Comparative Transcriptome Atlases Reveal Altered Gene Expression Modules between Two Cleomaceae C3 and C4 Plant Species

C-4 photosynthesis outperforms the ancestral C-3 state in a wide range of natural and agro-ecosystems by affording higher water-use and nitrogen-use efficiencies. It therefore represents a prime target for engineering novel, high-yielding crops by introducing the trait into C-3 backgrounds. However, the genetic architecture of C-4 photosynthesis remains largely unknown. To define the divergence in gene expression modules between C-3 and C-4 photosynthesis during leaf ontogeny, we generated comprehensive transcriptome atlases of two Cleomaceae species, Gynandropsis gynandra (C-4) and Tarenaya hassleriana (C-3), by RNA sequencing. Overall, the gene expression profiles appear remarkably similar between the C-3 and C-4 species. We found that known C-4 genes were recruited to photosynthesis from different expression domains in C-3, including typical housekeeping gene expression patterns in various tissues as well as individual heterotrophic tissues. Furthermore, we identified a structure-related module recruited from the C-3 root. Comparison of gene expression patterns with anatomy during leaf ontogeny provided insight into genetic features of Kranz anatomy. Altered expression of developmental factors and cell cycle genes is associated with a higher degree of endoreduplication in enlarged C-4 bundle sheath cells. A delay in mesophyll differentiation apparent both in the leaf anatomy and the transcriptome allows for extended vein formation in the C-4 leaf.