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Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants

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Abstract

Most plants are known as C3 plants because the first product of photosynthetic CO2 fixation is a three-carbon compound1. C4 plants, which use an alternative pathway in which the first product is a four-carbon compound, have evolved independently many times and are found in at least 18 families2,3. In addition to differences in their biochemistry, photosynthetic organs of C4 plants show alterations in their anatomy and ultrastructure4. Little is known about whether the biochemical or anatomical characteristics of C4 photosynthesis evolved first. Here we report that tobacco, a typical C3 plant, shows characteristics of C4 photosynthesis in cells of stems and petioles that surround the xylem and phloem, and that these cells are supplied with carbon for photosynthesis from the vascular system and not from stomata. These photosynthetic cells possess high activities of enzymes characteristic of C4 photosynthesis, which allow the decarboxylation of four-carbon organic acids from the xylem and phloem, thus releasing CO2 for photosynthesis. These biochemical characteristics of C4 photosynthesis in cells around the vascular bundles of stems of C3 plants might explain why C4 photosynthesis has evolved independently many times.

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Figure 1: Distribution of chlorophyll in petioles of celery and tobacco.
Figure 2: Incorporation of 14C into insoluble material in cells around the vascular system of celery and tobacco.
Figure 3: Photosynthesis around the veins of C3 and C4 plants.

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Acknowledgements

We thank J. C. Gray and W. D. Jeschke for discussions. J.M.H. thanks the BBSRC for a Sir David Phillips Research Fellowship.

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Authors and Affiliations

  1. Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge, CB2 3EA,, UK

    Julian M. Hibberd

  2. Department of Animal and Plant Sciences, Robert Hill Institute, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK

    W. Paul Quick

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  1. Julian M. Hibberd
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  2. W. Paul Quick
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Correspondence to Julian M. Hibberd.

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Hibberd, J., Quick, W. Characteristics of C4 photosynthesis in stems and petioles of C3 flowering plants. Nature 415, 451–454 (2002). https://doi.org/10.1038/415451a

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