Plasmodesmal connectivity in C4 Gynandropsis gynandra is induced by light and dependent on photosynthesis

In leaves of C4 plants the reactions of photosynthesis become restricted between two compartments. Typically, this allows accumulation of C4 acids in mesophyll cells and subsequent decarboxylation in the bundle sheath. In C4 grasses proliferation of plasmodesmata between these cell types is thought to increase cell-to-cell connectivity to allow efficient metabolite movement. However, it is not known if C4 dicotyledons also show this enhanced plasmodesmal connectivity and so whether this is a general requirement for C4 photosynthesis is not clear. How mesophyll and bundle sheath cells in C4 leaves become highly connected is also not known. We investigated these questions using 3D- and 2D- electron microscopy on the C4 dicotyledon Gynandropsis gynandra as well as phylogenetically close C3 relatives. The mesophyll-bundle sheath interface of C4 G. gynandra showed higher plasmodesmal frequency compared with closely related C3 species. Formation of these plasmodesmata was induced by light. Pharmacological agents that perturbed chloroplast development or photosynthesis reduced the number of plasmodesmata, but this inhibitory effect could be reversed by the provision of exogenous sucrose. We conclude that enhanced formation of plasmodesmata between mesophyll and bundle sheath cells is wired to the induction of photosynthesis in C4 G. gynandra.