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Genetics and Genomics Decipher Partner Biology in Arbuscular Mycorrhizas

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Genetics and Biotechnology

Part of the book series: The Mycota ((MYCOTA,volume 2))

Abstract

Arbuscular mycorrhizas (AMs) are the most widespread symbioses between plants and soil fungi. They play such a critical role in the nutrition of both partners that AM fungi cannot complete their life cycle in the absence of a host plant, and the existence of non-mycorrhizal individuals of AM host species is virtually unknown in natural ecosystems.

Even if the genetics of AM fungi have long been difficult to approach, decades of studies on model host plants and recent achievements in fungal genomics and transcriptomics have shed light on the molecular bases of this fascinating and ecologically crucial interaction.

In this chapter we review the most influential literature on this topic, outlining the genetic and physiological bases of obligate biotrophism in AM fungi, their unique adaptation to symbiotic lifestyle, the emerging role of secreted effectors, and signaling molecules. Such insights complement our more advanced knowledge of the host plant response to AM fungi, from signal transduction to cell reorganization, metabolic and physiological reprogramming, and systemic responses. Lastly, we comment on our current understanding of natural variation in AM interactions, exploring the reciprocal advantages and disadvantages that emerge when coupling different fungal isolates and wild or domesticated plant varieties.

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References

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043):824–827

    CAS  PubMed  Google Scholar 

  • Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51(7):1104–1117

    CAS  PubMed  PubMed Central  Google Scholar 

  • Alvey L, Harberd NP (2005) DELLA proteins: integrators of multiple plant growth regulatory inputs? Physiol Plant 123:153–160

    CAS  Google Scholar 

  • Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    PubMed  Google Scholar 

  • Antunes PM, Koch AM, Morton JB, Rillig MC, Klironomos JN (2011) Evidence for functional divergence in arbuscular mycorrhizal fungi from contrasting climatic origins. New Phytol 189:507–514

    PubMed  Google Scholar 

  • Ariel F, Romero-Barrios N, Jégu T, Benhamed M, Crespi M (2015) Battles and hijacks: noncoding transcription in plants. Trends Plant Sci 20:362–371

    CAS  PubMed  Google Scholar 

  • Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124:949–957

    CAS  PubMed  PubMed Central  Google Scholar 

  • Balestrini R, Bonfante P (2005) The interface compartment in arbuscular mycorrhizae: a special type of plant cell wall? Plant Biosystems 139:8–15

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Banba M, Gutjahr C, Miyao A, Hirochika H, Paszkowski U, Kouchi H, Imaizumi-Anraku H (2008) Divergence of evolutionary ways among common sym genes: CASTOR and CCaMK show functional conservation between two symbiosis systems and constitute the root of a common signalling pathway. Plant Cell Physiol 49(11):1659–1671

    CAS  PubMed  Google Scholar 

  • Bazin J, Baerenfaller K, Gosai SJ, Gregory BD, Crespi M, Bailey-Serres J (2017) Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation. Proc Natl Acad Sci U S A 114(46):E10018–E10027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4(7):1239–1247

    CAS  Google Scholar 

  • Besserer A, Bécard G, Jauneau A, Roux C, Séjalon-Delmas N (2008) 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(1):402–413

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bidartondo MI, Read DJ, Trappe JM, Merckx V, Ligrone R, Duckett JG (2011) The dawn of symbiosis between plants and fungi. Biol Lett 7:574–577

    PubMed  PubMed Central  Google Scholar 

  • Bonfante P (2001) At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In: Hock B (ed) The mycota, IX: fungal associations. Springer, Berlin, pp 45–61

    Google Scholar 

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

    PubMed  Google Scholar 

  • Bonfante P, Desirò A (2017) Who lives in a fungus? The diversity, origins and functions of fungal endobacteria living in Mucoromycota. ISME J 11:1727–1735

    PubMed  PubMed Central  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Comm 1:48

    Google Scholar 

  • Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak ‘plantish’ or ‘fungish’? Trends Plant Sci 20:150–154

    CAS  PubMed  Google Scholar 

  • Bonfante P, Requena N (2011) Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 14:451–457

    CAS  PubMed  Google Scholar 

  • Bravo A, York T, Pumplin N, Mueller LA, Harrison MJ (2016) Genes conserved for arbuscular mycorrhizal symbiosis identified through phylogenomics. Nat Plants 2:15208

    CAS  PubMed  Google Scholar 

  • Bravo A, Brands M, Wewer V, Dormann P, Harrison MJ (2017) Arbuscular mycorrhiza-specific enzymes FatM and RAM2 finetune lipid biosynthesis to promote development of arbuscular mycorrhiza. New Phytol 214:1631–1645

    CAS  PubMed  Google Scholar 

  • Breuillin-Sessoms F, Floss DS, Gomez SK, Pumplin N, Ding Y, Levesque-Tremblay V, Noar RD, Daniels DA, Bravo A, Eaglesham JB, Benedito VA, Udvardi MK, Harrison MJ (2015) Suppression of arbuscule degeneration in Medicago truncatula phosphate transporter4 mutants is dependent on the ammonium transporter 2 family protein AMT2;3. Plant Cell 27:1352–1366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976

    Article  PubMed  Google Scholar 

  • Bucher M, Hause B, Krajinski F, Kuster H (2014) Through the doors of perception to function in arbuscular mycorrhizal symbioses. New Phytol 204:833–840

    CAS  PubMed  Google Scholar 

  • Cai Q, Qiao LL, Wang M, He B-Y, Lin FM, Palmquist J, Jin H-L (2018) Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–1129

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Capoen W, Sun J, Wysham D, Otegui MS, Venkateshwaran M, Hirsch S, Miwa H, Downie JA, Morris RJ, Ané JM, Oldroyd GE (2011) Nuclear membranes control symbiotic calcium signaling of legumes. Proc Natl Acad Sci U S A 108:14348–14353

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carbonnel S, Gutjahr C (2014) Control of arbuscular mycorrhiza development by nutrient signals. Front Plant Sci 5:462

    PubMed  PubMed Central  Google Scholar 

  • Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12:1647–1665

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cervantes-Gámez RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza IE, Villalobos-López MA, Valdez-Ortíz A, López-Meyer M (2016) Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-seq analysis. Plant Mol Biol Rep 34:89–102

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chang Y, Desirò A, Na H, Sandor L, Lipzen A, Clum A, Barry K, Grigoriev IV, Martin FM, Stajich JE, Smith ME, Bonito G, Spatafora JW (2018) Phylogenomics of Endogonaceae and evolution of mycorrhizae within Mucoromycota. New Phytol 222(1):511–525. https://doi.org/10.1111/nph.15613

    Article  Google Scholar 

  • Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467–3479

    CAS  PubMed  PubMed Central  Google Scholar 

  • Charpentier M, Sun J, Vaz Martins T, Radhakrishnan GV, Findlay K, Soumpourou E, Thouin J, Véry AA, Sanders D, Morris RJ, Oldroyd GED (2016) Nuclear-localized cyclic nucleotide-gated channels mediate symbiotic calcium oscillations. Science 352:1102–1105

    CAS  PubMed  Google Scholar 

  • Chekanova JA (2015) Long non-coding RNAs and their functions in plants. Curr Opin Plant Biol 27:207–216

    CAS  PubMed  Google Scholar 

  • Chen C, Zou J, Zhang S, Zaitlin D, Zhu L (2009) Strigolactones are a new-defined class of plant hormones which inhibit shoot branching and mediate the interaction of plant-AM fungi and plant-parasitic weeds. Sci Chin C Life Sci/Chin Acad Sci 52(8):693–700

