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Plant function and evolutionary biology
REVIEW

Mycorrhiza induced resistance (MIR): a defence developed through synergistic engagement of phytohormones, metabolites and rhizosphere

Swapnil B. Kadam A , Anupama A. Pable B and Vitthal T. Barvkar https://orcid.org/0000-0003-4009-5924 A C
+ Author Affiliations
- Author Affiliations

A Department of Botany, Savitribai Phule Pune University, Pune-411007, India.

B Department of Microbiology, Savitribai Phule Pune University, Pune-411007, India.

C Corresponding authors. Email: bvitthal@unipune.ac.in; vbarvkar@gmail.com

Functional Plant Biology 47(10) 880-890 https://doi.org/10.1071/FP20035
Submitted: 5 February 2020  Accepted: 8 May 2020   Published: 26 June 2020

Abstract

Plants get phosphorus, water and other soil nutrients at the cost of sugar through mycorrhizal symbiotic association. A common mycorrhizal network (CMN) – a dense network of mycorrhizal hyphae – provides a passage for exchange of chemicals and signals between the plants sharing CMN. Mycorrhisation impact plants at hormonal, physiological and metabolic level and successful symbiosis also regulates ecology of the plant rhizosphere. Apart from nutritional benefits, mycorrhisation provides an induced resistance to the plants known as mycorrhiza induced resistance (MIR). MIR is effective against soil as well as foliar pathogens and pest insects. In this review, molecular mechanisms underlying MIR such as role of phytohormones, their cross talk and priming effect are discussed. Evidence of MIR against economically important pathogens and pest insects in different plants is summarised. Mycorrhiza induces many plant secondary metabolites, many of which have a role in plant defence. Involvement of these secondary metabolites in mycorrhisation and their putative role in MIR are further reviewed. Controversies about MIR are also briefly discussed in order to provide insights on the scope for research about MIR. We have further extended our review with an open ended discussion about the possibilities for transgenerational MIR.

Additional keywords: arbuscular mycorrhizal fungi, mycorrhiza induced resistance, transgenerational effects.


References

Agrawal AA, Laforsch C, Tollrian R (1999) Transgenerational induction of defences in animals and plants. Nature 401, 60–63.
Transgenerational induction of defences in animals and plants.Crossref | GoogleScholarGoogle Scholar |

Akiyama K (2007) Chemical identification and functional analysis of apocarotenoids involved in the development of arbuscular mycorrhizal symbiosis. Bioscience, Biotechnology, and Biochemistry 71, 1405–1414.
Chemical identification and functional analysis of apocarotenoids involved in the development of arbuscular mycorrhizal symbiosis.Crossref | GoogleScholarGoogle Scholar | 17587670PubMed |

Akkopru A, Demir S (2005) Biological control of fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria. Journal of Phytopathology 153, 544–550.
Biological control of fusarium wilt in tomato caused by Fusarium oxysporum f. sp. lycopersici by AMF Glomus intraradices and some rhizobacteria.Crossref | GoogleScholarGoogle 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 Physiologiae Plantarum 35, 867–880.
Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants.Crossref | GoogleScholarGoogle Scholar |

Awasthi A, Bharti N, Nair P, Singh R, Shukla AK, Gupta MM, Darokar MP, Kalra A (2011) Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L. Applied Soil Ecology 49, 125–130.
Synergistic effect of Glomus mosseae and nitrogen fixing Bacillus subtilis strain Daz26 on artemisinin content in Artemisia annua L.Crossref | GoogleScholarGoogle Scholar |

Azcón-Aguilar C, Barea JM (1997) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved. Mycorrhiza 6, 457–464.
Arbuscular mycorrhizas and biological control of soil-borne plant pathogens – an overview of the mechanisms involved.Crossref | GoogleScholarGoogle Scholar |

