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
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
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
Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotechnol 20:642–650
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
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
Barea JM, Pozo MJ, Azcon R, Azcon-Aguilar C (2005) Microbial co-operation in the rhizosphere. J Exp Bot 56:1761–1778
Bertin C, Yang XH, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
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
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:1–11
Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364
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
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
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
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
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
Foo E, Davies NW (2011) Strigolactones promote nodulation in pea. Planta 243:1073–1081
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
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
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
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
Hanlon MT, Coenen C (2011) Genetic evidence for auxin involvement in arbuscular mycorrhiza initiation. New Phytol 189:701–709
Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110
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
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
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
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
Javot H, Pumplin N, Harrison MJ (2007) Phosphate in the arbuscular mycorrhizal symbiosis: transport properties and regulatory roles. Plant Cell Environ 30:310–322
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
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
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
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
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
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
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
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
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
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
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
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
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
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
López-Ráez JA, Pozo MJ, García-Garrido JM (2011b) Strigolactones: a cry for help in the rhizosphere. Botany 89:513–522
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
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
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
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
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
Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739
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
Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant Physiol Biochem 47:511–517
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
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
Ohmiya A (2009) Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol 26:351–358
Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775
Pozo MJ, Azcón-Aguilar C (2007) Unravelling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398
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
Rouached H, Arpat AB, Poirier Y (2010) Regulation of phosphate starvation responses in plants: signaling players and cross-talks. Mol Plant 3:288–299
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
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
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
Sbrana C, Giovannetti M (2005) Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 15:539–545
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
Siegler DS (1998) Plant secondary metabolism. Kluwer Academic, Boston, MA
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic, London
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
Sprent JI (2009) Legume nodulation. A global perspective. Wiley-Blackwell, Chichester
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
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
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
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
Xie XN, Yoneyama K, Yoneyama K (2010) The strigolactone story. Annu Rev Phytopathol 48:93–117
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
Yoneyama K, Xie X, Yoneyama K, Takeuchi Y (2009) Strigolactones: structures and biological activities. Pest Manag Sci 65:467–470
Zsogon A, Lambais MR, Benedito VA, Figueira AVD, Peres LEP (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Scientia Agricola 65:259–267
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
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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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