, Volume 179, Issue 1, pp 115–122 | Cite as

Recycling of respiratory CO2 during Crassulacean acid metabolism: alleviation of photoinhibition in Pyrrosia piloselloides

  • H. Griffiths
  • B. L. Ong
  • P. N. Avadhani
  • C. J. Goh


The regulation of Crassulacean acid metabolism (CAM) in the fern Pyrrosia piloselloides (L.) Price was investigated in Singapore on two epiphytic populations acclimated to sun and shade conditions. The shade fronds were less succulent and had a higher chlorophyll content although the chlorophyll a:b ratio was lower and light compensation points and dark-respiration rates were reduced. Dawn-dusk variations in titratable acidity and carbohydrate pools were two to three times greater in fronds acclimated to high photosynthetically active radiation (PAR), although water deficits were also higher than in shade fronds. External and internal CO2 supply to attached fronds of the fern was varied so as to regulate the magnitude of CAM activity. A significant proportion of titratable acidity was derived from the refixation of respiratory CO2 (27% and 35% recycling for sun and shade populations, respectively), as measured directly under CO2-free conditions. Starch was shown to be the storage carbodydrate for CAM in Pyrrosia, with a stoichiometric reduction of “C3-skeleton” units in proportion to malic-acid accumulation. Measurements of photosynthetic O2 evolution under saturating CO2 were used to compare the light responses of sun and shade fronds for each CO2 supply regime, and also following the imposition of a photoinhibitory PAR treatment (1600 μmol·m-2·s-1 for 3 h). Apparent quantum yield declined following the high-PAR treatment for sun- and shade-adapted plants, although for sun fronds CAM activity derived from respiratory CO2 prevented any further reduction in photosynthetic efficiency. Recycling of respiratory CO2 by shade plants could only partly prevent photoinhibitory damage. These observations provide experimental evidence that respiratory CO2 recycling, ubiquitous in CAM plants, may have developed so as to alleviate photoinhibition.

Key words

Acclimation (sun/shade) Crassulacean acid metabolism Photoinhibition of photosynthesis Pteridophytes Pyrrosia Respiratory CO2, recycling 

