Skip to main content
SpringerLink
Log in

Strigolactones and Their Role in Arbuscular Mycorrhizal Symbiosis

  • Chapter
  • First Online:
Arbuscular Mycorrhizas: Physiology and Function

Abstract

Molecular signals are exchanged between arbuscular mycorrhizal (AM) fungi and their host plants during the pre-symbiotic stage, and help mutual recognition prior to any contact between the two partners. In particular, root exudates from host plants are known to trigger a switch in fungal development and metabolism, committing the fungus towards the establishment of the symbiosis. Strigolactones, a group of carotenoid-derived metabolites exuded by plant roots, are major contributors to this effect. Their importance in the normal development of mycorrhizae has been established through the analysis of strigolactone-deficient mutants. Interestingly, strigolactones were previously known as germination stimulants of the parasitic plants Striga and Orobanche. In addition, our group and others recently proposed that strigolactones or related compounds are novel hormones regulating shoot branching in monocots and dicots. The activity of strigolactones on three different types of organisms has stimulated progress in the understanding of their functions. This chapter reviews the current knowledge of strigolactone structural features, and recent advances and prospects in the elucidation of their biosynthetic pathway and of their mode of action.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AM:

Arbuscular mycorrhizal

CCD:

Carotenoid cleavage dioxygenase

RNAi:

RNA interference

SMS:

Shoot multiplication signal

NCED:

Nice-Cis-Epoxycarotenoid dioxygenase

ABA:

Abscisic acid

GA:

Gibberellic acid

References

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

    Article  CAS  PubMed  Google Scholar 

  • Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424

    Article  CAS  PubMed  Google Scholar 

  • Ayling SM, Smith SE, Smith FA (2000) Transmembrane electric potential difference of germ tubes of arbuscular mycorrhizal fungi responds to external stimuli. New Phytol 147:631–639

    Article  Google Scholar 

  • Bassel GW, Mullen RT, Bewley JD (2008) Procera is a putative DELLA mutant in tomato (Solanum lycopersicum): effects on the seed and vegetative plant. J Exp Bot 59:585–593

    Article  CAS  PubMed  Google Scholar 

  • Bécard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW (1995) Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbioses. Mol Plant Microbe Interact 8:252–258

    Article  Google Scholar 

  • Besserer A, Puech-Pages 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:e226

    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 148:402–413

    Article  CAS  PubMed  Google Scholar 

  • Besserer A, Bécard G, Roux C, Séjalon-Delmas N (2009) Role of mitochondria in the response of arbuscular mycorrhizal fungi to strigolactones. Plant Signal Behav 4:75–77

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya C, Bonfante P, Deagostino A, Kapulnik Y, Larini P, Occhiato EG, Prandi C, Venturello P (2009) A new class of conjugated strigolactone analogues with fluorescent properties: synthesis and biological activity. Org Biomol Chem 7:3413–3420

    Article  CAS  PubMed  Google Scholar 

  • Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8:443–449

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150:482–493

    Article  CAS  PubMed  Google Scholar 

  • Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from root exudates. Mol Plant Microbe Interact 13:693–698

    Article  PubMed  Google Scholar 

  • Butler LG (1995) Chemical communication between the parasitic weed Striga and its crop host. A new dimension in allelochemistry. In: Inderjit KM, Dakshini M, Enhelling FA (eds) Allelopathy, organisms, processes and applications, vol 582. American Chemical Society, Washington, DC

    Google Scholar 

  • Cook CE, Whichard LP, Turner B, Wall ME, Egley GH (1966) Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–1190

    Article  CAS  PubMed  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 

  • Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593

    Article  Google Scholar 

  • Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi. New Phytol 133:65–71

    Article  Google Scholar 

  • Goldwasser Y, Yoneyama K, Xie X, Yoneyama K (2008) Production of strigolactones by Arabidopsis thaliana responsible for Orobanche aegyptiaca seed germination. Plant Growth Regul 55:21–28

