Proof of C₄ photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae)

Abstract

SummaryKranz anatomy, with its separation of elements of the C 4 pathway between two cells, has been an accepted criterion for function of C 4 photosynthesis in terrestrial plants. However, Bienertia cycloptera (Chenopodiaceae), which grows in salty depressions of Central Asian semi-deserts, has unusual chlorenchyma, lacks Kranz anatomy, but has photosynthetic features of C 4 plants. Its photosynthetic response to varying CO 2 and O 2 is typical of C 4 plants having Kranz anatomy. Lack of night-time CO 2 ®xation indicates it is not acquiring carbon by Crassulacean acid metabolism. This species exhibits an independent, novel solution to function of the C 4 mechanism through spatial compartmentation of dimorphic chloroplasts, other organelles and photosynthetic enzymes in distinct positions within a single chlorenchyma cell. The chlorenchyma cells have a large, spherical central cytoplasmic compartment interconnected by cytoplasmic channels through the vacuole to the peripheral cytoplasm. This compartment is ®lled with mitochondria and granal chloroplasts, while the peripheral cytoplasm apparently lacks mitochondria and has grana-de®cient chloroplasts. Immunolocalization studies show enzymes compartmentalized selectively in the CC compartment, including Rubisco in chloroplasts, and NAD-malic enzyme and glycine decarboxylase in mitochondria, whereas pyruvate, Pi dikinase of the C 4 cycle is localized selectively in peripheral chloroplasts. Phosphoenolpyruvate carboxylase, a cytosolic C 4 cycle enzyme, is enriched in the peripheral cytoplasm. Our results show Bienertia utilizes strict compartmentation of organelles and enzymes within a single cell to effectively mimic the spatial separation of Kranz anatomy, allowing it to function as a C 4 plant having suppressed photorespiration; this raises interesting questions about evolution of C 4 mechanisms.

Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae)

“…4) Bienertia cycloptera (Voznesenskaya et al 2002;Voznesenskaya et al 2001) (Table 4). In contrast, terrestrial C 3 plants and aquatic plants lacking a biochemical concentrating mechanism have PEPC:RuBisCO ratios substantially less than 1 (Table 4).…”

“…NAD-ME is a mitochondrial enzyme that can act as the decarboxylating enzyme in the terrestrial single-celled C 4 plants B. aralocaspica and Bienertia cycloptera (Voznesenskaya et al 2002;Voznesenskaya et al 2001) (Table 4). The apparent decarboxylation by NAD-ME in Ottelia, if confirmed, would be the first report of an aquatic plant belonging to the NAD-ME C 4 -subtype.…”

“…However, a dramatic variant of C 4 plant was discovered in a submersed monocot, Hydrilla verticillata (Hydrocharitaceae; Holaday and Bowes 1980; Bowes 2011) that operates an inducible single-celled C 4 metabolism with CO 2 concentrating in the chloroplast. About a decade ago, C 4 metabolism was also described in single-cells of two land plants (Chenopodiaceae), Biernertia cycloptera and Borszczowia aralocapsica with RuBisCO and PEPC in different parts of the same cell (Edwards et al 2004;Voznesenskaya et al 2002;Voznesenskaya et al 2001). …”

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

“…As well as this diversity within the biochemistry of C 4 photosynthesis, there is also variation in terms of the leaf anatomy associated with the C 4 pathway. Although several examples of C 4 photosynthesis operating in single cells have been described (Reiskind et al, 1997;Casati et al, 2000;Reinfelder et al, 2000;Voznesenskaya et al, 2002Voznesenskaya et al, , 2003, most C 4 species compartmentalize carboxylation and decarboxylation activities into two distinct cell types. At least 22 variations of two-celled "Kranz" anatomy have been documented (Dengler and Nelson, 1999;Edwards and Voznesenskaya, 2011;Sage et al, 2012) whereby different cell types have been coopted as the photosynthetic carbon assimilation and photosynthetic carbon reduction tissue.…”

The Role of the C4 Pathway in Carbon Accumulation and Fixation in a Marine Diatom

“…The absence of upstream targeting sequences adjacent to the genes for PEPCase and PPDK in T. pseudonana is consistent with cytoplasmic localizations. The localization of PEPCase in the cytoplasm provides the necessary intracellular compartmentalization for simultaneous carbon fixation by PEPCase and Rubisco in a single cell (Magnin et al, 1997;Voznesenskaya et al, 2002). PEPCKase localization cannot be evaluated with certainty from the gene targeting sequence of T. pseudonana, but its activity was found to follow that of Rubisco in crude cell fractions of T. weissflogii (Reinfelder et al, 2000) and PEPCKase protein was immunolocalized within the chloroplast of the marine diatom Skeletonema costatum (Cabello-Pasini et al, 2001).…”