Abbreviations and symbols


Crassulacean acid metabolism


maximal photosystem II fluorescence


terminal steady-state fluorescence


photosynthetically active radiation, 400–700 nm


(dawn-dusk) variation in titratable acidity


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  1. Adams, W.W., III (1988) Photosynthetic acclimation and photoinhibition of terrestrial and epiphytic CAM tissues growing in full sunlight and deep shade. Aust. J. Plant Physiol. 15, 123–134Google Scholar
  2. Adams, W.W., III, Osmond, C.B. (1988) Internal CO2 supply during photosynthesis of sun and shade grown CAM plants in relation to photoinhibition. Plant Physiol. 86, 117–123Google Scholar
  3. Adams, W.W., III, Terashima, I., Brugnoli E., Demmig B. (1988) Comparisons of photosynthesis and photoinhibition in the CAM vine Hoya australis and several vines growing on the coast of eastern Australia. Plant Cell Environ. 11, 173–181Google Scholar
  4. Borland, A.M., Griffiths, H. (1989) The regulation of citric acid accumulation and carbon recycling during CAM in Ananas comosus. J. Exp. Bot. 40, 57–64Google Scholar
  5. Gil, F. (1986) Origin of CAM as an alternative photosynthetic carbon fixation pathway. Photosynthetica 20, 494–507Google Scholar
  6. Griffiths, H. (1988a) Crassulacean acid metabolism: a re-appraisal of physiological plasticity in form and function. Adv. Bot. Res. 15, 43–92Google Scholar
  7. Griffiths, H. (1988b) Carbon balance during CAM: an assessment of respiratory CO2 recycling in the epiphytic bromeliads Aechmea nudicaulis and Aechmea fendleri. Plant Cell Environ. 11, 603–611Google Scholar
  8. Griffiths, H. (1989) Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. In: Phylogeny and ecophysiology of epiphytes, Lüttge, U. ed. Ecological Studies, No. 76. Springer, Berlin Heidelberg New York (in press)Google Scholar
  9. Griffiths, H., Lüttge, U., Stimmel, K-H., Crook, C.E., Griffiths, N.M., Smith, J.A.C. (1986) Comparative ecophysiology of CAM and C3 bromeliads. III. Environmental influences in CO2 assimilation and transpiration. Plant Cell Environ. 9, 385–393Google Scholar
  10. Griffiths, H., Smith, J.A.C., Lüttge, U., Popp, M., Cram, W.J.C., Lee, H.S.J., Medina, E., Schäfer, C., Stimmel, K.-H. (1989) Ecophysiology of xerophytic and halophytic vegetation of a coastal alluvial plain in northern Venezuela. IV. Tillandsia flexuosa and Schomburkgia humboldtiana, epiphytic CAM plants. New Phytol. 111, 273–282Google Scholar
  11. Hovenkamp, P. (1986) A monograph of the fern genus Pyrrosia. Leiden Bot. Ser. 9, 1–80Google Scholar
  12. Hylton C.M., Rawsthorne, S., Smith, A.M., Jones, D.A., Woolhouse, H.W. (1988) Glycine decarboxylase is confined to the bundle-sheath cells of leaves of C3 — C4 intermediate species. Planta 175, 452–459Google Scholar
  13. Kenyon, W.H., Severson, R.F., Black, C.C. (1985) Maintenance of carbon cycle in Crassulacean acid metabolism plant leaves. Plant Physiol. 77, 183–189Google Scholar
  14. Kluge, M., Freimert, V., Ong, B.L., Brulfert, J., Goh, C.J. (1989) In situ studies of crassulacean acid metabolism in Drymoglossum piloselloides, an epiphytic fern of the humid tropics. J. Exp. Bot. (in press)Google Scholar
  15. Krause, G.H. (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanims. Physiol. Plant. 74, 566–574Google Scholar
  16. Lüttge, U., Ball, E. (1987) Dark respiration of CAM plants. Plant Physiol. Biochem. 25, 3–10Google Scholar
  17. Martin, C.E., Higley, M.H., Wang, W.-Z. (1988) Ecophysiological significance of CO2-recycling via crassulacean acid metabolism in Talinum calycinum Engelm. (Portulacaceae). Plant Physiol. 86, 562–568Google Scholar
  18. Ong, B.L., Kluge, M., Friemert, V. (1986) Crassulacean acid metabolism in the epiphytic ferns Drymoglossum piloselloides and Pyrrosia longifolia: studies on responses to environmental signals. Plant Cell Environ. 9, 547–557Google Scholar
  19. Osmond, C.B., Winter, K., Powles, S. (1980) Adaptive significance of carbon dioxide recycling during photosynthesis in water-stressed plants, In: Adaptation of plants to water and high temperature stress, pp. 139–154, Turner, N.C., Kramer, P.J., eds. John Wiley & Sons, New YorkGoogle Scholar
  20. Ravensberg, W.J., Hennipman, E. (1986) The Pyrrosia species formerly referred to Drymoglossum and Saxiglossum. Leiden Bot. Ser. 9, 281–310Google Scholar
  21. Szarek, S.R., Johnson, I.P., Ting, I.P. (1973) Drought adaptation in Opuntia basilaris. Significance of recycling carbon through crassulacean acid metabolism. Plant Physiol. 52, 539–541Google Scholar
  22. Winter, K. (1985) Crassulacean acid metabolism. In: Photosynthetic mechanisms and the environment, pp. 329–387, Barber, J., Baker, N.R., eds. Elsevier, AmsterdamGoogle Scholar
  23. Winter, K., Osmond, C.B., Hubick, K. (1986a) Crassulacean acid metabolism in the shade. Studies on an epiphytic fern, Pyrrosia longifolia, and other rainforest species. Oecologia 68, 224–230Google Scholar
  24. Winter, K., Schröppel-Meier, G., Caldwell, M.M. (1986b) Respiratory CO2 as carbon source for nocturnal acid synthesis at high temperatures in species exhibiting crassulacean acid metabolism. Plant Physiol. 78, 390–394Google Scholar
  25. Wong, S.C., Hew, C.S. (1976) Diffusive resistance, titratable acidity and CO2 fixation in two tropical epiphytic ferns. Am. Fern J. 4, 121–124Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • H. Griffiths
    • 1
  • B. L. Ong
    • 1
  • P. N. Avadhani
    • 1
  • C. J. Goh
    • 1
  1. 1.Department of BotanyNational University of SingaporeSingaporeRepublic of Singapore

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