The Response of Leaf Tissues of the C₄ Euhalophyte Suaeda altissima (L.) Pall. To Salinity Stress

Impact of long-term (17-day) exposure to growth-stimulating (250 mM) and growth-inhibitory (750 mM) NaCl concentrations on biochemical characteristics related to C₄ pathway, anatomy and ultrastructure of chloroplasts of leaf tissues in the euhalophyte S. altissima was investigated. Immunological and biochemical studies identified C₄ enzymes, phosphoenol pyruvate carboxylase (PEPC), NAD-malic enzyme (NAD-ME), and NAD-malate dehydrogenase (NAD-MDH). Anatomical studies revealed Kranz anatomy with mesophyll (MCs) and Kranz cells (KCs) at the leaf periphery. Water-storage cells (WSCs) and vascular bundle chlorenchyma cells (VBCCs), both located in the leaf middle, contained chloroplasts, as did MCs and KCs. Electron microscopy revealed granal chloroplasts containing starch granules, while immunogold labeling revealed Rubisco in chloroplasts of all chlorophyllous tissues. The highest Rubisco content was found in KC chloroplasts. These results are consistent with the notion that S. altissima is a C₄ plant; however, they do not exclude its belonging to an intermediate C₃-C₄ form. The growth-stimulating NaCl concentration increased Rubisco content in all chlorophyllous tissues and activity of NAD-ME in leaves activating, probably, the C₄ pathway. In contrast, the growth-inhibitory NaCl concentration reduced Rubisco content, decreasing it below the level observed in the absence of NaCl. An increase in cell size was observed in the chlorophyllous tissues in response to both the growth-stimulating and growth-inhibitory salinity, leading to an increase in leaf succulence. The greatest increase in size was observed in WSCs. Chloroplasts from different tissues differed in their ability to maintain native structure and robustness of Rubisco-chloroplast binding under salinity, suggesting chloroplast heterogeneity and different Rubisco sensitivities to NaCl.