Babikova Z, Gilbert L, Bruce TJA, Birkett M, Caulfield JC, Woodcock C, Pickett JA, Johnson D (2013) Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters 16, 835–843.
Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack.Crossref | GoogleScholarGoogle Scholar | 23656527PubMed |

Barto EK, Hilker M, Müller F, Mohney BK, Weidenhamer JD, Rillig MC (2011) The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One 6, e27195
The fungal fast lane: common mycorrhizal networks extend bioactive zones of allelochemicals in soils.Crossref | GoogleScholarGoogle Scholar | 22110615PubMed |

Barto EK, Weidenhamer JD, Cipollini D, Rillig MC (2012) Fungal superhighways: do common mycorrhizal networks enhance below ground communication? Trends in Plant Science 17, 633–637.
Fungal superhighways: do common mycorrhizal networks enhance below ground communication?Crossref | GoogleScholarGoogle Scholar | 22818769PubMed |

Baslam M, Esteban R, García-plazaola JI, Goicoechea N (2013) Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces. Applied Microbiology and Biotechnology 97, 3119–3128.
Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces.Crossref | GoogleScholarGoogle Scholar | 23108529PubMed |

Bending GD, Aspray T, Whipps JM (2006) Significance of microbial interactions in the mycorrhizosphere. Advances in Applied Microbiology 60, 97–132.
Significance of microbial interactions in the mycorrhizosphere.Crossref | GoogleScholarGoogle Scholar | 17157634PubMed |

Benhamou N, Fortin JA, Hamel C, St-Arnaud M, Shatilla A (1994) Resistance responses of mycorrhizal Ri T-DNA-transformed carrot roots to infection by Fusarium oxysporum f. sp. chrysanthemi. Phytopathology 84, 958–968.
Resistance responses of mycorrhizal Ri T-DNA-transformed carrot roots to infection by Fusarium oxysporum f. sp. chrysanthemi.Crossref | GoogleScholarGoogle Scholar |

Bennett AE, Garcia JA, Bever JD, Bennett AE, Alers-garcia J, Bever JD (2006) Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. American Naturalist 167, 141–152.
Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis.Crossref | GoogleScholarGoogle Scholar | 16670976PubMed |

Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends in Plant Science 17, 478–486.
The rhizosphere microbiome and plant health.Crossref | GoogleScholarGoogle Scholar | 22564542PubMed |

Brown MS, Bethlenfalvay GJ (1988) The Glycine-Glomus-Rhizobium symbiosis: VII. Photosynthetic nutrient-use efficiency in nodulated, mycorrhizal soybeans. Plant Physiology 86, 1292–1297.
The Glycine-Glomus-Rhizobium symbiosis: VII. Photosynthetic nutrient-use efficiency in nodulated, mycorrhizal soybeans.Crossref | GoogleScholarGoogle Scholar | 16666069PubMed |

Cameron DD, Neal AL, van Wees SCM, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends in Plant Science 18, 539–545.
Mycorrhiza-induced resistance: more than the sum of its parts?Crossref | GoogleScholarGoogle Scholar | 23871659PubMed |

Camprubi A, Pinochet J, Calvet C, Estaun V (1993) Effects of the root-lesion nematode Pratylenchus vulnus and the vesicular-arbuscular mycorrhizal fungus Glomus mosseae on the growth of three plum rootstocks. Plant and Soil 153, 223–229.
Effects of the root-lesion nematode Pratylenchus vulnus and the vesicular-arbuscular mycorrhizal fungus Glomus mosseae on the growth of three plum rootstocks.Crossref | GoogleScholarGoogle Scholar |

Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman M-A, Piterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-mani B (2006) Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19, 1062–1071.
Priming: getting ready for battle.Crossref | GoogleScholarGoogle Scholar | 17022170PubMed |

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. Molecular Plant-Microbe Interactions 11, 1017–1028.
Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus.Crossref | GoogleScholarGoogle Scholar |

Daft MJ, Okusanya BO (1973) Effect of endogone mycorrhiza on plant growth v. Influence of infection on the multiplication of viruses in tomato, petunia and strawberry. New Phytologist 72, 975–983.
Effect of endogone mycorrhiza on plant growth v. Influence of infection on the multiplication of viruses in tomato, petunia and strawberry.Crossref | GoogleScholarGoogle Scholar |

Dehne HW (1982) Interaction between vesicular-arbuscular mycorrhizal fungi and plant pathogens. Phytopathology 72, 1115–1119.

