Competing carboxylases: Circadian and metabolic regulation of Rubisco in C 3 and CAM Mesembryanthemum crystallinum L.

Plant, Cell and Environment

Volumn 35, Issue 7, 2012, Pages 1211-1220

  Davies, B N ^a   Griffiths, H ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Carbon isotope discrimination; Continuous light; Crassulacean acid metabolism (CAM); PEPc

Indexed keywords

CARBON DIOXIDE; PHOSPHOENOLPYRUVATE CARBOXYLASE; RIBULOSEBISPHOSPHATE CARBOXYLASE;

ACCUMULATION; CARBON ISOTOPE; CIRCADIAN RHYTHM; DICOTYLEDON; ENZYME ACTIVITY; GAS EXCHANGE; ISOTOPIC RATIO; LIGHT EFFECT; METABOLISM; TOLERANCE;

ARTICLE; CIRCADIAN RHYTHM; ENZYMOLOGY; LIGHT; MESEMBRYANTHEMUM; METABOLISM;

CARBON DIOXIDE; CIRCADIAN RHYTHM; LIGHT; MESEMBRYANTHEMUM; PHOSPHOENOLPYRUVATE CARBOXYLASE; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

CRASSULACEAE; MESEMBRYANTHEMUM; MESEMBRYANTHEMUM CRYSTALLINUM; TRITICUM AESTIVUM;

EID: 84862115671     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2012.02483.x     Document Type: Article

References (55)

