4.7 Article

Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C-3, intermediate, and C-4 photosynthesis

Journal

JOURNAL OF EXPERIMENTAL BOTANY
Volume 64, Issue 12, Pages 3583-3604

Publisher

OXFORD UNIV PRESS
DOI: 10.1093/jxb/ert191

Keywords

C-3 plants; C3C4 intermediate; C-4 plants; Chenopodiaceae; immunolocalization; leaf anatomy; photosynthetic enzymes; Salsola divaricata; Salsola genistoides; Salsola masenderanica; Salsola montana; Salsola webbii

Categories

Funding

  1. National Science Foundation [IBN 0641232, MCB 1146928]
  2. NSF Isotope Facility grant [DBI-0116203]
  3. Civilian Research and Development Foundation [RB1-2502-ST-03, RUB1-2829-ST-06, RUB1-2982-ST-10]
  4. Russian Foundation of Basic Research [10-04-92512, 12-04-00721]
  5. Research Council University of Tehran
  6. INSF [842951]
  7. Div Of Molecular and Cellular Bioscience [1146928] Funding Source: National Science Foundation

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In subfamily Salsoloideae (family Chenopodiaceae) most species are C-4 plants having terete leaves with Salsoloid Kranz anatomy characterized by a continuous dual chlorenchyma layer of Kranz cells (KCs) and mesophyll (M) cells, surrounding water storage and vascular tissue. From section Coccosalsola sensu Botschantzev, leaf structural and photosynthetic features were analysed on selected species of Salsola which are not performing C-4 based on leaf carbon isotope composition. The results infer the following progression in distinct functional and structural forms from C-3 to intermediate to C-4 photosynthesis with increased leaf succulence without changes in vein density: From species performing C-3 photosynthesis with Sympegmoid anatomy with two equivalent layers of elongated M cells, with few organelles in a discontinuous layer of bundle sheath (BS) cells (S. genistoides, S. masenderanica, S. webbii) > development of proto-Kranz BS cells having mitochondria in a centripetal position and increased chloroplast number (S. montana) > functional C3C4 intermediates having intermediate CO2 compensation points with refixation of photorespired CO2, development of Kranz-like anatomy with reduction in the outer M cell layer to hypodermal-like cells, and increased specialization (but not size) of a Kranz-like inner layer of cells with increased cell wall thickness, organelle number, and selective expression of mitochondrial glycine decarboxylase (Kranz-like Sympegmoid, S. arbusculiformis; and Kranz-like Salsoloid, S. divaricata) > selective expression of enzymes between the two cell types for performing C-4 with Salsoloid-type anatomy. Phylogenetic analysis of tribe Salsoleae shows the occurrence of C-3 and intermediates in several clades, and lineages of interest for studying different forms of anatomy.

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