Metabolic Interactions at the Mycobiont-Photobiont Interface in Lichens

  • R. Honegger
Part of the The Mycota book series (MYCOTA, volume 5)

Abstract

Lichen-forming fungi are, like plant pathogens or mycorrhizal fungi, a polyphyletic, taxonomically heterogeneous group of nutritional specialists (Table 1; Gargas et al. 1995). As ecologically obligate biotrophs, they acquire fixed carbon from a population of minute, extracellularly located algal and/or cyanobacterial cells. In contrast to pathogenic interactions of fungi and fungus-like organisms with unicellular algae (e.g., van Donk and Bruning 1992), the photobiont cells of lichen thalli are not severely damaged by the fungal partner. Geosiphon pyriforme, the only known fungal (zygomycetous) symbiosis with an intracellularly located cyanobacterium (Nostoc sp.; Mollenhauer 1992), is not normally considered as a lichen.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahmadjian V, Jacobs JB (1981) Relationship between fungus and alga in the lichen Cladonia cristatella Tuck. Nature 389: 169–172CrossRefGoogle Scholar
  2. Brown DH (1991) Lichen mineral studies — currently clarified or confused. Symbiosis 11: 207–223Google Scholar
  3. Brown DH, Rapsch S, Beckett A, Ascaso C (1987) The effect of desiccation on cell shape in the lichen Parmelia sulcata Taylor. New Phytol 105: 295–299CrossRefGoogle Scholar
  4. Bubrick P, Frensdorff A, Galun M (1985) Selectivity in the lichen symbiosis. In: Brown DH (ed) Lichen physiology and cell biology. Plenum, New York, pp 319–334CrossRefGoogle Scholar
  5. Büdel B (1992) Taxonomy of lichenized procaryotic blue-green algae. In: Reisser W (ed) Algae and symbioses. Plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 301–324Google Scholar
  6. Crittenden PD, Katucka I, Oliver E (1994) Does nitrogen supply limit the growth of lichens? Cryptogam Bot 4: 143–155Google Scholar
  7. deBary A (1866) Morphologie und Physiologie der Pilze, Flechten und Myxomyceten. W Engelmann, LeipzigGoogle Scholar
  8. deVries OMH, Fekkes MP, Wösten HAB, Wessels JGH (1993) Insoluble hydrophobin complexes in the walls of Schizophyllum commune and other filamentous fungi. Arch Microbiol 159: 330–335CrossRefGoogle Scholar
  9. Dudley SA, Lechowicz MJ (1987) Losses of polyol through leaching in subarctic lichens. Plant Physiol 83: 813–815PubMedCrossRefGoogle Scholar
  10. Englund B (1977) The physiology of the lichen Peltigera aphthosa, with special reference to the blue-green phycobiont (Nostoc sp.). Physiol Plant 41: 298–304CrossRefGoogle Scholar
  11. Fahselt D (1994a) Secondary biochemistry of lichens. Symbiosis 16: 117–165Google Scholar
  12. Fahselt D (1994b) Carbon metabolism in lichens. Symbiosis 17: 127–182Google Scholar
  13. Farrar JF (1988) Physiological buffering. In: Galun M (ed) CRC Handbook of lichenology, vol 2. CRC Press, Boca Raton, pp 101–105Google Scholar
  14. Feige GB, Niemann L, Jahnke S (1990) Lichens and mosses–silent chronists of the Chernobyl accident. Bibl Lichenol 38: 63–77Google Scholar
  15. Fiechter E (1990) Thallusdifferenzierung und intrathalline Sekundärstoffverteilung bei Parmeliaceae (Lecanorales, lichenisierte Ascomyceten). Inaugural-Dissertation, Philosophische Fakultät I I, Universität Zürich, ZürichGoogle Scholar
  16. Friedl T (1989) Systematik und Biologie von Trebouxia (Microthamniales, Chlorophyta) als Phycobiont der Parmeliaceae (lichenisierte Ascomyceten). Inaugural-Dissertation, Fak Biol, Universität Bayreuth, BayreuthGoogle Scholar
