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

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 implicates the BS in specific roles in sulphur 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 indicates that at least some of the characteristics of BS cells in C4 plants are likely ancestral traits unrelated to the C4 photosynthesis.