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  • Review Article
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Unique and common traits in mycorrhizal symbioses

Abstract

Mycorrhizas are among the most important biological interkingdom interactions, as they involve ~340,000 land plants and ~50,000 taxa of soil fungi. In these mutually beneficial interactions, fungi receive photosynthesis-derived carbon and provide the host plant with mineral nutrients such as phosphorus and nitrogen in exchange. More than 150 years of research on mycorrhizas has raised awareness of their biology, biodiversity and ecological impact. In this Review, we focus on recent phylogenomic, molecular and cell biology studies to present the current state of knowledge of the origin of mycorrhizal fungi and the evolutionary history of their relationship with land plants. As mycorrhizas feature a variety of phenotypes, depending on partner taxonomy, physiology and cellular interactions, we explore similarities and differences between mycorrhizal types. During evolution, mycorrhizal fungi have refined their biotrophic capabilities to take advantage of their hosts as food sources and protective niches, while plants have developed multiple strategies to accommodate diverse fungal symbionts. Intimate associations with pervasive ecological success have originated at the crossroads between these two evolutionary pathways. Our understanding of the biological processes underlying these symbioses, where fungi act as biofertilizers and bioprotectors, provides the tools to design biotechnological applications addressing environmental and agricultural challenges.

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Fig. 1: Major mycorrhizal types.
Fig. 2: Arbuscular mycorrhizal symbiosis in extant bryophytes.
Fig. 3: Unique and common traits in mycorrhizal interactions.

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References

  1. Smith, S. E. & Read, D. Mycorrhizal Symbiosis, 3rd edn (Academic Press, 2008).

  2. Bahadur, A. et al. Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int. J. Mol. Sci. 20, E4199 (2019).

    PubMed  Google Scholar 

  3. Johnson, N., Gehring, C. & Jansa, J. Mycorrhizal mediation of soil (Elsevier, 2016).

  4. van der Heijden, M. A., Martin, F. M., Selosse, M.-A. & Sanders, I. R. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol. 205, 1406–1423 (2015).

    PubMed  Google Scholar 

  5. Ferlian, O. et al. Mycorrhiza in tree diversity-ecosystem function relationships: conceptual framework and experimental implementation. Ecosphere 9, e02226 (2018).

    PubMed  PubMed Central  Google Scholar 

  6. Tedersoo, L., Bahram, M. & Zob, M. How mycorrhizal associations drive plant population and community. Science 367, eaba1223 (2020).

    CAS  PubMed  Google Scholar 

  7. Fernie, A. R. & Yan, J. De novo domestication: an alternative route toward new crops for the future. Mol. Plant 12, 615–631 (2019).

    CAS  PubMed  Google Scholar 

  8. Peterson, R. L., Massicotte, H. B., & Melville, L. H. Mycorrhizas: anatomy and cell biology (CABI Publishing, 2004).

  9. Bonfante, P. The future has roots in the past: the ideas and scientists that shaped mycorrhizal research. New Phytol. 220, 982–995 (2018).

    PubMed  Google Scholar 

  10. Simard, S. W. et al. Mycorrhizal networks: mechanisms, ecology and modelling. Fung. Biol. Rev. 26, 39–60 (2012).

    Google Scholar 

  11. Bonfante, P., Venice, F. & Lanfranco, L. The mycobiota: fungi take their place between plants and bacteria. Curr. Opin. Microbiol. 49, 18–25 (2019).

    CAS  PubMed  Google Scholar 

  12. Compant, S., Samad, A., Faist, H. & Sessitsch, A. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J. Adv. Res. 19, 29–37 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Elinav, E., Garrett, W. S., Trinchieri, G. & Wargo, J. The cancer microbiome. Nat. Rev. Cancer 19, 371–376 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Strullu-Derrien, C., Selosse, M. A., Kenrick, P. & Martin, F. M. The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics. New Phytol. 220, 1012–1030 (2018). This review is a precious resource of data linking fossil reports with fungal genome sequences.

    PubMed  Google Scholar 

  15. Field, K. J. & Pressel, S. Unity in diversity: structural and functional insights into the ancient partnerships between plants and fungi. New Phytol. 220, 996–1011 (2018).

    CAS  PubMed  Google Scholar 

  16. Remy, W., Taylor, T. N., Hass, H. & Kerp, H. Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc. Natl Acad. Sci. USA 91, 11841–11843 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Spatafora, J. W. et al. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108, 1028–1046 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Strullu-Derrien, C. et al. Fungal associations in Horneophyton ligneri from the Rhynie Chert (c. 407 Ma) closely resemble those in extant lower land plants: novel insights into ancestral plant-fungus symbioses. New Phytol. 203, 964–979 (2014).

    PubMed  Google Scholar 

  19. Feijen, F. A. A., Vos, R. A., Nuytinck, J. & Merckx, V. S. F. T. Evolutionary dynamics of mycorrhizal symbiosis in land plant diversification. Sci. Rep. 8, 10698 (2018).