    CAS  Google Scholar 

  • Chen EC, Mathieu S, Hoffrichter A, Sedzielewska-Toro K, Peart M, Pelin A, Ndikumana S, Ropars J, Dreissig S, Fuchs J, Brachmann A, Corradi N (2018) Single nucleus sequencing reveals evidence of inter-nucleus recombination in arbuscular mycorrhizal fungi. elife 7:pii:e39813. https://doi.org/10.7554/eLife.39813

    Article  Google Scholar 

  • Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S, Charron P, St-Onge C, Giorgi J, Krüger M, Marton T, Ropars J, Grigoriev IV, Hainaut M, Henrissat B, Roux C, Martin F, Corradi N (2018b) High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 220:1161–1171

    CAS  PubMed  Google Scholar 

  • Chialva M, Salvioli A, Daghino S, Ghignone S, Bagnaresi P, Chiapello M, Novero M, Spadaro D, Perotto S, Bonfante P (2018) Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytol 220:1296–1308

    CAS  PubMed  Google Scholar 

  • Chu Q, Wang XX, Yang Y, Chen FJ, Zhang FS, Feng G (2013) Mycorrhizal responsiveness of maize (Zea mays L.) genotypes as related to releasing date and available P content in soil. Mycorrhiza 23:497–505

    CAS  PubMed  Google Scholar 

  • Corradi C, Brachmann A (2017) Fungal mating in the most widespread plant symbionts? Trends Plant Sci 22:175–183

    CAS  PubMed  Google Scholar 

  • Czaja LF, Hogekamp C, Lamm P, Maillet F, Andres Martinez E, Samain E, Dénarié J, Kuster H, Hohnjec N (2012) 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daviere JM, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151

    CAS  PubMed  Google Scholar 

  • Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Pärtel M, Reier U, Saks U, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973

    CAS  PubMed  Google Scholar 

  • Davison J, Moora M, Öpik M, Ainsaar L, Ducousso M, Hiiesalu I, Jairus T, Johnson N, Jourand P, Kalamees R, Koorem K, Meyer JY, Püssa K, Reier U, Pärtel M, Semchenko M, Traveset A, Vasar M, Zobel M (2018) Microbial island biogeography: isolation shapes the life history characteristics but not diversity of root symbiotic fungal communities. ISME J12:2211–2224

    Google Scholar 

  • Delaux PM, Séjalon-Delmas N, Bécard G, Ané M (2013) Evolution of the plant-microbe symbiotic “toolkit.”. Trends Plant Sci 18(6):298–304

    CAS  PubMed  Google Scholar 

  • Delaux PM, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M, Volkening JD, Sekimoto H, Nishiyama T, Melkonian M, Pokorny L, Rothfels CJ, Sederoff HW, Stevenson DW, Surek B, Zhang Y, Sussman MR, Dunand C, Morris RJ, Roux C, Wong GK-S, Oldroyd GED, Ané J-M (2015) Algal ancestor of land plants was preadapted for symbiosis. Proc Natl Acad Sci U S A 112:13390–13395

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dénarié J, Cullimore J (1993) Lipo-oligosaccharide nodulation factors: a minireview new class of signaling molecules mediating recognition and morphogenesis. Cell 74:951–954

    PubMed  Google Scholar 

  • Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

    PubMed  Google Scholar 

  • Desirò A, Duckett JG, Pressel S, Villarreal JC, Bidartondo MI (2013) Fungal symbioses in hornworts: a chequered history. Proc Biol Sci 280(1759):20130207

    PubMed  PubMed Central  Google Scholar 

  • De Vita P, Avio L, Sbrana C, Laidò G, Marone D, Mastrangelo AM, Cattivelli L, Giovannetti M (2018) Genetic markers associated to arbuscular mycorrhizal colonization in durum wheat. Sci Rep 8:10612

    Google Scholar 

  • Devers EA, Branscheid A, May P, Krajinski F (2011) Stars and symbiosis: microRNA- and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol 156:1990–2010

    CAS  PubMed  PubMed Central  Google Scholar 

  • Devers E, Teply J, Reinert A, Gaude N, Krajinski F (2013) An endogenous artificial microRNA system for unraveling the function of root endosymbioses related genes in Medicago truncatula. BMC Plant Biol 13:82

    CAS  PubMed  PubMed Central  Google Scholar 

  • Diédhiou I, Diouf D (2018) Transcription factors network in root endosymbiosis establishment and development. World J Microbiol Biotechnol 34(3):37

    PubMed  Google Scholar 

  • Dörmann P, Kim H, Ott T, Schulze-Lefert P, Trujillo M, Wewer V, Hückelhoven R (2014) Cell-autonomous defense, reorganization and trafficking of membranes in plant-microbe interactions. New Phytol 204(4):815–822

    PubMed  Google Scholar 

  • Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost and metabolism of arbuscular mycorrhizae in arbuscular mycorrhizas: physiology and function. In: Kapulnick Y, Douds DD Jr (eds) Arbuscular mycorrhizas: molecular biology and physiology. Kluwer Academic, Dordrecht

    Google Scholar 

  • Fassi B, Fontana A, Trappe JM (1969) Ectomycorrhizae formed by Endogone lactiflua with species of Pinus and Pseudotsuga. Mycologia 61:412–414

    Google Scholar 

  • Favre P, Bapaume L, Bossolini E, Delorenzi M, Falquet L, Reinhardt D (2014) A novel bioinformatics pipeline to discover genes related to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants. BMC Plant Biol 14:333

    PubMed  PubMed Central  Google Scholar 

  • Feddermann N, Boller T, Salzer P, Elfstrand S, Wiemken A, Elfstrand M (2008) Medicago truncatula shows distinct patterns of mycorrhiza-related gene expression after inoculation with three different arbuscular mycorrhizal fungi. Planta 227:671–680

    CAS  PubMed  Google Scholar 

  • Feddermann N, Muni RRD, Zeier T, Stuurman J, Ercolin F, Schorderet M, Reinhardt D (2010) The PAM1 gene of petunia, required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN. Plant J 64:470–481

    CAS  PubMed  Google Scholar 

  • Ferlian O, Eisenhauer N, Aguirrebengoa M, Camara M, Ramirez-Rojas I, Santos F, Thakur MP (2018) Invasive earthworms erode soil biodiversity: a meta-analysis. J Anim Ecol 87:162–172

    PubMed  Google 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 Phytol 184:975–987

    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 pathogen in wheat. Sci Rep 8:9625

    PubMed  PubMed Central  Google Scholar 

  • Flematti GR, Ghisalberti EL, Dixon KW, Trengove RD (2004) A compound from smoke that promotes seed germination. Science 305:977

    CAS  PubMed  Google Scholar 

  • Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 110:E5025–E5034

    CAS  PubMed  PubMed Central  Google Scholar 

  • Floss DS, Lévesque-Tremblay V, Park H-J, Harrison MJ (2016) DELLA proteins regulate expression of a subset of AM symbiosis- induced genes in Medicago truncatula. Plant Signal Behav 11:e1162369

    PubMed  PubMed Central  Google Scholar 

  • Floss DS, Gomez SK, Park HJ, McLean AM, Muller LM, Bhattarai KK, Lévesque-Tremblay V, Maldonado-Mendoza IE, Harrison MJ (2017) A transcriptional program for arbuscule degeneration during AM symbiosis is regulated by MYB1. Curr Biol 27:1206–1212

