Skip to main content
SpringerLink
Log in

Recognition mechanisms during the pre-contact state of lichens: I. Mycobiont-photobiont interactions of the mycobiont of Fulgensia bracteata

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Lichens are an association of a photoautotrophic alga/cyanobacteria (photobiont) and a heterotrophic fungus (mycobiont) constituting the lichen thallus as a complex phenotype. Many mycobionts reproduce sexually and the ascospores are dispersed without the photobiont. For successful re-lichenization the specific photobiont must be recognized, contacted, and incorporated by the mycobiont. A so-called pre-contact stage has been postulated as the initial step of a gradual recognition process. In the present study, the effect of the specific Trebouxia photobiont, an unspecific Asterochloris photobiont and the non-lichenizing green alga Myrmecia bisecta on the development of the mycobiont Fulgensia bracteata was assessed by pre-contact assays. Three hypotheses were confirmed: (i) the pre-contact stage exists, (ii) it is characterized by morphological reactions in the development of the mycobiont, and (iii) the reactions depend on the interacting alga. Control conditions revealed a mycelial growth arrest but this effect was not observed in the presence of any of the three algae. Different algae induce distinct growth patterns with respect to hyphal length, morphological characteristics, and formation of mucilage. The specific Trebouxia photobiont had a positive impact on hyphal growth, branching frequency, and mucilage formation. These effects were less explicit with the non-specific Asterochloris photobiont. Myrmecia bisecta induced uncharacteristic growth patterns with pronounced hyphal growth and high numbers of aerial hyphae but less formation of mucilage. These results indicate that symbiont recognition mechanisms are established before physical contact. Pre-contact reactions may be an evolutionary advantage that supports the persistence of the mycobiont on newly colonized sites and improves the probability of re-lichenization.

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

Similar content being viewed by others

Abbreviations

ABP:

Algal binding protein

ITS rDNA:

Internal transcribed spacer ribosomal DNA

MYS1:

Malt yeast extract medium with 1 % sucrose

PPFD:

Photosynthetic photon flux density

SD:

Standard deviation

TOM:

Trebouxia Organic Medium

VAM:

Vesicular-arbuscular mycorrhiza

References

  • Ahmadjian V (1967) A guide to the algae occuring as lichen symbionts: Isolation, culture, cultural physiology, and identification. Phycol 6:127–160

    Article  CAS  Google Scholar 

  • Ahmadjian V (1982) Algal/fungal symbiosis. In: Round FE, Chapman DJ (eds) Progress in Physiological Research I. Elsevier, Amsterdam, pp 179–233

    Google Scholar 

  • Ahmadjian V (1992) Basic mechanism of signal exchange, recognition, and regulation in lichens. In: Reisser W (ed) Algae and Symbioses. Biopress Limited, Bristol, pp 675–697

    Google Scholar 

  • Ahmadjian V (1993) The Lichen Symbiosis. John Wiley & Sons, New York

    Google Scholar 

  • Ahmadjian V (2002) Trebouxia: Reflections on a perplexing and controversial lichen photobiont. In: Seckbach J (ed) Symbiosis: Mechanisms and Model Systems. Kluwer Academic Publishing, Dordrecht, Boston, pp 373–384

    Google Scholar 

  • Ahmadjian V, Jacobs JB (1981) Relationship between fungus and alga in the lichen Cladonia cristatella tuck. Nature 289(5794):169–172

    Article  Google Scholar 

  • Ahmadjian V, Jacobs JB (1983) Algal-fungal relationships in lichens: recognition, synthesis and development. In: Goff LJ (ed) Algal Symbiosis. Cambridge University Press, Cambridge, pp 147–172

    Google Scholar 

  • Ahmadjian V, Jacobs JB, Russell LA (1978) Scanning electron microscopy study of early lichen synthesis. Science, N.Y. 200:1062–1064

    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 

  • Beck A (1999) Photobiont inventory of a lichen community growing on heavy-metal rich rock. Lichenologist 31:501–510

    Google Scholar 

  • Beck A, Friedl T, Rambold G (1998) Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol 139:709–720

    Article  CAS  Google Scholar 

  • Beck A, Kasalicky G, Rambold G (2002) Myco-photobiontal selection in a mediterranean cryptogram community with Fulgensia fulgens. New Phytol 153:317–326