    PubMed  PubMed Central  Google Scholar 

  20. Hoysted, G. A. et al. A mycorrhizal revolution. Curr. Opin. Plant Biol. 44, 1–6 (2018).

    CAS  PubMed  Google Scholar 

  21. Bonfante, P. & Venice, F. Mucoromycota: going to the roots of plant-interacting fungi. Fung. Biol. Rev. 34, 100–113 (2020).

    Google Scholar 

  22. Beimforde, C. et al. Ectomycorrhizas from a Lower Eocene angiosperm forest. New Phytol. 192, 988–996 (2011).

    PubMed  Google Scholar 

  23. Jin-Hua, R., Shen, T. T., Wang, M. M. & Wang, X. Q. Phylogenomics resolves the deep phylogeny of seed plants and indicates partial convergent or homoplastic evolution between Gnetales and angiosperms. Proc. R. Soc. 285, 20181012 (2018).

    Google Scholar 

  24. Ramirez, S. R., Gravendeel, B., Singer, R. B., Marshall, C. R. & Pierce, N. E. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448, 1042–1045 (2007).

    CAS  PubMed  Google Scholar 

  25. Freudenstein, J. V., Broe, B. B. & Feldenkris, E. R. Phylogenetic relationships at the base of Ericaceae: implications for vegetative and mycorrhizal evolution. Taxon 65, 794–804 (2016).

    Google Scholar 

  26. Ligrone, R. et al. Glomeromycotean associations in liverworts: a molecular, cellular, and taxonomic analysis. Am. J. Bot. 94, 1756–1777 (2007).

    CAS  PubMed  Google Scholar 

  27. Rimington, W. R., Duckett, J. G., Field, K. J., Bidartondo, M. I. & Pressel, S. The distribution and evolution of fungal symbioses in ancient lineages of land plants. Mycorrhiza 29, 551–565 (2020).

    Google Scholar 

  28. Benucci, G. M. et al. Evidence for co-evolutionary history of early diverging Lycopodiaceae plants with fungi. Front. Microbiol. 10, 2944 (2020).

    PubMed  PubMed Central  Google Scholar 

  29. Humphreys, C. P. et al. Mutualistic mycorrhiza-like symbiosis in the most ancient group of land plants. Nat. Commun. 1, 103 (2010).

    PubMed  Google Scholar 

  30. Bona, E. et al. Arbuscular mycorrhizal symbiosis affects the grain proteome of Zea mays: a field study. Sci. Rep. 6, 26439 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Fiorilli, V. et al. Omics approaches revealed how arbuscular mycorrhizal symbiosis enhances yield and resistance to leaf pathogen in wheat. Sci. Rep. 8, 9625 (2018).

    PubMed  PubMed Central  Google Scholar 

  32. Koide, R. T. & Lu, X. Mycorrhizal infection of wild oats: maternal effects on offspring growth and reproduction. Oecologia 90, 218–226 (1992).

    PubMed  Google Scholar 

  33. Varga, S., Vega-Frutis, R. & Kytöviita, M. M. Transgenerational effects of plant sex and arbuscular mycorrhizal symbiosis. New Phytol. 199, 812–821 (2013).

    PubMed  Google Scholar 

  34. Martin, F., Kohler, A., Murat, C., Veneault-Fourrey, C. & Hibbett, D. S. Unearthing the roots of ectomycorrhizal symbioses. Nat. Rev. Microbiol. 14, 760–773 (2016).

    CAS  PubMed  Google Scholar 

  35. Toruño, T. Y., Stergiopoulos, I. & Coaker, G. Plant-pathogen effectors: cellular probes interfering with plant defenses in spatial and temporal manners. Annu. Rev. Phytopathol. 54, 419–441 (2016).

    PubMed  PubMed Central  Google Scholar 

  36. Franceschetti, M. et al. Effectors of filamentous plant pathogens: commonalities amid diversity. Microbiol. Mol. Biol. Rev. 81, e00066-16 (2017).

    PubMed  PubMed Central  Google Scholar 

  37. Kohler, A. et al. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nat. Genet. 47, 410–415 (2015). This article compares the genomes of almost 50 fungi and reveals that, during evolution, all ECM fungi originating from saprotrophic ancestors experienced substantial loss of genes coding for plant cell wall-degrading enzymes.

    CAS  PubMed  Google Scholar 

  38. Hibbett, D. S., Gilbert, L. B. & Donoghue, M. J. Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407, 506–508 (2000).

    CAS  PubMed  Google Scholar 

  39. Floudas, D. et al. The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336, 1715–1719 (2012).

    CAS  PubMed  Google Scholar 

  40. Martin, F. et al. Symbiosis insights from the genome of the mycorrhizal basidiomycete Laccaria bicolor. Nature 452, 88–92 (2008). The article describes the first sequenced genome of a mycorrhizal fungus.

    CAS  PubMed  Google Scholar 

  41. Pellitier, P. T. & Zak, D. R. Ectomycorrhizal fungi and the enzymatic liberation of nitrogen from soil organic matter: why evolutionary history matters. New Phytol. 217, 68–73 (2018).