    CAS  PubMed  Google Scholar 

  • Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 234(5):1073–1081

    CAS  PubMed  Google Scholar 

  • Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gallego-Bartolome J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadi D, Blazquez MA (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci U S A 109:13446–13451

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    CAS  PubMed  Google Scholar 

  • Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2012) Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J 69:510–528

    CAS  PubMed  Google Scholar 

  • Gehrig H, Schüßler A, Kluge M (1996) Geosiphon pyriformis, a fungus forming endocytobiosis with Nostoc (cyanobacteria), is an ancestral member of the Glomerales: evidence by SSU rRNA analysis. J Mol Evol 43:71–81

    CAS  PubMed  Google Scholar 

  • Genre A, Russo G (2016) Does a common pathway transduce symbiotic signals in plant–microbe interactions? Front Plant Sci 7:96

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420

    CAS  PubMed  PubMed Central  Google Scholar 

  • Genre A, Ivanov S, Fendrych M, Faccio A, Zársky V, Bisseling T, Bonfante P (2012) Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol 53(1):244–255

    CAS  PubMed  Google Scholar 

  • Genre A, Chabaud M, Balzergue C, Puech-Pagès V, Novero M, Rey T, Fournier J, Rochange S, Bécard G, Bonfante P, Barker DG (2013) 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 198:190–202

    PubMed  Google Scholar 

  • Ghignone S, Salvioli A, Anca I, Lumini E, Ortu G, Petiti L, Cruveiller S, Bianciotto V, Piffanelli P, Lanfranco L, Bonfante P (2012) The genome of the obligate endobacterium of an AM fungus reveals an interphylum network of nutritional interactions. ISME J 6:136–145

    CAS  PubMed  Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8(10):1871–1883

    PubMed  PubMed Central  Google Scholar 

  • Gianinazzi-Pearson V, Morandi D, Dexheimer J, Gianinazzi S (1981) Ultrastructural and ultracytochemical features of a Glomus tenuis mycorrhiza. New Phytol 88:633–639

    Google Scholar 

  • Giovannetti M, Ayio L, Sbrana C, Citernesi AS (1993) Factors affecting appressorium development in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae (Nicol. and Gerd.) Gerd. And Trappe. New Phytol 123:115–122

    Google Scholar 

  • Gobbato E (2015) Recent developments in arbuscular mycorrhizal signaling. Curr Opin Plant Biol 26:1–7

    PubMed  Google Scholar 

  • Gobbato E, Marsh JF, Vernié T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P, Mysore KS, Dénarié J, Schultze M, Oldroyd GED (2012) A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr Biol 22:2236–2241

    CAS  PubMed  Google Scholar 

  • Gobbato E, Wang E, Higgins G, Bano SA, Henry C, Schultze M, Oldroyd GED (2013) RAM1 and RAM2 function and expression during arbuscular mycorrhizal symbiosis and Aphanomyces euteiches colonization. Plant Signal Behav 8(10):pii:e26049. https://doi.org/10.4161/psb.26049

    Article  CAS  Google Scholar 

  • Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455(7210):189–194

    CAS  PubMed  Google Scholar 

  • Groth M, Takeda N, Perry J, Uchida H, Dräxl S, Brachmann A, Sato S, Tabata S, Kawaguchi M, Wang TL, Parniske M (2010) NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22(7):2509–2526

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gutjahr C, Novero M, Guether M, Montanari O, Udvardi M, Bonfante P (2009) Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots. New Phytol 183(1):53–61

    CAS  PubMed  Google Scholar 

  • Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, Casieri L, An K, An G, Guiderdoni E, Kumar CS, Sundaresan V, Harrison MJ, Paszkowski U (2012) The half- size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J 69:906–920

    CAS  PubMed  Google Scholar 

  • Gutjahr C, Gobbato E, Choi J, Riemann M, Johnston MG, Summers W, Carbonnel S, Mansfield C, Yang SY, Nadal M, Acosta I, Takano M, Jiao WB, Schneeberger K, Kelly KA, Paszkowski U (2015) Rice perception of symbiotic arbuscular mycorrhizal fungi requires the karrikin receptor complex. Science 350:1521–1524

    CAS  PubMed  Google Scholar 

  • Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an a/b hydrolase likely to be involved in the perception of the plant branching hormone strigolactone. Curr Biol 22:2032–2036

    CAS  PubMed  Google Scholar 

  • Handa Y, Nishide H, Takeda N, Suzuki Y, Kawaguchi M, Saito K (2015) RNA-seq transcriptional profiling of an arbuscular mycorrhiza provides insights into regulated and coordinated gene expression in Lotus japonicus and Rhizophagus irregularis. Plant Cell Physiol 56:1490–1511

    CAS  PubMed  Google Scholar 

  • Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J 9:491–503

    CAS  PubMed  Google Scholar 

  • Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 15(6):691–698

    CAS  PubMed  Google Scholar 

  • Hart MM, Reader RJ (2002) Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium. Biol Fertil Soils 36:357–366

    Google Scholar 

  • Havaux M (2014) Carotenoid oxidation products as stress signals in plants. Plant J 79:597–606

    CAS  PubMed  Google Scholar 

  • Heard S, Brown NA, Hammond-Kosack K (2015) An interspecies comparative analysis of the predicted secretomes of the necrotrophic plant pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS One 10:e0130534. https://doi.org/10.1371/journal.pone.0130534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heck C, Kuhn H, Heidt S, Walter S, Rieger N, Requena N (2016) Symbiotic fungi control plant root cortex development through the novel GRAS transcription factor MIG1. Curr Biol 26:2770–2778

    CAS  PubMed  Google Scholar 

  • Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hirsch S, Kim J, Munoz A, Heckmann AB, Downie JA, Oldroyd GED (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21:545–557

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hogekamp C, Kuster H (2013) A roadmap of cell-type specific gene expression during sequential stages of the arbuscular mycorrhiza symbiosis. BMC Genomics 14:306

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hogekamp C, Arndt D, Pereira PA, Becker JD, Hohnjec N, Küster H (2011) Laser microdissection unravels cell-type- specific transcription in arbuscular mycorrhizal roots, including CAAT-box transcription factor gene expression correlating with fungal contact and spread. Plant Physiol 157(4):2023–2043

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hohnjec N, Vieweg M, Puhler A, Becker A, Kuster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights in the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hong JJ, Park YS, Bravo A, Bhattarai KK, Daniels DA, Harrison MJ (2012) Diversity of morphology and function in arbuscular mycorrhizal symbioses in Brachypodium distachyon. Planta 236:851–865

    CAS  PubMed  Google Scholar 

  • Huisman R, Hontelez J, Mysore KS, Wen JQ, Bisseling T, Limpens E (2016) A symbiosis- dedicated SYNTAXIN OF PLANTS 13II isoform controls the formation of a stable host-microbe interface in symbiosis. New Phytol 211:1338–1351

    CAS  PubMed  Google Scholar 

  • Ikeda Y, Shimura H, Kitahara R, Masuta C, Ezawa (2012) A novel virus-like double-stranded RNA in an obligate biotroph arbuscular mycorrhizal fungus: a hidden player in mycorrhizal symbiosis. Mol Plant-Microbe Interact 25:1005–1012

