Distinctive diel growth cycles in leaves and cladodes of CAM plants: differences from C3 plants and putative interactions with substrate availability, turgor and cytoplasmic pH
Liezel M. Gouws A B C , C. Barry Osmond A D , Ulrich Schurr B and Achim Walter A B EA Biosphere 2 Laboratory, Columbia University, Oracle, AZ 85623, USA.
B Institute for Chemistry and Dynamics of the Geosphere: Phytosphere (ICG-III), Research Centre Jülich, 52425 Jülich, Germany.
C Institute of Plant Biotechnology, Stellenbosch University, Bloemfontein, South Africa.
D School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia.
E Corresponding author. Email: a.walter@fz-juelich.de
F This paper originates from a presentation at the IVth International Congress on Crassulacean Acid Metabolism, Tahoe City, California, USA, July–August 2004
Functional Plant Biology 32(5) 421-428 https://doi.org/10.1071/FP05074
Submitted: 1 April 2005 Accepted: 5 May 2005 Published: 27 May 2005
Abstract
Distinct diel rhythms of leaf and cladode expansion growth were obtained in crassulacean acid metabolism (CAM) plants under water-limited conditions, with maxima at mid-day during phase III of CO2 assimilation. This pattern coincided with the availability of CO2 for photosynthesis and growth during the decarboxylation of malic acid, with maximum cell turgor due to the nocturnally accumulated malic acid, and with the period of low cytoplasmic pH associated with malic acid movement from vacuole to cytosol. Maximum growth rates were generally only 20% of those in C3 plants and were reached at a different time of the day compared with C3 plants. The results suggest that malic acid, as a source of carbohydrates, and a determinant of turgor and cytoplasmic pH, plays a major role in the control of diel growth dynamics in CAM plants under desert conditions. The observed plasticity in phasing of growth rhythms under situations of differing water availability suggests that a complex network of factors controls the diel growth patterns in CAM plants and needs to be investigated further.
Keywords: image processing, Opuntia, spatio-temporal dynamics.
Acknowledgments
We thank Dr Ed Bobich for help with the experiments and for fruitful discussions, and Ralf Küsters for assistance with growth calibration measurements. The δ13C values were provided by Thanh Tran and Dr Karl Bil’. Financial support was provided by a Feodor Lynen Fellowship from the Alexander von Humboldt Stiftung, and by program enhancement grants made available by Dr Michael Crow, Executive Vice-Provost, Columbia University, for use in the Biosphere 2 Laboratory sustained by the generosity of Mr Edward P Bass.
Black, CC ,
Chen, J-Q ,
Doong, RL ,
Angelov, MV ,
and
Sung, SJS (1996). Alternative carbohydrate reserves used in the daily cycle of Crassulacean acid metabolism. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’ pp. 31–45. (Springer-Verlag: Berlin)
Borland AM, Dodd AN
(2002) Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Functional Plant Biology 29, 707–716.
| Crossref | GoogleScholarGoogle Scholar |
Christopher JT, Holtum JAM
(1996) Patterns of carbon partitioning in leaves of Crassulacean acid metabolism species during deacidification. Plant Physiology 112, 393–399.
| PubMed |
Cosgrove DJ
(1999) Enzymes and other agents that enhance cell wall extensibility. Annual Review of Plant Physiology and Plant Molecular Biology 50, 391–417.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Cushman JC, Bohnert HJ
(1999) Crassulacean acid metabolism: molecular genetics. Annual Review of Plant Physiology and Plant Molecular Biology 50, 305–332.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Dale JE
(1988) The control of leaf expansion. Annual Review of Plant Physiology and Plant Molecular Biology 39, 267–295.
| Crossref | GoogleScholarGoogle Scholar |
Haag-Kerwer A,
Franco AC, Lüttge U
(1992) The effect of temperature and light on gas exchange and acid accumulation in the C3–CAM plant Clusia minor L. Journal of Experimental Botany 43, 345–352.
Hafke JB,
Neff R,
Hütt M-T,
Lüttge U, Thiel G
(2001) Day-to-night variations of cytoplasmic pH in a crassulacean acid metabolism plant. Protoplasma 216, 164–170.
| PubMed |
Hanscom Z, Ting IP
(1977) Physiological responses to irrigation in Opuntia basilaris Engelm. & Bigel. Botanical Gazette 138, 159–167.
| Crossref | GoogleScholarGoogle Scholar |
Hartsock TL, Nobel PS
(1976) Watering converts a CAM plant to daytime CO2 uptake. Nature 262, 574–576.
Hartwell J,
Nimmo GA,
Wilkins MB,
Jenkins GI, Nimmo HG
(2002) Probing the circadian control of phosphoenolpyruvate carboxylase kinase expression in Kalanchoë fedtschenkoi.