    CAS  PubMed  Google Scholar 

  42. Peter, M. et al. Ectomycorrhizal ecology is imprinted in the genome of the dominant symbiotic fungus Cenococcum geophilum. Nat. Commun. 7, 12662 (2016).

    PubMed  PubMed Central  Google Scholar 

  43. Murat, C. et al. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. Nat. Ecol. Evol. 2, 1956–1965 (2018).

    PubMed  Google Scholar 

  44. Ferrari, S. et al. Oligogalacturonides: plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 4, 49 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Martino, E. et al. Comparative genomics and transcriptomics depict ericoid mycorrhizal fungi as versatile saprotrophs and plant mutualists. New Phytol. 217, 1213–1229 (2018).

    CAS  PubMed  Google Scholar 

  46. Perotto, S., Daghino, S. & Martino, E. Ericoid mycorrhizal fungi and their genomes: another side to the mycorrhizal symbiosis? New Phytol. 220, 1141–1147 (2018).

    PubMed  Google Scholar 

  47. Wilson, A. W., Hosaka, K. & Mueller, G. M. Evolution of ectomycorrhizas as a driver of diversification and biogeographic patterns in the model mycorrhizal mushroom genus Laccaria. New Phytol. 213, 1862–1873 (2017).

    CAS  PubMed  Google Scholar 

  48. Albalat, R. & Cañestro, C. Evolution by gene loss. Nat. Rev. Genet. 17, 379–391 (2016).

    CAS  PubMed  Google Scholar 

  49. Selosse, M.-A., Schneider-Maunoury, L. & Martos, F. Time to re-think fungal ecology? Fungal ecological niches are often prejudged. New Phytol. 217, 968–972 (2018).

    PubMed  Google Scholar 

  50. Chen, E. C. H. et al. High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol. 220, 1161–1171 (2018).

    CAS  PubMed  Google Scholar 

  51. Venice, F. et al. At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions. Environ. Microbiol. 22, 122–141 (2020).

    PubMed  Google Scholar 

  52. Harrison, M. J. & van Buuren, M. L. A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378, 626–629 (1995).

    CAS  PubMed  Google Scholar 

  53. Wewer, V., Brands, M. & Dörmann, P. Fatty acid synthesis and lipid metabolism in the obligate biotrophic fungus Rhizophagus irregularis during mycorrhization of Lotus japonicus. Plant J. 79, 398–412 (2014).

    CAS  PubMed  Google Scholar 

  54. Jang, Y. et al. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356, 1172–1175 (2017). This is a seminal contribution to the concept that AM fungi depend on their host plant for lipids.

    Google Scholar 

  55. Luginbuehl, L. H. et al. Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356, 1175–1178 (2017). This study provides insight into the dependence of AM fungi on their hosts for fatty acids.

    CAS  PubMed  Google Scholar 

  56. Schüßler A. in The Mycota - Fungal Associations (ed. Hock, B.) 77–91 (Springer, 2012).

  57. Oldroyd, G. E. D. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252–263 (2013).

    CAS  PubMed  Google Scholar 

  58. Delaux, P. M., Radhakrishnan, G. & Oldroyd, G. Tracing the evolutionary path to nitrogen-fixing crops. Curr. Opin. Plant Biol. 26, 95–99 (2015).

    CAS  PubMed  Google Scholar 

  59. Radhakrishnan, G. V. et al. An ancestral signalling pathway is conserved in intracellular symbioses-forming plant lineages. Nat. Plants 6, 1–10 (2020). This extensive analysis of multiple genomes and transcriptomes outlines a set of genes conserved across plant clades that host intracellular symbionts.

    Google Scholar 

  60. Gutjahr, C. & Parniske, M. Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 29, 593–617 (2013).

    CAS  PubMed  Google Scholar 

  61. Genre, A. & Russo, G. Does a common pathway transduce symbiotic signals in plant–microbe interactions? Front. Plant Sci. 7, 9 (2016).

    Google Scholar 

  62. Barker, D. G., Chabaud, M., Russo, G. & Genre, A. Nuclear Ca2+ signalling in arbuscular mycorrhizal and actinorhizal endosymbioses: on the trail of novel underground signals. New Phytol. 214, 533–538 (2017).

    CAS  PubMed  Google Scholar 

  63. Bravo, A., York, T., Pumplin, N., Mueller, L. A. & Harrison, M. J. Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat. Plants 2, 15208 (2016).

    CAS  PubMed  Google Scholar 

  64. Kamel, L. et al. The comparison of expressed candidate secreted proteins from two arbuscular mycorrhizal fungi unravels common and specific molecular tools to invade different host plants. Front. Plant Sci. 8, 124 (2017).