Dugassa GD, Von Alten H, Schonbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant and Soil 185, 173–182.
Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens.Crossref | GoogleScholarGoogle Scholar |

Elsen A, Gervacio D, Swennen R, De Waele D (2008) AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza 18, 251–256.
AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect.Crossref | GoogleScholarGoogle Scholar | 18392645PubMed |

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.
Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria.Crossref | GoogleScholarGoogle Scholar |

Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytologist 184, 975–987.
Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus.Crossref | GoogleScholarGoogle Scholar | 19765230PubMed |

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 pathogen in wheat. Scientific Reports 8, 9625
Omics approaches revealed how arbuscular mycorrhizal symbiosis enhances yield and resistance to leaf pathogen in wheat.Crossref | GoogleScholarGoogle Scholar | 29941972PubMed |

French KE (2017) Engineering mycorrhizal symbioses to alter plant metabolism and improve crop health. Frontiers in Microbiology 8, 1403
Engineering mycorrhizal symbioses to alter plant metabolism and improve crop health.Crossref | GoogleScholarGoogle Scholar | 28785256PubMed |

Fritz M, Jakobsen I, Foged MF, Thordal-Christensen H, Pons-Kühnemann J (2006) Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani. Mycorrhiza 16, 413–419.
Arbuscular mycorrhiza reduces susceptibility of tomato to Alternaria solani.Crossref | GoogleScholarGoogle Scholar | 16614816PubMed |

Gallou A, Patricio H, Mosquera L, Cranenbrouck S, Pablo J, Declerck S (2011) Physiological and molecular plant pathology mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans. Physiological and Molecular Plant Pathology 76, 20–26.

Garmendia I, Goicoechea N, Aguirreolea J (2004) Effectiveness of three Glomus species in protecting pepper (Capsicum annuum L.) against verticillium wilt. Biological Control 31, 296–305.
Effectiveness of three Glomus species in protecting pepper (Capsicum annuum L.) against verticillium wilt.Crossref | GoogleScholarGoogle Scholar |

Gernns H, von Alten H, Poehling H-M (2001) Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen – is a compensation possible? Mycorrhiza 11, 237–243.
Arbuscular mycorrhiza increased the activity of a biotrophic leaf pathogen – is a compensation possible?Crossref | GoogleScholarGoogle Scholar |

Gilbert L, Johnson D (2017) Plant - plant communication through common mycorrhizal networks. Advances in Botanical Research 82, 83–97.
Plant - plant communication through common mycorrhizal networks.Crossref | GoogleScholarGoogle Scholar |

Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C, Scarpato R (2012) Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants. British Journal of Nutrition 107, 242–251.
Nutraceutical value and safety of tomato fruits produced by mycorrhizal plants.Crossref | GoogleScholarGoogle Scholar | 21733294PubMed |

Graham JHMJA (1982) Influence of vesicular-arbuscular mycorrhizae and soil phosphorous on take-all disease of wheat. Phytopathology 72, 95–98.
Influence of vesicular-arbuscular mycorrhizae and soil phosphorous on take-all disease of wheat.Crossref | GoogleScholarGoogle Scholar |

Graham MY, Graham TL (1991) Rapid accumulation of anionic peroxidases and phenolic polymers in soybean cotyledon tissues following treatment with Phytophthora megasperma f. sp. glycinea wall glucan. Plant Physiology 97, 1445–1455.
Rapid accumulation of anionic peroxidases and phenolic polymers in soybean cotyledon tissues following treatment with Phytophthora megasperma f. sp. glycinea wall glucan.Crossref | GoogleScholarGoogle Scholar | 16668570PubMed |