    Article  CAS  Google Scholar 

  • Gomez-Roldan V, Roux C, Girard D, Bécard G, Puech V (2007) Strigolactones: promising plant signals. Plant Signal Behav 2:163–164

    Article  PubMed  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 455:189–194

    Article  CAS  PubMed  Google Scholar 

  • Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and ­strigolactone in shoot branching control. Plant Physiol 151:400–412

    Article  CAS  PubMed  Google Scholar 

  • Helber N, Requena N (2008) Expression of the fluorescence markers DsRed and GFP fused to a nuclear localization signal in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 177:537–548

    CAS  PubMed  Google Scholar 

  • Hirano K, Ueguchi-Tanaka M, Matsuoka M (2008) GID1-mediated gibberellin signaling in plants. Trends Plant Sci 13:192–199

    Article  CAS  PubMed  Google Scholar 

  • Johnson X, Brcich T, Dun EA, Goussot M, Haurogné K, Beveridge CA, Rameau C (2006) Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol 142:1014–1026

    Article  CAS  PubMed  Google Scholar 

  • Jolicoeur M, Germette S, Gaudette M, Perrier M, Bécard G (1998) Intracellular pH in arbuscular mycorrhizal fungi: a symbiotic physiological marker. Plant Physiol 116:1279–1288

    Article  CAS  PubMed  Google Scholar 

  • Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié 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

    Article  CAS  PubMed  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 USA 105:9823–9828

    Article  CAS  PubMed  Google Scholar 

  • Lei J, Bécard G, Catford JG, Piché Y (1991) Root factors stimulate 32P uptake and plasmalemma ATPase activity in the vesicular–arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol 118:289–294

    Article  CAS  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 

  • Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z, Yan C, Jiang B, Su Z, Li J, Wang Y (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Wu C, Fu Y, Hu G, Si H, Zhu L, Luan W, He Z, Sun Z (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230:649–658

    Article  CAS  PubMed  Google Scholar 

  • Logan DC, Stewart GR (1991) Role of ethylene in the germination of the hemiparasite Striga hermonthica. Plant Physiol 97:1435–1438

    Article  CAS  PubMed  Google Scholar 

  • Logan DC, Millar AH, Sweetlove LJ, Hill SA, Leaver CJ (2001) Mitochondrial biogenesis during germination in maize embryos. Plant Physiol 125:662–672

    Article  CAS  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 

  • Mangnus EM, Zwanenburg B (1992) Tentative molecular mechanism for germination stimulation of Striga and Orobanche seeds by strigol and its synthetic analogues. J Agric Food Chem 40:1066–1070

    Article  CAS  Google Scholar 

  • Martin F, Gianinazzi-Pearson V, Hijri M, Lammers P, Requena N, Sanders IR, Shachar-Hill Y, Shapiro H, Tuskan GA, Young JP (2008) The long hard road to a completed Glomus intraradices genome. New Phytol 180:747–750

    Article  CAS  PubMed  Google Scholar 

  • Matusova R, Rani K, Verstappen FW, Franssen MC, 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  CAS  PubMed  Google Scholar 

  • Mosse B (1988) Some studies relating to “independent” growth of vesicular–arbuscular endophytes. Can J Bot 66:2533–2540

    Article  Google Scholar 

  • Mosse B, Hepper C (1975) Vesicular–arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5:215–223

    Article  Google Scholar 

  • Nagahashi G, Douds DD Jr (1999) A rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotech Tech 13:893–897

    Article  CAS  Google Scholar 

  • Nagahashi G, Douds D Jr (2007) Separated components of root exudate and cytosol stimulate different morphologically identifiable types of branching responses by arbuscular mycorrhizal fungi. Mycol Res 111:487–492

    Article  PubMed  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

    Article  CAS  PubMed  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

    Article  PubMed  Google Scholar 

  • Paszkowski U (2006) Mutualism and parasitism: the yin and yang of plant symbioses. Curr Opin Plant Biol 9:364–370

