Most photorespiratory genes are preferentially expressed in the bundle sheath cells of the C(4) grass Sorghum bicolor

One of the hallmarks of C(4) plants is the division of labor between two different photosynthetic cell types, the mesophyll and the bundle sheath cells. C(4) plants are of polyphyletic origin and, during the evolution of C(4) photosynthesis, the expression of thousands of genes was altered and many genes acquired a cell type-specific or preferential expression pattern. Several lines of evidence, including computational modeling and physiological and phylogenetic analyses, indicate that alterations in the expression of a key photorespiration-related gene, encoding the glycine decarboxylase P subunit, was an early and important step during C(4) evolution. Restricting the expression of this gene to the bundle sheath led to the establishment of a photorespiratory CO(2) pump. We were interested in whether the expression of genes related to photorespiration remains bundle sheath specific in a fully optimized C(4) species. Therefore we analyzed the expression of photorespiratory and C(4) cycle genes using RNA in situ hybridization and transcriptome analysis of isolated mesophyll and bundle sheath cells in the C(4) grass Sorghum bicolor. It turns out that the C(4) metabolism of Sorghum is based solely on the NADP-dependent malic enzyme pathway. The majority of photorespiratory gene expression, with some important exceptions, is restricted to the bundle sheath.