Developmental and Subcellular Organization of Single-Cell C4 Photosynthesis in Bienertia sinuspersici Determined by Large-Scale Proteomics and cDNA Assembly from 454 DNA Sequencing

• Published in: Journal of proteome research Vol. 14; no. 5; pp. 2090 - 2108
• Main Authors: Offermann, Sascha, Friso, Giulia, Doroshenk, Kelly A, Sun, Qi, Sharpe, Richard M, Okita, Thomas W, Wimmer, Diana, Edwards, Gerald E, van Wijk, Klaas J
• Format: Journal Article
• Language: English
• Published: United States American Chemical Society 01.05.2015
• Subjects: Amaranthaceae - genetics; Amaranthaceae - metabolism; Carbon Dioxide - metabolism; Cell Compartmentation; Chloroplasts - classification; Chloroplasts - genetics; Chloroplasts - metabolism; DNA, Complementary - genetics; DNA, Complementary - metabolism; DNA, Plant - genetics; DNA, Plant - metabolism; Gene Expression Regulation, Developmental; Gene Expression Regulation, Plant; High-Throughput Nucleotide Sequencing; Molecular Sequence Annotation; Photosynthesis - genetics; Plant Cells - metabolism; Plant Leaves - cytology; Plant Leaves - metabolism; Proteomics; single-cell C4; proteomics; photosynthesis; Bienertia sinuspersici; carbon-concentrating mechanism; protein targeting; spectral counting; chloroplast development
• ISSN: 1535-3893; 1535-3907
• DOI: 10.1021/pr5011907

Kranz C4 species strictly depend on separation of primary and secondary carbon fixation reactions in different cell types. In contrast, the single-cell C4 (SCC4) species Bienertia sinuspersici utilizes intracellular compartmentation including two physiologically and biochemically different chloroplast types; however, information on identity, localization, and induction of proteins required for this SCC4 system is currently very limited. In this study, we determined the distribution of photosynthesis-related proteins and the induction of the C4 system during development by label-free proteomics of subcellular fractions and leaves of different developmental stages. This was enabled by inferring a protein sequence database from 454 sequencing of Bienertia cDNAs. Large-scale proteome rearrangements were observed as C4 photosynthesis developed during leaf maturation. The proteomes of the two chloroplasts are different with differential accumulation of linear and cyclic electron transport components, primary and secondary carbon fixation reactions, and a triose-phosphate shuttle that is shared between the two chloroplast types. This differential protein distribution pattern suggests the presence of a mRNA or protein-sorting mechanism for nuclear-encoded, chloroplast-targeted proteins in SCC4 species. The combined information was used to provide a comprehensive model for NAD-ME type carbon fixation in SCC4 species.