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

• Published in: Plant physiology (Bethesda) 2008-09, Vol.148 (1), p.593-610
• Main Authors: Lara, María Valeria, Offermann, Sascha, Smith, Monica, Okita, Thomas W., Andreo, Carlos Santiago, Edwards, Gerald E.
• Format: Article
• Language: English
• Subjects: Bioenergetics and Photosynthesis; Biological and medical sciences; Bundle sheath cells; Carbon Dioxide - metabolism; Carbon Isotopes - metabolism; Chenopodiaceae - cytology; Chenopodiaceae - physiology; Chlorenchyma; Chlorophyll - metabolism; Chloroplasts; Developmental biology; Enzymes; Fundamental and applied biological sciences. Psychology; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; Leaves; Light; Peptides - metabolism; Photosynthesis; Plant cells; Plant growth; Plant Leaves - cytology; Plant Leaves - growth & development; Plant Leaves - metabolism; Plant physiology and development; Plant Proteins - metabolism; Plants; Starches; Water - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.108.124008

Bienertia sinuspersici performs C₄ photosynthesis in individual chlorenchyma cells by the development of two cytoplasmic domains (peripheral and central) with dimorphic chloroplasts, an arrangement that spatially separates the fixation of atmospheric CO₂ into C₄ acids and the donation of CO₂ from C₄ acids to Rubisco in the C₃ cycle. In association with the formation of these cytoplasmic domains during leaf maturation, developmental stages were analyzed for the 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 Gly decarboxylase and Ser 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 toward C₄ photosynthesis. In most cases, there was a correlation between the accumulation of mRNA transcripts and the respective peptides, indicating at least partial control of the development of photosynthesis at the transcriptional level. During growth under moderate light, when branches containing mature leaves were enclosed in darkness for 1 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 1 month, there was a striking shift of the central cytoplasmic compartment toward the periphery of chlorenchyma cells; the mature leaves showed strong acclimation with a shade-type photosynthetic response to light while retaining C₄ features indicative of low photorespiration. These results indicate a progressive development of C₄ photosynthesis with differences in the control mechanisms for the expression of photosynthetic genes and peptide synthesis during leaf maturation and in response to light conditions.