  17. Friedl T (1995) Inferring taxonomic positions and testing genus level assignments in coccoid lichen algae: a phylogenetic analysis of 18s ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae cl. nov.). J Phycol 31: 632–639CrossRefGoogle Scholar
  18. Friedl T, Zeltner C (1994) Assessing the relationships of lichen algae and the Microthamniales (Chlorophyta) with 18S rRNA gene sequence comparisons. J Phycol 30: 500–506CrossRefGoogle Scholar
  19. Gargas A, Depriest PT, Grube M, Tehler A (1995) Multiple origins of lichen symbioses in fungi suggested by SSU rDNA phylogeny. Science 268: 1492–1495PubMedCrossRefGoogle Scholar
  20. Gärtner G (1992) Taxonomy of symbiotic eucaryotic algae. In: Reisser W (ed) Algae and symbioses. Plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 325–338Google Scholar
  21. Hawksworth DL (1988a) The fungal partner. In: Galun M (ed) CRC Handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 35–38Google Scholar
  22. Hawksworth DL (1988b) Effects of algae and lichen-forming fungi on tropical crops. In: Agnihotry VP, Sarbhoy KA, Kumar D (eds) Perspectives of mycopathology. Malhotra Publishing House, New Delhi, pp 76–83Google Scholar
  23. Hawksworth DL, Hill DJ (1984) The lichen-forming fungi. Blackie, GlasgowCrossRefGoogle Scholar
  24. Hawksworth DL, Honegger R (1994) The lichen thallus: a symbiotic phenotype of nutritionally specialized fungi and its response to gall producers. In: Williams MAJ (ed) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford, pp 77–98Google Scholar
  25. Hill DJ (1985) Changes in photobiont dimensions and numbers during co-development of lichen symbionts. In: Brown DH (ed) Lichen physiology and cell biology. Plenum, New York, pp 303–317CrossRefGoogle Scholar
  26. Hill DJ (1989) The control of the cell cycle in microbial symbionts. New Phytol 112: 175–184CrossRefGoogle Scholar
  27. Honegger R (1984) Cytological aspects of the mycobiontphycobiont relationship in lichens. Haustorial types, phycobiont cell wall types, and the ultrastructure of the cell wall surface layers in some cultured and symbiotic myco- and phycobionts. Lichenologist 16: 111–127CrossRefGoogle Scholar
  28. Honegger R (1985) Fine structure of different types of symbiotic relationships in lichens. In: Brown DH (ed) Lichen physiology and cell biology. Plenum Press, New York, pp 287–302CrossRefGoogle Scholar
  29. Honegger R (1986a) Ultrastructural studies in lichens. I. Haustorial types and their frequencies in a range of lichens with trebouxioid phycobionts. New Phytol 103: 785–795CrossRefGoogle Scholar
  30. Honegger R (1986b) Ultrastructural studies in lichens. II. Mycobiont and photobiont cell wall surface layers and adhering crystalline lichen products in four Parmeliaceae. New Phytol 103: 797–808CrossRefGoogle Scholar
  31. Honegger R (1987) Isidium formation and the development of juvenile thalli in Parmelia pastillifera (Lecanorales, lichenized Ascomycetes). Bot Hely 97: 147–152Google Scholar
  32. Honegger R (1990) Surface interactions in lichens. In: Wiessner W, Robinson DG, Starr RC (eds) Experimental phycology 1. Cell walls and surfaces, reproduction, photosynthesis. Springer, Berlin Heidelberg New York, pp 40–54Google Scholar
  33. Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Physiol Plant Mol Biol 42: 553–578CrossRefGoogle Scholar
