Transcript residency on ribosomes reveals a key role for the Arabidopsis thaliana bundle sheath in sulfur and glucosinolate metabolism

• Published in: The Plant journal : for cell and molecular biology Vol. 78; no. 4; pp. 659 - 673
• Main Authors: Aubry, Sylvain, Smith‐Unna, Richard D, Boursnell, Chris M, Kopriva, Stanislav, Hibberd, Julian M
• Format: Journal Article
• Language: English
• Published: England Blackwell Science 01.05.2014; Blackwell Publishing Ltd
• Subjects: Alternative Splicing; Arabidopsis - cytology; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; biosynthesis; bundle sheath; C3 plants; C4 evolution; C4 plants; ERS374056–ERS374061; gene expression regulation; Gene Expression Regulation, Plant; genes; glucosinolates; Glucosinolates - metabolism; guard cells; leaves; Mesophyll Cells - metabolism; messenger RNA; Metabolic Networks and Pathways - genetics; Metabolism; Microscopy, Confocal; phloem companion cells; Photosynthesis - genetics; Plant biology; Plant Leaves - cytology; Plant Leaves - genetics; Plant Leaves - metabolism; Plant Roots - cytology; Plant Roots - genetics; Plant Roots - metabolism; Plant Vascular Bundle - cytology; Plant Vascular Bundle - metabolism; Plants, Genetically Modified; Protein Isoforms - genetics; Protein Isoforms - metabolism; Ribonucleic acid; ribosomes; Ribosomes - genetics; Ribosomes - metabolism; RNA; RNA, Messenger - genetics; RNA, Messenger - metabolism; sieve elements; sulfur; Sulfur - metabolism; translatome; Trehalose - metabolism; Arabidopsis thaliana; sulfur; bundle sheath; translatome; C4 evolution; ERS374056-ERS374061
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.12502

Leaves of angiosperms are made up of multiple distinct cell types. While the function of mesophyll cells, guard cells, phloem companion cells and sieve elements are clearly described, this is not the case for the bundle sheath (BS). To provide insight into the role of the BS in the C₃ species Arabidopsis thaliana, we labelled ribosomes in this cell type with a FLAG tag. We then used immunocapture to isolate these ribosomes, followed by sequencing of resident mRNAs. This showed that 5% of genes showed specific splice forms in the BS, and that 15% of genes were preferentially expressed in these cells. The BS translatome strongly implies that the BS plays specific roles in sulfur transport and metabolism, glucosinolate biosynthesis and trehalose metabolism. Much of the C₄ cycle is differentially expressed between the C₃ BS and the rest of the leaf. Furthermore, the global patterns of transcript residency on BS ribosomes overlap to a greater extent with cells of the root pericycle than any other cell type. This analysis provides the first insight into the molecular function of this cell type in C₃ species, and also identifies characteristics of BS cells that are probably ancestral to both C₃ and C₄ plants.