Skip to main content
SpringerLink
Log in

Identification of genes involved in fungal responses to strigolactones using mutants from fungal pathogens

  • Original Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

Strigolactones (SLs) as components of root exudates induce hyphal branching of arbuscular mycorrhizal (AM) fungi which is thought to favor the establishment of the beneficial symbiosis. Little is known on how AM fungi respond to SLs. Since AM fungi are poor model systems due to their obligate biotrophism and the lack of genetic transformation protocols, we took advantage of the sensitivity of several phytopathogenic fungi to GR24, a synthetic SLs analog. With the aim to identify the molecular determinants involved in SLs response in AM fungi and assuming conserved mechanisms in the fungal kingdom, we exploited the fungal pathogens Botrytis cinerea and Cryphonectria parasitica, for which mutant collections are available. Exposure of B. cinerea and C. parasitica to GR24 embedded in solid medium led to reduction of fungal radial growth. We set up the screening of a set of well-characterized gene deletion mutants to isolate genotypes with altered responses to SLs. Two B. cinerea mutants (defective of BcTrr1, a thioredoxin reductase and BcLTF1, a GATA transcription factor) turned out to be less responsive to GR24. One feature shared by the two mutants is the overproduction of reactive oxygen species (ROS). Indeed, an oxidizing effect was observed in a B. cinerea strain expressing a redox-sensitive GFP2 in the mitochondrial intermembrane space upon exposure to GR24. ROS and mitochondria are, therefore, emerging as mediators of SLs actions.

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

Access this article

Log in via an institution

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

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

    Article  CAS  PubMed  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Babili S, Bouwmeester HJ (2015) Strigolactones, a novel carotenoid-derived plant hormone. Annu Rev Plant Biol 66:161–186

    Article  CAS  PubMed  Google Scholar 

  • Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP, Couloux A, Coutinho PM, de Vries RP, Dyer PS, Fillinger S, Fournier E, Gout L, Hahn M, Kohn L et al (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7(8):e1002230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arnér S, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109

    Article  PubMed  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 Pest Sci 33(2):138–145

    Article  CAS  Google Scholar 

  • Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S et al (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247

    Article  CAS  Google Scholar 

  • Besserer A, Becard G, Roux C, Jauneau A, Sejanon-Delmas N (2008) GR24, a synthetic analogue of strigolactones, stimulates mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energetic metabolism. Plant Physiol 148:402–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48

    Article  PubMed  Google Scholar 

  • Bonfante P, Genre A (2015) Arbuscular mycorrhizal dialogues: do you speak “plantish” or “fungish”? Trends Plant Sci 20(3):150–154

    Article  CAS  PubMed  Google Scholar 

  • Brewer PB, Koltai H, Beveridge CA (2013) Diverse roles of strigolactones in plant development. Mol Plant 6:18–28

    Article  CAS  PubMed  Google Scholar 

  • Büttner P, Koch F, Voigt K, Quidde T, Risch S, Blaich R, Brückner B, Tudzynski P (1994) Variations in ploidy among isolates of Botrytis cinerea: implications for genetic and molecular analyses. Curr Genet 25(5):445–450

  • Cavar S, Zwanenburg B, Tarkowski P (2014) Strigolactones: occurrence, structure, and biological activity in the rhizosphere. Phytochem Rev 14(4):691–711

    Article  Google Scholar 

  • Colot HV, Park G, Turner GE, Ringelberg C, Crew CM, Litvinkova L, Weiss RL, Borkovich KA, Dunlap JC (2006) A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. PNAS 103:10352–10357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Saint Germain A, Bonhomme S, Boyer FD, Rameau C (2013) Novel insights into strigolactone distribution and signaling. Curr Opin Plant Biol 163(2):1012–1025

    Google Scholar 

  • Döhlemann G, Berndt P, Hahn M (2006) Different signalling pathways involving a Galpha protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol Microbiol 59(3):821–835

  • Dor E, Joel DM, Koltai YKH, Hershenhorn J (2011) The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi. Planta 234:419–427

    Article  CAS  PubMed  Google Scholar 

  • Foo E, Blake SN, Fisher BJ, Smith JA, Reid JB (2016) The role of strigolactones during plant interactions with the pathogenic fungus Fusarium oxysporum. Planta 243(6):1387–1396

    Article  CAS  PubMed  Google Scholar 

  • Garcìa-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, Balzergue C, Puech-Pagég V, Novero M, Rey T, Fournier J, Rochange S, Bécard B, Bonfante 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

