Single nuclei sequencing reveals C₄photosynthesis is based on rewiring of ancestral cell identity networks

In multicellular systems changes to the patterning of gene expression drive modifications in cell function and trait evolution. One striking example is found in more than sixty plant lineages where compartmentation of photosynthesis between cell types allowed the evolution of the efficient C₄pathway from the ancestral C₃state. The molecular events enabling this transition are unclear. We used single nuclei sequencing to generate atlases for C₃rice and C₄sorghum during photomorphogenesis. Our analysis revealed that initiation of photosynthesis gene expression is conditioned by cell identity. In both species a conserved cistrome defines each cell type, and photosynthesis genes switching expression from mesophyll in rice to bundle sheath in sorghum acquire hallmarks of bundle sheath identity. The sorghum bundle sheath has also acquired gene networks associated with C₃guard cells. We conclude C₄photosynthesis is based on rewiring incisthat exapts cell identity networks of C₃plants.