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Differentiation of cellular and biochemical features of the single-cell C₄ syndrome during leaf development in Bienertia cycloptera (Chenopodiaceae)¹

²Laboratory of Anatomy and Morphology, V. L. Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov Street 2, 197376, St. Petersburg, Russia; ³School of Biological Sciences, Washington State University, Pullman, Washington 99164-4236 USA; ⁴Department of Biology, Faculty of Science, University of Tehran, P.O. Box 14155-6455, Tehran, Iran

ABSTRACT

The terrestrial plant Bienertia cycloptera has been shown to accomplish C₄ photosynthesis within individual chlorenchyma cells by spatially separating the phases of carbon assimilation into distinct peripheral and central compartments. In this study, anatomical, physiological, and biochemical techniques were used to determine how this unique compartmentation develops. Western blots show ribulose-1,5-bisphosphate carboxylase (Rubisco) (chloroplastic) is present in the youngest leaves and increases during development, while levels of C₄ enzymes—pyruvate,Pi dikinase (chloroplastic), phosphoenolpyruvate carboxylase (PEPC) (cytosol), and NAD-malic enzyme (mitochondrial)—increase later in development. Immunolocalization confirmed this for Rubisco and PEPC. The youngest chlorenchyma cells have a central nucleus surrounded by monomorphic granal chloroplasts containing Rubisco. Later stages show progressive development of a central cytoplasmic compartment enriched with chloroplasts and mitochondria and of a peripheral cytoplasm with chloroplasts. A complex reticulum of connections between the compartments also developed and was characterized. ¹³C isotope analyses show mature leaves have distinct C₄-type isotope composition, while the composition in younger leaves is "C₄-like." Based on the results, this form of single-cell C₄ photosynthesis develops from a common pool of organelles through partitioning to separate compartments, and the development of biochemically and ultrastructurally dimorphic chloroplasts.

Key Words: anatomy • Bienertia cycloptera • C₄ photosynthesis • C₄ plants • development • immunolocalization • ultrastructure

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