First published online July 24, 2003; 10.1104/pp.103.023481
Plant Physiology 132:2267-2275 (2003)
© 2003 American Society of Plant Biologists
BIOENERGETICS AND PHOTOSYNTHESIS
The Chlamydomonas reinhardtii cia3 Mutant Lacking a Thylakoid Lumen-Localized Carbonic Anhydrase Is Limited by CO2 Supply to Rubisco and Not Photosystem II Function in Vivo
David Thomas Hanson,
Linda A. Franklin,
Goran Samuelsson and
Murray R. Badger*
University of New Mexico, Department of Biology, Albuquerque, New Mexico
87131 (D.T.H.); Smithsonian Environmental Research Center, P.O. Box 28,
Edgewater, Maryland, 21037 (L.A.F.); Umeå Plant Science Center,
Department of Plant Physiology, University of Umeå, S–901 87
Umeå, Sweden (G.S.); and Molecular Plant Physiology Group, Research
School of Biological Sciences, Australian National University, G.P.O. Box 475,
Canberra, Australian Capital Territory 2601, Australia (M.R.B.)
The Chlamydomonas reinhardtii cia3 mutant has a phenotype
indicating that it requires high-CO2 levels for effective
photosynthesis and growth. It was initially proposed that this mutant was
defective in a carbonic anhydrase (CA) that was a key component of the
photosynthetic CO2-concentrating mechanism (CCM). However, more
recent identification of the genetic lesion as a defect in a lumenal CA
associated with photosystem II (PSII) has raised questions about the role of
this CA in either the CCM or PSII function. To resolve the role of this
lumenal CA, we re-examined the physiology of the cia3 mutant. We
confirmed and extended previous gas exchange analyses by using membrane-inlet
mass spectrometry to
monitor16O2,18O2, and
CO2 fluxes in vivo. The results demonstrate that PSII electron
transport is not limited in the cia3 mutant at low inorganic carbon
(Ci). We also measured metabolite pools sizes and showed that the RuBP pool
does not fall to abnormally low levels at low Ci as might be expected by a
photosynthetic electron transport or ATP generation limitation. Overall, the
results demonstrate that under low Ci conditions, the mutant lacks the ability
to supply Rubisco with adequate CO2 for effective CO2
fixation and is not limited directly by any aspect of PSII function. We
conclude that the thylakoid CA is primarily required for the proper
functioning of the CCM at low Ci by providing an ample supply of
CO2 for Rubisco.
*
Corresponding author; fax 011–61–2–6125–5075; e-mail
Murray.Badger{at}anu.edu.au.
Received March 13, 2003;
returned for revision April 17, 2003;
accepted May 15, 2003.
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