Skip to main content
SpringerLink
Log in

The role of pre-symbiotic auxin signaling in ectendomycorrhiza formation between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

The ectendomycorrhizal fungus Terfezia boudieri is known to secrete auxin. While some of the effects of fungal auxin on the plant root system have been described, a comprehensive understanding is still lacking. A dual culture system to study pre mycorrhizal signal exchange revealed previously unrecognized root–fungus interaction mediated by the fungal auxin. The secreted fungal auxin induced negative taproot gravitropism, attenuated taproot growth rate, and inhibited initial host development. Auxin also induced expression of Arabidopsis carriers AUX1 and PIN1, both of which are involved in the gravitropic response. Exogenous application of auxin led to a root phenotype, which fully mimicked that induced by ectomycorrhizal fungi. Co-cultivation of Arabidopsis auxin receptor mutants tir1-1, tir1-1 afb2-3, tir1-1 afb1-3 afb2-3, and tir1-1 afb2-3 afb3-4 with Terfezia confirmed that auxin induces the observed root phenotype. The finding that auxin both induces taproot deviation from the gravity axis and coordinates growth rate is new. We propose a model in which the fungal auxin induces horizontal root development, as well as the coordination of growth rates between partners, along with the known auxin effect on lateral root induction that increases the availability of accessible sites for colonization at the soil plane of fungal spore abundance. Thus, the newly observed responses described here of the root to Terfezia contribute to a successful encounter between symbionts.

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

  • Barker SJ, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144–154

    CAS  PubMed  Google Scholar 

  • Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2013) SCFTIR1/AFB-auxin signaling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32:260–274

    Article  CAS  PubMed  PubMed Central  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 

  • Blancaflor EB, Masson PH (2003) Plant gravitropism. Unraveling the ups and downs of a complex process. Plant Physiol 133:1677–1690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482:103–6

    Article  CAS  PubMed  Google Scholar 

  • Buer CS, Sukumar P, Muday GK (2006) Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol 140:1384–1396

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campanoni P, Nick P (2005) Auxin-dependent cell division and cell elongation. 1-Naphthaleneacetic acid and 2,4-dichlorophenoxyacetic acid activate different pathways. Plant Physiol 137:939–948

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ditengou FA, Lapeyrie F (2000) Hypaphorine from the ectomycorrhizal fungus Pisolithus tinctorius counteracts activities of indole-3-acetic acid and ethylene but not synthetic auxins in eucalypt seedlings. Mol Plant Microbe Interact 13:151–158

    Article  CAS  PubMed  Google Scholar 

  • Ditengou FA, Béguiristain T, Lapeyrie F (2000) Root hair elongation is inhibited by hypaphorine, the indole alkaloid from the ectomycorrhizal fungus Pisolithus tinctorius, and restored by indole-3-acetic acid. Planta 211:722–728

    Article  CAS  PubMed  Google Scholar 

  • Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legué V (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol 151:1991–2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gay G, Normand L, Marmeisse R, Sotta B, Debaud JC (1994) Auxin overproducer mutants of hebeloma cylindrosporum romagnesi have increased mycorrhizal activity. New Phytol 128:645–657

    Article  CAS  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    Article  CAS  PubMed  Google Scholar 

  • Herrmann S, Oelmüller R, Buscot F (2004) Manipulation of the onset of ectomycorrhiza formation by indole-3-acetic acid, activated charcoal or relative humidity in the association between oak microcuttings and Piloderma croceum: influence on plant development and photosynthesis. J Plant Physiol 161:509–517

    Article  CAS  PubMed  Google Scholar 

  • Horan DP, Chilvers GA, Lapeyrie FF (1988) Time sequence of the infection process in eucalypt ectomycorrhizas. New Phytol 109:451–458

    Article  Google Scholar 

  • Jung JKH, McCouch S (2013) Getting to the roots of it: genetic and hormonal control of root architecture. Front Plant Sci 4:186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kagan-Zur V, Zaretsky M, Sitrit Y, Roth-Bejerano N (2008) Hypogeous pezizaceae: physiology and molecular genetics. In: Varma A (ed) Mycorrhiza. Springer, Berlin, pp 161–183

