Advertisement

Planta

, Volume 198, Issue 1, pp 6–16 | Cite as

The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2-concentrating mechanism and carbon isotope discrimination in lichens and bryophytes

  • E. C. Smith
  • H. GriffithsEmail author
Article

Abstract

The organic-matter carbon isotope discrimination (Δ) of lichens with a wide range of photobiont and/or cyanobiont associations was used to determine the presence or absence of a carbon-concentrating mechanism (CCM). Two groups were identified within the lichens with green algal photobionts. One group was characterised by low, more C4-like Δ values (Δ < 15‰), the other by higher, more C3-like Δ values (Δ > 18‰). Tri-partite lichens (lichens with a green alga as the primary photobiont and cyanobacteria within internal or external cephalodia) occurred in both groups. All lichens with cyanobacterial photobionts had low Δ values (Δ < 15‰). The activity of the CCM, organic-matter Δ values, on-line Δ values and gas-exchange characteristics correlated with the presence of a pyrenoid in the algal chloroplast. Consistent with previous findings, lichens with Trebouxia as the primary photobiont possessed an active CCM while those containing Coccomyxa did not. Organic Δ values for lichens with Stichococcus as the photobiont varied between 11 and 28‰. The lichen genera Endocarpon and Dermatocarpon (Stichococcus + pyrenoid) had C4-like organic Δ values (Δ = 11 to 16.5‰) whereas the genus Chaenotheca (Stichococcus — pyrenoid) was characterised by high C3-like Δ values (Δ = 22 to 28‰), unless it associated with Trebouxia (Δ = 16‰). Gas-exchange measurements demonstrated that Dermatocarpon had an affinity for CO2 comparable to those species which possessed the CCM, with K0.5 = 200–215 μ1 · 1−1, compensation point (Γ) = 45–48 μl · l−1, compared with K0.5 = 195 μ1 · 1−1, Γ = 44μ1 · 1−1 for Trebouxioid lichens. Furthermore, lichens with Stichococcus as their photobiont released a small pool (24.2 ± 1.9 to 34.2 ± 2.5 nmol · mg−1 Chl) of inorganic carbon similar to that released by Trebouxioid lichens [CCM present, dissolved inorganic carbon (DIC) pool size = 51.0 ± 2.8 nmol · mg−1 Chl]. Lichens with Trentepohlia as photobiont did not possess an active CCM, with high C3-like organic Δ values (Δ = 18‰ to 23‰). In particular, Roccella phycopsis had very high on-line Δ values (Δ = 30 to 33‰), a low affinity for CO2 (K0.5 = 400 μ1 · 1−1,Γ = 120 μ1 · −1) and a negligible DIC pool. These responses were comparable to those from lichens with Coccomyxa as the primary photobiont with Nostoc in cephalodia (organic Δ = 17 to 25‰, on-line Δ = 16 to 21‰, k0.5 = 388 μ1 · 1−1, Γ = 85 μ1 · 1−1, DIC pool size = 8.5 ± 2.4 nmol · mg−1 Chl). The relative importance of refixation of respiratory CO2 and variations in source isotope signature were considered to account for any variation between on-line and organic Δ. Organic Δ was also measured for species of Anthocerotae and Hepaticae which contain pyrenoids and/or Nostoc enclosed within the thallus. The results of this screening showed that the pyrenoid is correlated with low, more C4-like organic Δ values (Δ = 7 to 12‰ for members of the Anthocerotae with a pyrenoid compared with Δ = 17 to 28‰ for the Hepaticae with and without Nostoc in vesicles) and confirms that the pyrenoid plays a fundamental role in the functioning of the CCM in microalgal photobionts and some bryophytes.

