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Gas exchange and carbon isotope discrimination in lichens: Evidence for interactions between CO2-concentrating mechanisms and diffusion limitation

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Abstract

The characteristics of gas exchange and carbon isotope discrimination were determined for a number of lichen species, representing contrasting associations between fungal (mycobiont) and photosynthetic (photobiont) organism. These parameters were evaluated with regard to the occurrence of any CO2-concentrating mechanism (CCM) expressed specifically by the green algal (phycobiont) or cyanobacterial (cyanobiont) partner. Carbon isotope discrimination (Δ) fell into three categories. The highest Δ, found in lichens comprising a phycobiont plus cyanobacteria limited to pockets in the thallus (known as cephalodia), ranged from 24 to 28‰, equivalent to a carbon isotope ratio (δ13C) of around -32 to-36‰ vs. Pee Dee Belemnite (PDB) standard. Further evidence was consistent with CO2 supply to the carboxylating system entirely mediated by diffusion rather than a CCM, in that thallus CO2 compensation point and online instantaneous Δ were also high, in the range normally associated with C3 higher plants. For lichens consisting of phycobiont or cyanobiont alone, organic material Δ formed two distinct ranges around 15‰ (equivalent to a δ13C of -23%.). Thallus compensation point and instantaneous Δ were lower in the cyanobiont group, which also showed higher maximum rates of net photosynthesis, whether expressed on the basis of thallus dry weight, chlorophyll content or area. These data provide additional evidence for the activity of a CCM in cyanobiont lichens, which only show photosynthetic activity when reactivated with liquid water. Rates of net CO2 uptake were lower in both phycobiont associations, but were relatively constant across a wide working range of thallus water contents, usually in parallel with on-line Δ. The phycobiont response was consistent whether photosynthesis had been reactivated with liquid water or water vapour. The effect of diffusion limitation could generally be seen with a 3–4‰ decrease in instantaneous Δ at the highest water contents. The expression of a CCM in phycobiont algae, although reduced compared with that in cyanobacteria, has already been related to the occurrence of pyrenoids in chloroplasts. In view of the inherent requirement of cyanobacteria for some form of CCM, and the smaller pools of dissolved inorganic carbon (DIC = CO2 + HCO su−inf3 + CO su2−inf3 ) associated with phycobiont lichens, it appears that Δ characteristics provide a good measure of the magnitude of any CCM, albeit tempered by diffusion limitation at the highest thallus water contents.

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Abbreviations

ANOVA:

analysis of variance

CCM:

CO2-concentrating mechanism

cyanobiont:

cyanobacterium

DIC:

CO2 + HCO su−inf3 + CO su2−inf3 (dissolved inorganic carbon)

photobiont:

photosynthetic organism present in the association

phycobiont:

green alga

phycobiont + cephalodia:

green algae + cyanobacteria in cephalodia

Pmax:

maximum photosynthetic rate

PPFD:

photosynthetic photon flux density, 400–700 nm

Rubisco:

ribulose-1,5-bisphosphate carboxylase/oxygenase

Δ:

carbon isotope discrimination (‰)

δ13C:

carbon isotope ratio (‰)

References

  • Badger, M.R., Price, G.D. (1989) Carbonic anhydrase associated with the cyanobacterium Synechococcus PCC7942. Plant Physiol. 89, 56–60

    Google Scholar 

  • Badger, M.R., Price, G.D. (1992) The CO2-concentrating mechanism in cyanobacteria and microalgae. Physiol. Plant. 84, 606–615

    Google Scholar 

  • Badger, M.R., Pfanz, H., Budel, B., Heber, U., Lange, O. (1993) Evidence for the functioning of photosynthetic CO2-concentrating mechanisms in lichens containing green algal and cyanobacterial photobionts. Planta 191, 59–72

    Google Scholar 

  • Bauer, H. (1984) Net photosynthetic CO2 compensation concentrations of some lichens. Z. Pflanzenphysiol. 114, 49–50

    Google Scholar 

  • Beardall, J., Griffiths, H., Raven, J.A. (1982) Carbon isotope discrimination and the CO2 accumulating mechanism in Chlorella emersonii. J. Exp. Bot. 33, 729–737

    Google Scholar 

  • Bilger, W., Rimke, S., Schreiber, U., Lange, O. (1989) Inhibition of energy-transfer to photosystem II in lichens by dehydration: different properties of reversibility with green and blue-green phycobionts. J. Plant Physiol. 134, 261–268

    Google Scholar 

  • Broadmeadow, M.S.J., Griffiths, H., Maxwell, C., Borland, A.M. (1992) The carbon isotope ratio of plant organic material reflects temporal and spatial variations in CO2 partial pressure and δ13C within tropical forest formations in Trinidad. Oecologia 89, 435–441

    Google Scholar 

  • Cowan, I.R., Lange, O., Green, T.G.A. (1992) Carbon-dioxide exchange in lichens: determination of transport and carboxylation characteristics. Planta 187, 282–294

    Google Scholar 

  • Demmig-Adams, B., Máguas, C., Adams, W.W., III, Meyer, A., Kilian, E., Lange, O. (1990 a) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue-green phycobionts. Planta 180, 400–409

    Google Scholar 

  • Demmig-Adams, B., Adams, W.W., III, Czygan, F-C, Schreiber, U., Lange, O. (1990b) Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in carotenoid composition. Planta 180, 582–589

    Google Scholar 

  • Ehleringer, J., Hall, A.E., Farquhar, G.D. (1993) Stable isotopes and plant carbon water relations. Academic Press, New York

    Google Scholar 

  • Evans, J.R., Sharkey, T., Berry, B., Farquhar, G. (1986) Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants. Aust. J. Plant Physiol. 13, 281–292

