On the significance of C3—C4 intermediate photosynthesis to the evolution of C4 photosynthesis

Authors

  • R. K. MONSON,

    Corresponding author
    1. Department of Environmental, Population and Organismic Biology, University of Colorado, Boulder, CO80309, U.S.A.
      Dr R. K. Monson, Department of EPO Biology, Campus Box 334, University of Colorado, Boulder, CO 80309, U.S.A.
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  • B. d. MOORE

    1. Department of Biochemistry, University of Nevada-Reno, Reno, NV 89557, U.S.A.
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Dr R. K. Monson, Department of EPO Biology, Campus Box 334, University of Colorado, Boulder, CO 80309, U.S.A.

Abstract

Abstract Evidence is drawn from previous studies to argue that C3—C4 intermediate plants are evolutionary intermediates, evolving from fully-expressed C3 plants towards fully-expressed C4 plants. On the basis of this conclusion, C3—C4 intermediates are examined to elucidate possible patterns that have been followed during the evolution of C4 photosynthesis. An hypothesis is proposed that the initial step in C4-evolution was the development of bundle-sheath metabolism that reduced apparent photorespiration by an efficient recycling of CO2 using RuBP carboxylase. The CO2-recycling mechanism appears to involve the differential compartmentation of glycine decarboxylase between mesophyll and bundle-sheath cells, such that most of the activity is in the bundlesheath cells. Subsequently, elevated phosphoenolpyruvate (PEP) carboxylase activities are proposed to have evolved as a means of enhancing the recycling of photorespired CO2. As the activity of PEP carboxylase increased to higher values, other enzymes in the C4-pathway are proposed to have increased in activity to facilitate the processing of the products of C4-assimilation and provide PEP substrate to PEP carboxylase with greater efficiency. Initially, such a ‘C4-cycle’ would not have been differentially compartmentalized between mesophyll and bundlesheath cells as is typical of fully-expressed C4 plants. Such metabolism would have limited benefit in terms of concentrating CO2 at RuBP carboxylase and, therefore, also be of little benefit for improving water- and nitrogen-use efficiencies. However, the development of such a limited C4-cycle would have represented a preadaptation capable of evolving into the leaf biochemistry typical of fully-expressed C4 plants. Thus, during the initial stages of C4-evolution it is proposed that improvements in photorespiratory CO2-loss and their influence on increasing the rate of net CO2 assimilation per unit leaf area represented the evolutionary ‘driving-force’. Improved resourceuse efficiency resulting from an efficient CO2-concentrating mechanism is proposed as the driving force during the later stages.

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