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Published on July 30, 2008; 10.1104/pp.108.124008

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Received June 3, 2008
Accepted July 21, 2008

Leaf development in the single-cell C4 system in Bienertia sinuspersici: Expression of genes and peptide levels for C4 metabolism in relation to chlorenchyma structure under different light conditions

Maria Valeria Lara , Sascha Offermann , Monica Smith , Thomas W. Okita , Carlos Santiago Andreo , and Gerald E. Edwards *

Centro de Estudios Fotosinteticos y Bioquimicos, Facultad de Ciencias Bioquimicas y Farmaceuticas. Suipacha 531, Rosario 2000, Argentina; School of Biological Sciences and Institute of Biological Chemistry Washington State University, Pullman, WA 99164 USA

* Corresponding author; email: edwardsg{at}wsu.edu.

Bienertia sinuspersici performs C4 photosynthesis in individual chlorenchyma cells by development of two cytoplasmic domains (peripheral and central) with dimorphic chloroplasts, an arrangement which spatially separates fixation of atmospheric CO2 into C4 acids and donation of CO2 from C4 acids to Rubisco in the C3 cycle. In association with formation of these cytoplasmic domains during leaf maturation, developmental stages were analyzed for expression of a number of photosynthetic genes including Rubisco small and large subunits and key enzymes of the C4 cycle. Early in development, Rubisco subunits, and glycine decarboxylase and serine hydroxymethyltransferase of the glycolate pathway, accumulated more rapidly than enzymes associated with the C4 cycle. The levels of pyruvate,Pi dikinase and phosphoenolpyruvate carboxylase were especially low until spatial cytoplasmic domains developed and leaves reached maturity, indicating a developmental transition towards C4 photosynthesis. In most cases, there was a correlation between accumulation of mRNA transcripts and the respective peptides, indicating at least partial control of development of photosynthesis at the transcriptional level. During growth under moderate light, when branches containing mature leaves were enclosed in darkness for one month, spatial domains were maintained and there was high retention of a number of photosynthetic peptides, including Rubisco subunits and pyruvate,Pi dikinase, despite a reduction in transcript levels. When plants were transferred from moderate to low light conditions for one month, there was a striking shift of the central cytoplasmic compartment towards the periphery of chlorenchyma cells; and, the mature leaves showed strong acclimation with a shade type photosynthetic response to light, while retaining C4 features indicative of low photorespiration. The results indicate a progressive development of C4 photosynthesis with differences in control mechanisms for expression of photosynthetic genes and peptide synthesis during leaf maturation and in response to light conditions.




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