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Photosynthesis Research

, Volume 39, Issue 3, pp 413–425 | Cite as

Acclimation of photosynthetic proteins to rising atmospheric CO2

  • Andrew N. Webber
  • Gui-Ying Nie
  • Stephen P. Long
Terrestrial photosynthesis Minireview

Abstract

In this review we discuss how the photosynthetic apparatus, particularly Rubisco, acclimates to rising atmospheric CO2 concentrations (ca). Elevated ca alters the control exerted by different enzymes of the Calvin cycle on the overall rate of photosynthetic CO2 assimilation, so altering the requirement for different functional proteins. A decreased flux of carbon through the photorespiratory pathway will decrease requirements for these enzymes. From modeling of the response of CO2 uptake (A) to intracellular CO2 concentration (ci) it is shown that the requirement for Rubisco is decreased at elevated ca, whilst that for proteins limiting ribulose 1,5 bisphosphate regeneration may be increased. This balance may be altered by other interactions, in particular plasticity of sinks for photoassimilate and nitrogen supply; hypotheses on these interactions are presented. It is speculated that increased accumulation of carbohydrate in leaves developed at elevated ca may signal the ‘down regulation’ of Rubisco. The molecular basis of this ‘down regulation’ is discussed in terms of the repression of photosynthetic gene expression by the elevated carbohydrate concentrations. This molecular model is then used to predict patterns of acclimation of perennials to long term growth in elevated ca.