    Article  Google Scholar 

  • Belandria G, Asta J, Nurit F (1989) Effects of sulphur dioxide and fluoride on ascospore germination of several lichens. Lichenologist 21:79–86

    Article  Google Scholar 

  • Bubrick P, Galun M, Frensdorff A (1984) Observations on free-living Trebouxia de Puymaly and Pseudotrebouxia archibald, and evidence that both symbionts from Xanthoria parietina (L.) Th. Fr. can be found free-living in nature. New Phytol 97:455–462

    Article  Google Scholar 

  • Bubrick P, Galun M, Frensdorff A (1985) Proteins from the lichen Xanthoria parietina which bind to phycobiont cell walls. Isolation and partial purification of an algal-binding protein. Symbiosis 1:85–92

    CAS  Google Scholar 

  • Clayden SR (1998) Thallus initiation and development in the lichen Rhizocarpon lecanorinum. New Phytol 139:685–695

    Article  Google Scholar 

  • Daniels BA, Trappe JM (1980) Factors affecting spore germination of the vesicular-arbuscular mycorrhizal fungus Glomus epigaeus. Mycologia 72:457–471

    Article  CAS  Google Scholar 

  • De Priest PR, Piercey-Normore M, Sikaroodi M, Kärkäinen K, Oksanen I, Yahr R, Ahti T (2000) Phylogenetic relationships among sections of Cladonia and Cladina. In: Book of Abstracts, 14. The Fourth IAL Symposium, Progress and Problems in Lichenology at the Turn of the Millenium, Barcelona

  • Friedl T (1995) Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: a phylogenetic analysis of 18S ribosomal sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov.). J Phycol 31:632–639

    Article  CAS  Google Scholar 

  • Friedl T, Bhattacharya D (2002) Origin and evolution of green lichen algae. In: Seckbach J (ed) Symbiosis: Mechanisms and Model Systems. Kluwer Academic Publishers, Dordrecht, pp 341–357

    Google Scholar 

  • Friedl T, O’Kelly CJ (2002) Phylogenetic relationships of green algae assigned to the genus Planophila (Chlorophyta): evidence from 18S rDNA sequence data and ultrastructure. Eur J Phycol 37:373–384

    Article  Google Scholar 

  • Friedl T, Zeltner C (1994) Assessing the relationships of some coccoid green lichen algae and the microthamniales (Chlorophyta) with 18S rRNA gene sequence comparisons. J Phycol 30(3):500–506

    Article  CAS  Google Scholar 

  • Friedmann EI, Lipkin Y, Ocampo-Paus R (1967) Desert algae of the negev (Israel). Phycol 6:185–196

    Article  Google Scholar 

  • Galun M (1988) Lichenization. In: Galun M (ed) CRC Handbook of Lichenology, vol II. CRC Press, Boca Ranton, Florida, pp 153–169

    Google Scholar 

  • Galun M, Paran N, Ben-Shaul Y (1970) Structural modifications of the phycobiont in the lichen thallus. Protoplasma 96:85–96

    Article  Google Scholar 

  • Garty J, Delarea J (1987) Some initial stages in the formation of epilithic crustose lichens in nature: a SEM study. Symbiosis 3:49–56

    Google Scholar 

  • Giovanetti M (2002) Survival strategies in arbuscular mycorrhizal symbionts. In: Seckbach J (ed) Symbiosis: Mechanisms and Model Systems. Kluwer Academic Press, Dordrecht, pp 293–321

    Google Scholar 

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

    Article  Google Scholar 

  • Hawksworth DL (1988) The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot J Linnean Soc 96:3–20

    Article  Google Scholar 

  • Helms G, Friedl T, Rambold G, Mayrhofer H (2001) Identification of photobionts from lichen family Physciaceae using algal-specific IST rDNA sequencing. Lichenologist 33(1):73–86

    Article  Google Scholar 

  • Henssen A, Jahns HM (1974) Lichenes. Eine Einführung in die Flechtenkunde. Georg Thieme Verlag, Stuttgart

    Google Scholar 

  • Hepper CM, Smith GA (1976) Observations on the germination of Endogone spores. Trans Br Mycol Soc 66:189–194

