title: The unique structural and biochemical development of single cell C4 photosynthesis along longitudinal leaf gradients in Bienertia sinuspersici and Suaeda aralocaspica (Chenopodiaceae).
abstract: Temporal and spatial patterns of photosynthetic enzyme expression and structural maturation of chlorenchyma cells along longitudinal developmental gradients were characterized in young leaves of two single cell C4 species, Bienertia sinuspersici and Suaeda aralocaspica Both species partition photosynthetic functions between distinct intracellular domains. In the C4-C domain, C4 acids are formed in the C4 cycle during capture of atmospheric CO2 by phosphoenolpyruvate carboxylase. In the C4-D domain, CO2 released in the C4 cycle via mitochondrial NAD-malic enzyme is refixed by Rubisco. Despite striking differences in origin and intracellular positioning of domains, these species show strong convergence in C4 developmental patterns. Both progress through a gradual developmental transition towards full C4 photosynthesis, with an associated increase in levels of photosynthetic enzymes. Analysis of longitudinal sections showed undeveloped domains at the leaf base, with Rubisco rbcL mRNA and protein contained within all chloroplasts. The two domains were first distinguishable in chlorenchyma cells at the leaf mid-regions, but still contained structurally similar chloroplasts with equivalent amounts of rbcL mRNA and protein; while mitochondria had become confined to just one domain (proto-C4-D). The C4 state was fully formed towards the leaf tips, Rubisco transcripts and protein were compartmentalized specifically to structurally distinct chloroplasts in the C4-D domains indicating selective regulation of Rubisco expression may occur by control of transcription or stability of rbcL mRNA. Determination of CO2 compensation points showed young leaves were not functionally C4, consistent with cytological observations of the developmental progression from C3 default to intermediate to C4 photosynthesis.
authors.affiliation: Laboratory of Anatomy and Morphology, VL Komarov Botanical Institute of Russian Academy of Sciences, St Petersburg, 197376, Russia.
authors.forename: Nuria K
authors.identifier: 0000-0002-7507-4560
authors.initials: NK
authors.lastname: Koteyeva
authors.affiliation: Laboratory of Anatomy and Morphology, VL Komarov Botanical Institute of Russian Academy of Sciences, St Petersburg, 197376, Russia.
authors.forename: Elena V
authors.identifier: 0000-0002-5919-3340
authors.initials: EV
authors.lastname: Voznesenskaya
authors.affiliation: Department of Biological Sciences, State University of New York, Buffalo, NY 14260, USA.
authors.forename: James O
authors.initials: JO
authors.lastname: Berry
authors.affiliation: School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA.
authors.forename: Asaph B
authors.initials: AB
authors.lastname: Cousins
authors.affiliation: School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA edwardsg@wsu.edu.
authors.forename: Gerald E
authors.initials: GE
authors.lastname: Edwards
mesh_terms: D015153:Blotting, Western; D019663:Chenopodiaceae / Q000033:anatomy & histology / Q000166:cytology / Q000378:metabolism / Q000502:physiology*; D002736:Chloroplasts / Q000502:physiology; D010788:Photosynthesis; D018515:Plant Leaves / Q000033:anatomy & histology / Q000166:cytology / Q000378:metabolism / Q000502:physiology*; D012273:Ribulose-Bisphosphate Carboxylase / Q000378:metabolism
chemical_list: D012273:Ribulose-Bisphosphate Carboxylase
keywords: Bienertia sinuspersici; C4 plants; CO2 compensation point; Suaeda aralocaspica; development; immunolocalization; in situ hybridization; leaf anatomy; single cell C4 photosynthesis; ultrastructure.