Key words

Anthocerotae Cyanobacterium Microalga Photobiont Photosynthesis 

Abbreviations and Symbols

CCM

carbon-concentrating mechanism

DIC

dissolved inorganic carbon (CO2 + HCO 3 - + CO 3 2- )

DW

dry weight

K0.5

external concentration of CO2 at which half-maximal rates of CO2 assimilation are reached

photobiont

photosynthetic organism present in the lichen

Rubisco

ribulose-1,5-bisphosphate carboxylase-oxygenase

Δ

carbon isotope discrimination (%)

δ13C

carbon isotope ratio (%)

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ahmadjian V (1967) A guide to the algae occurring as lichen symbionts; isolation, culture, cultural physiology, and identification. Phycologia 6: 127–160Google Scholar
  2. Ahmadjian V (1993) The lichen symbiosis. John Wiley and Sons, New YorkGoogle Scholar
  3. Ahmadijian V, Heikilla H (1970) The culture and synthesis of Endocarpon pusillum and Staurothele clopima. Lichenologist 4: 259–267Google Scholar
  4. Badger MR, Price GD (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol Plant 84: 606–615Google Scholar
  5. Badger MR, Pfanz H, Büdel B, Heber U, Lange OL (1993) Evidence for the functioning of photosynthetic CO2-concentrating mechanisms in lichens containing green algal and cyanobacterial photobionts. Planta 191: 57–70Google Scholar
  6. Beardall J, Griffiths H, Raven JA (1982) Carbon isotope discrimination and the CO2 accumulating mechanism in Chlorella emersonii. J Exp Bot 33(135): 729–737Google Scholar
  7. Coleman JR (1991) The molecular and biochemical analyses of carbon dioxide-concentrating mechanisms in cyanobacteria and microalgae. Plant Cell Environ 14(8): 861–868Google Scholar
  8. Cowan IR, Lange OL, Green TGA (1992) Carbon-dioxide exchange in lichens: determination of transport and carboxylation characteristics. Planta 187: 282–294Google Scholar
  9. Crittenden P (1991) Ecological significance of necromass production in mat-forming lichens. Lichenologist 23: 323–331Google Scholar
  10. Evans JR, Sharkey TD, Berry JD, Farquhar GD (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust J Plant Physiol 13: 281–292Google Scholar
  11. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40: 503–537CrossRefGoogle Scholar
  12. Griffiths H, Broadmeadow MSJ, Borland AM, Hetherington CS (1990) Short-term changes in carbon-isotope discrimination identify changes between C3 and C4 carboxylation during Crassulacean acid metabolism. Planta 181: 604–610Google Scholar
  13. Hogetsu D, Miyachi S (1977) Effects of CO2 concentration during growth on subsequent photosynthetic CO2 fixation in Chlorella. Plant Cell Physiol 18: 347–352Google Scholar
  14. 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, New York, pp 27–77Google Scholar
  15. Kaplan A, Schwarz R, Lieman HJ, Reinhold L (1991) Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol 97: 851–855Google Scholar
  16. Kuchitsu K, Tsuzuki M, Miyachi S (1991) Polypeptide composition and enzyme activities of the pyrenoid and its regulation by CO2 concentrations in unicellular green algae. Can J Bot 69: 1062–1069Google Scholar
  17. Lange OL (1980) Moisture content and CO2 exchange of lichens. Oecologia 45: 82–87Google Scholar
  18. Lange OL (1988) Ecophysiology of photosynthesis: Performance of poikilohydric lichens and homoiohydric mediterranean sclerophylls. J Ecol 76: 915–937Google Scholar
  19. Lange OL, Zeigler H (1986) Different limiting processes of photosynthesis in lichens. In: Marcelle R, Clistjers H, Poucke MV (eds) Biological control of photosynthesis. Martinus Nijhoff, Dortrecht, pp 147–161Google Scholar
  20. Lange OL, Green TGA, Ziegler H (1988) Water status related photosynthesis and carbon isotope discrimination in species of the lichen genus Pseudocyphellaria with green or bluegreen photobionts and in photosymbiodemes. Oecologia 75: 494–501Google Scholar