Hao Z, Fayolle L, van Tuinen D, Chatagnier O, Li X, Gianinazzi S, Gianinazzi-Pearson V (2012) Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine. Journal of Experimental Botany 63, 3657–2672.
Local and systemic mycorrhiza-induced protection against the ectoparasitic nematode Xiphinema index involves priming of defence gene responses in grapevine.Crossref | GoogleScholarGoogle Scholar | 22407649PubMed |

Heppell KB, Shumway DL, Koide RT (1998) The effect of mycorrhizal infection of Abutilon theophrasti on competitiveness of offspring. Functional Ecology 12, 171–175.
The effect of mycorrhizal infection of Abutilon theophrasti on competitiveness of offspring.Crossref | GoogleScholarGoogle Scholar |

Hill EM, Robinson LA, Abdul-sada A, Vanbergen AJ, Hodge A, Hartley SE (2018) Arbuscular mycorrhizal fungi and plant chemical defence: effects of colonisation on aboveground and belowground metabolomes. Journal of Chemical Ecology 44, 198–208.
Arbuscular mycorrhizal fungi and plant chemical defence: effects of colonisation on aboveground and belowground metabolomes.Crossref | GoogleScholarGoogle Scholar | 29392532PubMed |

Hou X, Rivers J, León P, Mcquinn RP, Pogson BJ (2016) Synthesis and function of apocarotenoid signals in plants. Trends in Plant Science 21, 792–803.
Synthesis and function of apocarotenoid signals in plants.Crossref | GoogleScholarGoogle Scholar | 27344539PubMed |

Hussein RA, El-Anssary AA (2018) Plants secondary metabolites: the key drivers of the pharmacological actions of medicinal plants. In ‘Herbal medicine’ (Ed. P Builders) pp. 11–30. (Intech Open) Available at https://www.intechopen.com/books/herbal-medicine/plants-secondary-metabolites-the-key-drivers-of-the-pharmacological-actions-of-medicinal-plants [Verified 9 June 2020]

Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. Journal of Chemical Ecology 38, 651–664.
Mycorrhiza-induced resistance and priming of plant defenses.Crossref | GoogleScholarGoogle Scholar | 22623151PubMed |

Kapoor R, Giri B, Mukerji KG (2002a) Mycorrhization of coriander (Coriandrum sativum L) to enhance the concentration and quality of essential oil. Journal of the Science of Food and Agriculture 82, 339–342.
Mycorrhization of coriander (Coriandrum sativum L) to enhance the concentration and quality of essential oil.Crossref | GoogleScholarGoogle Scholar |

Kapoor R, Giri B, Mukerji KG (2002b) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in dill (Anethum graveolens L.) and carum (Trachyspermum ammi (Linn.) Sprague). World Journal of Microbiology & Biotechnology 18, 459–463.
Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in dill (Anethum graveolens L.) and carum (Trachyspermum ammi (Linn.) Sprague).Crossref | GoogleScholarGoogle Scholar |

Khaosaad T, Garcıa-Garrido JM, Steinkellner S, Vierheilig H (2007) Take-all disease is systemically reduced in roots of mycorrhizal barley plants. Soil Biology & Biochemistry 39, 727–734.
Take-all disease is systemically reduced in roots of mycorrhizal barley plants.Crossref | GoogleScholarGoogle Scholar |

Kobra N, Jalil K, Youbert G (2009) Effects of three glomus species as biocontrol agents against verticillium-induced wilt in cotton. Journal of Plant Protection Research 49, 185–189.
Effects of three glomus species as biocontrol agents against verticillium-induced wilt in cotton.Crossref | GoogleScholarGoogle Scholar |

Leake J, Johnson D, Donnelly D, Muckle G, Boddy L, Read D (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany 82, 1016–1045.
Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning.Crossref | GoogleScholarGoogle Scholar |