    Google Scholar 

  • Farquhar, G., Ehleringer, J., Hubick, K. (1989) Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503–537

    Google Scholar 

  • Griffiths, H., Broadmeadow, J., Borland, A., Hetherington, C. (1990) Short-term changes in carbon-isotope discrimination identify transitions between C3 and C4 carboxylation during Crassulacean acid metabolism. Planta 181, 604–610

    Google Scholar 

  • Honegger, R. (1991) Functional aspects of the lichen symbiosis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42, 553–578

    Google Scholar 

  • James, P.W., Henssen, A. (1976) The morphological and taxonomic significance of cephalodia. In: Lichenology: progress and problems (Proceedings of an International Symposium held at the University of Bristol) pp. 27–78, Academic Press, London

    Google Scholar 

  • Lange, O., Ziegler, H. (1986). Different limiting processes of photosynthesis in lichens. In: Biological control of photosynthesis, Marcelle, R., Clistjers, H., Van Poucke, M. eds. pp. 147–161, Martinus Nijhoff Publishers, Dordrecht

    Google Scholar 

  • Lange, O.L. (1988). Ecophysiology of photosynthesis: performance of poikilohydric lichens and homoiohydric mediterranean sclerophylls. J. Ecol. 76, 915–937

    Google Scholar 

  • Lange, O.L., Green, T.G.A., Ziegler, H. (1988) Water status related photosynthesis and carbon isotope discrimination in species of the lichen genus Pseudocyphellaria with green and blue-green photobionts and in photosymbiodemes. Oecologia 75, 494–501

    Google Scholar 

  • Lange, O.L., Budel, B., Heber, U., Meyer, A., Zellner, H., Green, T.G.A. (1993) Temperate rainforest lichens in New Zealand: High thallus water content can severely limit photosynthetic CO2 exchange. Oecologia 95, 303–313

    Google Scholar 

  • Máguas, C., Griffiths, H., Ehleringer, J., Serôdio, J. (1993) Characterization of photobiont associations in lichens using carbon isotope discrimination techniques. In: Stable isotopes and plant carbon-water relations, Ehleringer, J., Hall, A., Farquhar, G. eds. pp. 201–212, Academic Press, New York

    Google Scholar 

  • Matthes, U., Feige, G. (1983) Ecophysiology of lichen symbioses. In: Encyclopedia of plant physiology, N. S., vol. 12C; Physiological plant ecology III, Lange, O., Nobel, P., Osmond, B., Ziegler, H. eds. pp. 423–458, Springer-Verlag, Berlin

    Google Scholar 

  • Palmqvist, K. (1993) Photosynthetic CO2-use efficiency in lichens and their isolated photobionts: The possible role of a CO2-concentrating mechanism in cyanobacterial lichens. Planta 191, 48–56

    Google Scholar 

  • Palmqvist, K., Máguas, C., Badger, M.R., Griffiths, H. (1994a) Assimilation, accumulation and isotope discrimination of inorganic carbon in lichens: further evidence for the operation of a CO2 concentrating mechanism in cyanobacterial lichens. Crypto. Bot. 4, 218–226

    Google Scholar 

  • Palmqvist, K., Ogren, E., Lernmark, U. (1994b) 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, 65–72

    Google Scholar 

  • Rai, A.N. (1989) Nitrogen metabolism. In: Handbook of lichenology, vol. 1, Galun, M., ed. pp. 201–237, CRC Press, Boca Raton

    Google Scholar 

  • Raven, J.A. (1991) Implications of inorganic carbon utilization: ecology, evolution and geochemistry. Can. J. Bot. 69, 908–92

    Google Scholar 

  • Raven, J.A., Johnston, A.M., Handley, L., McInroy, S.G. (1990) Transport and assimilation of inorganic carbon by Lichina pygmaea under emersed and submersed conditions. New Phytol. 114, 407–417

    Google Scholar 

  • Ronen, R., Galun, M. P. (1984). Pigment extraction from lichens with dimethyl sulfoxide (DMSO), and estimation of chlorophyll degradation. Environ. Exp. Bot. 24 (3), 239–245

    Google Scholar 

  • Sharkey, T.D., Berry, J. (1985) Carbon isotope fractionation of algae as influenced by an inducible CO2 concentrating mechanism. In: Inorganic carbon uptake by aquatic photosynthetic organisms, Lucas, W.J., Berry, J.A., eds. pp. 389–402, American Society of Plant Physiologists, Rockville, Md.

    Google Scholar 

  • Snelgar, W.P., Green, T.G.A. (1980) Carbon dioxide exchange in lichens: low carbon dioxide compensation levels and lack of apparent photorespiratory activity in some lichens. Bryologist 83, 505–507

    Google Scholar 

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Correspondence to H. Griffiths.

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We would like to thank Dr. Enrico Brugnoli (CNR, Porano, Italy) and E.C. Smith (University of Newcastle) for many helpful discussions. Dr. Kristin Palmqvist (Department of Plant Physiology, University of Umeå, Sweden) kindly provided the samples of Peltigera apthosa. In particularly, Cristina Máguas would like to thank to Prof. Fernando Catarino (University of Lisbon) for his support throughout this study. Cristina Máguas has been supported by JNICT-Science Programme studentship (BD/153/90-RN).

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Máguas, C., Griffiths, H. & Broadmeadow, M.S.J. Gas exchange and carbon isotope discrimination in lichens: Evidence for interactions between CO2-concentrating mechanisms and diffusion limitation. Planta 196, 95–102 (1995). https://doi.org/10.1007/BF00193222

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