2019) Mycorrhiza-induced resistance in potato involves priming of defense responses against cabbage looper (Noctuidae: Lepidoptera). Environ Entomol 48(2):370–381

    Article  CAS  PubMed  Google Scholar 

  • Schouteden N, De Waele D, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280

    Article  PubMed  PubMed Central  Google Scholar 

  • Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka M (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216

    Article  CAS  PubMed  Google Scholar 

  • Schussler A, Walker C (2011) Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In: Wöstemeyer J, Pöggeler S (eds) The Mycota. Evolution of fungi and fungal-like organisms, vol XIV. Springer, pp 163–185

    Chapter  Google Scholar 

  • Schussler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Selvaraj A, Thangavel K, Uthandi S (2020) Arbuscular mycorrhizal fungi (Glomus intraradices) and diazotrophic bacterium (Rhizobium BMBS) primed defense in blackgram against herbivorous insect (Spodoptera litura) infestation. Microbiol Res 231:126355

    Article  CAS  PubMed  Google Scholar 

  • Sharma DD, Govindaiah S, Katiyar RS, Das PK, Janardhan L, Bajpai AK, Choudhry PC, Janardhan L (1995) Effect of VA-mycorrhizal fungi on the incidence of major mulberry diseases. Indian J Seric 34:34–37

    Google Scholar 

  • Sharma E, Anand G, Kapoor R (2017) Terpenoids in plant and arbuscular mycorrhiza-reinforced defence against herbivorous insects. Ann Bot 119(5):791–801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant-Microbe Interact 12(11):1000–1007

    Article  CAS  PubMed  Google Scholar 

  • Siasou E, Standing D, Killham K, Johnson D (2009) Mycorrhizal fungi increase biocontrol potential of Pseudomonas fluorescens. Soil Biol Biochem 41:1341–1343

    Article  CAS  Google Scholar 

  • Siddiqui ZA, Mahmood I (1995) Biological control of Heterdora cajani and Fusarium udum by Bacillus subtilis, Bradhyrhizobium japonicum and Glomus fasciculatum on pigeon pea. Fundam Appl Nematol 18(6):559–566

    Google Scholar 

  • Singh R, Adholeya A, Mukerji KG (2000) Mycorrhiza in control of soil-borne pathogens. In: Mukerji KG, Chamola BP, Singh J (eds) Mycorrhizal biology. Kluwer, New York, pp 173–196

    Chapter  Google Scholar 

  • Sipahioglu MH, Demir S, Usta M, Akkopru A (2009) Biological relationship of potato virus Y and arbuscular mycorrhizal fungus Glomus intraradices in potato. Pest Tech 3:63–66

    Google Scholar 

  • Sistani RN, Desalegn G, Kaul HP, Wienkoop S (2020) Seed metabolism and pathogen resistance enhancement in Pisum sativum during colonization of arbuscular mycorrhizal fungi: an integrative metabolomics-proteomics approach. Front Plant Sci 11:872

    Article  Google Scholar 

  • Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York

    Google Scholar 

  • Smith SE, Dickson S, Walker NA (1992) Distribution of VA mycorrhizal entry points near the root apex: is there an un-infectible zone at the root tip of leek or clover. New Phytol 122(3):469–477

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Jakobsen I, Gronlund M, Smith FA (2011) Roles of arbuscular mycorrhizas in plant phosphorus nutrition: interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol 156(3):1050–1057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song YY, Ye M, Li CY, Wang RL, Wei XC, Luo SM, Zeng RS (2013) Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J Chem Ecol 39(7):1036–1044

    Article  PubMed  Google Scholar 

  • Song Y, Chen D, Lu K, Sun Z, Zeng R (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:786

    Article  PubMed  PubMed Central  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

    Article  Google Scholar 

  • Spaepen S, Bossuyt S, Engelen K, Marchal K, Vanderleyden J (2014) Phenotypical and molecular responses of Arabidopsis thaliana roots as a result of inoculation with the auxin-producing bacterium Azospirillum brasilense. New Phytol 201(3):850–861