Li H, Smith SE, Holloway RE, Zhu Y, Smith FA (2006a) Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses. New Phytologist 172, 536–543.
Arbuscular mycorrhizal fungi contribute to phosphorus uptake by wheat grown in a phosphorus-fixing soil even in the absence of positive growth responses.Crossref | GoogleScholarGoogle Scholar | 17083683PubMed |

Li H-Y, Yang G-D, Shu H-R, Yang Y-T, Ye B-X, Nishida I, Zheng C-C (2006b) Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3. Plant & Cell Physiology 47, 154–163.
Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitinase gene VCH3.Crossref | GoogleScholarGoogle Scholar |

Li Y, Liu Z, Hou H (2013) Arbuscular mycorrhizal fungi-enhanced resistance against Phytophthora sojae infection on soybean leaves is mediated by a network involving hydrogen peroxide, jasmonic acid, and the metabolism of carbon and nitrogen. Acta Physiologiae Plantarum 35, 3465–3475.
Arbuscular mycorrhizal fungi-enhanced resistance against Phytophthora sojae infection on soybean leaves is mediated by a network involving hydrogen peroxide, jasmonic acid, and the metabolism of carbon and nitrogen.Crossref | GoogleScholarGoogle Scholar |

Linderman RG (1988) Mycorrhizal interactions with the rhizosphere microflora: the mycorrhizosphere effect. Phytopathology 78, 366–371.

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 | 17419842PubMed |

Liu Y, Feng X, Gao P, Li Y, Christensen MJ, Duan T (2018) Arbuscular mycorrhiza fungi increased the susceptibility of Astragalus adsurgens to powdery mildew caused by Erysiphe pisi. Mycology 9, 223–232.
Arbuscular mycorrhiza fungi increased the susceptibility of Astragalus adsurgens to powdery mildew caused by Erysiphe pisi.Crossref | GoogleScholarGoogle Scholar | 30181928PubMed |

López-Ráez JA, Flors V, García JM, Pozo MJ (2010) AM symbiosis alters phenolic acid content in tomato roots. Plant Signaling & Behavior 5, 1138–1140.
AM symbiosis alters phenolic acid content in tomato roots.Crossref | GoogleScholarGoogle Scholar |

Luna E, Bruce TJA, Roberts MR, Flors V, Ton J (2012) Next-generation systemic acquired resistance. Plant Physiology 158, 844–853.
Next-generation systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 22147520PubMed |

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, 179–186.
The arbuscular mycorrhizal symbiosis attenuates symptom severity and reduces virus concentration in tomato infected by Tomato yellow leaf curl Sardinia virus (TYLCSV).Crossref | GoogleScholarGoogle Scholar | 24072193PubMed |

Martín-Rodríguez JA, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, García-Garrido M (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytologist 190, 193–205.
Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi.Crossref | GoogleScholarGoogle Scholar | 21232061PubMed |

Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annual Review of Plant Biology 68, 485–512.
Defense priming: an adaptive part of induced resistance.Crossref | GoogleScholarGoogle Scholar | 28226238PubMed |

Meng J, Wang L, Wang J, Zhao X, Cheng J, Yu W, Jin D, Li Q, Gong Z (2018) METHIONINE ADENOSYLTRANSFERASE4 mediates DNA and histone methylation. Plant Physiology 177, 652–670.
METHIONINE ADENOSYLTRANSFERASE4 mediates DNA and histone methylation.Crossref | GoogleScholarGoogle Scholar | 29572390PubMed |

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. Molecular Plant-Microbe Interactions 24, 1562–1572.
Arbuscular mycorrhizal symbiosis limits foliar transcriptional responses to viral infection and favors long-term virus accumulation.Crossref | GoogleScholarGoogle Scholar | 21899386PubMed |

Mishina TE, Zeier J (2007) Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. The Plant Journal 50, 500–513.
Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17419843PubMed |