    Article  PubMed  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(8):519–530

    Article  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 22:1–6

    Article  Google Scholar 

  • Gronover CS, Kasulke D, Tudzynski P, Tudzynski B (2001) The role of G protein alpha subunits in the infection process of the gray mold fungus Botrytis cinerea. Mol Plant Microbe Interact. 14(11):1293–1302

  • Gronover CS, Schumacher J, Hantsch P, Tudzynski B (2005) A novel seven-helix transmembrane protein BTP1 of Botrytis cinerea controls the expression of GST-encoding genes, but is not essential for pathogenicity. Mol Plant Pathol 6(3):243–256

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

    Article  CAS  Google Scholar 

  • Hamm H, Gilchrist A (1996) Heterotrimeric G proteins. Curr Opin Cell Biol 8189:196

    Google Scholar 

  • Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9

    Google Scholar 

  • Harren K, Schumacher J, Tudzynski B (2012) The Ca2+/calcineurin-dependent signaling pathway in the gray mold Botrytis cinerea: the role of calcipressin in modulating calcineurin activity. PLoS One 7(7):e41761

  • Heller J, Meyer AJ, Tudzynski P (2012) Redox-sensitive GFP2: use of the genetically encoded biosensor of the redox status in the filamentous fungus Botrytis cinerea. Mol Plant Pathol 13(8):935–947

    Article  CAS  PubMed  Google Scholar 

  • Klimpel A, Gronover CS, Williamson B, Stewart JA, Tudzynski B (2002) The adenylate cyclase (BAC) in Botrytis cinerea is required for full pathogenicity. Mol Plant Pathol 3(6):439–450

  • 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 

  • Lanfranco L, Young JPW (2012) Genetic and genomic glimpses of the elusive arbuscular mycorrhizal fungi. Curr Opin Plant Biol 15(4):454–461

    Article  CAS  PubMed  Google Scholar 

  • Li L, Wright SJ, Krystofova S, Park G, Borkovich KA (2007) Heterotrimeric G protein signaling in filamentous fungi. Annu Rev Microbiol 61:423–452

    Article  CAS  PubMed  Google Scholar 

  • Lin K, Limpens E, Zhang ZH, Ivanov S, Saunders DGO, Mu DS et al (2014) Single nucleus genome sequencing reveals high similarity among nuclei of an endomycorrhizal fungus. PLoS Genet 10:e1004078

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu J, Lovisolo C, Schubert A, Cardinale F (2013) Signaling role of strigolactones at the interface between plants, (micro)organisms, and a changing environment. J Plant Interact 8(1):17–33

    Article  CAS  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 

  • Marschall R, Schumacher J, Siegmund U, Tudzynski P (2016) Chasing stress signals––exposure to extracellular stimuli differentially affects the redox state of cell compartments in the wild type and signaling mutants of Botrytis cinerea. Fungal Genet Biol 90(2016):12–22

    Article  CAS  PubMed  Google Scholar 

  • Michielse CB, Becker M, Heller J, Moraga J, Collado IG, Tudzynski P (2011) The Botrytis cinerea Reg1 protein, a putative transcriptional regulator, is required for pathogenicity, conidiogenesis, and the production of secondary metabolites. Mol Plant Microbe Interact 24(9):1074–1085

  • Moretti M, Rossi M, Ciuffo N, Turina M (2014) Functional characterization of the three mitogen-activated protein kinase kinases (MAP2Ks) present in the Cryphonectria parasitica genome reveals the necessity of Cpkk1 and Cpkk2, but not Cpkk3, for pathogenesis on chestnut (Castanea spp.). Mol Plant Pathol 15(5):500–512

    Article  CAS  PubMed  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

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Nagahashi G, Douds DD, Ferhatoglu Y (2010) Functional categories of root exudate compounds and their relevance to AM fungal growth. In: Arbuscular mycorrhizas physiology and function. Springer,Netherlands pp 33–56

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

    Article  CAS  PubMed  Google Scholar 

  • Pontecorvo G, Roper JA, Hemmons LM, MacDonald KD, Bufton AW (1953) The genetics of Aspergillus nidulans. Adv Genet 5:141–238

    CAS  PubMed  Google Scholar 

  • Prandi C, Occhiato EG, Tabasso S, Bonfante P, Novero M, Scarpi D, Bova ME, Miletto I (2011) New potent fluorescent analogues of strigolactones: synthesis and biological activity in parasitic weed germination and fungal branching. Eur J Org Chem 2011(20-21):3781–3793