1. Adams P., Nelson D.E., Yamada S., Chmara W., Jensen R.G., Bohnert H.J. & Griffiths H. (1998) Growth and development of Mesembryanthemum crystallinum (Aizoaceae). New Phytologist 138, 171-190.
2. Booij-James I.S., Swegle W.M., Edelman M. & Mattoo A.K. (2002) Phosphorylation of the D1 Photosystem II reaction center protein is controlled by an endogenous circadian rhythm. Plant Physiology 130, 2069-2075.
3. Borland A.M., Griffiths H., Hartwell J. & Smith J.A.C. (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. Journal of Experimental Botany 60, 2879-2896.
4. Boxall S.F., Foster J.M., Bohnert H.J., Cushman J.C., Nimmo H.G. & Hartwell J. (2005) Conservation and divergence of circadian clock operation in a stress-inducible Crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiology 137, 969-982.
5. Bradford M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilising the principle of protein dye binding. Analytical Biochemistry 72, 248-254.
6. Buchanan-Bollig I.C. & Smith J.A.C. (1984) Circadian rhythms in crassulacean acid metabolism: phase relationships between gas exchange, leaf water relations and malate metabolism in Kalanchoë daigremontiana. Planta 161, 314-319.
7. von Caemmerer S. & Edmondson D.L. (1986) Relationship between steady-state gas exchange, in vivo Ribulose bisphosphate carboxylase activity and some carbon reduction cycle intermediates in Raphanus sativus. Australian Journal of Plant Physiology 13, 669-688.
8. von Caemmerer S. & Farquhar G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153, 376-387.
9. Carter P.J., Nimmo H.G., Fewson C.A. & Wilkins M.B. (1990) Bryophyllum fedtschenkoi protein phosphatase type 2A can dephosphorylate phosphoenolpyruvate carboxylase. FEBS Letters 263, 233-236.
10. Casati P., Drincovich M.F., Edwards G.E. & Andreo C.S. (1999) Malate metabolism by NADP-malic enzyme in plant defense. Photosynthesis Research 61, 99-105.
11. Chang G.G. & Tong L. (2003) Structure and function of malic enzymes, a new class of oxidative decarboxylases. Biochemistry 42, 12721-12733.
12. Chen L.S., Lin Q. & Nose A. (2002) A comparative study on diurnal changes in metabolite levels in the leaves of three Crassulacean acid metabolism (CAM) species, Ananas comusus, Kalanchoe daigremontiana and K. pinnata. Journal of Experimental Botany 53, 341-350.
13. Cook R.M., Lindsay J.G., Wilkins M.B. & Nimmo H.G. (1995) Decarboxylation of malate in the Crassulacean acid metabolism plant Bryophyllum (Kalanchoe) fedtschenkoi. Plant Physiology 109, 1301-1307.
14. 3 photosynthesis and Crassulacean acid metabolism (CAM). Journal of Experimental Botany 59, 1875-1894.
15. Dodd A.N., Griffiths H., Taybi T., Cushman J.C. & Borland A.M. (2003) Integrating diel starch metabolism with the circadian and environmental regulation of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta 216, 789-797.
16. Dodd A.N., Parkinson K. & Webb A.A.R. (2004) Independent circadian regulation of assimilation and stomatal conductance in the ztl-1 mutant of Arabidopsis. New Phytologist 162, 63-70.
17. Dodd A.N., Salathia N., Hall A., Kevei E., Toth R., Nagy F., Hibberd J.M., Millar A.J. & Webb A.A.R. (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633.
18. 2 diffusion in leaves of higher plants. Australian Journal of Plant Physiology 13, 281-292.
19. Farquhar G.D., Ehleringer J.R. & Hubrick K.T. (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503-537.
20. Ferreyra M.L.F., Andreo C.S. & Podesta F.E. (2003) Purification and physical and kinetic characterization of a photosynthetic NADP-dependent malic enzyme from the CAM plant Aptenia cordifolia. The Plant Science 164, 95-102.
21. Fredeen A.L., Hennessey T.L. & Field C.B. (1991) Biochemical correlates of the circadian rhythm in photosynthesis in Phaseolus vulgaris. Plant Physiology 97, 415-419.
22. 4 species Flaveria bidentis. Plant Physiology 144, 1936-1945.
23. Graf A. & Smith A.M. (2011) Starch and the clock: the dark side of plant productivity. Trends in Plant Science 16, 169-175.
24. 4 carboxylation during Crassulacean acid metabolism. Planta 181, 604-610.
25. Griffiths H., Helliker B., Roberts A., Haslam R.P., Girnus J., Robe W.E., Borland A.M. & Maxwell K. (2002) Regulation of Rubisco activity in Crassulacean acid metabolism plants: better late than never. Functional Plant Biology 29, 689-696.
26. Griffiths H., Robe W.E., Girnus J. & Maxwell K. (2008) Leaf succulence determines the interplay between carboxylase systems and light use during crassulacean acid metabolism species. Journal of Experimental Botany 59, 1851-1861.
27. Harmer S.L., Hogenesch J.B., Straume M., Chang H.-S., Han B., Zhu T., Wang X., Kreps J.A. & Kay S.A. (2000) Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110-2113.
