A Specific Transcriptome Signature for Guard Cells from the C 4 Plant Gynandropsis gynandra 1[OPEN]

International audienceC 4 photosynthesis represents an excellent example of convergent evolution that results in the optimization of both carbon and water usage by plants. In C 4 plants, a carbon-concentrating mechanism divided between bundle sheath and mesophyll cells increases photosynthetic efficiency. Compared with C 3 leaves, the carbon-concentrating mechanism of C 4 plants allows photosynthetic operation at lower stomatal conductance, and as a consequence, transpiration is reduced. Here, we characterize transcriptomes from guard cells in C 3 Tareneya hassleriana and C 4 Gynandropsis gynandra belonging to the Cleomaceae. While approximately 60% of Gene Ontology terms previously associated with guard cells from the C 3 model Arabidopsis (Arabidopsis thaliana) are conserved, there is much less overlap between patterns of individual gene expression. Most ion and CO 2 signaling modules appear unchanged at the transcript level in guard cells from C 3 and C 4 species, but major variations in transcripts associated with carbon-related pathways known to influence stomatal behavior were detected. Genes associated with C 4 photosynthesis were more highly expressed in guard cells of C 4 compared with C 3 leaves. Furthermore, we detected two major patterns of cell-specific C 4 gene expression within the C 4 leaf. In the first, genes previously associated with preferential expression in the bundle sheath showed continually decreasing expression from bundle sheath to mesophyll to guard cells. In the second, expression was maximal in the mesophyll compared with both guard cells and bundle sheath. These data imply that at least two gene regulatory networks act to coordinate gene expression across the bundle sheath, mesophyll, and guard cells in the C 4 leaf