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C4 anatomy can evolve via a single developmental change

Lundgren, Marjorie R., Dunning, Luke T., Olofsson, Jill K., Moreno‐Villena, Jose J., Bouvier, Jacques W., Sage, Tammy L., Khoshravesh, Roxana, Sultmanis, Stefanie, Stata, Matt, Ripley, Brad S., Vorontsova, Maria S., Besnard, Guillaume, Adams, Claire, Cuff, Nicholas, Mapaura, Anthony, Bianconi, Matheus E., Long, Christine M., Christin, Pascal‐Antoine, Osborne, Colin P.
Ecology letters 2019 v.22 no.2 pp. 302-312
Alloteropsis, C4 photosynthesis, grasses, leaves, phenotype
C₄ photosynthesis is a complex trait that boosts productivity in warm environments. Paradoxically, it evolved independently in numerous plant lineages, despite requiring specialised leaf anatomy. The anatomical modifications underlying C₄ evolution have previously been evaluated through interspecific comparisons, which capture numerous changes besides those needed for C₄ functionality. Here, we quantify the anatomical changes accompanying the transition between non‐C₄ and C₄ phenotypes by sampling widely across the continuum of leaf anatomical traits in the grass Alloteropsis semialata. Within this species, the only trait that is shared among and specific to C₄ individuals is an increase in vein density, driven specifically by minor vein development that yields multiple secondary effects facilitating C₄ function. For species with the necessary anatomical preconditions, developmental proliferation of veins can therefore be sufficient to produce a functional C₄ leaf anatomy, creating an evolutionary entry point to complex C₄ syndromes that can become more specialised.