  • Quidde T, Buttner P, Tudzynski P (1999) Evidence for three different specific saponin-detoxifying activities in Botrytis cinerea and cloning and functional analysis of a gene coding for a putative avenacinase. Eur J Plant Pathol 105:273–283

    Article  CAS  Google Scholar 

  • Rasmussen A, Depuydt S, Goormachtig S, Geelen D (2013) Strigolactones fine-tune the root system. Planta 238:615–626

    Article  CAS  PubMed  Google Scholar 

  • Requena N, Helber N (2007) 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

    PubMed  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, Al-Babili S, van der Krol S, Bouwmeester HJ (2013) The biology of strigolactones. Trends Plant Sci 18:72–83

    Article  CAS  PubMed  Google Scholar 

  • Sabbagh SK (2011) Effect of GR24, a synthetic analogue of strigolactones, on gene expression of solopathogenic strain of Sporisorium reilianum. Afr J Biotechnol 10(70):15739–15743

    Article  CAS  Google Scholar 

  • Sabbagh SK, Mazaheri M, Penjenhken N, Salari M (2012) Transcriptomic analysis of Sporisorium reilianum in response to the strigolactone analogue GR24. Phytopathol Mediterr 51(2):283–291

    CAS  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

  • Scaffidi A, Waters MT, Sun YK, Skelton BW, Dixon KW, Ghisalberti EL, Flematti GR, Smith SM (2014) Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol 165:1221–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmitz AM, Harrison MJ (2015) Signaling events during initiation of arbuscular mycorrhizal symbiosis. J Integr Plant Biol 56(3):250–261

    Article  Google Scholar 

  • Schumacher J (2015) DHN melanin biosynthesis in the plant pathogenic fungus Botrytis cinerea is based on two developmentally regulated key enzyme (PKS)-encoding genes. Mol Microbiol 99(4):729–748

    Article  PubMed  Google Scholar 

  • Schumacher J, Pradier JM, Simon A, Traeger S, Moraga J, Collado IG, Viaud M, Tudzynski B (2012) Natural variation in the VELVET gene bcvel1 affects virulence and light-dependent differentiation in Botrytis cinerea. PLoS Genet 7(10):e47840

  • Schumacher J, Viaud M, Simon A, Tudzynski B (2008a) The G alpha subunit BCG1, the phospholipase C (BcPLC1) and the calcineurin phosphatase co-ordinately regulate gene expression in the grey mould fungus Botrytis cinerea. Mol Microbiol 67(5):1027–1050

  • Schumacher J, Kokkelink L, Huesmann C, Jimenez-Teja D, Collado IG, Barakat R, Tudzynski P, Tudzynski B (2008b) The cAMP-dependent signaling pathway and its role in conidial germination, growth, and virulence of the gray mold Botrytis cinerea. Mol Plant Microbe Interact 21(11):1443–1459

  • Schumacher J, Simon A, Cohrs KC, Viaud M, Tudzynski P (2014) The transcription factor BcLTF1 regulates virulence and light responses in the necrotrophic plant pathogen Botrytis cinerea. PLoS Genet 10(1):e1004040

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulze Gronover C, Schorn C, Tudzynski B (2004) Identification of Botrytis cinerea genes up-regulated during infection and controlled by the G alpha subunit BCG1 using suppression subtractive hybridization (SSH). Mol Plant Microbe Interact 17(5):537–546

  • Segmüller N, Ellendorf U, Tudzynski B, Tudzynski P (2007) BcSAK1, a stress-activated mitogen-activated protein kinase, is involved in vegetative differentiation and pathogenicity in Botrytis cinerea. Eukaryot Cell 6(2):211–221

  • Segmüller N, Kokkelink L, Giesbert S, Odinius D, van Kan J, Tudzynski P (2008) NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol Plant Microbe Interact 21(6):808–819

  • Siegmund U, Heller J, van Kan JA, Tudzynski P (2013) The NADPH oxidase complexes in Botrytis cinerea: evidence for a close association with the ER and the tetraspanin Pls1. PLoS One 8(2):e55879

  • Siegmund U, Marschall R, Tudzynski P (2015) BcNoxD, a putative ER protein, is a new component of the NADPH oxidase complex in Botrytis cinerea. Mol Microbiol 95(6):988–1005