    PubMed  PubMed Central  Google Scholar 

  65. Zipfel, C. & Oldroyd, G. E. Plant signalling in symbiosis and immunity. Nature 543, 328–336 (2017).

    CAS  PubMed  Google Scholar 

  66. Akiyama, K., Matsuzaki, K. & Hayashi, H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824–827 (2005).

    CAS  PubMed  Google Scholar 

  67. Al-Babili, S. & Bouwmeester, H. J. Strigolactones, a novel carotenoid-derived plant hormone. Annu. Rev. Plant Biol. 66, 161–186 (2015).

    CAS  PubMed  Google Scholar 

  68. Besserer, A., Bécard, G., Jauneau, A., Roux, C. & Séjalon-Delmas, N. GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol. 148, 402–413 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Salvioli, A. et al. Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J. 10, 130–144 (2016).

    CAS  PubMed  Google Scholar 

  70. Maillet, F. et al. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58–63 (2011). This article identifies lipochito-oligosaccharides as the fungal molecules required for AM establishment.

    CAS  PubMed  Google Scholar 

  71. Genre, A. et al. Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 198, 179–189 (2013). This article identifies chito-oligosaccharides as additional fungal molecules required for AM establishment.

    PubMed  Google Scholar 

  72. Sun, J. et al. Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27, 823–838 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Chabaud, M. et al. Chitotetraose activates the fungal-dependent endosymbiotic signaling pathway in actinorrhizal plant species. PLoS One 10, e0223149 (2019).

    Google Scholar 

  74. He, J. et al. A LysM receptor heteromer mediates perception of arbuscular mycorrhizal symbiotic signal in rice. Mol. Plant 12, 1561–1576 (2019). This article presents the first description of a bona fide Myc-factor receptor mediating the AM-specific activation of symbiotic signalling.

    CAS  PubMed  Google Scholar 

  75. Hohnjec, N., Vieweg, M. F., Pühler, A., Becker, A. & Küster, H. Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137, 1283–1301 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Schmitz, A. M. & Harrison, M. J. Signaling events during initiation of arbuscular mycorrhizal symbiosis. J. Integ. Plant Biol. 56, 250–261 (2014). This is an outstanding review of the plant–fungus dialogue required for AM symbiosis.

    Google Scholar 

  77. Czaja, L. F. et al. Transcriptional responses towards diffusible signals from symbiotic microbes reveal MtNFP-and MtDMI3- dependent reprogramming of host gene expression by arbuscular mycorrhizal fungal lipochitooligosaccharides. Plant Physiol. 159, 1671–1685 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Genre, A., Chabaud, M., Timmers, T., Bonfante, P. & Barker, D. G. Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489–3499 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Gutjahr, C. et al. Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots. New Phytol. 183, 53–61 (2009).

    CAS  PubMed  Google Scholar 

  80. Kosuta, S. et al. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol. 131, 952–962 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Miura, C. et al. The mycoheterotrophic symbiosis between orchids and mycorrhizal fungi possesses major components shared with mutualistic plant-mycorrhizal symbioses. Mol. Plant Microbe Interact. 31, 1032–1047 (2018).

    CAS  PubMed  Google Scholar 

  82. Yuan, Y. et al. The Gastrodia elata genome provides insights into plant adaptation to heterotrophy. Nat. Commun. 9, 1615 (2018).

    PubMed  PubMed Central  Google Scholar 

  83. Cope, K. R. et al. The ectomycorrhizal fungus Laccaria bicolor produces lipochitooligosaccharides and uses the common symbiosis pathway to colonize Populus roots. Plant Cell 31, 2386–2410 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Sanchez, L. et al. Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol. 139, 1065–1077 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Weerasinghe, R. R., Bird, D. & Allen, N. S. Root-knot nematodes and bacterial Nod factors elicit common signal transduction events in Lotus japonicus. Proc. Natl Acad. Sci. USA 102, 3147–3152 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Fernández-Aparicio, M. et al. Parasitic plant infection is partially controlled through the symbiotic pathways. Weed Res. 50, 76–82 (2009).

    Google Scholar 

  87. Skiada, V., Avramidou, M., Bonfante, P., Genre, A. & Papadopoulou., K. K. Symbiotic signalling is at the core of an endophytic Fusarium solani-legume association. Preprint at bioRxiv https://doi.org/10.1101/740043 (2019).

    Article  Google Scholar 

  88. Genre, A., Ortu, G., Bertoldo, C., Martino, E. & Bonfante, P. Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol. 149, 1424–1434 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Esseling, J. J., Lhuissier, F. G. & Emons, A. M. A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16, 933–944 (2004).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Kobae, Y. et al. Strigolactone biosynthesis genes of rice is required for the punctual entry of arbuscular mycorrhizal fungi into the roots. Plant Cell Physiol. 59, 544–553 (2018).

    CAS  PubMed  Google Scholar 

  91. Genre, A. & Bonfante, P. Check-in procedures for plant cell entry by biotrophic microbes. Mol. Plant Microbe Interact. 9, 1023–1030 (2007).