Key words

elevated CO2 gene expression Rubisco rbcL rbcS 

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References

  1. Arp WJ (1991) Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14: 869–876Google Scholar
  2. Baker JT, Allen JLH, Boote KJ, Jones J and Jones JW (1989) Response of soybean to air temperature and carbon dioxide concentration. Crop Sci 29: 98–105Google Scholar
  3. Berry JO, Carr JP and Klessig DF (1988) mRNAs encoding ribulose-1,5-bisphosphate carboxylase remain bound to polysomes but are not translated in amaranth seedlings transferred to darkness. Proc Natl Acad Sci USA 85: 4190–4194Google Scholar
  4. Bowes G (1991) Growth at elevated CO2: Photosynthetic responses mediated through Rubisco. Plant Cell Environ 14: 795–806Google Scholar
  5. Cure JD, Rufty TW and Israel DW (1989) Alterations in soybean leaf development and photosynthesis in a CO2-enriched atmosphere. Botanical Gazette 150: 337–345Google Scholar
  6. Cure JD, Israel DW and Rufty TWJ (1988) Nitrogen stress effects on growth and seed yield of nonnodulated soybean exposed to elevated carbon dioxide. Crop Sci 28: 671–677Google Scholar
  7. Curtis PS, Drake BG, Leadly PW, Arp WJ and Whigham DF (1989) Growth and senescence in plant communities exposed to elevated CO2 concentrations on an estuarine marsh. Oecologia 78: 20–26Google Scholar
  8. Deng X-W and Gruissem W (1987) Control of plastid gene expression during development: The limited role of transcriptional regulation. Cell 49: 379–387Google Scholar
  9. Evans JR (1988) Acclimation by the thylakoid membranes to growth irradiance and the partitioning of nitrogen between soluble and thylakoid proteins. In: Evans JR (ed) Ecology of Photosynthesis in Sun and Shade, pp 93–106. CSIRO, CanberraGoogle Scholar
  10. Evans JR and Farquhar GD (1991) Modeling canopy photosynthesis from the biochemistry of the C3 chloroplast. In: Boote KJ and Loomis RS (eds) Modeling Crop Photosynthesis-From Biochemistry to Canopy, pp 1–16. Crop Science Society of America, Inc, Madison, WIGoogle Scholar
  11. Evans JR and Terashima I (1988) Photosynthetic characteristics of spinach leaves grown with different nitrogen treatments. Plant Cell Physiol 29: 157–168Google Scholar
  12. Farage PK, Long SP, Lechner EG and Baker NR (1991) The sequence of change within the photosynthetic apparatus of wheat following short-term exposure to ozone. Plant Physiol 95: 529–535Google Scholar
  13. Farquhar GD, VonCaemmerer S and Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149: 78–90Google Scholar
  14. Fujiwara S, Fukuzawa H, Tachiki A and Miyachi S (1990) Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 9779–9783Google Scholar
  15. Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisio-Sese ML and Miyachi S (1990) cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: Regulation by environmental CO2 concentration. Proc Natl Acad Sci USA 87: 4383–4387Google Scholar
  16. Gallagher TF, Jenkins GF and Ellis RJ (1985) Rapid modulation of transcription of nuclear genes encoding chloroplast proteins by light. FEBS Lett 186: 241–245Google Scholar
  17. Grime JP, Hodgson JG and Hunt R (1988) Comparative Plant Ecology: A Functional Approach. Unwin Hyman, LondonGoogle Scholar
  18. Hensel LL, Grbic V, Baumgarten DA and Bleecker AB (1993) Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissue in Arabadopsis. The Plant Cell 5: 553–564Google Scholar
  19. Herold A (1986) Regulation of photosynthesis by sink activity — the missing link. New Phytol 86: 131–144Google Scholar
  20. Hunt R, Hand DW, Hannah MA and Neal AM (1991) Response to CO2 enrichment in 27 herbaceous species. Functional Ecol 5: 410–421Google Scholar
  21. Idso SB and Kimball BA (1991) Downward regulation of photosynthesis and growth at high CO2 levels. Plant Physiol 96: 990–992Google Scholar
  22. Idso SB, Kimball BA and Mauney JR (1987) Effects of atmospheric CO2 enrichment on plant growth: The interactive role of air temperature. Agr Ecosys Environ 20: 1–10Google Scholar
  23. Kimball BA Mauney JR, Radin JW, Nakayama FS, Idso SB, Hendrix DL et al. (1986) Effects of increasing atmospheric CO2 on the growth, water relations and physiology of plants grown under optimal and limiting levels of water and nitrogen. In: Strain BR and Cure JD (eds) Direct Effects of Increasing Carbon Dioxide on Vegetation, pp 187–204. United States Department of Energy, Office of Energy Research, Carbon Dioxide Research Division, Washington DCGoogle Scholar
  24. Krapp A, Quick WP and Stitt M (1991) Ribulose-1,5-bisphosphate carboxylase oxygenase, other Calvin enzymes, and chlorophyll decrease when glucose is supplied to mature spinach leaves via the transpiration stream. Planta 186: 58–69Google Scholar
  25. Krapp A, Hofmann B, Schäfer C and Stitt M (1993) Regulation of the expression of rbcS and other photosynthetic genes by carbohydrates: A mechanism for the ‘sink regulation’ of photosynthesis? Plant J 3: 817–828Google Scholar
  26. Kriedemann PE and Wong SC (1984) Growth response and photosynthetic acclimation to CO2: Comparitive behavior in two C3 crop species. Acta Hort 162: 113–120Google Scholar