    CAS  PubMed  Google Scholar 

  • Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531

    CAS  PubMed  Google Scholar 

  • Ivanov S, Harrison MJ (2014) A set of fluorescent protein-based markers expressed from constitutive and arbuscular mycorrhiza-inducible promoters to label organelles, membranes and cytoskeletal elements in Medicago truncatula. Plant J 80:1151–1163

    CAS  PubMed  Google Scholar 

  • Ivanov S, Fedorova EE, Limpens E, De Mita S, Genre A, Bonfante P, Bisseling T (2012) Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc Natl Acad Sci U S A 109(21):8316–8321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jashni MK, Mehrabi R, Collemare J, Mesarich CH, de Wit PJ (2015) The battle in the apoplast: further insights into the roles of proteases and their inhibitors in plant-pathogen interactions. Front Plant Sci 6:584

    PubMed  PubMed Central  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci U S A 104(5):1720–1725

    CAS  PubMed  PubMed Central  Google Scholar 

  • Javot H, Penmetsa RV, Breuillin F, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965

    CAS  PubMed  Google Scholar 

  • Jiang Y, Wang W, Xie O, Liu N, Liu L, Wang D, Zhang X, Yang C, Chen X, Tang D, Wang E (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172–1175

    CAS  PubMed  Google Scholar 

  • Jin Y, Liu H, Luo DX, Yu N, Dong WT, Wang C, Zhang XW, Dai HL, Yang J, Wang ET (2016) DELLA proteins are common components of symbiotic rhizobial and mycorrhizal signalling pathways. Nat Commun 7:12433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson LJ, Koulman A, Christensen M, Lane GA, Fraser K, Forester N, Johnson RD, Bryan GT, Rasmussen S (2013) An extracellular siderophore is required to maintain the mutualistic interaction of Epichloë festucae with Lolium perenne. PLoS Pathog 9(5):e1003332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant-Microbe Interact 14(6):737–748

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signalling through a plasma membrane receptor. Proc Natl Acad Sci U S A 103(29):11086–11091

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GED (2005) Nodulation signalling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308(5729):1786–1789

    PubMed  Google Scholar 

  • Kamel L, Tang NW, Malbreil M, San Clemente H, Le Marquer M, Roux C, Frei Dit Frey N (2017) 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

    PubMed  PubMed Central  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci U S A 103:359–336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kapulnik Y, Kushnir U (1991) Growth dependency of wild, primitive and modern cultivated wheat lines on vesicular-arbuscular mycorrhiza fungi. Euphytica 56:27–36

    Google Scholar 

  • Kevei Z, Lougnon G, Mergaert P, Horváth GV, Kereszt A, Jayaraman D, Zaman N, Marcel F, Regulski K, Kiss GB, Kondorosi A, Endre G, Kondorosi E, Ané JM (2007) 3-hydroxy-3-methylglutaryl coenzyme a reductase 1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19(12):3974–3989

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keymer A, Pimprikar P, Wewer V, Huber C, Brands M, Bucerius SL, Delaux PM, Klingl V, von Röpenack-Lahaye E, Wang TL, Eisenreich W, Dörmann P, Parniske M, Gutjahr C (2017) Lipid transfer from plants to arbuscular mycorrhiza fungi. elife 6:e29107

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kobae Y, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353

    CAS  PubMed  Google Scholar 

  • Kobae Y, Tamura Y, Takai S, Banba M, Hata S (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol 51:1411–1415

    CAS  PubMed  Google Scholar 

  • Kobayashi Y, Maeda T, Yamaguchi K, Kameoka H, Tanaka S, Ezawa T, Shigenobu S, Kawaguchi M (2018) The genome of Rhizophagus clarus HR1 reveals a common genetic basis for auxotrophy among arbuscular mycorrhizal fungi. BMC Genomics 19:465

    PubMed  PubMed Central  Google Scholar 

  • Koch AM, Antunes PM, Maherali H, Hart MM, Klironomos JN (2017) Evolutionary asymmetry in the arbuscular mycorrhizal symbiosis; conservatism in the fungal morphology does not predict host plant growth. New Phytol 214:1330–1337

    CAS  PubMed  Google Scholar 

  • Koegel S, Ait Lahmidi N, Arnould C, Chatagnier O, Walder F, Ineichen K, Boller T, Wipf D, Wiemken A, Courty PE (2013) The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol 198:853–865

    CAS  PubMed  Google Scholar 

  • Koltai H, Kapulnik Y (2010) Arbuscular mycorrhizas: physiology and function. Springer, Heidelberg, pp 209–236

    Google Scholar 

  • Konvalinkova T, Jansa J (2016) Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci 7:782

    PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci U S A 105:9823–9828

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krajinski F, Courty PE, Sieh D, Franken P, Zhang H, Bucher M, Gerlach N, Kryvoruchko I, Zoeller D, Udvardi M, Hause B (2014) The H+-ATPase HA1 of Medicago truncatula is essential for phosphate transport and plant growth during arbuscular mycorrhizal symbiosis. Plant Cell 26:1808–1817

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn H, Küster H, Requena N (2010) Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol 185:716–733

    CAS  PubMed  Google Scholar 

  • Lahrmann U, Ding Y, Banhara A, Rath M, Hajirezaei MR, Döhlemann S, von Wirén N, Parniske M, Zuccaro A (2013) Host-related metabolic cues affect colonization strategies of a root endophyte. Proc Natl Acad Sci U S A 110:13965–13970

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lanfranco L, Fiorilli V, Gutjahr C (2018) Partner communication and role of nutrients in the arbuscular mycorrhizal symbiosis. New Phytol 220:1031–1046

    PubMed  Google Scholar 

  • Laparre J, Malbreil M, Letisse F, Portais JC, Roux C, Becard G, Puech-Pagès V (2014) Combining metabolomics and gene expression analysis reveals that propionyland butyryl-carnitines are involved in late stages of arbuscular mycorrhizal symbiosis. Mol Plant 7:554–566

    CAS  PubMed  Google Scholar 

  • Lee SJ, Kong M, Harrison P, Hijri M (2018) Conserved proteins of the RNA interference system in the arbuscular mycorrhizal fungus Rhizoglomus irregulare provide new insight into the evolutionary history of glomeromycota. Genome Biol Evol 10:328–343

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lehmann A, Barto EK, Powell JR, Rillig MC (2012) Mycorrhizal responsiveness trends in annual crop plants and their wild relatives - a meta-analysis on studies from 1981 to 2010. Plant Soil 355:231–250

    CAS  Google Scholar 

  • Lehnert H, Serfling A, Enders M, Friedt W, Ordon F (2017) Genetics of mycorrhizal symbiosis in winter wheat (Triticum aestivum). New Phytol 215:779–791

    CAS  PubMed  Google Scholar 

  • Lekberg Y, Koide RT (2005) Is plant performance limited by abundance of arbuscular mycorrhizal fungi? A meta analysis of studies published between 1988 and 2003. New Phytol 168:189–204

    CAS  PubMed  Google Scholar 

  • Lelandais-Briére C, Moreau J, Hartmann C, Crespi M (2016) Non-coding RNAs, emerging regulators in root endosymbioses. Mol Plant-Microbe Interact 29:170–180

    PubMed  Google Scholar 

  • Lin K, Limpens E, Zhang Z, Ivanov S, Saunders DGO, Mu D, Pang E, Cao H, Cha H, Lin T, Zhou Q, Shang Y, Li Y, Sharma T, van Velzen R, de Ruijter N, Aanen DK, Win J, Kamoun S, Bisseling T, Geurts R, Huang S (2014) Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 10:e1004078

