TY - JOUR

T1 - Developmental and Subcellular Organization of Single-Cell C₄ Photosynthesis in Bienertia sinuspersici Determined by Large-Scale Proteomics and cDNA Assembly from 454 DNA Sequencing

AU - Offermann, Sascha

AU - Friso, Giulia

AU - Doroshenk, Kelly A

AU - Sun, Qi

AU - Sharpe, Richard M

AU - Okita, Thomas W

AU - Wimmer, Diana

AU - Edwards, Gerald E

AU - van Wijk, Klaas J

PY - 2015/5/1

Y1 - 2015/5/1

N2 - 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.

AB - 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.

KW - Amaranthaceae/genetics

KW - Carbon Dioxide/metabolism

KW - Cell Compartmentation

KW - Chloroplasts/classification

KW - DNA, Complementary/genetics

KW - DNA, Plant/genetics

KW - Gene Expression Regulation, Developmental

KW - Gene Expression Regulation, Plant

KW - High-Throughput Nucleotide Sequencing

KW - Molecular Sequence Annotation

KW - Photosynthesis/genetics

KW - Plant Cells/metabolism

KW - Plant Leaves/cytology

KW - Proteomics

U2 - 10.1021/pr5011907

DO - 10.1021/pr5011907

M3 - Article

C2 - 25772754

VL - 14

SP - 2090

EP - 2108

JO - Journal of proteome research

JF - Journal of proteome research

SN - 1535-3893

IS - 5

ER -