Mechanism of C(4) Photosynthesis: the Size and Composition of the Inorganic Carbon Pool in Bundle Sheath Cells

Overview

Journal Plant Physiol

Specialty Physiology

Date 1987 Dec 1

PMID 16665838

Citations 59

Authors

R T Furbank

M D Hatch

Affiliations

Soon will be listed here.

Abstract

We sought to characterize the inorganic carbon pool (CO(2) plus HCO(3) (-)) formed in the leaves of C(4) plants when C(4) acids derived from CO(2) assimilation in mesophyll cells are decarboxylated in bundle sheath cells. The size and kinetics of labeling of this pool was determined in six species representative of the three metabolic subgroups of C(4) plants. The kinetics of labeling of the inorganic carbon pool of leaves photosynthesizing under steady state conditions in (14)CO(2) closely paralleled those for the C-4 carboxyl of C(4) acids for all species tested. The inorganic carbon pool size, determined from its (14)C content at radioactivity saturation, ranged between 15 and 97 nanomoles per milligram of leaf chlorophyll, giving estimated concentrations in bundle sheath cells of between 160 and 990 micromolar. The size of the pool decreased, together with photosynthesis, as light was reduced from 900 to 95 microeinsteins per square meter per second or as external CO(2) was reduced from 400 to 98 microliters per liter. A model is developed which suggests that the inorganic carbon pool existing in the bundle sheath cells of C(4) plants during steady state photosynthesis will comprise largely of CO(2); that is, CO(2) will only partially equlibrate with bicarbonate. This predominance of CO(2) is believed to be vital for the proper functioning of the C(4) pathway.

Citing Articles

Increasing Rubisco as a simple means to enhance photosynthesis and productivity now without lowering nitrogen use efficiency.

Salesse-Smith C, Wang Y, Long S New Phytol. 2024; 245(3):951-965.

PMID: 39688507 PMC: 11711929. DOI: 10.1111/nph.20298.

Cell wall thickness spectrum of photosynthetic cells in herbaceous C, C, and crassulacean acid metabolism plants.

Ueno O J Plant Res. 2024; 138(2):197-213.

PMID: 39658745 DOI: 10.1007/s10265-024-01603-7.

Using Carbon Stable Isotopes to Study C and C Photosynthesis: Models and Calculations.

Ubierna N, Holloway-Phillips M, Wingate L, Ogee J, Busch F, Farquhar G Methods Mol Biol. 2024; 2790:163-211.

PMID: 38649572 DOI: 10.1007/978-1-0716-3790-6_10.

Overexpression of chloroplastic Zea mays NADP-malic enzyme (ZmNADP-ME) confers tolerance to salt stress in Arabidopsis thaliana.

Kandoi D, Tripathy B Photosynth Res. 2023; 158(1):57-76.

PMID: 37561272 DOI: 10.1007/s11120-023-01041-x.

Short- and long-term warming events on photosynthetic physiology, growth, and yields of field grown crops.

Bernacchi C, Ruiz-Vera U, Siebers M, DeLucia N, Ort D Biochem J. 2023; 480(13):999-1014.

PMID: 37418286 PMC: 10422931. DOI: 10.1042/BCJ20220433.

References

Hatch M . Mechanism of C4 photosynthesis in Chloris gayana: pool sizes and kinetics of 14CO2 incorporation into 4-carbon and 3-carbon intermediates. Arch Biochem Biophys. 1979; 194(1):117-27. DOI: 10.1016/0003-9861(79)90601-5. View

Jordan D, Chollet R . Inhibition of ribulose bisphosphate carboxylase by substrate ribulose 1,5-bisphosphate. J Biol Chem. 1983; 258(22):13752-8. View

Schurmann P . Separation of phosphate esters and algal extracts by thin-layer electrophoresis and chromatography. J Chromatogr. 1969; 39(4):507-9. View

Heldt W, Werdan K, Milovancev M, Geller G . Alkalization of the chloroplast stroma caused by light-dependent proton flux into the thylakoid space. Biochim Biophys Acta. 1973; 314(2):224-41. DOI: 10.1016/0005-2728(73)90137-0. View

Jenkins C, Burnell J, Hatch M . Form of inorganic carbon involved as a product and as an inhibitor of c(4) Acid decarboxylases operating in c(4) photosynthesis. Plant Physiol. 1987; 85(4):952-7. PMC: 1054375. DOI: 10.1104/pp.85.4.952. View

Johnson H, Hatch M . The C4-dicarboxylic acid pathway of photosynthesis. Identification of intermediates and products and quantitative evidence for the route of carbon flow. Biochem J. 1969; 114(1):127-34. PMC: 1184804. DOI: 10.1042/bj1140127. View

Belknap W, Portis A . Exchange Properties of the Activator CO(2) of Spinach Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase. Plant Physiol. 1986; 80(3):707-10. PMC: 1075187. DOI: 10.1104/pp.80.3.707. View

Cooper T, Filmer D . The active species of "CO2" utilized by ribulose diphosphate carboxylase. J Biol Chem. 1969; 244(3):1081-3. View

Hatch M, Heldt H . Synthesis, storage, and stability of [4-14C]oxaloacetic acid. Anal Biochem. 1985; 145(2):393-7. DOI: 10.1016/0003-2697(85)90379-3. View

10.

Hatch M . The C 4 -pathway of photosynthesis. Evidence for an intermediate pool of carbon dioxide and the identity of the donor C 4 -dicarboxylic acid. Biochem J. 1971; 125(2):425-32. PMC: 1178076. DOI: 10.1042/bj1250425. View

11.

Hatch M, Slack C . Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation. Biochem J. 1966; 101(1):103-11. PMC: 1270070. DOI: 10.1042/bj1010103. View

12.

Wong S, Cowan I, Farquhar G . Leaf Conductance in Relation to Rate of CO(2) Assimilation: I. Influence of Nitrogen Nutrition, Phosphorus Nutrition, Photon Flux Density, and Ambient Partial Pressure of CO(2) during Ontogeny. Plant Physiol. 1985; 78(4):821-5. PMC: 1064830. DOI: 10.1104/pp.78.4.821. View