    Article  Google Scholar 

  • Hill DJ (1989) The control of the cell cycle in microbal symbionts. New Phytol 112:175–184

    Article  Google Scholar 

  • Hill DJ (1992) The co-ordination of development in symbionts mutualistic symbiosis with reference to the cell cycle of the photobiont in lichens. Symbiosis 14:325–333

    Google Scholar 

  • Honegger R (1987) Questions about pattern formation in the algal layer of lichens with stratified (heteromerous) thalli. In: Peveling E (ed) Progress and Problems in Lichenology in the Eighties. Bibliotheca Lichenologica 25. Verlag J. Cramer: 59–71

  • Honegger R (1998) The lichen symbiosis – What is so spectacular about it? Lichenologist 30(3):193–212

    Google Scholar 

  • Ishida K, Green BR, Cavalier-Smith T (1999) Diversification of a chimaeric algal group, the chlorarachniophytes: phylogeny of nuclear and nucleomorph small-subunit rRNA genes. Mol Biol Evol 16(3):321–331

    Article  CAS  Google Scholar 

  • Ishii T, Narutaki A, Sawada K, Aikawa J, Matsumoto I, Kadoya K (1997) Growth stimulatory substances for vesicular-arbuscular mycorrhizal fungi in bahia grass (Paspalum notatum Flügge.) roots. Plant Soil 106:301–307

    Article  Google Scholar 

  • Jahns HM (1988) The lichen thallus. In: Galun M (ed) CRC Handbook of Lichenology, vol I. CRC Press, Boca Ranton, Florida, pp 95–143

    Google Scholar 

  • Joneson S, Lutzoni F (2009) Compatibility and thigmotropism in the lichen symbiosis: a reappraisal. Symbiosis 47:109–115

    Article  Google Scholar 

  • Jonesson S, Armaleo D, Lutzoni F (2011) Fungal and Algal gene expression in early developmental stages of lichen-symbiosis. Mycologia 103(2):291–306

    Article  Google Scholar 

  • Kardish N, Silberstein L, Fleminger G, Galun M (1991) Lectin from the lichen Nephroma laevigatum Ach localisation and function. Symbiosis 11:47–62

    CAS  Google Scholar 

  • Legaz ME, Fontaniella B, Millanes AM, Vicente C (2004) Secreted arginases from phylogenetically farrelated lichen species act as cross-recognition factors for two different algal cells. Eur J Cell Biol 83:1–12

    Article  Google Scholar 

  • Lehr H, Galun M, Ott S, Jahns HM, Fleminger G (2000) Cephalodia of the lichen Peltigera aphthosa (L.) wild. Specific recognition of the compatible photobiont. Symbiosis 29:357–365

    Google Scholar 

  • Meeßen J, Eppenstein S, Ott S (2013) Recognition mechanisms during the precontact state of lichens: II. Influence of algal exudates and ribitol on the response of the mycobiont of Fulgensia bracteata. Symbiosis. doi:10.1007/s13199-012-0219-6

  • Miao VPW, Manoharan SS, Snæbjarnarson V, Andrésson ÓS (2012) Expression of lec-1, a mycobiont gene encoding a galectin-like protein in the lichen Peltigera membranacea. Symbiosis. doi:10.1007/s13199-012-0175-1

  • Mosse B (1959) The regular germination of resting spores and some observations on the growth requirements of an Endogone sp. causing vesicular-arbuscular mycorrhiza. Trans Br Mycol Soc 42:273–286

    Article  Google Scholar 

  • Nelsen MP, Gargas A (2006) Actin type I introns offer potential for increasing phylogenetic resolution in Asterochloris (Chlorophyta, Trebouxiophyceae). Lichenologist 38:435–440

    Article  Google Scholar 

  • Ott S (1987) Sexual reproduction and developmental adaptations in Xanthoria parietina. Nord J Bot 7:219–228

    Article  Google Scholar 

  • Ott S, Zwoch I (1992) Ethylene production by lichens. Lichenologist 24(1):73–80

    Google Scholar 

  • Ott S, Meier T, Jahns HM (1995) Development, regeneration, and parasitic interactions between the lichens Fulgensia bracteata and Toninia caerulonigricans. Can J Bot 73(suppl 1):595–602