Morandi D (1996) Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control. Plant and Soil 185, 241–251.
Occurrence of phytoalexins and phenolic compounds in endomycorrhizal interactions, and their potential role in biological control.Crossref | GoogleScholarGoogle Scholar |

Nemec S, Myhre D (1984) Virus-Glomus etunicatum interactions in Citrus rootstocks. Plant Disease 68, 311–314.
Virus-Glomus etunicatum interactions in Citrus rootstocks.Crossref | GoogleScholarGoogle Scholar |

Niederhuth CE, Schmitz RJ (2017) Putting DNA methylation in context: from genomes to gene expression in plants. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1860, 149–156.

Pagare S, Bhatia M, Tripathi N, Pagare S, Bansal YK (2015) Secondary metabolites of plants and their role: overview. Current Trends in Biotechnology and Pharmacy 9, 293–304.

Pandey DK, Kaur P, Dey A (2018) Arbuscular mycorrhizal fungi: effects on secondary metabolite production in medicinal plants. In ‘Fungi and their role in sustainable development: current perspectives’. (Eds P Gehlot, J Singh) pp. 507–538. (Springer: Singapore)

Paszkowski U (2006) Mutualism and parasitism: the yin and yang of plant symbioses. Current Opinion in Plant Biology 9, 364–370.
Mutualism and parasitism: the yin and yang of plant symbioses.Crossref | GoogleScholarGoogle Scholar | 16713732PubMed |

Pinochet J, Camprubi A, Caivet C (1993) Effects of the root-lesion nematode Pratylenchus vulnus and the mycorrhizal fungus Glomus mosseae on the growth of EMLA-26 apple rootstock. Mycorrhiza 4, 79–83.
Effects of the root-lesion nematode Pratylenchus vulnus and the mycorrhizal fungus Glomus mosseae on the growth of EMLA-26 apple rootstock.Crossref | GoogleScholarGoogle Scholar |

Pinochet J, Calvet C, Camprubi A, Fernandez C (1995a) Interaction between the root-lesion nematode Pratylenchus vulnus and the mycorrhizal association of Glomus intraradices and Santa Lucia 64 cherry rootstock. Plant and Soil 170, 323–329.
Interaction between the root-lesion nematode Pratylenchus vulnus and the mycorrhizal association of Glomus intraradices and Santa Lucia 64 cherry rootstock.Crossref | GoogleScholarGoogle Scholar |

Pinochet J, Calvet C, Camprubi A, Fernandez C (1995b) Growth and nutritional response of Nemared peach rootstock infected with Pratylenchus vulnus and the mycorrhizal fungus Glomus mosseae. Fundamental and Applied Nematology 18, 205–210.

Pozo MJ, Azcón-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Current Opinion in Plant Biology 10, 393–398.
Unraveling mycorrhiza-induced resistance.Crossref | GoogleScholarGoogle Scholar | 17658291PubMed |

Pozo MJ, Azon-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 |

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

Rasmann S, De Vos M, Casteel CL, Tian D, Halitschke R, Sun JY, Agrawal AA, Felton GW, Jander G (2012) Herbivory in the previous generation primes plants for enhanced insect resistance. Plant Physiology 158, 854–863.
Herbivory in the previous generation primes plants for enhanced insect resistance.Crossref | GoogleScholarGoogle Scholar | 22209873PubMed |

Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in ‘lower’ land plants. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 815–831.
Symbiotic fungal associations in ‘lower’ land plants.Crossref | GoogleScholarGoogle Scholar | 10905611PubMed |

Rúa MA, Umbanhowar J, Hu S, Burkey KO, Mitchell CE (2013) Elevated CO2 spurs reciprocal positive effects between a plant virus and an arbuscular mycorrhizal fungus. New Phytologist 199, 541–549.
Elevated CO2 spurs reciprocal positive effects between a plant virus and an arbuscular mycorrhizal fungus.Crossref | GoogleScholarGoogle Scholar | 23594373PubMed |