    PubMed  PubMed Central  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 50:529–544

    CAS  PubMed  Google Scholar 

  • Lo Presti L, Lanver D, Schweizer G, Tanaka S, Liang L, Tollot M, Zuccaro A, Reissmann S, Kahmann R (2015) Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545

    CAS  PubMed  Google Scholar 

  • Luginbuehl LH, Oldroyd GE (2017) Understanding the arbuscule at the heart of endomycorrhizal symbioses in plants. Curr Biol 27:R952–R963

    CAS  PubMed  Google Scholar 

  • Luginbuehl LH, Menard GN, Kurup S, Van Erp H, Radhakrishnan GV, Breakspear A, Oldroyd GED, Eastmond PJ (2017) Fatty acids in arbuscular mycorrhizal fungi are synthesized by the host plant. Science 356:1175–1178

    CAS  PubMed  Google Scholar 

  • Maillet F, Poinsot V, André O, Puech-Pagès V, Haouy A, Gueurnier M, Cromer L, Giraudet D, Formey D, Niebel A, Andres Martinez E, Driguez H, Bécard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–64

    CAS  PubMed  Google Scholar 

  • Martin FM, Tuskan GA, DiFazio SP, Lammers P, Newcombe G, Podila GK (2004) Symbiotic sequencing for the Populus mesocosm. New Phytol 161:330–335

    PubMed  Google Scholar 

  • Martín-Robles N, Lehmann A, Seco E, Aroca R, Rillig MC, Milla R (2018) Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species. New Phytol 218(1):322–334

    PubMed  Google Scholar 

  • Martinez-Medina A, Flors V, Heil M, Mauch-Mani B, Pieterse C, Pozo M, Ton J, van Dam N, Conrath U (2016) Recognizing plant defense priming. Trends Plant Sci 21:818–822

    CAS  PubMed  Google Scholar 

  • Mateus ID, Masclaux FG, Aletti C, Rojas EC, Savary R, Dupuis C, Sanders IR (2019) Dual RNA-seq reveals large-scale non-conserved genotype×genotype-specific genetic reprograming and molecular crosstalk in the mycorrhizal symbiosis. ISME J 13(5):1226–1238. https://doi.org/10.1038/s41396-018-0342-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matusova R, Rani K, Verstappen W, Franssen M, Beale M, Bouwmeester H (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    CAS  PubMed  PubMed Central  Google Scholar 

  • McLean AM, Bravo A, Harrison MJ (2017) Plant signaling and metabolic pathways enabling arbuscular symbiosis. Plant Cell 29:2319–2335

    Google Scholar 

  • Miller JB, Pratap A, Miyahara A, Zhou L, Bornemann S, Morris RJ, Oldroyd GED (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 25:5053–5066

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104:19613–19618

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miyata K, Kozaki T, Kouzai Y, Ozawa K, Ishii K, Asamizu E, Okabe Y, Umehara Y, Miyamoto A, Kobae Y, Akiyama K, Kaku H, Nishizawa Y, Shibuya N, Nakagawa T (2014) The bifunctional plant receptor, OsCERK1, regulates both chitin-triggered immunity and arbuscular mycorrhizal symbiosis in rice. Plant Cell Physiol 55:1864–1872

    CAS  PubMed  Google Scholar 

  • Morin E, Miyauchi S, San Clemente H, Chen ECH, Pelin A, de la Providencia I, Ndikumana S, Beaudet D, Hainaut M, Drula E, Kuo A, Tang N, Roy S, Viala J, Henrissat B, Grigoriev IV, Corradi N, Roux C, Martin FM (2018) Comparative genomics of Rhizophagus irregularis, R. cerebriforme, R. diaphanus and Gigaspora rosea highlights specific genetic features in Glomeromycotina. New Phytol 222(3):1584–1598. https://doi.org/10.1111/nph.15687

    Article  CAS  Google Scholar 

  • Moscatiello R, Sello S, Novero M, Negro A, Bonfante P, Navazio L (2014) The intracellular delivery of TAT-aequorin reveals calcium-mediated sensing of environmental and symbiotic signals by the arbuscular mycorrhizal fungus Gigaspora margarita. New Phytol 203(3):1012–1020

    CAS  PubMed  Google Scholar 

  • Mukherjee A, Ané J-M (2011) Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Mol Plant-Microbe Interact 24:260–270

    CAS  PubMed  Google Scholar 

  • Mullis KB (1990) The unusual origin of the polymerase chain reaction. Sci Am 262(4):56–61. 64–65

    CAS  PubMed  Google Scholar 

  • Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164:357–364

    PubMed  Google Scholar 

  • Murat C, Payen T, Noel B, Kuo A, Morin E, Chen J, Kohler A, Krizsán K, Balestrini R, Da Silva C, Montanini B (2018) Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle. Nat Ecol Evol 2:1956–1965

    PubMed  Google Scholar 

  • Murray JD, Muni RR, Torres-Jerez I, Tang Y, Allen S, Andriankaja M, Li G, Laxmi A, Cheng X, Wen J, Vaughan D, Schultze M, Sun J, Charpentier M, Oldroyd G, Tadege M, Ratet P, Mysore KS, Chen R, Udvardi MK (2011) Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J 65(2):244–252

    CAS  PubMed  Google Scholar 

  • Nadal M, Sawers R, Naseem S, Bassin B, Kulicke C, Sharman A, An G, An K, Ahern KR, Romag A, Brutnell TP, Gutjahr C, Geldner N, Roux C, Martinoia E, Konopka JB, Paszkowski U (2017) An N-acetylglucosamine transporter required for arbuscular mycorrhizal symbioses in rice and maize. Nat Plants 26:17073

    Google Scholar 

  • Nagahashi G, Douds DD (2011) The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biol 115(4–5):351–358

    CAS  PubMed  Google Scholar 

  • Nagahashi G, Douds DD Jr (1997) Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol 136:299–304

    Google Scholar 

  • Nagata M, Yamamoto N, Shigeyama T, Terasawa Y, Anai T, Sakai T, Inada S, Arima S, Hashiguchi M, Akashi R, Nakayama H, Ueno D, Hirsch AM, Suzuki A (2015) Red/far red light controls arbuscular mycorrhizal colonization via jasmonic acid and strigolactone signaling. Plant Cell Physiol 56:2100–2109

    CAS  PubMed  Google Scholar 

  • Naito M, Morton JB, Pawlowska TE (2015) Minimal genomes of mycoplasma-related endobacteria are plastic and contain host-derived genes for sustained life within Glomeromycota. Proc Natl Acad Sci U S A 112:7791–7796

    CAS  PubMed  PubMed Central  Google Scholar 

  • Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson DC, Flematti GR, Riseborough JA, Ghisalberti EL, Dixon KW, Smith SM (2010) Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 107:7095–7100

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oláh B, Brière C, Bécard G, Dénarié J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207

    PubMed  Google Scholar 

  • Oldroyd GED (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11(4):252–263

    CAS  PubMed  Google Scholar 

  • Oldroyd GED, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 9:351–357

    CAS  PubMed  Google Scholar 

  • Op Den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, Ammiraju JS, Kudrna D, Wing R, Untergasser A, Bisseling T, Geurts R (2011) LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in non legume Parasponia. Science 331:909–912

    Google Scholar 

  • Orchard S, Hilton S, Bending GD, Dickie IA, Standish RJ, Gleeson RD, Jeffery P, Powell JR, Walker C, Bass D, Monk J, Simonin A, Ryan MH (2017) Fine endophytes (Glomus tenue) are related to Mucoromycotina not Glomeromycota. New Phytol 213:481–486