    Google Scholar 

  92. Mello, A. & Balestrini, R. Recent insights on biological and ecological aspects of ectomycorrhizal fungi and their interactions. Front. Microbiol. 9, 2016 (2018).

    Google Scholar 

  93. Zhang, F. et al. The ectomycorrhizal basidiomycete Laccaria bicolor releases a secreted β-1,4 endoglucanase that plays a key role in symbiosis development. New Phytol. 220, 1309–1321 (2018).

    CAS  PubMed  Google Scholar 

  94. Vayssières et al. Development of the poplar-Laccaria bicolor ectomycorrhiza modifies root auxin metabolism, signaling, and response. Plant Physiol. 169, 890–902 (2015).

    PubMed  PubMed Central  Google Scholar 

  95. Bonfante, P. et al. The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Mol. Plant Microbe Interact. 13, 1109–1120 (2000).

    CAS  PubMed  Google Scholar 

  96. Perotto, S. et al. Gene expression in mycorrhizal orchid protocorms suggests a friendly plant-fungus relationship. Planta 239, 1337–1349 (2014).

    CAS  PubMed  Google Scholar 

  97. Zhao, X. et al. Deep sequencing-based comparative transcriptional profiles of Cymbidium hybridum roots in response to mycorrhizal and non-mycorrhizal beneficial fungi. BMC Genomics 15, 747 (2014).

    PubMed  PubMed Central  Google Scholar 

  98. Fournier, J. et al. Remodeling of the infection chamber prior to infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol. 167, 1233–1242 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Svistoonoff, S., Hocher, V. & Gherbi, H. Actinorhizal root nodule symbioses: what is signalling telling on the origins of nodulation? Curr. Opin. Plant Biol. 20, 11–18 (2014).

    PubMed  Google Scholar 

  100. Porras-Alfaro, A. & Bayman, P. Hidden fungi, emergent properties: endophytes and microbiomes. Annu. Rev. Phytopathol. 49, 291–315 (2011).

    CAS  PubMed  Google Scholar 

  101. Rosenblueth, M. & Martínez-Romero, E. Bacterial endophytes and their interactions with hosts. Mol. Plant Microbe Interact. 19, 827–837 (2006).

    CAS  PubMed  Google Scholar 

  102. Mendgen, K. & Kahn, M. Plant infection and the establishment of fungal biotrophy. Trends Plant Sci. 7, 352–356 (2002).

    CAS  PubMed  Google Scholar 

  103. Mihwa, Y. & Valent, B. Communication between filamentous pathogens and plants at the biotrophic interface. Ann. Rev. Phytopathol. 51, 587–611 (2013).

    Google Scholar 

  104. Spanu, P. D. & Panstruga, R. Editorial: biotrophic plant-microbe interactions. Front. Plant Sci. 8, 192 (2017).

    PubMed  PubMed Central  Google Scholar 

  105. Tarkka, M. T. et al. OakContigDF159.1, a reference library for studying differential gene expression in Quercus robur during controlled biotic interactions: use for quantitative transcriptomic profiling of oak roots in ectomycorrhizal symbiosis. New Phytol. 199, 529–540 (2013).

    CAS  PubMed  Google Scholar 

  106. Duplessis, S., Courty, P. E., Tagu, D. & Martin, F. Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol. 165, 599–611 (2005).

    CAS  PubMed  Google Scholar 

  107. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006). This is a reference article for studies of plant immunity.

    CAS  PubMed  Google Scholar 

  108. Garcia-Garrido, J. M. & Ocampo, J. A. Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J. Exp. Bot. 53, 1377–1386 (2002).

    CAS  PubMed  Google Scholar 

  109. Liu, J. et al. Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15, 2106–2123 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Giovannetti, M., Mari, A., Novero, M. & Bonfante, P. Early Lotus japonicus root transcriptomic responses to symbiotic and pathogenic fungal exudates. Front. Plant Sci. 6, 480 (2015).

    PubMed  PubMed Central  Google Scholar 

  111. Martinez-Medina, A. et al. Nitric oxide and phytoglobin PHYTOGB1 are regulatory elements in the Solanum lycopersicum-Rhizophagus irregularis mycorrhizal symbiosis. New Phytol. 223, 1560–1574 (2019).

    CAS  PubMed  Google Scholar 

  112. Martinez-Medina, A. et al. Recognizing plant defense priming. Trends Plant Sci. 21, 818–822 (2016).

    CAS  PubMed  Google Scholar 

  113. Pozo, M. J. & Azcón-Aguilar, C. Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393–398 (2007).

    CAS  PubMed  Google Scholar 

  114. Jung, S., Martinez-Medina, A., Lopez-Raez, J. & Pozo, M. Mycorrhiza-induced resistance and priming of plant defenses. J. Chem. Ecol. 38, 651–664 (2012).

    CAS  PubMed  Google Scholar 

  115. Miozzi, L. et al. Arbuscular mycorrhizal symbiosis: plant friend or foe in the fight against viruses? Front. Microbiol. 10, 1238 (2019).

