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

Abstract

Recently, three Chenopodiaceae species, Bienertia cycloptera, Bienertia sinuspersici, and Suaeda aralocaspica, were shown to possess novel C 4 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.

Resolving the Compartmentation and Function of C4 Photosynthesis in the Single-Cell C4 Species Bienertia sinuspersici

“…Previous immunolocalization studies have shown that PPDK accumulates predominantly in the P-CP of B. cycloptera Chuong et al, 2006). This study shows that isolated P-CP are not only enriched in PPDK; indeed, they possess a fully functional pathway for the light-driven conversion of Pyr to PEP, which indicates that they function analogous to MC chloroplasts in Kranz-type C 4 species.…”

“…Based on the selective accumulation of PPDK in P-CP and RBCL in the C-CP in immunolocalization studies of B. sinuspersici, it was previously proposed that they function analogous to BSC and MC in Kranztype C 4 species (Voznesenskaya et al, 2002Chuong et al, 2006). However, the occurrence of an enzyme does not provide direct proof of a functional pathway or its capacity.…”

“…It has been established from gas-exchange measurements, isotope discrimination analysis, and in situ immunolocalization of a few photosynthetic enzymes that Bienertia species perform C 4 photosynthesis within a single photosynthetic cell (Voznesenskaya et al, 2002Chuong et al, 2006;Smith et al, 2009;Leisner et al, 2010). Accordingly, it has been proposed that in B. sinuspersici, P-CP might function analogous to MC and C-CP might function analogous to BSC in Kranz-type C 4 species; however, proof of function from studies at the subcellular level is lacking.…”

“…Recently, three species in family Chenopodiaceae have been shown to lack the requirement for Kranz anatomy in order to perform C 4 photosynthesis (Voznesenskaya et al, , 2002Chuong et al, 2006). Common to these so-called single-cell C 4 (SCC 4 ) species is that they do not possess MC and BSC but rather have two biochemically and morphologically different chloroplast types, which are spatially separated between two cytoplasmic domains within individual photosynthetic cells.…”

“…They have one chloroplast type distributed throughout the periphery (peripheral chloroplast [P-CP]) of the cell and the other chloroplast type (central compartment chloroplast [C-CP]) concentrated in a central compartment (CC) along with the mitochondria and peroxisomes, forming a ball-like structure in the center of the cell. The two compartments are spatially separated by a large vacuole and interconnected by a vacuole-spanning system of thin cytoplasmic channels Chuong et al, 2006).…”