    PubMed  Google Scholar 

  • Pan HR, Oztas O, Zhang XW, Wu XY, Stonoha C, Wang E, Wang B, Wang D (2016) A symbiotic SNARE protein generated by alternative termination of transcription. Nat Plants 2:15197

    CAS  PubMed  Google Scholar 

  • Pandey P, Wang M, Baldwin IT, Pandey SP, Groten K (2018) Complex regulation of microRNAs in roots of competitively-grown isogenic Nicotiana attenuata plants with different capacities to interact with arbuscular mycorrhizal fungi. BMC Genomics 19(1):937

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park H-J, Floss DS, Levesque-Tremblay V, Bravo A, Harrison MJ (2015) Hyphal branching during arbuscule development requires RAM1. Plant Physiol 169:2774–2788

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421

    CAS  PubMed  Google Scholar 

  • Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6(10):763–775

    CAS  PubMed  Google Scholar 

  • Pellegrin C, Morin E, Martin FM, Veneault-Fourrey C (2015) Comparative analysis of secretomes from ectomycorrhizal fungi with an emphasis on small-secreted proteins. Front Microbiol 6:1278

    PubMed  PubMed Central  Google Scholar 

  • Pfeffer PE, Douds DD, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120:587–598

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pimprikar P, Gutjahr C (2018) Transcriptional regulation of arbuscular mycorrhiza development. Plant Cell Physiol 59:673–690

    PubMed  Google Scholar 

  • Pimprikar P, Carbonnel S, Paries M, Katzer K, Klingl V, Bohmer MJ, Karl L, Floss DS, Harrison MJ, Parniske M, Gutjahr C (2016) A CCaMK-CYCLOPS-DELLA complex activates transcription of RAM1 to regulate arbuscule branching. Curr Biol 26:987–998

    CAS  PubMed  Google Scholar 

  • Pumplin N, Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151:809–819

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ (2010) Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61:482–494

    CAS  PubMed  Google Scholar 

  • Pumplin N, Zhang X, Noar RD, Harrison MJ (2012) Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proc Natl Acad Sci USA 109:E665–E672

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ramirez-Flores MR, Rellan-Alvarez R, Wozniak B, Gebreselassie MN, Jakobsen I, Olalde-Portugal V, Baxter I, Paszkowski U, RJH S (2017) Coordinated changes in the accumulation of metal ions in maize (Zea mays ssp. mays L.) in response to inoculation with the arbuscular mycorrhizal fungus Funneliformis mosseae. Plant Cell Physiol 58:1689–1699

    PubMed  Google Scholar 

  • Rich MK, Schorderet M, Bapaume L, Falquet L, Morel P, Vandenbussche M, Reinhardt D (2015) The Petunia GRAS transcription factor ATA/RAM1 regulates symbiotic gene expression and fungal morphogenesis in arbuscular mycorrhiza. Plant Physiol 168:788–797

    CAS  PubMed  Google Scholar 

  • Rimington WR, Pressel S, Duckett JG, Bidartondo MI (2015) Fungal associations of basal vascular plants: reopening a closed book? New Phytol 205:1394–1398

    CAS  PubMed  Google Scholar 

  • Rivero J, Álvarez D, Flors V, Azcón-Aguilar C, Pozo MJ (2018) Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol 220(4):1322–1336

    CAS  PubMed  Google Scholar 

  • Ropars J, Lo Y-C, Dumas E, Snirc A, Begerow D, Rollnik T, Lacoste S, Dupont J, Giraud T, López-Villavicencio M (2016) Fertility depression among cheese-making Penicillium roqueforti strains suggests degeneration during domestication. Evolution 70(9):2099–2109

    CAS  PubMed  PubMed Central  Google Scholar 

  • Russo G, Spinella S, Sciacca E, Bonfante P, Genre A (2013) Automate analysis of calcium spiking profiles with CaSA software: two case studies from root-microbe symbioses. BMC Plant Biol 13:224

    PubMed  PubMed Central  Google Scholar 

  • Sagan M, Morandi D, Tarenghi E, Duc G (1995) Selection of nodulation and mycorrhizal mutants in the model plant Medicago truncatula (Gaertn.) after c-ray mutagenesis. Plant Sci 111:63–71

    CAS  Google Scholar 

  • Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624

    CAS  PubMed  PubMed Central  Google Scholar 

  • Salvioli A, Ghignone S, Novero M, Navazio L, Venice F, Bagnaresi P, Bonfante P (2016) Symbiosis with an endobacterium increases the fitness of a mycorrhizal fungus, raising its bioenergetic potential. ISME J 10:130–144

    CAS  PubMed  Google Scholar 

  • Sawers RJH, Gebreselassie MN, Janos DP, Paszkowski U (2010) Characterizing variation in mycorrhiza effect among diverse plant varieties. Theor Appl Genet 120:1029–1039

    PubMed  Google Scholar 

  • Sawers RJH, Svane SF, Quan C, Grønlund M, Wozniak B, Gebreselassie MN, González Muñoz E, Chávez Montes RA, Baxter I, Goudet J, Jakobsen I, Paszkowski U (2017) Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol 214:632–643

    CAS  PubMed  Google Scholar 

  • Schirawski J, Mannhaupt G, Munch K, Brefort T, Schipper K, Doehlemann G, Di Stasio M, Rossel N, Mendoza-Mendoza A, Pester D, Muller O, Winterberg B, Meyer E, Ghareeb H, Wollenberg T, Munsterkotter M, Wong P, Walter M, Stukenbrock E, Guldener U, Kahmann R (2010) Pathogenicity determinants in smut fungi revealed by genome comparison. Science 330:1546–1548

    CAS  PubMed  Google Scholar 

  • Schornack S, Huitema E, Cano LM, Bozkurt TO, Oliva R, Van Damme M et al (2009) Ten things to know about oomycete effectors. Mol Plant Pathol 10:795–803

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schweiger R, Baier MC, Persicke M, Muller C (2014) High specificity in plant metabolic responses to arbuscular mycorrhiza. Nat Commun 5:3886

    CAS  PubMed  Google Scholar 

  • Sędzielewska Toro K, Brachmann A (2016) The effector candidate repertoire of the arbuscular mycorrhizal fungus Rhizophagus clarus. BMC Genomics 17:101. https://doi.org/10.1186/s12864-016-2422-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu T, Nakano T, Takamizawa D, Desaki Y, Ishii-Minami N, Nishizawa Y, Minami E, Okada K, Yamane H, Kaku H, Shibuya N (2010) Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J 64:204–214

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shimoda Y, Han L, Yamazaki T, Suzuki R, Hayashi M, Imaizumi-Anraku H (2012) Rhizobial and fungal symbioses show different requirements for calmodulin binding to calcium calmodulin-dependent protein kinase in Lotus japonicus. Plant Cell 24(1):304–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Siciliano V, Genre A, Balestrini R, Cappellazzo G, Dewit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Silvestri A, Fiorilli V, Miozzi L, Accotto GP, Turina M, Lanfranco L (2019) In silico analysis of fungal small RNA accumulation reveals putative plant mRNA targets in the symbiosis between an arbuscular mycorrhizal fungus and its host plant. BMC Genomics 20:169

    PubMed  PubMed Central  Google Scholar 

  • Singh AK, Hamel C, DePauw RM, Knox RE (2012) Genetic variability in arbuscular mycorrhizal fungi compatibility supports the selection of durum wheat genotypes for enhancing soil ecological services and cropping systems. Can J Microbiol 58(2012):293–302

