Skip to main content
Log in

The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi

  • Rapid Communication
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Strigolactones that are released by plant roots to the rhizosphere are involved in both plant symbiosis with arbuscular mycorrhizal fungi and in plant infection by root parasitic plants. In this paper, we describe the response of various phytopathogenic fungi to the synthetic strigolactone GR24. When GR24 was embedded in the growth medium, it inhibited the growth of the root pathogens Fusarium oxysporum f. sp. melonis, Fusarium solani f. sp. mango, Sclerotinia sclerotiorum and Macrophomina phaseolina, and of the foliar pathogens Alternaria alternata, Colletotrichum acutatum and Botrytis cinerea. In the presence of this synthetic strigolactone, intense branching activity was exhibited by S. sclerotiorum, C. acutatum and F. oxysporum f. sp. melonis. Slightly increased hyphal branching was observed for A. alternata, F. solani f. sp. mango and B. cinerea, whereas suppression of hyphal branching by GR24 was observed in M. phaseolina. These results suggest that strigolactones not only affect mycorrhizal fungi and parasitic plants, but they also have a more general effect on phytopathogenic fungi.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Abbreviations

AM:

Arbuscular mycorrhizal

BF:

Branching factor

SL:

Strigolactone

References

  • Akiyama K (2007) Chemical identification and functional analysis of apocarotenoids involved in the development of arbuscular mycorrhizal symbiosis. Biosci Biotechnol Biochem 71:1405–1414

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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, Hayashi H (2010) Structural requirement of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117

    Article  PubMed  CAS  Google Scholar 

  • Asante A, Hashidoko Y, Deora A, Tahara S (2008) Antagonistic Gluconobacter sp. induces abnormal morphodifferentiation to Fusarium oxysporum f. sp. lycopersici hyphae. J Pestic Sci 33:138–145

    Article  CAS  Google Scholar 

  • Bécard G, Fortin JA (1988) Early events of vesicular–arbuscular mycorrhiza formation on Ri-T-DNA transformed roots. New Phytol 108:211–218

    Article  Google Scholar 

  • Bécard G, Piché Y (1990) Physiological factors determining vesicular–arbuscular mycorrhizal formation in host and non-host Ri TDNA transformed roots. Can J Bot 68:1260–1264

    Article  Google Scholar 

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

    Article  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 148:402–413

    Article  PubMed  CAS  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  PubMed  CAS  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, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Dor E, Alperin B, Wininger S, Ben-Dor B, Somvanshi VS, Koltai H, Kapulnik Y, Hershenhorn J (2010) Characterization of a novel tomato mutant resistant to Orobanche and Phelipanche spp. weedy parasites. Euphytica 171:371–380

    Article  CAS  Google Scholar 

  • Dor E, Yoneyama K, Wininger S, Kapulnik Y, Yoneyama K, Koltai H, Xie X, Hershenhorn J (2011) Strigolactone deficiency confers resistance in tomato line SL-ORT1 to the parasitic weeds Phelipanche spp. and Orobanche spp. Phytopathology 101:213–222

    Article  PubMed  CAS  Google Scholar 

  • Elias KS, Safir GR (1987) Hyphal elongation of Glomus fasciculatus in response to root exudates. Appl Environ Microbiol 53:1928–1933

    PubMed  CAS  Google Scholar 

  • Fernández-Aparicio F, Yoneyama K, Rubiales D (2011) The role of strigolactones in host specificity of Orobanche and Phelipanche seed germination. Seed Sci Res 21:55–61

    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 

  • Ghosh M (2006) Antifungal properties of haem peroxidase from Acorus calamus. Ann Bot 98:1145–1153

    Article  PubMed  CAS  Google Scholar 

  • Gianinazzi-Pearson V, Branzanti B, Gianinazzi S (1989) In vitro enhancement of spore germination and early hyphal growth of a vesicular–arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255

    CAS  Google Scholar 

  • Giovannetti M, Sbrana C (1998) Meeting a non-host: the behavior of AM fungi. Mycorrhiza 8:123–130

    Article  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, Logi C (1994) Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol 127:703–709

