First published online June 12, 2003; 10.1104/pp.103.021246
Plant Physiology 132:1577-1585 (2003)
© 2003 American Society of Plant Biologists
BIOENERGETICS AND PHOTOSYNTHESIS
C4 Photosynthesis at Low Temperature. A Study Using Transgenic Plants with Reduced Amounts of Rubisco1
David S. Kubien*,2,
Susanne von Caemmerer,
Robert T. Furbank and
Rowan F. Sage
Department of Botany, University of Toronto, 25 Willcocks Street,
Toronto, Ontario, Canada M5S 3B2 (D.S.K., R.F.S.); Research School of
Biological Sciences, Australian National University, G.P.O. 475, Canberra
2601, Australia (S.v.C.); and Commonwealth Scientific and Industrial Research
Organisation, Division of Plant Industry, G.P.O. 1600, Canberra 2601,
Australia (R.T.F.)
C4 plants are rare in the cool climates characteristic of high
latitudes and elevations, but the reasons for this are unclear. We tested the
hypothesis that CO2 fixation by Rubisco is the rate-limiting step
during C4 photosynthesis at cool temperatures. We measured
photosynthesis and chlorophyll fluorescence from 6°C to 40°C, and in
vitro Rubisco and phosphoenolpyruvate carboxylase activity from
0°C to 42°C, in Flaveria bidentis modified by an antisense
construct (targeted to the nuclear-encoded small subunit of Rubisco,
anti-RbcS) to have 49% and 32% of the wild-type Rubisco content.
Photosynthesis was reduced at all temperatures in the anti-Rbcs
plants, but the thermal optimum for photosynthesis (35°C) did not differ.
The in vitro turnover rate (kcat) of fully carbamylated Rubisco was
3.8 mol mol–1 s–1 at
24°C, regardless of genotype. The in vitro kcat (Rubisco Vcmax
per catalytic site) and in vivo kcat (gross photosynthesis per
Rubisco catalytic site) were the same below 20°C, but at warmer
temperatures, the in vitro capacity of the enzyme exceeded the realized rate
of photosynthesis. The quantum requirement of CO2 assimilation
increased below 25°C in all genotypes, suggesting greater leakage of
CO2 from the bundle sheath. The Rubisco flux control coefficient
was 0.68 at the thermal optimum and increased to 0.99 at 6°C. Our results
thus demonstrate that Rubisco capacity is a principle control over the rate of
C4 photosynthesis at low temperatures. On the basis of these
results, we propose that the lack of C4 success in cool climates
reflects a constraint imposed by having less Rubisco than their C3
competitors.
Article, publication date, and citation information can be found at
www.plantphysiol.org/cgi/doi/10.1104/pp.103.021246.
1 This work was supported by the Natural Sciences and Engineering Research
Council of Canada (grant no. OGP0154273 to R.F.S.).
2 Present address: Institute of Molecular BioSciences, Massey University,
Private Bag 11 222, Palmerston North, New Zealand.
*
Corresponding author; e-mail
d.kubien{at}massey.ac.hz;
fax 64–6–350–5688.
Received January 29, 2003;
returned for revision February 19, 2003;
accepted March 24, 2003.
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