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Proof of C 4 photosynthesis without Kranz anatomy in Bienertia cycloptera (Chenopodiaceae)
Author(s) -
Voznesenskaya Elena V.,
Franceschi Vincent R.,
Kiirats Olavi,
Artyusheva Elena G.,
Freitag Helmut,
Edwards Gerald E.
Publication year - 2002
Publication title -
the plant journal
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 3.058
H-Index - 269
eISSN - 1365-313X
pISSN - 0960-7412
DOI - 10.1046/j.1365-313x.2002.01385.x
Subject(s) - crassulacean acid metabolism , chloroplast , phosphoenolpyruvate carboxylase , biology , photosynthesis , cytoplasm , rubisco , compartment (ship) , plastid , cellular compartment , organelle , biochemistry , microbiology and biotechnology , cell , oceanography , gene , geology
Summary Kranz 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 fixation 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 filled with mitochondria and granal chloroplasts, while the peripheral cytoplasm apparently lacks mitochondria and has grana‐deficient 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.