Salvioli A, Bonfante P (2013) Plant Science Systems biology and ‘omics’ tools: a cooperation for next-generation mycorrhizal studies. Plant Science 203–204, 107–114.
Plant Science Systems biology and ‘omics’ tools: a cooperation for next-generation mycorrhizal studies.Crossref | GoogleScholarGoogle Scholar | 23415334PubMed |

Sauter M, Moffatt B, Saechao MC, Hell R, Wirtz M (2013) Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. The Biochemical Journal 451, 145–154.
Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis.Crossref | GoogleScholarGoogle Scholar | 23535167PubMed |

Selosse M-A, Richard F, He X, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends in Ecology & Evolution 21, 621–628.
Mycorrhizal networks: des liaisons dangereuses?Crossref | GoogleScholarGoogle 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. Molecular Plant-Microbe Interactions 12, 1000–1007.
Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves.Crossref | GoogleScholarGoogle Scholar | 10550896PubMed |

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

Smith SE, Read DJ (2010) ‘Mycorrhizal symbiosis.’ (Academic Press: New York, NY, USA)

Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annual Review of Plant Biology 62, 227–250.
Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales.Crossref | GoogleScholarGoogle Scholar | 21391813PubMed |

Song YY, Cao M, Xie LJ, Liang XT, Sen Zeng R, Su YJ, Huang JH, Wang RL, Luo SM (2011) Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight. Mycorrhiza 21, 721–731.
Induction of DIMBOA accumulation and systemic defense responses as a mechanism of enhanced resistance of mycorrhizal corn (Zea mays L.) to sheath blight.Crossref | GoogleScholarGoogle Scholar | 21484338PubMed |

Song YY, Simard SW, Carroll A, Mohn WW, Sen Zeng R (2015a) Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ectomycorrhizal networks. Scientific Reports 5, 8495
Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ectomycorrhizal networks.Crossref | GoogleScholarGoogle Scholar | 25683155PubMed |

Song Y, Chen D, Lu K, Sun Z, Zeng R (2015b) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science 6, 786
Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus.Crossref | GoogleScholarGoogle Scholar | 26442091PubMed |

Srivastava D, Mukerji KG (1995) Field response of mycorrhizal and nonmycorrhizal Medicago sativa var. local in the F1 generation. Mycorrhiza 5, 219–221.
Field response of mycorrhizal and nonmycorrhizal Medicago sativa var. local in the F1 generation.Crossref | GoogleScholarGoogle Scholar |

Stolyarchuk IM, Shevchenk TP, Polischuk VP, Kripka A V (2009) Virus infection course in different plant species under influence of arbuscular mycorrhiza. Microbiology & biotechnology 172, 70–75.

Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytologist 172, 22–34.
Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots.Crossref | GoogleScholarGoogle Scholar | 16945086PubMed |

Suresh CK, Bagyaraj DJ, Reddy DDR (1985) Effect of vesicular-arbuscular mycorrhiza on survival, penetration and development of root-knot nematode in tomato. Plant and Soil 87, 305–308.
Effect of vesicular-arbuscular mycorrhiza on survival, penetration and development of root-knot nematode in tomato.Crossref | GoogleScholarGoogle Scholar |

Thaler JS, Bostock RM (2004) Interactions between abscisic‐acid‐mediated responses and plant resistance to pathogens and insects. Ecology 85, 48–58.
Interactions between abscisic‐acid‐mediated responses and plant resistance to pathogens and insects.Crossref | GoogleScholarGoogle Scholar |

Thiem D, Szmidt-jaworska A, Baum C, Muders K, Niedojadło K, Hrynkiewicz K (2014) Interactive physiological response of potato (Solanum tuberosum L.) plants to fungal colonization and Potato virus Y (PVY) infection. Acta Mycologica 49, 291–303.
Interactive physiological response of potato (Solanum tuberosum L.) plants to fungal colonization and Potato virus Y (PVY) infection.Crossref | GoogleScholarGoogle Scholar |