    Article  Google Scholar 

  • Ott S, Krieg T, Spanier U, Schieleit P (2000) Phytohormones in lichens with emphasis on ethylene biosynthesis and functional aspects on lichen symbiosis. Phyton 40:83–94

    CAS  Google Scholar 

  • Palmqvist K (2000) Carbon economy in lichens. Tansley Review No. 117. New Phytol 148:11–36

    Article  CAS  Google Scholar 

  • Richardson DHS (1973) Photosynthesis and carbohydrate movement. In: Ahmadjian V, Hale ME (eds) The Lichens. Academic, New York and London, pp 249–288

    Chapter  Google Scholar 

  • Richardson DHS, Hill DH, Smith DC (1968) Lichen physiology. XI. The role of the alga in determining the pattern of carbohydrate movement between lichen symbionts. New Phytol 67:469–486

    Article  CAS  Google Scholar 

  • Romeike J, Friedl T, Helms G, Ott S (2002) Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized Ascomycetes) along a transect of the Antarctic Peninsula. Mol Biol Evol 19(8):1209–1217

    Article  PubMed  CAS  Google Scholar 

  • Schaper GM, Ott S (2003) Photobiont selectivity and interspecific interactions in lichen communities. Culture experiments with the mycobiont Fulgensia bracteata. Plant Biol 5:441–450

    Article  Google Scholar 

  • Siqueira JO, Safir GR, Nair MG (1991) Stimulation of vesicular-arbuscular mycorrhiza formation and growth of white clover by flavonoid compounds. New Phytol 118:87–93

    Article  CAS  Google Scholar 

  • Smith AL (1921) Lichens. Cambridge University Press, Cambridge

    Google Scholar 

  • Smith DC, Douglas AE (1987) The Biology of Symbiosis. Edward Arnold Ltd, London, pp 113–145

    Google Scholar 

  • Tschermak-Woess E (1978) Myrmecia reticulata as a phycobiont and free-living – free-living Trebouxia – the problem of Stenocybe septata. Lichenologist 10:69–79

    Article  Google Scholar 

  • Tschermak-Woess E (1989) The algal partner. In: Galun M (ed) CRC Handbook of Lichenology, vol I. CRC Press, Boca Ranton, Florida, pp 39–92

    Google Scholar 

  • Van den Hoek C, Jahns HM, Mann DG (1995) Algen. 3. neubearbeitete Auflage. Georg Thieme Verlag, Stuttgart, New York: 341

  • Yahr R, Vilgalys R, De Priest PT (2004) Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Mol Ecol 13:3367–3378

    Article  PubMed  CAS  Google Scholar 

  • Yoshimura I, Yamamoto Y, Nakano T, Finnie J (2002) Isolation and culture of lichen photobionts and mycobionts. In: Krammer I, Beckett R, Varma A (eds) Protocols in Lichenology. Culturing, Biochemistry, Ecophysiology and Use in Biomonitoring. Springer, Berlin, pp 3–33

    Chapter  Google Scholar 

Download references

Acknowledgements

Our special thanks are due to Eva Posthoff for her invaluable technical support. The authors are very grateful to the Düsseldorf Entrepreneurs Foundation for financial support. We also thank David Richardson and Pete Convey for kindly improving the English language as well as for critical comments and suggestions. The results are included in the doctoral thesis of Joachim Meeßen. Thanks are also due to the anonymous reviewers for their comments.

Author information

Authors and Affiliations

  1. Institute of Botany, Heinrich-Heine-University, Universitaetsstr. 1, 40225, Duesseldorf, Germany

    Joachim Meeßen & Sieglinde Ott

Authors
  1. Joachim Meeßen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sieglinde Ott
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sieglinde Ott.

Additional information

Dedicated to Margalith Galun. In honour of her inspiring work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meeßen, J., Ott, S. Recognition mechanisms during the pre-contact state of lichens: I. Mycobiont-photobiont interactions of the mycobiont of Fulgensia bracteata . Symbiosis 59, 121–130 (2013). https://doi.org/10.1007/s13199-013-0232-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-013-0232-4

Keywords

Search

Navigation