Anatomy, chloroplast structure and compartmentation of enzymes relative to photosynthetic mechanisms in leaves and cotyledons of species in the tribe Salsoleae (Chenopodiaceae)

Certain members of the family Chenopodiaceae are the dominant species ofthe deserts of Central Asia; many of them are succulent halophytes whichexhibit C4-type CO2 fixation of the NAD- or NADP-ME (malic enzyme)subgroup. In four C4 species of the tribe Salsoleae, the Salsoloid-typeKranz anatomy in leaves or stems was studied in relation to the diversityin anatomy which was found in cotyledons. Halocharisgossypina, has C4 NAD-ME Salsoloid-type photosynthesis in leavesand C3 photosynthesis in dorsoventral non-Kranz cotyledons;Salsola laricina has C4 NAD-ME Salsoloid-type leavesand C4 NAD-ME Atriplicoid-type cotyledons; Haloxylonpersicum, has C4 NADP-ME Salsoloid-type green stems and C3isopalisade non-Kranz cotyledons; and S. richteri hasC4 NADP-ME Salsoloid-type leaves and cotyledons. Immunolocalization studieson Rubisco showed strong labelling in bundle sheath cells of leaves andcotyledons of organs having Kranz anatomy. The C4 pathway enzymephosphoenolpyruvate carboxylase was localized in mesophyll cells, while themalic enzymes were localized in bundle sheath cells of Kranz-type tissue.Immunolocalization by electron microscopy showed NAD-ME is in mitochondriawhile NADP-ME is in chloroplasts of bundle sheath cells in the respectiveC4 types. In some C4 organs, it was apparent that subepidermal cells andwater storage cells also contain some chloroplasts which have Rubisco,store starch, and thus perform C3 photosynthesis. In non-Kranz cotyledonsof Halocharis gossypina and Haloxylonpersicum, Rubisco was found in chloroplasts of both palisade andspongy mesophyll cells with the heaviest labelling in the layers ofpalisade cells, whereas C4 pathway proteins were low or undetectable. Thepattern of starch accumulation correlated with the localization of Rubisco,being highest in the bundle sheath cells and lowest in the mesophyll cellsof organs having Kranz anatomy. In NAD-ME-type Kranz organs (leaves andcotyledons of S. laricina and leaves of H.gossypina the granal index (length of appressed membranes as apercentage of total length of all membranes) of bundle sheath chloroplastsis 1.5 to 2.5 times higher than that of mesophyll chloroplasts. Incontrast, in the NADP-ME-type Kranz organs (S.richteri leaves and cotyledons and H.persicum stems) the granal index of mesophyll chloroplasts is1.5 to 2.2 times that of the bundle sheath chloroplasts. The mechanism ofphotosynthesis in these species is discussed in relation to structuraldifferences.