    PubMed  PubMed Central  Google Scholar 

  116. Jwa, N. S. & Hwang, B. K. Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Front. Plant Sci. 8, 1687 (2017).

    PubMed  PubMed Central  Google Scholar 

  117. Chialva, M. et al. Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytol. 220, 1296–1308 (2018).

    CAS  PubMed  Google Scholar 

  118. Miyata, K. et al. The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol. 55, 1864–1872 (2014).

    CAS  PubMed  Google Scholar 

  119. Zhang, X. et al. The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J. 81, 258–267 (2015).

    CAS  PubMed  Google Scholar 

  120. Shinya, T., Nakagawa, T., Kaku, H. & Shibuya, N. Chitin-mediated plant-fungal interactions: catching, hiding and handshaking. Curr. Opin. Plant Biol. 26, 64–71 (2015).

    CAS  PubMed  Google Scholar 

  121. Zeng, T. et al. LysM effector subverts chitin-triggered immunity to facilitate arbuscular mycorrhizal symbiosis. New Phytol. 225, 448–460 (2020).

    CAS  PubMed  Google Scholar 

  122. Sauter, M. & Hager, A. The mycorrhizal fungus Amanita muscaria induces chitinase activity in roots and in suspension-cultured cells of its host Picea abies. Planta 179, 61–66 (1989).

    CAS  PubMed  Google Scholar 

  123. Münzenberger, B., Otter, T., Wüstrich, D. & Polle, A. Peroxidase and laccase activities in mycorrhizal and non-mycorrhizal fine roots of Norway spruce (Picea abies) and larch (Larix decidua). Can. J. Bot. 75, 932–938 (1997).

    Google Scholar 

  124. Pozo, M. J., López-Ráez, J. A., Azcón-Aguilar, C. & García-Garrido, J. M. Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol. 205, 1431–1436 (2015).

    CAS  PubMed  Google Scholar 

  125. Plett, J. M. et al. The effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses JA-responsive genes. Proc. Natl Acad. Sci. USA 111, 8299 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Tisserant, E. et al. Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl Acad. Sci. USA 110, 20117–20122 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Lin, K. et al. Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet. 10, e1004078 (2014).

    PubMed  PubMed Central  Google Scholar 

  128. Zeng, T. et al. Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plant J. 94, 411–425 (2018).

    CAS  PubMed  Google Scholar 

  129. Kloppholz, S., Kuhn, H. & Requena, N. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204–1209 (2011).

    CAS  PubMed  Google Scholar 

  130. Voß, S., Betz, R., Heidt, S., Corradi, N. & Requena, N. RiCRN1, a crinkler effector from the arbuscular mycorrhizal fungus Rhizophagus irregularis, functions in arbuscule development. Front. Microbiol. 9, 2068 (2018).

    PubMed  PubMed Central  Google Scholar 

  131. Casarrubia, S. et al. The hydrophobin-like OMSSP1 may be an effector in the ericoid mycorrhizal symbiosis. Front. Plant Sci. 9, 546 (2018).

    PubMed  PubMed Central  Google Scholar 

  132. Teixeira, P. J., Colaianni, N. R., Fitzpatrick, C. R. & Dangl, J. L. Beyond pathogens: microbiota interactions with the plant immune system. Curr. Opin. Microbiol. 49, 7–17 (2019).

    CAS  PubMed  Google Scholar 

  133. Hynson, N. A. et al. in Mycoheterotrophy (ed. Merckx, V.) 297–342 (Springer, 2013).

  134. Balzergue, C., Chabaud, M., Barker, D. G., Bécard, G. & Rochange, S. F. High phosphate reduces host ability to develop arbuscular mycorrhizal symbiosis without affecting root calcium spiking responses to the fungus. Front. Plant Sci. 4, 426 (2013).

    PubMed  PubMed Central  Google Scholar 

  135. Ruytinx, J. et al. in Molecular Mycorrhizal Symbiosis (ed. Martin, F.) 277–298 (John Wiley & Sons, 2016).

  136. Muller, L. M. & Harrison, M. J. Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis. Curr. Opin. Plant Biol. 50, 132–139 (2019).

    CAS  PubMed  Google Scholar 

  137. Desirò, A. et al. Mollicutes-related endobacteria thrive inside liverwort-associated arbuscular mycorrhizal fungi. Environ. Microbiol. 15, 822–836 (2013).

    PubMed  Google Scholar 

  138. Genre, A., & Bonfante, P. in The Mycota: Fungal Associations, 2nd Edn, (ed. Hock, B.) 39–49 (Springer, 2012).

  139. Luginbuehl, L. H. & Oldroyd, G. E. Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Curr. Biol. 27, R952–R963 (2017).

    CAS  PubMed  Google Scholar 

  140. Bonfante, P. in Fungal Associations. The Mycota, Vol 9 (ed. Hock, B.) (Springer, 2000).

  141. Ivanov, S., Austin, J., Berg, R. H. & Harrison, M. J. Extensive membrane systems at the host–arbuscular mycorrhizal fungus interface. Nat. Plants 5, 194–203 (2019).