    CAS  PubMed  Google Scholar 

  • Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial nod factor-induced transcription. Science 308(5729):1789–1791

    CAS  PubMed  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524

    Google Scholar 

  • Soto MJ, Domínguez-Ferreras A, Pérez-Mendoza D, Sanjuán J, Olivares J (2009) Mutualism versus pathogenesis: the give-and- take in plant-bacteria interactions. Cell Microbiol 11(3):381–388

    CAS  PubMed  Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O'Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Steinkellner S, Hage-Ahmed K, Garcia-Garrido JM, Illana A, Ocampo JA, Vierheilig H (2012) A comparison of wild-type, old and modern tomato cultivars in the interaction with the arbuscular mycorrhizal fungus Glomus mosseae and the tomato pathogen Fusarium oxysporum f. sp. lycopersici. Mycorrhiza 22:189–194

    PubMed  Google Scholar 

  • Sun J, Miller JB, Granqvist E, Wiley-Kalil A, Gobbato E, Maillet F, Cottaz S, Samain E, Venkateshwaran M, Fort S, Morris RJ, Ané JM, Dénarié J, Oldroyd GED (2015) Activation of symbiosis signaling by arbuscular mycorrhizal fungi in legumes and rice. Plant Cell 27:823–838

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Chen W, Ivanov S, MacLean AM, Wight H, Ramaraj T, Mudge J, Harrison MJ, Fei Z (2018) Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts. New Phytol 221(3):1556–1573. https://doi.org/10.1111/NPH.15472

    Article  PubMed  Google Scholar 

  • Takeda N, Handa Y, Tsuzuki S, Kojima M, Sakakibara H, Kawaguchi M (2015) Gibberellins interfere with symbiosis signaling and gene expression and alter colonization by arbuscular mycorrhizal fungi in Lotus japonicus. Plant Physiol 167:545–557

    CAS  PubMed  Google Scholar 

  • Tamayo E, Gómez-Gallego T, Azcón-Aguilar C, Ferrol N (2014) Genome-wide analysis of copper, iron and zinc transporters in the arbuscular mycorrhizal fungus Rhizophagus irregularis. Front Plant Sci 5:547

    PubMed  PubMed Central  Google Scholar 

  • Tanaka Y, Yano K (2005) Nitrogen delivery to maize via mycorrhizal hyphae depends on the form of N supplied. Plant Cell Environ 28:1247–1254

    CAS  Google Scholar 

  • Tisserant E, Kohler A, Dozolme-Seddas P, Balestrini R, Benabdellah K, Colard A, Croll D, Da Silva C, Gomez SK, Koul R, Ferrol N, Fiorilli V, Formey D, Franken P, Helber N, Hijri M, Lanfranco L, Lindquist E, Liu Y, Malbreil M, Morin E, Poulain J, Shapiro H, van Tuinen D, Waschke A, Azcón-Aguilar C, Bécard G, Bonfante P, Harrison MJ, Küster H, Lammers P, Paszkowski U, Requena N, Rensing SA, Roux C, Sanders IR, Shachar-Hill Y, Tuskan G, Young JP, Gianinazzi-Pearson V, Martin F (2012) The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol 193(3):755–769

    CAS  PubMed  Google Scholar 

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, Frei dit Frey N, Gianinazzi-Pearson V, Gilbert LB, Handa Y, Herr JR, Hijri M, Koul R, Kawaguchi M, Krajinski F, Lammers PJ, Masclaux FG, Murat C, Morin E, Ndikumana S, Pagni M, Petitpierre D, Requena N, Rosikiewicz P, Riley R, Saito K, San Clemente H, Shapiro H, van Tuinen D, Bécard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young JP, Sanders IR, Henrissat B, Rensing SA, Grigoriev IV, Corradi N, Roux C, Martin F (2013) Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc Natl Acad Sci U S A 110(50):20117–20122

    CAS  PubMed  PubMed Central  Google Scholar 

  • Torres-Cortés G, Ghignone S, Bonfante P, Schüßler A (2015) Mosaic genome of endobacteria in arbuscular mycorrhizal fungi: transkingdom gene transfer in an ancient mycoplasma–fungus association. Proc Natl Acad Sci U S A 112:7785–7790

    PubMed  PubMed Central  Google Scholar 

  • Tsuzuki S, Handa Y, Takeda N, Kawaguchi M (2016) Strigolactone-induced putative secreted protein 1 is required for the establishment of symbiosis by the arbuscular mycorrhizal fungus Rhizophagus irregularis. Mol Plant-Microbe Interact 29:277–286

    CAS  PubMed  Google Scholar 

  • Turina M, Ghignone S, Astolfi N, Silvestri A, Bonfante P, Lanfranco L (2018) The virome of the arbuscular mycorrhizal fungus Gigaspora margarita reveals the first report of DNA fragments corresponding to replicating nonretroviral RNA viruses in fungi. Environ Microbiol 20(6):2012–2025. https://doi.org/10.1111/1462-2920.14060

    Article  CAS  PubMed  Google Scholar 

  • Turrini A, Sbrana C, Avio L, Mugendi Njeru E, Bocci G, Bàrberi P, Giovannetti M (2016) Changes in the composition of native root arbuscular mycorrhizal fungal communities during a short-term cover crop-maize succession. Biol Fertil Soils 52:643–653

    Google Scholar 

  • Turrini A, Avio L, Giovannetti M, Agnolucci M (2018) Functional complementarity of arbuscular mycorrhizal fungi and associated microbiota: the challenge of translational research. Front Plant Sci 9:1407

    PubMed  PubMed Central  Google Scholar 

  • Uehling J, Gryganskyi A, Hameed K, Tschaplinski T, Misztal PK, Wu S, Desirò A, Vande Pol N, Du Z, Zienkiewicz A, Zienkiewicz K, Morin E, Tisserant E, Splivallo R, Hainaut M, Henrissat B, Ohm R, Kuo A, Yan J, Lipzen A, Nolan M, LaButti K, Barry K, Goldstein AH, Labbé J, Schadt C, Tuskan G, Grigoriev I, Martin F, Vilgalys R, Bonito G (2017) Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens. Environ Microbiol 19(8):2964–2983

    CAS  PubMed  Google Scholar 

  • Van Buuren ML, Maldonado-Mendoza IE, Trieu AT, Blaylock LA, Harrison MJ (1999) Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Mol Plant-Microbe Interact 12(3):171–181

    PubMed  Google Scholar 

  • Venkateshwaran M, Cosme A, Han L, Banba M, Satyshur KA, Schleiff E, Parniske M, Imaizumi-Anraku H, Ané JM (2012) The recent evolution of a symbiotic ion channel in the legume family altered ion conductance and improved functionality in calcium signaling. Plant Cell 24:2528–2545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venkateshwaran M, Jayaraman D, Chabaud M, Genre A, Balloon AJ, Maeda J, Forshey K, den Os D, Kwiecien NW, Coon JJ, Barker DG, Ané J-M (2015) A role for the mevalonate pathway in early plant symbiotic signaling. Proc Natl Acad Sci U S A 112:9781–9786

    CAS  PubMed  PubMed Central  Google Scholar 

  • Venice F, Ghignone S, Salvioli A, Amselem J, Novero M, Xianan X, Sedzielewska Toro K, Morin E, Lipzen A, Grigoriev IV, Henrissat B, Martin F, Bonfante P (2019) 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