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

    Article  CAS  PubMed  Google Scholar 

  • Temme N, Oeser B, Massaroli M, Heller J, Simon A, Collado IG, Viaud M, Tudzynski P (2012) BcAtf1, a global regulator, controls various differentiation processes and phytotoxin production in Botrytis cinerea. Mol Plant Pathol 13(7):704–718

  • Temme N, Tudzynski P (2009) Does Botrytis cinerea ignore H2O2-induced oxidative stress during infection? Characterization of botrytis activator protein 1. Mol Plant Microbe Interact 22(8):987–998

  • Tisserant E, Malbreil M, Kuo A, Kohler A, Symeonidi A, Balestrini R, Charron P, Duensing N, dit Frey NF, 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, Becard G, Bonfante P, Paszkowski U, Shachar-Hill YY, Tuskan GA, Young PW, 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 USA 110:20117–20122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15(2):211–216

    Article  CAS  PubMed  Google Scholar 

  • Van der Heijden MGA, Martin F, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present and the future. New Phytol 205:1406–1423

    Article  PubMed  Google Scholar 

  • Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pêcheur P, Kunduru AR, Leroux P, Legendre L. (2006) A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Mol Plant Microbe Interact 19(9):1042–1050

  • Viefhues A, Heller J, Temme N, Tudzynski P (2014) Redox systems in Botrytis cinerea: impact on development and virulence. Mol Plant-Microbe Interact 27(8):858–874

    Article  CAS  PubMed  Google Scholar 

  • Viefhues A, Schlathoelter I, Simon A, Viaud M, Tudzynski P (2015) Unraveling the function of the response regulator BcSkn7 in the stress signaling network of Botrytis cinerea. Eukaryot Cell 14(7):636–651

  • Xie X, Yoneyama K, Kisugi T, Uchida K, Ito S et al (2013) Confirming stereochemical structures of strigolactones produced by rice and tobacco. Mol Plant 6:153–163

    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 

  • Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactones production and exudation? Planta 235(6):1197–1207

    Article  CAS  PubMed  Google Scholar 

  • Young JP (2015) Genome diversity in arbuscular mycorrhizal fungi. Curr Opin Plant Biol 26:113–119

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Campbell M, Murphy J, Lam S, Xu JR (2000) The BMP1 gene is essential for pathogenicity in the gray mold fungus Botrytis cinerea. Mol Plant Microbe Interact 13(7):724–732

  • Zwanenburg B, Zeljkovic SC, Pospisil T (2016a) Synthesis of strigolactones, a strategic account. Pest Manag Sci 72:637

    Article  CAS  PubMed  Google Scholar 

  • Zwanenburg B, Pospisil T, Zeljkovic SC (2016b) Strigolactones: new plant hormones in action. Planta 243:1311–1326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This research was funded by SLEPS and 60 % Projects (University of Torino) to LL and CP and part of the research was supported by COST Action FA1206 STREAM, supported by COST (European Cooperation in Science and Technology). We would like to thank Massimo Turina for the C. parasitica strains, Mara Novero and Luca Musselli for technical assistance and Francesca Cardinale for fruitful discussions. We thank Julia Schumacher for discussion and providing the strains of B. cinerea.

Author information

Authors and Affiliations

  1. Department of Life Sciences and Systems Biology, University of Torino, Viale Mattioli 25, 10125, Turin, Italy

    S. Belmondo & L. Lanfranco

  2. Institut für Biologie und Biotechnologie der Pflanzen, Westf. Wilhelms-Universität Münster, Schlossplatz 8, 48143, Münster, Germany

    R. Marschall & P. Tudzynski

  3. Soil Microbiology and Symbiotic Systems’ Estacion Experimental del Zaidin (CSIC), Profesor Albareda 1, 18008, Granada, Spain

    J. A. López Ráez

  4. Department of Chemistry, University of Torino, via Giuria 7, 10125, Turin, Italy

    E. Artuso & C. Prandi

  5. Center for Molecular Systems Biology, University of Torino, Viale Mattioli 25, 10125, Turin, Italy

    L. Lanfranco

Authors
  1. S. Belmondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Marschall
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Tudzynski
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. A. López Ráez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Artuso
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Prandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. L. Lanfranco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Lanfranco.

Additional information

Communicated by M. Kupiec.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 94 kb)

Supplementary material 2 (PDF 2977 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Belmondo, S., Marschall, R., Tudzynski, P. et al. Identification of genes involved in fungal responses to strigolactones using mutants from fungal pathogens. Curr Genet 63, 201–213 (2017). https://doi.org/10.1007/s00294-016-0626-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-016-0626-y

Keywords

Search

Navigation