Functional Plant Biology 29, 663–668.
| Crossref | GoogleScholarGoogle Scholar |
Holtum JAM, Osmond CB
(1981) The gluconeogenic metabolism of pyruvate during deacidification in plants performing Crassulacean acid metabolism. Australian Journal of Plant Physiology 8, 31–44.
Jones MGK,
Outlaw WH, Lowry OH
(1977) Enzymatic assay of 10–7 to10–14 moles of sucrose in plant tissue. Plant Physiology 60, 379–383.
Kluge, M ,
and
Ting, IP (1978).
Lüttge U, Ball E
(1977) Water relations parameters of the CAM plant Kalanchoë daigremontiana in relation to diurnal malate oscillations. Oecologia 31, 85–94.
| Crossref | GoogleScholarGoogle Scholar |
Lüttge U, Nobel PS
(1984) Day-night variations in malate concentration, osmotic pressure, and hydrostatic pressure in Cereus validus.
Plant Physiology 75, 804–807.
Nimmo HG
(2000) The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5, 75–80.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nobel, PS (1988).
Osmond CB
(1978) Crassulacean acid metabolism, a curiosity in context. Annual Review of Plant Physiology 29, 379–414.
| Crossref | GoogleScholarGoogle Scholar |
Osmond CB,
Nott DL, Firth PM
(1979) Carbon assimilation patterns and growth of the introduced CAM plant Opuntia inermis in Eastern Australia. Oecologia 40, 331–350.
| Crossref | GoogleScholarGoogle Scholar |
Robinson SA,
Osmond CB, Giles L
(1993) Interpretations of gradients in δ13C value in thick photosynthetic tissues of plants with Crassulacean acid metabolism. Planta 190, 271–276.
| Crossref | GoogleScholarGoogle Scholar |
Schmundt D,
Stitt M,
Jähne B, Schurr U
(1998) Quantitive analysis of the local rates of growth of dicot leaves at a high temporal and spatial resolution, using image sequence analysis. The Plant Journal 16, 505–514.
| Crossref | GoogleScholarGoogle Scholar |
Scharr, H ,
and
Küsters, R (2002). A linear model for simultaneous estimation of 3D motion and depth. In ‘Proceedings of IEEE workshop on motion and video computing: Motion 2000, Orlando, Florida, USA’. pp. 220–225.
Smith JAC, Lüttge U
(1985) Day-night changes in leaf water relations associated with the rhythm of crassulacean acid metabolism in Kalanchoe daigremontiana.
Planta 163, 272–282.
| Crossref | GoogleScholarGoogle Scholar |
Spoehr, HA (1919).
Steudle E,
Smith JAC, Lüttge U
(1980) Water relations parameters of individual mesophyll cells of the crassulacean acid metabolism plant Kalanchoë daigremontiana.
Plant Physiology 66, 1155–1163.
Szarek SR, Troughton JH
(1976) Carbon isotope ratios in crassulacean acid metabolism plants: seasonal patterns from plants in natural stands. Plant Physiology 58, 367–370.
Sutton BG
(1975) Glycolysis in CAM plants. Australian Journal of Plant Physiology 2, 389–402.
Taybi T,
Cushman JC, Borland AM
(2002) Environmental, hormonal and circadian regulation of crassulacean acid metabolism expression. Functional Plant Biology 29, 669–678.
| Crossref | GoogleScholarGoogle Scholar |
Walter A, Schurr U
(2005) Dynamics of leaf and root growth — endogenous control versus environmental impact. Annals of Botany 95, 891–900.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walter A,
Rascher U, Osmond B
(2004) Transitions in photosynthetic parameters of midvein and interveinal regions of leaves and their importance during leaf growth and development. Plant Biology 6, 184–191.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Walter A,
Christ MM,
Barron-Gafford GA,
Grieve KA,
Murthy R, Rascher U
(2005) The effect of elevated CO2 on diel leaf growth cycle, leaf carbohydrate content and canopy growth performance of Populus deltoides.
Global Change Biology In press ,
Wang N,
Zhang H, Nobel PS
(1998) Carbon flow and carbohydrate metabolism during sink-to-source transition for developing cladodes of Opuntia ficus-indica.
Journal of Experimental Botany 49, 1835–1843.
| Crossref | GoogleScholarGoogle Scholar |
Winter K
(1973) CO2-Fixierungsreaktionen bei der Salzpflanze Mesembryanthemum crystallinum unter variierten Außenbedingungen. Planta 114, 75–85.
| Crossref | GoogleScholarGoogle Scholar |
Winter, K ,
and
Smith, JAC (1996). Crassulacean acid metabolism: current status and perspectives. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. pp. 398–426. (Springer-Verlag: Berlin)
Winter K, Holtum JAM
(2002) How closely do the δ13C values of Crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night. Plant Physiology 129, 1843–1851.
| Crossref | GoogleScholarGoogle Scholar | PubMed |