    PubMed  Google Scholar 

  • Vijayakumar V, Liebisch G, Buer B, Xue L, Gerlach N, Blau S, Schmitz J, Bucher M (2015) Integrated multi-omics analysis supports role of lysophosphatidylcholine and related glycerophospholipids in the Lotus japonicus–Glomus intraradices mycorrhizal symbiosis. Plant Cell Environ 39(2):393–415

    PubMed  Google Scholar 

  • Voß S, Betz R, Heidt S, Corradi N, Requena N (2018) RiCRN1, a crinkler fffector from the arbuscular mycorrhizal fungus Rhizophagus irregularis, functions in arbuscule development. Front Microbiol 9:2068. https://doi.org/10.3389/fmicb.2018.02068. eCollection 2018

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang B, Yeun LH, Xue JY, Liu Y, Ané JM, Qiu YL (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525

    PubMed  Google Scholar 

  • Wang E, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GED (2012) A common signalling process that promotes mycorrhizal and oomycete colonization of plants. Curr Biol 22(23):2242–2246

    CAS  PubMed  Google Scholar 

  • Wang M, Weiberg A, Dellota E, Yamane D, Jin H (2017) Botrytis smallRNABcsiR37 suppresses plant defense genes by cross-kingdom RNAi. RNA Biol 14:421–428

    PubMed  PubMed Central  Google 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 (2018) Blumenols as shoot markers of root symbiosis with arbuscular mycorrhizal fungi. elife 7:e37093. https://doi.org/10.7554/eLife.37093

    Article  PubMed  PubMed Central  Google Scholar 

  • Waters MT, Brewer PB, Bussell JD, Smith SM, Beveridge CA (2012) The Arabidopsis ortholog of rice DWARF27 acts upstream of MAX1 in the control of plant development by strigolactones. Plant Physiol 159(3):1073–1085

    CAS  PubMed  PubMed Central  Google Scholar 

  • Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322

    Google Scholar 

  • Wu P, Wu Y, Liu C-C, Liu L-W, Ma F-F, Wu X-Y, Wu M, Hang Y-Y, Chen J-Q, Shao Z-Q, Wang B (2016) Identification of arbuscular mycorrhiza (AM)-responsive microRNAs in tomato. Front Plant Sci 7:429

    PubMed  PubMed Central  Google Scholar 

  • Xing X, Koch AM, Jones AMP, Ragone D, Murch S, Hart MM (2012) Mutualism breakdown in breadfruit domestication. Proc Biol Sci 279:1122–1130

    PubMed  Google Scholar 

  • Xue L, Cui H, Buer B, Vijayakumar V, Delaux P-M, Junkermann S, Bucher M (2015) Network of GRAS transcription factors involved in the control of arbuscule development in Lotus japonicus. Plant Physiol 167:854–871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto K, Endo N, Degawa Y, Fukuda M, Yamada A (2017) First detection of Endogone ectomycorrhizas in natural oak forests. Mycorrhiza 27:295–301

    CAS  PubMed  Google Scholar 

  • Yang S-Y, Grønlund M, Jakobsen I, Grotemeyer MS, Rentsch D, Miyao A, Hirochika H, Santhosh Kumar C, Sundaresan V, Salamin N, Catausan S, Mattes N, Heuer S, Paszkowski U (2012) Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the phosphate transporter1 gene family. Plant Cell 24:4236–4251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yano K, Yoshida S, Müller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, Murooka Y, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc Natl Acad Sci U S A 105(51):20540–20545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Kameoka H, Tempo M, Akiyama K, Umehara M, Yamaguchi S, Hayashi H, Kyozuka J, Shirasu K (2012) The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol 196:1208–1216

    CAS  PubMed  Google Scholar 

  • Yu N, Luo D, Zhang X, Liu J, Wang W, Jin Y, Dong W, Liu J, Liu H, Yang W, Zeng L, Li Q, He Z, Oldroyd GED, Wang E (2014) A DELLA protein complex controls the arbuscular mycorrhizal symbiosis in plants. Cell Res 24:130–133

    CAS  PubMed  Google Scholar 

  • Zeng T, Holmer R, Hontelez J, Te Lintel HB, Marufu L, de Zeeuw T, Wu F, Schijlen E, Bisseling T, Limpens E (2018) Host- and stage-dependent secretome of the arbuscular mycorrhizal fungus Rhizophagus irregularis. Plant J 94:411–425

    CAS  PubMed  Google Scholar 

  • Zhang X, Dong W, Sun J, Feng F, Deng Y, He Z, Oldroyd GE, Wang E (2015) The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant J 81:258–267

    CAS  PubMed  Google Scholar 

  • Zhang X, Pumplin N, Ivanov S, Harrison MJ (2015b) EXO70I is essential for development of a sub-domain of the periarbuscular membrane during arbuscular mycorrhizal symbiosis. Curr Biol 25:2189–2195

    CAS  PubMed  Google Scholar 

  • Zhong Z, Norvienyeku J, Chen M, Bao J, Lin L, Chen L, Lin Y, Wu X, Cai Z, Zhang Q, Lin X, Hong Y, Huang J, Xu L, Zhang H, Chen L, Tang W, Zheng H, Chen X, Wang Y, Lian B, Zhang L, Tang H, Lu G, Ebbole DJ, Wang B, Wang Z (2016) Directional selection from host plants is a major force driving host specificity in Magnaporthe species. Sci Rep 6:25591

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu YG, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255

    CAS  Google Scholar 

  • Zipfel C, Oldroyd GE (2017) Plant signalling in symbiosis and immunity. Nature 15:328–336

    Google Scholar 

  • Zouari I, Salvioli A, Chialva M, Novero M, Miozzi L, Tenore G, Bagnaresi P, Bonfante P (2014) From root to fruit: RNA-Seq analysis shows that arbuscular mycorrhizal symbiosis may affect tomato fruit metabolism. BMC Genomics 15:221

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

Research is supported by the Italian Ministry for University and Research (MIUR - UNITO Ricerca Locale 2016) and by TOMRES from the European Union’s Horizon 2020 research and innovation program under grant agreement no. 727929 to L.L. and by the Italian Ministry for University and Research (MIUR - UNITO Ricerca Locale 2016) and Fondazione Cassa di Risparmio di Cuneo (AMforQuality – Bando Ricerca Scientifica 2015) to A.G.

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  1. Dipartimento di Scienze della Vita e Biologia dei Sistemi, Università di Torino, Torino, Italy

    Luisa Lanfranco, Gennaro Carotenuto, Andrea Genre & Paola Bonfante

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  1. Luisa Lanfranco
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  2. Gennaro Carotenuto
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  3. Andrea Genre
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  4. Paola Bonfante
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Correspondence to Luisa Lanfranco or Paola Bonfante .

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  1. TUM School of Life Sciences Weihenstephan, Holzforschung München – Fungal Biotechnology in Wood Science, Technische Universität München, Freising, Germany

    J. Philipp Benz

  2. Institut für Mikrobiologie, Department Biologie, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany

    Kerstin Schipper

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Lanfranco, L., Carotenuto, G., Genre, A., Bonfante, P. (2020). Genetics and Genomics Decipher Partner Biology in Arbuscular Mycorrhizas. In: Benz, J.P., Schipper, K. (eds) Genetics and Biotechnology. The Mycota, vol 2. Springer, Cham. https://doi.org/10.1007/978-3-030-49924-2_7

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