    Article  CAS  PubMed  Google Scholar 

  • Spagnoletti F, Carmona M, Gómez NET, Chiocchio V, Lavado RS (2017) Arbuscular mycorrhiza reduces the negative effects of M. phaseolina on soybean plants in arsenic-contaminated soils. Appl Soil Ecol 121:41–47

    Article  Google Scholar 

  • Spagnoletti FN, Carmona M, Balestrasse K, Chiocchio V, Giacometti R, Lavado RS (2021) The arbuscular mycorrhizal fungus Rhizophagus intraradices reduces the root rot caused by Fusarium pseudograminearum in wheat. Rhizosphere 19:100369

    Article  Google Scholar 

  • Sparling GP, Tinker PB (1978) Mycorrhizal infection in Pennine grassland. 1. Levels of infection in the field [England]. J Appl Ecol (UK)

    Google Scholar 

  • Sprent JI (2007) Evolving ideas of legume evolution and diversity: a taxonomic perspective on the occurrence of nodulation. New Phytol 174:11–25

    Article  CAS  PubMed  Google Scholar 

  • Sturmer S (2012) A history of the taxonomy and systematics of arbuscular mycorrhizal fungi belonging to the phylum Glomeromycota. Mycorrhiza 22:247–258

    Article  PubMed  Google Scholar 

  • Sui XL, Li AR, Chen Y, Guan KY, Zhuo L, Liu YY (2014) Arbuscular mycorrhizal fungi: potential biocontrol agents against the damaging root hemiparasite Pedicularis kansuensis. Mycorrhiza 24(3):187–195

    Article  PubMed  Google Scholar 

  • Sulieman S, Tran LSP (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43

    Article  CAS  PubMed  Google Scholar 

  • Tahat MM, Kamaruzaman S, Othman R (2010) Mycorrhizal fungi as a biocontrol agent. Plant Pathol J 9(4):198–207

    Article  Google Scholar 

  • Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M (2015) Gibberellin regulates infection and colonization of host roots by arbuscular mycorrhizal fungi. Plant Signal Behav 10(6):e1028706

    Article  PubMed  PubMed Central  Google Scholar 

  • Tao L, Ahmad A, de Roode JC, Hunter MD (2016) Arbuscular mycorrhizal fungi affect plant tolerance and chemical defences to herbivory through different mechanisms. J Ecol 104(2):561–571

    Article  Google Scholar 

  • Tian L, Zou YN, Wu QS, Kuca K (2021) Mycorrhiza-induced plant defence responses in trifoliate orange infected by Phytophthora parasitica. Acta Physiol Planta 43(3):1–8

    Article  Google Scholar 

  • Todd TC, Winkler HE, Wilson GWT (2001) Interaction of Heterodera glycines and Glomus mosseae on soybean. J Nematol 33(4S):306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Udvardi MK, Day DA (1997) Metabolite transport across symbiotic membranes of legume nodules. Ann Rev Plant Physiol Plant Mol Biol 48:493–523

    Article  CAS  Google Scholar 

  • Vierheilig H, Steinkellner S, Khaosaad T, Garcia-Garrido JM (2008) The biocontrol effect of mycorrhization on soilborne fungal pathogens and the autoregulation of the AM symbiosis: one mechanism, two effects?. In: Mycorrhiza. Springer, Berlin, pp 307–320

    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(4):509–514

    Article  Google Scholar 

  • Villani A, Tommasi F, Paciolla C (2021) The arbuscular mycorrhizal fungus Glomus viscosum improves the tolerance to verticillium wilt in artichoke by modulating the antioxidant defense systems. Cell 10(8):1944

    Article  CAS  Google Scholar 

  • Waceke JW, Waudo SW, Sikora R (2002) Effect of inorganic phosphatic fertilizers on the efficacy of an arbuscular mycorrhiza fungus against a root-knot nematode on pyrethrum. Int J Pest Manag 48(4):307–313

    Article  CAS  Google Scholar 

  • Walker C, Harper CJ, Brundrett MC, Krings M (2018) Looking for arbuscular mycorrhizal fungi in the fossil record: an illustrated guide. In: Krings M, Cuneo N, Harper CJ, Rothwell GW (eds) Transformative paleobotany. Academic Press/Elsevier, Papers to Commemorate the Life and Legacy of Thomas N. Taylor, pp 481–517