    Article  Google Scholar 

  • Giovannetti M, Sbrana C, Silvia A, Avio L (1996) Analysis of factors involved in fungal recognition response 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 

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

    Article  PubMed  Google Scholar 

  • Graham JH (1982) Effect of citrus exudates on germination of chlamydospores of the vesicular–arbuscular mycorrhizal fungus Glomus epigaeum. Mycologia 74:831–835

    Article  Google Scholar 

  • Graz M, Jarosz-Wilkolazka A, Pawlikowska-Pawlega B (2009) Abortiporus biennis tolerance to insoluble metal oxides: oxalate secretion, oxalate oxidase activity, and mycelial morphology. Biometals 22:401–410

    Article  PubMed  CAS  Google Scholar 

  • Gworgwor NA, Weber HC (2003) Arbuscular mycorrhizal fungi–parasite–host interaction for the control of Striga hermonthica (Del.) Benth. in sorghum [Sorghum bicolor (L.) Moench]. Mycorrhiza 13:277–281

    Article  PubMed  Google Scholar 

  • Hao S, Xue J, Guo D, Wang D (2010) Earliest rooting system and root: shoot ratio from a new Zosterophyllum plant. New Phytol 185:217–225

    Article  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  PubMed  CAS  Google Scholar 

  • Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium-legume symbiosis. Fungal Genet Biol 23:205–212

    Article  PubMed  CAS  Google Scholar 

  • Hsiao AI, Warsham AD, Moreland DE (1983) Leaching and degradation of dl-strigol in soil. Weed Sci 31:763–765

    CAS  Google Scholar 

  • Islam MT (2008) Disruption of ultrastructure and cytoskeletal network is involved with biocontrol of damping-off pathogen Aphanomyces cochlioides by Lysobacter sp. strain SB-K88. Biol Contr 46:312–321

    Article  Google Scholar 

  • Jha G, Anjaiah V (2007) Metabolites of rhizobacteria antagonistic towards fungal plant pathogens. Ann Microbiol 57:127–130

    Article  Google Scholar 

  • Joel DM, Chaudhuri SK, Plakhine D, Ziadna H, Steffens JC (2011) Dehydrocostus lactone is exuded from sunflower roots and stimulates germination of the root parasite Orobanche cumana. Phytochemistry 72:624–634

    Article  PubMed  CAS  Google Scholar 

  • Koltai H, LekKala SP, Bahattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E, Yoneyama K, Yoneyama K, Hershenhorn J, Joel DM, Kapulnik Y (2009) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61:1739–1749

    Article  Google Scholar 

  • Kozlova OV, Egorov SY, Kupriyanova-Ashina FG (2010) The relationship between cellular and calcium responses of Aspergillus awamori to external influences. Microbiology 79:294–299

    Article  CAS  Google Scholar 

  • Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648–657

    Article  PubMed  Google Scholar 

  • Lendzemo VW (2004) The tripartite interaction between sorghum, Striga hermonthica, and arbuscular mycorrhizal fungi. Ph.D. Thesis, Wageningen University, Wageningen, The Netherlands

  • Lendzemo VW, Kuyper TW (2001) Effects of arbuscular mycorrhizal fungi on damage by Striga hermonthica on two contrasting cultivars of sorghum, Sorghum bicolor. Agric Ecosyst Environ 87:29–35

    Article  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 Crops 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 

  • Lendzemo L, Kuyper TW, Vierheilig H (2009) Striga seed germination activity of root exudates and compounds present in stems of Striga host and nonhost (trap crop) plants is reduced due to root colonization by arbuscular mycorrhizal fungi. Mycorrhiza 19:287–294

    Article  PubMed  CAS  Google Scholar 

  • Liang J, Zhao L, Challis R, Leyser O (2010) Strigolactone regulation of shoot branching in chrysanthemum (Dendranthema grandiflorum). J Exp Bot 61:3069–3078

    Article  PubMed  CAS  Google Scholar 

  • Martinez C, Buée M, Jauneau A, Bécard G, Dargent R, Roux C (2001) Effects of a fraction from maize root exudates on haploid strains of Sporisorium reilianum f. sp. zeae. Plant Soil 236:145–153