    Chapter  Google Scholar 

  • Kagan-Zur V, Turgeman T, Roth-Bejerano N, Morte A, Sitrit Y (2014) Benefits conferred on plants. In: Kagan-Zur V, Roth-Bejerano N, Sitrit Y, Morte A (eds) Desert truffles. Soil biology. Springer-Verlag, Berlin Heidelberg, pp 93–104

    Chapter  Google Scholar 

  • Koren D, Resnick N, Mayzlish Gati E, Belausov E, Weininger S, Kapulnik Y, Koltai H (2013) Strigolactone signaling in the endodermis is sufficient to restore root responses and involves SHORT HYPOCOTYL 2 (SHY2) activity. New Phytol 198:866–74

    Article  CAS  PubMed  Google Scholar 

  • Lewis DR, Miller ND, Splitt BL, Guosheng Wu G, Spalding EP (2007) Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19:1838–1850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macdougal DT, Dufrenoy J (1944) Mycorrhizal symbiosis in aplectrum, corallorhiza and Pinus. Plant Physiol 19:440–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchant A, Kargul J, May S, Muller P, Delbarre A, Perrot-Rechenmann C, Bennett MJ (1999) AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–2073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, Sandberg G (2002) AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 14:589–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2001) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154

    Article  CAS  Google Scholar 

  • Mayzlish-Gati E, LekKala SP, Resnick N, Wininger S, Bhattacharya C, Lemcoff JH, Kapulnik Y, Koltai H (2010) Strigolactones are positive regulators of light-harvesting genes in tomato. J Exp Bot 61:3129–3136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morita MT (2010) Directional gravity sensing in gravitropism. Annu Rev Plant Biol 61:705–20

    Article  CAS  PubMed  Google Scholar 

  • Morte A, Lovisolo C, Schubert A (2000) Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense-Terfezia claveryi. Mycorrhiza 10:115–119

    Article  CAS  Google Scholar 

  • Morte A, Navarro-Ródenas A, Nicolás E (2010) Physiological parameters of desert truffle mycorrhizal helianthemun almeriense plants cultivated in orchards under water deficit conditions. Symbiosis 52:133–139

    Article  Google Scholar 

  • Niemi K, Vuorinen T, Ernstsen A, Haggmane H (2002) Ectomycorrhizal fungi and exogenous auxins influence root and mycorrhiza formation of Scots pine hypocotyl cuttings in vitro. Tree Physiol 22:1231–1239

    Article  CAS  PubMed  Google Scholar 

  • Rahman A, Takahashi M, Shibasaki K, Wu S, Inaba T, Tsurumi S, Baskin TI (2010) Gravitropism of Arabidopsis thaliana roots requires the polarization of PIN2 toward the root tip in meristematic cortical cells. Plant Cell 22:1762–1776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raudaskoski M, Kothe E (2014) Novel findings on the role of signal exchange in arbuscular and ectomycorrhizal symbioses. Mycorrhiza 25:243–52

    Article  PubMed  Google Scholar 

  • Rigas S, Ditengou FA, Ljung K, Daras G, Tietz O, Palme K, Hatzopoulos P (2013) Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol 197:1130–1141

    Article  CAS  PubMed  Google Scholar 

  • Rincón A, Priha O, Sotta B, Bonnet M, Le Tacon F (2003) Comparative effects of auxin transport inhibitors on rhizogenesis and mycorrhizal establishment of spruce seedlings inoculated with Laccaria bicolor. Tree Physiol 23:785–791

    Article  PubMed  Google Scholar 

  • Rosquete MR, von Wangenheim D, Marhavý P, Barbez E, Stelzer EH, Benková E, Maizel A, Kleine-Vehn J (2013) An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr Biol 23:817–22

    Article  CAS  PubMed  Google Scholar 

  • Rudawska ML, Kieliszewska-Rokicka B (1997) Mycorrhizal formation by Paxillus involutus strains in relation to their IAA-synthesizing activity. New Phytol 137:509–517

    Article  CAS  Google Scholar 

  • Saul-Tchrkas V, Steingerger Y (2011) Soil microbial diversity in the vicinity of a Negev desert shrub - reaumuria negevensis. Microb Ecol 61:64–81

