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The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species

Simon D.X. Chuong, Vincent R. Franceschi, Gerald E. Edwards
Simon D.X. Chuong
School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236
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Vincent R. Franceschi
School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236
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Gerald E. Edwards
School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236
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Published September 2006. DOI: https://doi.org/10.1105/tpc.105.036186

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Abstract

Recently, three Chenopodiaceae species, Bienertia cycloptera, Bienertia sinuspersici, and Suaeda aralocaspica, were shown to possess novel C4 photosynthesis mechanisms through the compartmentalization of organelles and photosynthetic enzymes into two distinct regions within a single chlorenchyma cell. Bienertia has peripheral and central compartments, whereas S. aralocaspica has distal and proximal compartments. This compartmentalization achieves the equivalent of spatial separation of Kranz anatomy, including dimorphic chloroplasts, but within a single cell. To characterize the mechanisms of organelle compartmentalization, the distribution of the major organelles relative to the cytoskeleton was examined. Examination of the distribution of the cytoskeleton using immunofluorescence studies and transient expression of green fluorescent protein–tagged cytoskeleton markers revealed a highly organized network of actin filaments and microtubules associating with the chloroplasts and showed that the two compartments in each cell had different cytoskeletal arrangements. Experiments using cytoskeleton-disrupting drugs showed in Bienertia and S. aralocaspica that microtubules are critical for the polarized positioning of chloroplasts and other organelles. Compartmentalization of the organelles in these species represents a unique system in higher plants and illustrates the degree of control the plant cell has over the organization and integration of multiorganellar processes within its cytoplasm.

  • Received July 14, 2005.
  • Revised June 28, 2006.
  • Accepted July 21, 2006.
  • Published August 11, 2006.
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The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species
Simon D.X. Chuong, Vincent R. Franceschi, Gerald E. Edwards
The Plant Cell Sep 2006, 18 (9) 2207-2223; DOI: 10.1105/tpc.105.036186

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The Cytoskeleton Maintains Organelle Partitioning Required for Single-Cell C4 Photosynthesis in Chenopodiaceae Species
Simon D.X. Chuong, Vincent R. Franceschi, Gerald E. Edwards
The Plant Cell Sep 2006, 18 (9) 2207-2223; DOI: 10.1105/tpc.105.036186
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The Plant Cell Online: 18 (9)
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Vol. 18, Issue 9
September 2006
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