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Chemical Signalling in the Arbuscular Mycorrhizal Symbiosis: Biotechnological Applications

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Symbiotic Endophytes

Part of the book series: Soil Biology ((SOILBIOL,volume 37))

Abstract

Plants are living organisms that continuously interact with other organisms both above- and belowground. The rhizosphere constitutes a very dynamic environment harbouring the plant roots and many organisms, including beneficial microorganisms such as arbuscular mycorrhizal (AM) fungi. The AM symbiosis is one of the best studied beneficial associations established between fungi of the phylum Glomeromycota and the vast majority of terrestrial plants, including most agricultural and horticultural crop species. Symbiosis establishment and functioning requires a signal exchange between the two partners that leads to mutual recognition and orchestrates complex symbiotic programmes. Plant–AM fungi communication relies on chemicals among which the strigolactones play a key role. Under deficient nutrient conditions, the host plant increases the production and exudation of strigolactones into the rhizosphere to promote fungal development, thus acting as a “cry for help” signal. On the other hand, the metabolically active fungus produces and releases the so-called Myc factors that induce the molecular responses in the host plant required for a successful colonization.

We review here current knowledge on the chemical signalling that gives rise to AM symbiosis establishment, paying special attention to the molecules involved in the very early stages of the interaction. Their potential use in sustainable agriculture is discussed.

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References

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Aroca R, Ruiz-Lozano JM, Zamarreño AM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170(1):47–55. doi:10.1016/j.jplph.2012.08.020

    Article  PubMed  CAS  Google Scholar 

  • Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20:642–650

    Article  PubMed  CAS  Google Scholar 

  • Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266

    Article  PubMed  CAS  Google Scholar 

  • Balzergue C, Puech-Pages V, Becard G, Rochange SF (2011) The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J Exp Bot 62:1049–1060

    Article  PubMed  CAS  Google Scholar 

  • Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778

    Article  PubMed  CAS  Google Scholar 

  • Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11

    Article  Google Scholar 

  • Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, Bucher M, Kretzschmar T, Bossolini E, Kuhlemeier C, Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J 64:1002–1017

    Article  PubMed  CAS  Google Scholar 

  • Cook CE, Whichard LP, Wall ME, Egley GH, Coggon P, Luhan PA, McPhail AT (1972) Germination stimulants. 2. The structure of strigol-a potent seed germination stimulant for witchweed (Striga lutea Lour.). J Am Chem Soc 94:6198–6199

    Article  CAS  Google Scholar 

  • Den Herder G, Van Isterdael G, Beeckman T, De Smet I (2010) The roots of a new green revolution. Trends Plant Sci 15:600–607

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 243:1073–1081

    Article  Google Scholar 

  • García-Garrido JM, Lendzemo V, Castellanos-Morales V, Steinkellner S, Vierheilig H (2009) Strigolactones, signals for parasitic plants and arbuscular mycorrhizal fungi. Mycorrhiza 19:449–459

    Article  PubMed  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

    Article  PubMed  CAS  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Gómez-Roldán V, Fermas S, Brewer PB, Puech-Pagés 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 455:189–194

    Article  PubMed  Google Scholar 

  • Hanlon MT, Coenen C (2011) Genetic evidence for auxin involvement in arbuscular mycorrhiza initiation. New Phytol 189:701–709

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo-Bote JA, García-Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564

    Article  PubMed  CAS  Google Scholar 

  • Herrera-Medina MJ, Tamayo MI, Vierheilig H, Ocampo JA, García-Garrido JM (2008) The jasmonic acid signalling pathway restricts the development of the arbuscular mycorrhizal association in tomato. J Plant Growth Regul 27:221–230

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322

    Article  PubMed  CAS  Google Scholar 

  • Joel DM, Hershenhom Y, Eizenberg H, Aly R, Ejeta G, Rich JP, Ransom JK, Sauerborn J, Rubiales D (2007) Biology and management of weedy root parasites. Hort Rev 33:267–349

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kapulnik Y, Delaux PM, Resnick N, Mayzlish-Gati E, Wininger S, Bhattacharya C, Sejalon-Delmas N, Combier JP, Bécard G, Belausov E, Beeckman T, Dor E, Hershenhorn J, Koltai H (2011a) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216

    Article  PubMed  CAS  Google Scholar 

  • Kapulnik Y, Resnick N, Mayzlish-Gati E, Kaplan Y, Wininger S, Hershenhorn J, Koltai H (2011b) Strigolactones interact with ethylene and auxin in regulating root-hair elongation in Arabidopsis. J Exp Bot 62:2915–2924

    Article  PubMed  CAS  Google Scholar 

  • Kohlen W, Charnikhova T, Lammers M, Pollina T, Tóth P, Haider I, Pozo MJ, de Maagd RA, Ruyter-Spira C, Bouwmeester HJ, López-Ráez JA (2012) The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol 196:535–547

    Article  PubMed  CAS  Google Scholar 

  • Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier JB, Reinhardt D, Bours R, Bouwmeester HJ, Martinoia E (2012) A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483:341–344

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lendzemo VW, Kuyper TW, Matusova R, Bouwmeester HJ, van Ast A (2007) Colonization by arbuscular mycorrhizal fungi of sorghum leads to reduced germination and subsequent attachment and emergence of Striga hermonthica. Plant Signal Behav 2:58–62