    PubMed  Google Scholar 

  142. Roth, R. et al. Arbuscular cell invasion coincides with extracellular vesicles and membrane tubules. Nat. Plants 5, 204–211 (2019).

    CAS  PubMed  Google Scholar 

  143. Bender, S. F., Wagg, C. & van der Heijden, M. G. An underground revolution: biodiversity and soil ecological engineering for agricultural sustainability. Trends Ecol. Evol. 31, 440–452 (2016).

    PubMed  Google Scholar 

  144. Mello, A., Zampieri, E. & Balestrini, R. in Plant Microbes Symbiosis: Applied Facets (ed. Arora, N. K.) 315–326 (Springer, 2015).

  145. Kipfer, T., Moser, B., Egli, S., Wohlgemuth, T. & Ghazoul, J. Ectomycorrhiza succession patterns in Pinus sylvestris forests after stand-replacing fire in the Central Alps. Oecologia 167, 219–228 (2011).

    PubMed  Google Scholar 

  146. Khosla, B. & Reddy, M. S. Response of ectomycorrhizal fungi on the growth and mineral nutrition of Eucalyptus seedlings in bauxite mined soil. Am. Eurasian J. Agric. Env. Sci. 3, 123–126 (2008).

    Google Scholar 

  147. Sousa, N. R., Franco, A. R., Oliveira, R. S. & Castro, P. M. L. Ectomycorrhizal fungi as an alternative to the use of chemical fertilisers in nursery production of Pinus pinaster. J. Environ. Manag. 95, S269–S274 (2012).

    CAS  Google Scholar 

  148. Oliveira, R. S., Franco, A. R. & Castro, P. M. L. Combined use of Pinus pinaster plus and inoculation with selected ectomycorrhizal fungi as an ecotechnology to improve plant performance. Ecol. Eng. 43, 95–103 (2012).

    Google Scholar 

  149. Zhang, H. H., Tang, M., Chen, H. & Zheng, C. L. Effects of inoculation with ectomycorrhizal fungi on microbial biomass and bacterial functional diversity in the rhizosphere of Pinus tabulaeformis seedlings. Eur. J. Soil. Biol. 46, 55–61 (2010).

    Google Scholar 

  150. Oliveira, R. S., Franco, A. R., Vosátka, M. & Castro, P. M. L. Management of nursery practices for efficient ectomycorrhizal fungi application in the production of Quercus ilex. Symbiosis 52, 125–131 (2010).

    Google Scholar 

  151. Bauman, J. M., Keiffer, C. H., Hiremath, S. & McCarthy, B. C. Soil preparation methods promoting ectomycorrhizal colonization and American chestnut Castanea dentata establishment in coal mine restoration. J. Appl. Ecol. 50, 721–729 (2013).

    Google Scholar 

  152. Danell, E. & Camacho, F. J. Successful cultivation of the golden chanterelle. Nature 385, 303 (1997).

    CAS  Google Scholar 

  153. Mello, A. in Edible Ectomycorrhizal Mushrooms. Soil Biology Vol. 34 (eds Zambonelli, A. & Bonito, G. M.) 73–81 (Springer, 2012).

  154. Murat, C. Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25, 77–81 (2015).

    PubMed  Google Scholar 

  155. Zambonelli, A., Iotti, M. & Murat, C. True Truffle (Tuber spp.) in the World (Springer, 2016).

  156. Ceballos, I. et al. The in vitro mass-produced model mycorrhizal fungus, Rhizophagus irregularis, significantly increases yields of the globally important food security crop cassava. PLoS One 8, e70633 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  157. Rodriguez, A. & Sanders, I. R. The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME J. 9, 1053–1061 (2015).

    PubMed  Google Scholar 

  158. Hijri, M. Analysis of a large dataset of mycorrhiza inoculation field trials on potato shows highly significant increases in yield. Mycorrhiza 26, (2016).

  159. Rocha, I. et al. Seed coating with arbuscular mycorrhizal fungi for improved field production of chickpea. Agronomy 9, 471–482 (2019).

    CAS  Google Scholar 

  160. Berruti, A., Lumini, E., Balestrini, R. & Bianciotto, V. Arbuscular mycorrhizal fungi as natural biofertilizers: let’s benefit from past successes. Front. Microbiol. 6, 1559 (2016).

    PubMed  PubMed Central  Google Scholar 

  161. Chen, M., Arato, M., Borghi, L., Nouri, E. & Reinhardt, D. Beneficial services of arbuscular mycorrhizal fungi - from ecology to application. Front. Plant Sci. 9, 1270 (2018).

    PubMed  PubMed Central  Google Scholar 

  162. Lehmann, A., Veresoglou, S. D., Leifheit, E. F. & Rillig, M. C. Arbuscular mycorrhizal influence on zinc nutrition in crop plants – a meta-analysis. Soil. Biol. Biochem. 69, 123–131 (2014).