  27. Larigauderie A, Hilbert DW and Oechel WC (1988) Effect of CO2 enrichment and nitrogen availability on resource acquisition and resource allocation in a grass, Bromus mollis. Oecologia 77: 544–549Google Scholar
  28. Long SP (1985) Leaf gas exchange. In: Barber J and Baker NR (eds) Photosynthetic Mechanisms and the Environment, pp 453–499. Elsevier Science Publishers, AmsterdamGoogle Scholar
  29. Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: Has its importance been underestimated? Plant Cell Environ 14: 729–740Google Scholar
  30. Long SP and Drake BG (1992) Photosynthetic CO2 assimilation and rising atmospheric CO2 concentrations. In: Baker NR and Thomas H (eds) Crop Photosynthesis: Spatial and Temporal Determinants, pp 69–95. Elsevier Science Publishers, AmsterdamGoogle Scholar
  31. Long SP, Nie G-N, Drake BG, Farage PK, Hendrey GR and Lewin KH (1992) The implications of concurrent increases in temperature and CO2 concentration for terrestrial C3 photosynthesis. In: Murata N (ed) Photosynthesis Research, Vol IV, pp 811–817. Kluwer Academic Publishers, DordrechtGoogle Scholar
  32. Mullet JE and Klein RR (1987) Transcription and RNA stability are important determinants of higher plant chloroplast RNA levels. EMBO J 6: 1571–1579Google Scholar
  33. Nie G-Y and Long SP (1992) The effects of prolonged growth in elevated CO2 concentrations in the field on the amounts of different leaf proteins. In: Murata N (ed) Photosynthesis Research, Vol IV, pp 855–858. Kluwer Academic Publishers, DordrechtGoogle Scholar
  34. Peet MM, Huber SC and Patterson DT (1986) Acclimation to high CO2 in monoecious cucumbers II. Carbon exchange rates, enzyme activities, and starch and nutrient concentrations. Plant Physiol 80: 63–67Google Scholar
  35. Raines CA, Horsnell PR, Holder C and Lloyd JC (1992) Arabidopsis thaliana carbonic anhydrase: cDNA sequence and effect of CO2 on mRNA levels. Plant Mol Biol 20: 1143–1148Google Scholar
  36. Raines CA, Lloyd CJ and Dyer TA (1991) Molecular biology of the C3 photosynthetic carbon reduction cycle. Photosynth Res 27: 1–14Google Scholar
  37. Rodermel SR, Abbott MS and Bogorad L (1988) Nuclearorganelle interactions: Nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell 55: 673–681Google Scholar
  38. Sage RF, Sharkey TD and Seemann JR (1989) Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol 89: 590–596Google Scholar
  39. Schmidt GW and Mishkind ML (1983) Rapid degradation of unassembled ribulose 1,5-bisphosphate carboxylase small subunits in chloroplasts. Proc Natl Acad Sci USA 80: 2632–2636Google Scholar
  40. Sharkey TD and Socias X (1994) CO2 responses of photosynthesis in elevated CO2. In: Alscher R and Wellburn A (eds) Gaseous Pollutants and Plant Metabolism. Elsevier Applied Sci, London (in press)Google Scholar
  41. Sheen J (1990) Metabolic repression of transcription in higher plants. Plant Cell 2: 1027–1038Google Scholar
  42. Sheen J, Huang H, Schaeffner AR, Leon P and Jang J-C (1992) Sugars, fatty acids, and photosynthetic gene expression. Photosynth Res 34: 107Google Scholar
  43. Shirley BW and Meagher RB (1990) A potential role for mRNA turnover in the light regulation of plant gene expression: Ribulose-1,5-bisphosphate carboxylase small subunit in soybean. Nucleic Acids Res 18: 3377–3385Google Scholar
  44. Stitt M (1991) Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14: 741–762Google Scholar
  45. Stitt M, VonSchaewen A and Willmitzer L (1991) Sinkregulation of photosynthetic metabolism in transgenic tobacco plants expressing yeast invertase in their cell wall involves a decrease of the Calvin cycle enzymes and an increase of glycolytic enzymes. Planta 183: 40–50Google Scholar
  46. Thompson WF and White MJ (1991) Physiological and molecular studies of light-regulated nuclear genes in higher plants. Annu Rev Plant Physiol Plant Mol Biol 42: 423–466Google Scholar
  47. Vu JCV, Allen LH and Bowes G (1989) Leaf ultrastructure, carbohydrates and protein of soybeans grown under CO2 enrichment. Environ Exp Bot 29: 141–147Google Scholar
  48. Winder TL, Anderson JC and Spalding MH (1992) Translational regulation of the large and small subunits of ribulose bisphosphate carboxylase/oxygenase during induction of the CO2-concentrating mechanism in Chlamydomonas reinhardtii. Plant Physiol 98: 1409–1414Google Scholar
  49. Wong SC (1979) Elevated atmospheric partial pressure of CO2 and plant growth. I. Interactions of nitrogen nutrition and photosynthetic capacity in C3 and C4 plants. Oecologia: 68–74Google Scholar
  50. Yelle S, Beeson RCJr, Trudel MJ and Gosselin A (1989) Acclimation of two tomato species to high atmospheric CO2. I. Sugar and starch concentrations. Plant Physiol 90: 1465–1472Google Scholar

Copyright information

© Kluwer Academic Publishers 1994

Authors and Affiliations

  • Andrew N. Webber
    • 1
  • Gui-Ying Nie
    • 2
  • Stephen P. Long
    • 3
  1. 1.Department of Botany and Center for the Study of Early Events in PhotosynthesisArizona State UniversityTempeUSA
  2. 2.Department of Applied ScienceBrookhaven National LaboratoryUptonUSA
  3. 3.Department of BiologyUniversity of EssexColchesterUK

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