    Article  PubMed  Google Scholar 

  • Rani K, Zwanenburg B, Sugimoto Y, Yoneyama K, Bouwmeester HJ (2008) Biosynthetic considerations could assist the structure elucidation of host plant produced rhizosphere signalling compounds (strigolactones) for arbuscular mycorrhizal fungi and parasitic plants. Plant Physiol Biochem 46:617–626

    Article  CAS  PubMed  Google Scholar 

  • Reizelman A, Wigchert SC, del-Bianco C, Zwanenburg B (2003) Synthesis and bioactivity of labelled germination stimulants for the isolation and identification of the strigolactone receptor. Org Biomol Chem 1:950–959

    Article  CAS  PubMed  Google Scholar 

  • Requena N, Serrano E, Ocón A, Breuninger M (2007) Plant signals and fungal perception during arbuscular mycorrhiza establishment. Phytochemistry 68:33–40

    Article  CAS  PubMed  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Vierheilig H, Ocampo JA, Godeas A (2005) Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycol Res 109:789–794

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SH, Qin X, Loewen MC (2004) The biochemical characterization of two carotenoid cleavage enzymes from Arabidopsis indicates that a carotenoid-derived compound inhibits lateral branching. J Biol Chem 279:46940–46945

    Article  CAS  PubMed  Google Scholar 

  • Silverstone AL, Mak PY, Martínez EC, Sun TP (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146:1087–1099

    CAS  PubMed  Google Scholar 

  • Splivallo R, Fischer U, Göbel C, Feussner I, Karlovsky P (2009) Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol 150:2018–2029

    Article  CAS  PubMed  Google Scholar 

  • Stirnberg P, Furner IJ, Leyser HMO (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J 50:80–94

    Article  CAS  PubMed  Google Scholar 

  • Takikawa H, Jikumaru S, Sugimoto Y, Xie X, Yoneyama K, Sasaki M (2009) Synthetic disproof of the structure proposed for solanacol, the germination stimulant for seeds of root parasitic weeds. Tetrahedron Lett 50:4549–4551

    Article  CAS  Google Scholar 

  • Tamasloukht M, Séjalon-Delmas N, Kluever A, Jauneau A, Roux C, Bécard G, Franken P (2003) Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol 131:1468–1478

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Vierheilig H (2004) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J Plant Physiol 161:339–341

    Article  CAS  PubMed  Google Scholar 

  • Vierheilig H, Lerat S, Piché Y (2003) Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae. Mycorrhiza 13:167–170

    Article  CAS  PubMed  Google Scholar 

  • Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant Microbe Interact 17:1385–1393

    Article  CAS  PubMed  Google Scholar 

  • Xie X, Yoneyama K, Harada Y, Fusegi N, Yamada Y, Ito S, Yokota T, Takeuchi Y, Yoneyama K (2009) Fabacyl acetate, a germination stimulant for root parasitic plants from Pisum sativum. Phytochemistry 70:211–215

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) Nitrogen deficiency as well as phosphorus 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  CAS  PubMed  Google Scholar 

  • Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038

    Article  CAS  PubMed  Google Scholar 

  • Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Surfaces Cellulaires et Signalisation chez les Végétaux, Université de Toulouse; UPS; CNRS, UMR 5546, 24 chemin de Borde Rouge, F-31326, Castanet-Tolosan, France

    Soizic Rochange

Authors
  1. Soizic Rochange
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Soizic Rochange .

Editor information

Editors and Affiliations

  1. , Volcani Center, Agricultural Research Organization, Bet Dagan, 50250, Israel

    Hinanit Koltai

  2. Dept. Agronomy & Natural Resources, Sec. Forestry, Agricultural Research Organization (ARO), Bet Dagan, 50250, Israel

    Yoram Kapulnik

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Rochange, S. (2010). Strigolactones and Their Role in Arbuscular Mycorrhizal Symbiosis. In: Koltai, H., Kapulnik, Y. (eds) Arbuscular Mycorrhizas: Physiology and Function. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-9489-6_4

Download citation

Publish with us

Policies and ethics

Search

Navigation