C4 photosynthesis is a remarkable example of convergent evolution of a complex trait. It has independently evolved more than 70-times in monocotyledonous and dicotyledonous flowering plants, including at least two independent origins in the Brassicales. With few exceptions, all C4 plant species display a distinct leaf anatomy called Kranz-anatomy as well as similar metabolic and biochemical features. Using computational modeling, we have shown that C4 photosynthesis evolves from C3 photosynthesis on a smooth upward trajectory via C3-C4 intermediate states (Heckmann et al., 2013). C3-C4 intermediacy evolves via simple loss of function mutations and causes a nitrogen disbalance between leaf mesophyll and bundle sheath cells. Overcoming this nitrogen disbalance requires the shuttling of organic acids between mesophyll and bundle sheath cells, which under permissive conditions sets the system on a slippery slope towards C4 photosynthesis (Mallmann et al., 2014).
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