Ton J, Flors V, Mauch-mani B (2009) The multifaceted role of ABA in disease resistance. Trends in Plant Science 14, 310–317.
The multifaceted role of ABA in disease resistance.Crossref | GoogleScholarGoogle Scholar | 19443266PubMed |

Varga S, Soulsbury CD (2019) Arbuscular mycorrhizal fungi change host plant DNA methylation systemically. Plant Biology 21, 278–283.
Arbuscular mycorrhizal fungi change host plant DNA methylation systemically.Crossref | GoogleScholarGoogle Scholar | 30253017PubMed |

Vierheilig H (2004) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. Journal of Plant Physiology 161, 339–341.
Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization.Crossref | GoogleScholarGoogle Scholar | 15077632PubMed |

Vierheilig H, Piché Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. In ‘Flavonoids in cell function. Advances in experimental medicine and biology, vol 505’. (Eds BD Buslig, JA Manthey) pp. 23–39. (Springer: Boston, MA)

Walker V, Couillerot O, Von Felten A, Bellvert F, Jansa J, Maurhofer M, Bally R, Moënne-Loccoz Y, Comte G (2012) Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions. Plant and Soil 356, 151–163.
Variation of secondary metabolite levels in maize seedling roots induced by inoculation with Azospirillum, Pseudomonas and Glomus consortium under field conditions.Crossref | GoogleScholarGoogle Scholar |

Walter MH, Floß DS, Hans J, Fester T, Strack D (2007) Apocarotenoid biosynthesis in arbuscular mycorrhizal roots: contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation. Phytochemistry 68, 130–138.
Apocarotenoid biosynthesis in arbuscular mycorrhizal roots: contributions from methylerythritol phosphate pathway isogenes and tools for its manipulation.Crossref | GoogleScholarGoogle Scholar | 17084869PubMed |

Wang Y, Yin Q, Qu Y, Li G, Hao L (2018a) Arbuscular mycorrhiza‐mediated resistance in tomato against Cladosporium fulvum‐induced mould disease. Journal of Phytopathology 166, 67–74.
Arbuscular mycorrhiza‐mediated resistance in tomato against Cladosporium fulvum‐induced mould disease.Crossref | GoogleScholarGoogle Scholar |

Wang M, Schäfer M, Li D, Halitschke R, Dong C, Mcgale E, Paetz C, Song Y, Li S, Dong J, Heiling S, Groten K, Franken P, Bitterlich M, Harrison MJ, Paszkowski U, Baldwin IT (2018b) Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi. eLife 7, e37093
Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar | 30412053PubMed |

Whipps JM (2004) Prospects and limitations for mycorrhizas in biocontrol of root pathogens. Canadian Journal of Botany 82, 1198–1227.
Prospects and limitations for mycorrhizas in biocontrol of root pathogens.Crossref | GoogleScholarGoogle Scholar |

Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L. Plant, Cell & Environment 21, 209–216.
Effects of VA mycorrhizal colonization on photosynthesis and biomass production of Trifolium repens L.Crossref | GoogleScholarGoogle Scholar |

Yao MK, Desilets H, Charles MT, Boulanger R, Tweddell RJ (2003) Effect of mycorrhization on the accumulation of rishitin and solavetivone in potato plantlets challenged with Rhizoctonia solani. Mycorrhiza 13, 333–336.
Effect of mycorrhization on the accumulation of rishitin and solavetivone in potato plantlets challenged with Rhizoctonia solani.Crossref | GoogleScholarGoogle Scholar | 14505123PubMed |

Zhi-lin Y, Chuan-chao D, Lian-qing C (2007) Regulation and accumulation of secondary metabolites in plant–fungus symbiotic system. African Journal of Biotechnology 6, 1266–1271.

Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. Journal of Phytopathology 152, 537–542.
Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum.Crossref | GoogleScholarGoogle Scholar |