    CAS  Google Scholar 

  163. Bona, E. et al. Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads improve yield, quality and nutritional value of tomato: a field study. Mycorrhiza 27, 1–11 (2017).

    CAS  PubMed  Google Scholar 

  164. Torres, N., Antolin, M. C. & Goicoechea, N. Arbuscular mycorrhizal symbiosis as a promising resource for improving berry quality in grapevines under changing environments. Front. Plant Sci. 9, 18 (2018).

    Google Scholar 

  165. Ryan, M. H. & Graham, J. H. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol. 220, 1092–1107 (2018).

    PubMed  Google Scholar 

  166. Rillig, M. C. et al. Towards an integrated mycorrhizal technology: harnessing mycorrhizae for sustainable intensification in agriculture. Front. Plant Sci. 7, 1625 (2016).

    PubMed  PubMed Central  Google Scholar 

  167. Cavagnaro, T. R., Bender, S. F., Asghari, H. R. & van der Heijden, M. G. A. The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci. 20, 283–290 (2015).

    CAS  PubMed  Google Scholar 

  168. Rillig, M. C. et al. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol. 222, 1171–1175 (2019).

    PubMed  Google Scholar 

  169. DeClerck, F. A. J. et al. Agricultural ecosystems and their services: the vanguard of sustainability? Curr. Opin. Environ. Sust. 23, 92–99 (2016).

    Google Scholar 

  170. Janos, D. P. Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17, 75–91 (2007).

    PubMed  Google Scholar 

  171. Kameoka, H. et al. Stimulation of asymbiotic sporulation in arbuscular mycorrhizal fungi by fatty acids. Nat. Microbiol. 4, 1654–1660 (2019). This seminal study breaks the dogma of unculturability of AM fungi by demonstrating that the addition of fatty acids to the medium permits their asexual reproduction in axenic culture.

    CAS  PubMed  Google Scholar 

  172. Sugiura, Y. et al. Myristate as a carbon and energy source for the asymbiotic growth of the arbuscular mycorrhizal fungus Rhizophagus irregularis. Preprint at bioRxiv https://doi.org/10.1101/731489 (2019).

    Article  Google Scholar 

  173. Sosa-Hernández, M. A., Leifheit, E. F., Ingraffia, R. & Rillig, M. C. Subsoil arbuscular mycorrhizal fungi for sustainability and climate-smart agriculture: a solution right under our feet? Front. Microbiol. 10, 744 (2019).

    PubMed  PubMed Central  Google Scholar 

  174. Volpe, V. et al. Short chain chito-oligosaccharides promote arbuscular mycorrhizal colonization in Medicago truncatula. Carbohydr. Polym. 229, 115505 (2020). This study shows that the perception of short-chain chito-oligosaccharides stimulates AM colonization and arbuscule development, providing crucial evidence in favour of the role of these soluble molecules as positive elicitors of symbiotic responses in the host plant.

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors apologize to colleagues whose work could not be cited due to space limitations. The authors are grateful to A. Desirò for agreeing to share Fig. 2 and to D. Chamberlain and J. Mach for language editing. Contributions to this Review were partially funded by Fondazione Cassa di Risparmio di Cuneo (Bando Ricerca Scientifica 2015 — project AM-FOR-Quality) and by the European Union’s Horizon 2020 research and innovation programme under grant agreement no. 727929 (TOMRES).

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Glossary

Angiosperms

Vascular plants with seeds and flowers; they are the largest and most diverse group within the kingdom Plantae.

Saprotrophic

A mode of microbial nutrition based on the extracellular digestion of dead or decaying organic matter.

Biotrophism

The nutritional strategy of a pathogen or a mutualist that needs its host to stay alive.

Rhynie chert

An Early Devonian sedimentary deposit located in Scotland and exhibiting exceptionally well preserved fossils of plants, fungi, lichens and animals from an early terrestrial ecosystem.

Gymnosperms

A group of vascular, non-flowering seed-producing plants that includes among conifers, cycads and Ginkgo biloba.

Gnepine hypothesis

According to this hypothesis on the evolution of gymnosperms, gnetophytes are a sister group of the Pinaceae.

Bryophytes

An informal group of early diverging, non-vascular plants, consisting of three divisions: liverworts, hornworts and mosses. All of them are characterized by a dominant gametophytic phase.

Auxotrophs

Organisms that are unable to synthetize a particular organic compound that is required for their own growth.

Cyanobacteria

A group of photosynthetic, nitrogen-fixing bacteria forming filamentous colonies arranged in a gelatinous sheath.

Protocorms

Intermediate tuber-like structures derived from the embryo after germination of orchid seeds and before seedling development.

Meristems

Plant tissues consisting of proliferating stem cells (meristematic cells) that generate tissues and organs.

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Genre, A., Lanfranco, L., Perotto, S. et al. Unique and common traits in mycorrhizal symbioses. Nat Rev Microbiol 18, 649–660 (2020). https://doi.org/10.1038/s41579-020-0402-3

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