    Article  CAS  Google Scholar 

  • Matusova R, van Mourik T, Bouwmeester HJ (2004) Changes in the sensitivity of parasitic weed seeds to germination stimulants. Seed Sci Res 14:335–344

    Article  CAS  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 

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

    Article  Google Scholar 

  • Munoz A, Lopez-Garcia B, Marcos JF (2006) Studies on the mode of action of the antifungal hexapeptide PAF26. Antimicrob Agents Chemother 50:3847–3855

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Plakhine D, Ziadna H, Joel DM (2009) Is seed conditioning essential for Orobanche germination?. Pest Manag Sci 65:492–496

    Article  PubMed  CAS  Google Scholar 

  • Proust H, Hoffmann B, Xie X, Yoneyama K, Schaefer DG, Yoneyama K, Nogué F, Rameau K (2011) Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531–1539

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez-Urra AB, Jimenez C, Duenas M, Ugalde U (2009) Bicarbonate gradients modulate growth and colony morphology in Aspergillus nidulans. Microbiol Lett 300:216–221

    Article  CAS  Google Scholar 

  • Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, Bezouwen L, de Ruijter N, Lopez-Raez 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 

  • Sabbagh SK (2008) Adaptation à la pénétration racinaire de deux Ustilaginaceae parasites du maïs: Ustilago maydis et Sporisorium reilianum—analyse microscopique et transcriptomique. Ph.D. Thesis, Université Toulouse, France

  • Scheffknecht S, Mammerler R, Steinkellner S, Vierheilig H (2006) Root exudates of mycorrhizal tomato plants exhibit a different effect on microconidia germination of Fusarium oxysporum f. sp. lycopersici than root exudates from non-mycorrhizal tomato plants. Mycorrhiza 16:365–370

    Article  PubMed  CAS  Google Scholar 

  • Scheffknecht S, Mammerler R, Vierheilig H (2008) Germination of Fusarium oxysporum in root exudates from tomato plants challenged with different Fusarium oxysporum strains. Eur J Plant Pathol 122:395–401

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic Press, San Diego

    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 

  • Sun Z, Hans J, Walter MH, Matusova R, Beekwilder J, Verstappen FWA, Ming Z, van Echtelt E, Strack D, Bisseling T, Bouwmeester HJ (2008) Cloning and characterisation of a maize carotenoid cleavage dioxygenase (ZmCCD1) and its involvement in the biosynthesis of apocarotenoids with various roles in mutualistic and parasitic interactions. Planta 228:789–801

    Article  PubMed  CAS  Google Scholar 

  • Tamasloukht MB, 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  PubMed  CAS  Google Scholar 

  • Tanaka A, Takemoto D, Hyon G-S, Park P, Scott B (2008) NoxA activation by the small GTPase RacA is required to maintain a mutualistic symbiotic association between Epichloë festucae and perennial ryegrass. Mol Microbiol 68:1165–1178

    Article  PubMed  CAS  Google Scholar 

  • Tawaraya K, Watanabe S, Yoshida E, Wagatsuma T (1996) Effect of onion (Allium cepa) root exudates on the hyphal growth of Gigaspora margarita. Mycorrhiza 6:57–59

    Article  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 

  • Wang B, Qiu YL (2006) Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16:299–363

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 179:484–492

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yulianti T, Sivasithamparam K, Turner DW (2006) Response of different forms of propagules of Rhizoctonia solani AG2-1 (ZG5) exposed to the volatiles produced in soil amended with green manures. Ann Appl Biol 148:105–111

    Article  Google Scholar 

Download references

Acknowledgments

We thank Prof. Koichi Yoneyama for kindly providing us with GR24, Mr. Eduard Belousov for assistance in microscopy and the anonymous reviewers for constructive comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Evgenia Dor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dor, E., Joel, D.M., Kapulnik, Y. et al. The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi. Planta 234, 419–427 (2011). https://doi.org/10.1007/s00425-011-1452-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-011-1452-6

Keywords

Navigation