    Article  PubMed  Google Scholar 

  • León-Morcillo RJ, Ángel J, Martín R, Vierheilig H, Ocampo JA, García-Garrido JM (2012) Late activation of the 9-oxylipin pathway during arbuscular mycorrhiza formation in tomato and its regulation by jasmonate signalling. J Exp Bot 63:3545–3558

    Article  PubMed  Google Scholar 

  • López-Ráez JA, Charnikhova T, Gómez-Roldán V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Bécard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874

    Article  PubMed  Google Scholar 

  • López-Ráez JA, Matusova R, Cardoso C, Jamil M, Charnikhova T, Kohlen W, Ruyter-Spira C, Verstappen F, Bouwmeester H (2009) Strigolactones: ecological significance and use as a target for parasitic plant control. Pest Manag Sci 64:471–477

    Article  Google Scholar 

  • López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TDH, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010a) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187:343–354

    Article  PubMed  Google Scholar 

  • López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010b) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601

    Article  PubMed  Google Scholar 

  • López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ (2011a) Arbuscular mycorrhizal symbiosis decreases strigolactone production in tomato. J Plant Physiol 168:294–297

    Article  PubMed  Google Scholar 

  • López-Ráez JA, Pozo MJ, García-Garrido JM (2011b) Strigolactones: a cry for help in the rhizosphere. Botany 89:513–522

    Article  Google Scholar 

  • López-Ráez JA, Bouwmeester H, Pozo MJ (2012) Communication in the rhizosphere, a target for pest management. In: Lichtfouse E (ed) Agroecology and strategies for climate change. Springer, Dordrecht, pp 109–133

    Chapter  Google Scholar 

  • Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Cromer L, Giraudet D, Formey D, Niebel A, Martinez EA, Driguez H, Becard G, Denarie J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469:58–63

    Article  PubMed  CAS  Google Scholar 

  • Martín-Rodríguez JA, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Muller J, García-Garrido JM (2010) Mycorrhization of the notabilis and sitiens tomato mutants in relation to abscisic acid and ethylene contents. J Plant Physiol 167:606–613

    Article  Google Scholar 

  • Martín-Rodríguez JA, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Muller J, García-Garrido JM (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739

    Article  PubMed  CAS  Google Scholar 

  • Mortier V, den Herder G, Whitford R, van de Velde W, Rombauts S, D’Haeseleer K, Holsters M, Goormachtig S (2010) CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiol 153:222–237

    Article  PubMed  CAS  Google Scholar 

  • Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47:511–517

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee A, Ane JM (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

    Article  PubMed  CAS  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 115:351–358

    Article  PubMed  CAS  Google Scholar 

  • Ohmiya A (2009) Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol 26:351–358

    Article  CAS  Google Scholar 

  • Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen A, Mason MG, De Cuyper C, Brewer PB, Herold S, Agusti J, Geelen D, Greb T, Goormachtig S, Beeckman T, Beveridge CA (2012) Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol 158:1976–1987

    Article  PubMed  CAS  Google Scholar 

  • Rouached H, Arpat AB, Poirier Y (2010) Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant 3:288–299

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Porcel R, Azcón C, Aroca R (2012) Regulation by arbuscular mycorrhizae of the integrated physiological response to salinity in plants: new challenges in physiological and molecular studies. J Exp Bot 63:4033–4044

    Article  PubMed  CAS  Google Scholar 

  • Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, López-Ráez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Calderón L, López-Bucio J, Chacón-López A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184

    Article  PubMed  Google Scholar 

  • Sbrana C, Giovannetti M (2005) Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 15:539–545

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Siegler DS (1998) Plant secondary metabolism. Kluwer Academic, Boston, MA

    Book  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London

    Google Scholar 

  • Soto MJ, Fernández-Aparicio M, Castellanos-Morales V, García-Garrido JM, Ocampo JA, Delgado MJ, Vierheilig H (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385

    Article  CAS  Google Scholar 

  • Sprent JI (2009) Legume nodulation. A global perspective. Wiley-Blackwell, Chichester

    Book  Google Scholar 

  • Staehelin C, Xie ZP, Illana A, Vierheilig H (2011) Long-distance transport of signals during symbiosis: are nodule formation and mycorrhization autoregulated in a similar way? Plant Signal Behav 6:372–377

    Article  PubMed  CAS  Google Scholar 

  • Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306

    Article  PubMed  CAS  Google Scholar 

  • Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200

    Article  PubMed  CAS  Google Scholar 

  • Vogel JT, Walter MH, Giavalisco P, Lytovchenko A, Kohlen W, Charnikhova T, Simkin AJ, Goulet C, Strack D, Bouwmeester HJ, Fernie AR, Klee HJ (2010) SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J 61:300–311

    Article  PubMed  CAS  Google Scholar 

  • Xie XN, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorous deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    Article  PubMed  CAS  Google Scholar 

  • Yoneyama K, Xie X, Yoneyama K, Takeuchi Y (2009) Strigolactones: structures and biological activities. Pest Manag Sci 65:467–470

    Article  PubMed  CAS  Google Scholar 

  • Zsogon A, Lambais MR, Benedito VA, Figueira AVD, Peres LEP (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Scientia Agricola 65:259–267

    Article  CAS  Google Scholar 

  • Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag Sci 65:478–491

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

Our research is supported by grant AGL2009-07691 from the National R&D Plan of the MINCIN.

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López-Ráez, J.A., Pozo, M.J. (2013). Chemical Signalling in the Arbuscular Mycorrhizal Symbiosis: Biotechnological Applications. In: Aroca, R. (eds) Symbiotic Endophytes. Soil Biology, vol 37. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-39317-4_11

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