    Chapter  Google Scholar 

  • Wang Y, Huang J, Gao Y (2012) Arbuscular mycorrhizal colonization alters subcellular distribution and chemical forms of cadmium in Medicago sativa L. and resists cadmium toxicity. PLoS One 7(11):e48669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang S, He G, Chen M, Zuo T, Xu W, Liu X (2017) The role of antioxidant enzymes in the ovaries. Oxidative medicine and cellular longevity

    Google Scholar 

  • Wang YY, Yin QS, Qu Y, Li GZ, Hao L (2018) Arbuscular mycorrhiza-mediated resistance in tomato against Cladosporium fulvum-induced mould disease. J Phytopathol 166(1):67–74

    Article  CAS  Google Scholar 

  • Wang M, Zhang R, Zhao L, Wang H, Chen X, Mao Z, Yin C (2021) Indigenous arbuscular mycorrhizal fungi enhance resistance of apple rootstock ‘M9T337’ to apple replant disease. Physiol Mol Plant Pathol 116:101717

    Article  CAS  Google Scholar 

  • Wang L, Yang D, Ma F, Wang G, You Y (2022) Recent advances in responses of arbuscular mycorrhizal fungi-plant symbiosis to engineered nanoparticles. Chemosphere 286:131644

    Article  CAS  PubMed  Google Scholar 

  • Wani KA, Manzoor J, Shuab R, Lone R (2017) Arbuscular mycorrhizal fungi as biocontrol agents for parasitic nematodes in plants. In: Mycorrhiza-nutrient uptake, biocontrol, ecorestoration, pp 195–210

    Google Scholar 

  • Wehner J, Antunes PM, Powell JR, Mazukatow J, Rillig MC (2010) Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia 53(3):197–201

    Article  Google Scholar 

  • Weng W, Yan J, Zhou M, Yao X, Gao A, Ma C, Ruan J (2022) Roles of arbuscular mycorrhizal fungi as a biocontrol agent in the control of plant diseases. Microorganisms 10(7):1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu M, Yan Y, Wang Y, Mao Q, Fu Y, Peng X, Ahammed GJ (2021) Arbuscular mycorrhizal fungi for vegetable (VT) enhance resistance to Rhizoctonia solani in watermelon by alleviating oxidative stress. Biol Control 152:104433

    Article  CAS  Google Scholar 

  • Xavier LJ, Boyetchko SM (2004) Arbuscular mycorrhizal fungi in plant disease control. In: Fungal biotechnology in agricultural, food, and environmental applications, pp 183–194

    Google Scholar 

  • Yao Q, Li X, Ai W, Christie P (2003) Bi-directional transfer of phosphorus between red clover and perennial ryegrass via arbuscular mycorrhizal hyphal links. Eur J Soil Biol 39(1):47–54

    Article  CAS  Google Scholar 

  • Yu L, Zhang W, Geng Y, Liu K, Shao X (2022) Cooperation with arbuscular mycorrhizal fungi increases plant nutrient uptake and improves defenses against insects. Front Ecol Evol 10

    Google Scholar 

  • Yuan W, Ruan S, Qi G, Wang R, Zhao X (2022) Plant growth-promoting and antibacterial activities of cultivable bacteria alive in tobacco field against Ralstonia solanacearum. Environ Microbiol 24(3):1411–1429

    Article  CAS  PubMed  Google Scholar 

  • Zhu B, Gao T, Zhang D, Ding K, Li C, Ma F (2022) Functions of arbuscular mycorrhizal fungi in horticultural crops. Sci Hortic 303:111219

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors sincerely acknowledge the facilities provided by the Department of Plant Pathology, Assam Agricultural University, Jorhat-13, Assam.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Supriya Sharma .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sharma, S. et al. (2023). Multitrophic Reciprocity of AMF with Plants and Other Soil Microbes in Relation to Biotic Stress. In: Mathur, P., Kapoor, R., Roy, S. (eds) Microbial Symbionts and Plant Health: Trends and Applications for Changing Climate. Rhizosphere Biology. Springer, Singapore. https://doi.org/10.1007/978-981-99-0030-5_13

Download citation

Publish with us

Policies and ethics