  34. Honegger R (1992) Lichens: mycobiont-photobiont relationships. In: Reisser W (ed) Algae and symbioses. Plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 255–275Google Scholar
  35. Honegger R (1993) Developmental biology of lichens. New Phytol 125: 659–677CrossRefGoogle Scholar
  36. Honegger R (1995) Experimental studies with foliose macrolichens: fungal responses to spatial disturbance at the organismic level and to spatial problems at the cellular level during drought stress events. Can J Bot 73 (Suppl 1): 569–578CrossRefGoogle Scholar
  37. Honegger R, Peter M (1994) Routes of solute translocation and the location of water in heteromerous lichens visualized with cryotechniques in light and electron microscopy. Symbiosis 16: 167–186Google Scholar
  38. Honegger R, Peter M, Scherrer S (1996) Drought-induced structural alterations at the mycobiont-photobiont interface in a range of foliose macrolichens. Protoplasma 190: 221–232CrossRefGoogle Scholar
  39. Huneck S, Yoshimura I (1996) Identification of lichen substances. Springer, BerlinCrossRefGoogle Scholar
  40. Ihda TA, Nakano T, Yoshimura I, Iwatsuki Z (1993) Phycobionts isolated from Japanese species of Anzia (lichenes). Arch Protistenkd 143: 163–172CrossRefGoogle Scholar
  41. Ingold CT, (1956) A gas phase in viable fungal spores. Nature 177: 1242–1243CrossRefGoogle Scholar
  42. Jahns HM (1988) The lichen thallus. In: Galun M (ed) CRC Handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 95–143Google Scholar
  43. James PW, Henssen A (1976) The morphological and taxonomic significance of cephalodia. In: Brown DH, Hawksworth DL, Bailey RH (eds) Lichenology: progress and problems. Academic Press, London, pp 27–77Google Scholar
  44. Kappen L (1988) Ecophysiological relationships in different climatic regions. In: Galun M (ed) CRC Handbook of lichenology, vol 2. CRC Press, Boca Raton, pp 37–100Google Scholar
  45. Kappen L (1993) Lichens in the antarctic region. In: Friedman EI (ed) Antarctic microbiology. Wiley-Liss, New York, pp 433–490Google Scholar
  46. Larson DW (1984) Habitat overlap/niche segregation in two Umbilicaria lichens: a possible mechanism. Oecologia 62: 118–125CrossRefGoogle Scholar
  47. Lawrey JD (1984) Biology of lichenized fungi. Praeger, New YorkGoogle Scholar
  48. Lawrey JD (1986) Biological role of lichen substances. Bryologist 89: 111–122CrossRefGoogle Scholar
  49. Lawrey JD (1993) Lichens as monitors of pollutant elements at permanent sites in Maryland and Virginia. Bryologist 96: 339–341CrossRefGoogle Scholar
  50. Lines CEM, Ratcliffe RG, Rees TAV, Southon TE (1989) A 13C NMR study of photosynthate transport and metabolism in the lichen Xanthoria calcicola Oxner. New Phytol 111: 447–456CrossRefGoogle Scholar
  51. MacFarlane JD, Kershaw KA (1985) Some aspects of carbohydrate metabolism in lichens. In: Brown DH (ed) Lichen physiology and cell biology. Plenum Press, New York, pp 1–8CrossRefGoogle Scholar
  52. Melick DR, Seppelt RD (1994) The effect of hydration on carbohydrate levels, pigment content and freezing point in Umbilicaria decussata at a continental Antarctic localitiy. Cryptogam Bot 4: 212–217Google Scholar
  53. Milburn JA (1970) Cavitation and osmotic potentials of Sordaria ascospores. New Phytol 69: 133–141CrossRefGoogle Scholar
  54. Mollenhauer D (1992) Geosiphon pyriforme. In: Reisser W (ed) Algae and symbioses. Plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 339–351Google Scholar