28. Hartwell J. (2005) The co-ordination of central plant metabolism by the circadian clock. Biochemical Society Transactions 33, 945-948.
29. Hartwell J., Smith L.H., Wilkins M.B., Jenkins G.I. & Nimmo H.G. (1996) Higher plant phosphoenolpyruvate carboxylase kinase is regulated at the level of translatable mRNA in response to light or a circadian rhythm. The Plant Journal 10, 1071-1078.
30. Hennessey T.L. & Field C.B. (1991) Circadian rhythms in photosynthesis: oscillations in carbon assimilation and stomatal conductance under constant conditions. Plant Physiology 96, 831-836.
31. Hennessey T.L., Freeden A.L. & Field C.B. (1993) Environmental effects of circadian rhythms in photosynthesis and stomatal opening. Planta 189, 369-376.
32. 18O incorporation into malic acid during nocturnal carbon dioxide fixation in Crassulacean acid metabolism plants - a new approach to estimating in vivo carbonic anhydrase activity. Journal of Biological Chemistry 259, 6870-6881.
33. Konieczny R., Obert B., Bleho J., Novák O., Heym C., Tuleja M., Müller J., Strnad M., Menzel D. & Samaj J. (2011) Stable transformation of Mesembryanthemum crystallinum (L.) with Agrobacterium rhizogenes harboring the green fluorescent protein targeted to the endoplasmic reticulum. Journal of Plant Physiology 168, 722-729.
34. Lonergan T.A. (1981) A circadian rhythm in the rate of light-induced electron flow in three leguminous species. Plant Physiology 68, 1041-1046.
35. 3 and Crassulacean acid metabolism epiphytic bromeliads. Functional Plant Biology 29, 679-687.
36. Maxwell K., Borland A.M., Haslam R.P., Helliker B.R., Roberts A. & Griffiths H. (1999) Modulation of Rubisco activity during the diurnal phases of the Crassulacean acid metabolism plant Kalanchoe daigremontiana. Plant Physiology 121, 849-856.
37. Moroney J.V., Bartlett S.G. & Samuelsson G. (2001) Carbonic anhydrases in plants and algae. Plant, Cell & Environment 24, 141-153.
38. Niewiadomska E., Bilger W., Gruca M., Mulisch M., Miszalski Z. & Krupinska K. (2011) CAM-related changes in chloroplastic metabolism of Mesembryanthemum crystallinum L. Planta 233, 275-285.
39. Nimmo G.A., Nimmo H.G., Hamilton H.D., Fewson C.A. & Wilkins M.B. (1984) Diurnal changes in the properties of phosphoenolpyruvate carboxylse from Bryophyllum fedtschenkoi. Biochemical Journal 239, 213-220.
40. Nimmo H.G. (2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5, 75-80.
41. O'Leary B., Park J. & Plaxton W.C. (2011) The remarkable diversity of plant PEPc (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPcs. Biochemical Journal 436, 15-34.
42. O'Neill J.S., van Ooijen G., Dixon L.E., Troein C., Corellou F., Bouget F., Reddy A.B. & Millar A.J. (2011) Circadian rhythms persist without transcription in a eukaryote. Nature 469, 554-558.
43. Osmond C.B. (1978) Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29, 379-414.
44. Pallas J.E. Jr, Samish Y.B. & Willmer C.M. (1974) Endogenous rhythmic activity of photosynthesis, transpiration, dark respiration, and carbon dioxide compensation point of peanut leaves. Plant Physiology 53, 907-911.
45. Plautz J.D., Straume M., Stanewsky R., Jamison C.F., Brandes C., Dowse H.B., Hall J.C. & Kay S.A. (1997) Quantitative analysis of Drosophila period gene transcription in living animals. Journal of Biological Rhythms 12, 204-217.
46. Portis A.R. (1995) The regulation of Rubisco by Rubisco activase. Journal of Experimental Botany 46, 1285-1291.
47. Portis A.R. (2003) Rubisco activase - Rubisco's catalytic chaperone. Photosynthesis Research 75, 11-27.
48. 2 fixation patterns and PEP-carboxylase properties. Journal of Plant Physiology 131, 285-296.
49. Tsuzuki M., Miyachi S., Winter K. & Edwards G.E. (1982) Localization of carbonic anhydrase in Crassulacean acid metabolism plants. Plant Science Letters 24, 211-218.
50. Vogt T., Ibdah M., Schmidt J., Wray V., Nimtz M. & Strack D. (1999) Light-induced betacyanin and flavonol accumulation in bladder cells of Mesembryanthemum crystallinum. Phytochemistry 52, 583-592.
51. Wilkins M.B. (1992) Circadian rhythms: their origin and control. New Phytologist 121, 347-375.
52. 2 exchange and control of the expression of Crassulacean acid metabolism in Mesembryanthemum crystallinum. Plant Physiology 143, 98-107.
53. 3 photosynthetic characteristics or performing Crassulacean acid metabxolism. Plant Physiology 69, 300-307.
54. 3 carboxylation to the circadian rhythm of carbon dioxide uptake in a Crassulacean acid metabolism plant Kalanchoe daigremontiana. Journal of Experimental Botany 54, 1471-1479.
55. Wyka T.P., Duarte H.M. & Lüttge U. (2005) Redundancy of stomatal control for the circadian photosynthetic rhythm in Kalanchoe daigremontiana Hamet et Perrier. Plant Biology 7, 176-181.