  21. Lange OL, Budel B, Zellner H, Zotz G, Meyer A (1994) Field measurement of water relations and CO2 exchange of the tropical cyanobacterial basidiolichen Dictyonema glabratum in a Panamanian rainforest. Bot Acta 107: 279–290Google Scholar
  22. Máguas C, Griffiths H, Broadmeadow MSJ (1995) Gas exchange and carbon isotope discrimination in lichens: Evidence for interaction between CO2-concentrating mechanisms and diffusion limitation. Planta 196: 95–102Google Scholar
  23. Máguas C, Griffiths H, Ehleringer J, Serodio J (1993a) Characterization of photobiont associations in lichens using carbon isotope discrimination tehniques. In: Ehleringer J, Hall A, Farquhar G (eds) Stable isotopes and plant carbon-water relations. Academic Press London, New York, pp. 201–212Google Scholar
  24. Munoz J, Merrett MJ (1988) Inorganic carbon uptake by a small-celled strain of Stichococcus bacillaris Planta 175: 460–464Google Scholar
  25. Osafune T, Ehara T, Yokota A, Hase E (1992) Immunogold localization of ribulose-1,5-bisphosphate carboxylase/oxygenase in developing proplastids to dark-grown wax-rich cells of Euglena gracilis. J Electron Microsc 41: 469–474Google Scholar
  26. Palmqvist K (1993) Photosynthetic CO2-use efficiency in lichens and their isolated photobionts: The possible role of a CO2-concentrating mechanism. Planta 191: 48–56Google Scholar
  27. Palmqvist K, Samuelsson G, Badger MR (1994a) Photobiont-related differences in carbon acquisistion among green-algal lichens. Planta 195: 70–79Google Scholar
  28. Palmqvist K, Máguas C, Badger MR, Griffiths H (1994b) Assimilation, accumulation and isotope discrimination of inorganic carbon in cyanobacterial lichens: evidence for the operation of a CO2 concentrating mechanism in cyanobacterial lichens. Crypto Bot 4: 218–226Google Scholar
  29. Palmqvist K, Ogren E, Lernmark U (1994c) The CO2-concentrating mechanism is absent in the green alga Coccomyxa: a comparative study of photosynthetic CO2 and light responses of Coccomyxa, Chlamydomonas reinhardtii and barley protoplasts. Plant Cell Environ 17: 65–72Google Scholar
  30. Pronina NA, Semenenko VE (1992) The role of pyrenoid in concentration, generation and fixation of carbon dioxide in chloroplasts of microalgae. Fiziol Rast 39(4): 723–732Google Scholar
  31. Purvis OW, Coppins BJ, Hawksworth DL, James PW, Moore DM (1992) The lichen flora of Great Britain and Ireland. Natural History Museum Publications, UKGoogle Scholar
  32. Ramazanov Z, Rawat M, Matthews SW, Mason CB, Moroney JV (1993) Role of the pyrenoid in the carbon dioxide concentrating mechanism in Chlamydomonas reinhardtii. (Abstr.) Plant Physiol: 102, Suppl 140Google Scholar
  33. Raven JA (1985) The CO2 concentrating mechanism. In: Lucas WJ, Berry JA (eds) Inorganic carbon uptake by aquatic photosynthetic organisms. The American Society of Plant Physiologists, Rockville, Md, pp 67–81Google Scholar
  34. Raven JA (1991) Implications of inorganic carbon utilisation: ecology, evolution and geochemistry. Can J Bot 69: 908–924Google Scholar
  35. Raven JA, Johnston AM, Handley LL, McInroy SG (1990) Transport and assimilation of inorganic carbon by Lichina pygmaea under emersed and submersed conditions. New Phytol 114: 407–417Google Scholar
  36. Rice SK, Giles L (1994) Climate in the Pleistocene. Nature 371: 111–112Google Scholar
  37. Ronen R, Galun MP (1984) Pigment extraction from lichens with dimethyl sulfoxide (DMSO), and estimation of chlorophyll degradation. Environ Exp Bot 24: 239–245Google Scholar
  38. Tschermak-Woess E (1982) The algal partner. In: Handbook of lichenology, vol I. Galun M (ed) CRC Press, Florida, USA, pp 39–92Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  1. 1.Department of Agricultural and Environmental ScienceUniversity of Newcastle upon TyneNewcastle upon TyneUK

Personalised recommendations