Evidence that inducible C4-type photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla, a submersed monocot

Hydrilla verticillata (L.L) Royle exhibits an inducible C4-type photosynthetic cycle, but lacks Kranz anatomy. Leaves in the C4-type state (but not C3-type) contained up to 5-fold higher internal dissolved inorganic carbon (DIC) concentrations than the medium, indicating that they possessed a CO2-co...

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Published in:	Plant, cell and environment Vol. 20; no. 2; pp. 211 - 220
Main Authors:	Reiskind, J.B, Madsen, T.V, Ginkel, L.C. van, Bowes, G
Format:	Journal Article
Language:	English
Published:	Oxford, UK Blackwell Publishing Ltd 1997 Blackwell
Subjects:	adenosine triphosphate Animal and plant ecology Animal, plant and microbial ecology Autoecology bicarbonate use Biological and medical sciences C3 photosynthesis, C4 photosynthesis carbon carbon dioxide chloroplasts cytochemistry Fundamental and applied biological sciences. Psychology gas exchange Hydrilla verticillata Hydrocharitaceae inhibition inorganic carbon internal dissolved inorganic carbon leaves Metabolism O2 inhibition oxygen pH polarity photosynthesis Photosynthesis, respiration. Anabolism, catabolism Plant physiology and development Plants and fungi Monocotyledones Oxygen Carbon dioxide Hydrocharitaceae C4-Type Ecophysiology Freshwater environment Regulation(control) Controlled environment study Angiospermae Spermatophyta Aquatic plant Biological accumulation Photosynthesis C3-Type
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Summary:	Hydrilla verticillata (L.L) Royle exhibits an inducible C4-type photosynthetic cycle, but lacks Kranz anatomy. Leaves in the C4-type state (but not C3-type) contained up to 5-fold higher internal dissolved inorganic carbon (DIC) concentrations than the medium, indicating that they possessed a CO2-concentrating mechanism (CCM). Several lines of evidence indicated that the chloroplast was the likely site of CO2 generation. From C4-type leaf [DIC] measurements, the estimated chloroplastic free [CO2] was 400 mmol m-3. This gave a calculated 2% O2 inhibition of photosynthesis, which was identical to the measured value, and provided independent evidence that the estimated [CO2] was close to the true value. A homogeneous distribution of DIC in the C4-type leaf could not account for such a high [CO2], or the resultant low O2 inhibition. For C3-type leaves the estimated chloroplastic [CO2] was only 7 mmol m-3, which gave high, and similar, calculated and measured O2 inhibition values of 22 and 26%, respectively. The CCM did not appear to be located at the plasma membrane, as it operated at low and high pH, indicating that it was independent of use of HCO3- from the medium. Also, both C3- and C4-type Hydrilla leaves showed pH polarity in the light, with abaxial and adaxial boundary layer values of about pH 4.0 and 10.5, respectively. Thus, pH polarity was not a direct component of the CCM, though it probably improved access to HCO3. Additionally, iodoacetamide and methyl viologen greatly reduced abaxial acidification, but not the steady-state CCM. Inhibitor studies suggested that the CCM required photosynthetically generated ATP, but Calvin cycle activity was not essential. Both leaf types accumulated DIC in the dark by an ATP-requiring process, possibly respiration, and C4-type leaves fixed CO2 at 11.8% of the light rate. The operation of a CCM to minimize photorespiration, and the ability to recapture respiratory CO2 at night, would conserve DIC in a densely vegetated lake environment where daytime [CO2] is severely limiting, while [O2] and temperatures are high.
ISSN:	0140-7791 1365-3040
DOI:	10.1046/j.1365-3040.1997.d01-68.x