A comparative anatomical and biochemical analysis in Salsola (Chenopodiaceae) species with and without a Kranz type leaf anatomy: A possible reversion of C-4 to C-3 photosynthesis

Leaf anatomy was studied by light and electron microscopy and the leaf activities of RUBP carboxylase, PEP carboxylase, and malic enzyme were assayed in: Salsola australis and S. oreophila grown on the West Pamirs at 1800 m altitude; in S. australis grown on the East Pamirs at 3860 m; and in S. arbusculiformis grown in the Kisil-Kum desert in Middle Asia near 500 m. Carbon isotope fractionation ratio values also were measured on whole leaf tissue for 18 Salsola species field collected in these and other regions of the former USSR. S. australis leaves are cylindrical and in cross section exhibit a peripheral ring of mesophyll and then an inner ring of bundle sheath type cells; and its biochemical characteristics and delta(13)C values are typical of a C-4 species of the NADP-malic enzyme malate-forming group. These traits were expressed independent of the plant growth altitude up to 4000 m. C-4 type delta(13)C values were obtained in 14 of the Salsola species. Anatomical, structural, and biochemical features typical of the C-4 syndrome were absent in S. oreophila and S. arbusculiformis. Four Salsola species, including these two, had C-3-type delta(13)C values. Their cylindrical leaves in cross section exhibited two to three peripheral rings as layers of palisade parenchyma. Although their vascular bundles were surrounded by green bundle sheath cells, their organelle numbers were comparable to those in mesophyll cells. Neither bundle sheath cell wall thickenings nor dimorphic chloroplasts in two leaf cell types were observed. In S. oreophila, there was a high activity of RuBP carboxylase, but a low activity of C-4 cycle enzymes. Interpretation of these data lends evidence to the hypothesis that a small group of C-3 Salsola species, including S. oreophila, S. arbusculiformis, S. montana, and S. pachyphylla, arose as the result of it reversion of a C-4 to a C-3 type of photosynthetic CO2 fixation in the cooler climates of Middle Asia.