    Article  Google Scholar 

  • Scheitz K, Lüthen H, Schenck D (2013) Rapid auxin-induced root growth inhibition requires the TIR and AFB auxin receptors. Planta 238:1171–1176

    Article  CAS  PubMed  Google Scholar 

  • Sitrit Y, Roth-Bejerano N, Kagan-Zur V, Turgeman T (2014) Pre-symbiotic interactions between the desert truffle Terfezia boudieri and its host plant Helianthemum sessiliflorum. In: Kagan-Zur V, Roth-Bejerano N, Sitrit Y, Morte A (eds) Desert truffles. Soil biology. Springer-Verlag, Berlin Heidelberg, pp 81–92

    Chapter  Google Scholar 

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

    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  PubMed Central  Google Scholar 

  • Sukumar P, Legué V, Vayssières A, Martin F, Tuskan GA, Kalluri UC (2013) Involvement of auxin pathways in modulating root architecture during beneficial plant-microorganism interactions. Plant Cell Environ 36:909–19

    Article  CAS  PubMed  Google Scholar 

  • Turgeman T, Ben Asher J, Roth-Bejerano N, Kagan-Zur V, Kapulnik Y, Sitrit Y (2011) Mycorrhizal association between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum alters plant physiology and fitness to arid conditions. Mycorrhiza 21:623–630

    Article  CAS  PubMed  Google Scholar 

  • Zaretsky M, Kagan-Zur V, Mills D, Roth-Bejerano N (2006a) Analysis of mycorrhizal associations formed by cistus incanus transformed root clones with Terfezia boudieri isolates. Plant Cell Rep 25:62–70

    Article  CAS  PubMed  Google Scholar 

  • Zaretsky M, Sitrit Y, Mills D, Roth-Bejerano N, Kagan-Zur V (2006b) Differential expression of fungal genes at preinfection and mycorrhiza establishment between Terfezia boudieri isolates and cistus incanus hairy root clones. New Phytol 171:837–846

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The Israeli Ministry of Science (grant numbers 4766, 3–9139) and The Chief Scientist of The Israeli Ministry of Agriculture (grant number 857-0626-11) supported this work.

Author information

Authors and Affiliations

  1. The Jacob Blaustein Institute for Desert Research, Ben-Gurion University of the Negev, Beer-Sheva, 84105, Israel

    Tidhar Turgeman & Yaron Sitrit

  2. Life Sciences Department, Ben-Gurion University of the Negev, 84105, Beer-Sheva, Israel

    Olga Lubinsky, Nurit Roth-Bejerano & Varda Kagan-Zur

  3. Institute of Plant Sciences, Agricultural Research Organization, Volcani Center, Bet-Dagan, 50250, Israel

    Yoram Kapulnik & Hinanit Koltai

  4. Agricultural Research Organization, Gilat Research Center, 85280, Beer-Sheva, Israel

    Eli Zaady

  5. Department of Biochemistry and Pharmacology, Faculty of Health Sciences, Ben-Gurion University of the Negev, 84105, Beer-Sheva, Israel

    Shimon Ben-Shabat

  6. Desert Agro-Research Center, Ramat-Negev R & D, D.N, 85515, Halutza, Israel

    Ofer Guy

  7. Department of Vegetable Crops, Newe Yaár Research Center, Agricultural Research Organization, P.O. Box 1021, Ramat Yishay, Israel

    Efraim Lewinsohn

Authors
  1. Tidhar Turgeman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olga Lubinsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nurit Roth-Bejerano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Varda Kagan-Zur
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoram Kapulnik
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hinanit Koltai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Eli Zaady
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shimon Ben-Shabat
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ofer Guy
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Efraim Lewinsohn
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yaron Sitrit
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yaron Sitrit.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Turgeman, T., Lubinsky, O., Roth-Bejerano, N. et al. The role of pre-symbiotic auxin signaling in ectendomycorrhiza formation between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum . Mycorrhiza 26, 287–297 (2016). https://doi.org/10.1007/s00572-015-0667-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-015-0667-y

Keywords

Search

Navigation