  55. Ott S (1987) Reproductive strategies in lichens. Bibl Lichenol 25: 81–93Google Scholar
  56. Plessl A (1963) Über die Beziehungen von Pilz und Alge im Flechtenthallus. Oesterr Bot Z 110: 194–269CrossRefGoogle Scholar
  57. Poelt J, Huneck S (1968) Lecanora vinetorum nova spec., ihre Vergesellschaftung, ihre Oekologie und ihre Chemie. Oesterr Bot Z 115: 411–422Google Scholar
  58. Poelt J, Mayrhofer H (1988) Über Cyanotrophie bei Flechten. Plant Syst Evol 158: 265–281CrossRefGoogle Scholar
  59. Rai AN (1988) Nitrogen metabolism. In: Galun M (ed) CRC Handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 201–237Google Scholar
  60. Richardson DHS (1973) Photosynthesis and carbohydrate movement. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 249–288CrossRefGoogle Scholar
  61. Scheidegger C (1994) Low-temperature scanning electron microscopy: the localization of free and perturbed water and its role in the morphology of the lichen symbionts. Cryptogam Bot 4: 290–299Google Scholar
  62. Scheidegger C, Schroeter B, Frey B (1995) Structural and functional processes during water vapour uptake and desiccation in selected lichens with green algal photobionts. Planta 197: 399–409CrossRefGoogle Scholar
  63. Schwendener S (1867) Ueber die wahre Natur der Flechten. Verh Schweiz Naturforsch Ges 51: 88–90Google Scholar
  64. Smith DC (1978) What can lichens tell us about real fungi? Mycologia 70: 915–935CrossRefGoogle Scholar
  65. Smith DC, Douglas A (1987) The biology of symbiosis. Edward Arnold, LondonGoogle Scholar
  66. Tagu D, Python M, Cretin C, Martin F (1996) Cloning symbiosis-related cDNAs from eucalypt ectomycorrhiza by PCR-assisted differential screening. New Phytol 125: 339–343CrossRefGoogle Scholar
  67. Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus, Magnaporthe grisea. Plant Cell 5: 1575–1590PubMedGoogle Scholar
  68. Talbot NJ, Kershaw MJ, Wakley GE, deVries OMH, Wessels JGH, Hamer JE (1996) MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8: 985–999PubMedGoogle Scholar
  69. Templeton MD, Rikkerink EHA, Beever RE (1994) Small, cysteine-rich proteins and recognition in fungal-plant interactions. Mol Plant-Microbe Interact 3: 320–325CrossRefGoogle Scholar
  70. Tschermak E (1941) Untersuchungen über die Beziehungen von Pilz und Alge im Flechtenthallus. Oesterr Bot Z 90: 233–307CrossRefGoogle Scholar
  71. Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) CRC Handbook of lichenology, vol 1. CRC Press, Boca Raton, pp 39–92Google Scholar
  72. van Donk E, Bruning K (1992) Ecology of aquatic fungi in and on algae. In: Reisser W (ed) Algae and symbioses. Plants, animals, fungi, viruses, interactions explored. Biopress, Bristol, pp 567–592Google Scholar
  73. Wessels JGH (1993) Wall growth, protein excretion, and morphogenesis in fungi. New Phytol 123: 397–413CrossRefGoogle Scholar
  74. Wösten HAB, Asgeirsdottir SA, Krook JH, Drenth JHH, Wessels JGH (1994) The fungal hydrophobin Sc3P self-assembles at the surface of aerial hyphae as a protein membrane constituting the hydrophobic rodlet layer. Eur J Cell Biol 63: 122–129PubMedGoogle Scholar
  75. Yamamoto Y, Miura Y, Higuchi M, Kinoshita Y, Yoshimura I (1993) Using lichen tissue cultures in modern biology. Bryologist 96: 384–393CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1997

Authors and Affiliations

  • R. Honegger
    • 1
  1. 1.Institute of Plant BiologyUniversity of ZürichZürichSwitzerland

Personalised recommendations