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Key innovations in the evolution of Kranz anatomy and C₄ vein pattern in Flaveria (Asteraceae)¹

Department of Botany, University of Toronto, Toronto, Ontario, M5S 3B2, Canada

ABSTRACT

Kranz anatomy and C₄ vein pattern are required for C₄ biochemical functioning in C₄ plants; however, the evolutionary timing of anatomical and biochemical adaptations is unknown. From the genus Flaveria, 16 species (C₃, C₄, intermediates [C₃–C₄, C₄-like]) were analyzed, novel anatomical and vein pattern characters were analyzed and key anatomical differences among photosynthetic groups were highlighted. A stepwise acquisition of anatomical and vein pattern traits prior to derived biochemistry was outlined on the basis of the phylogeny of Flaveria. Increased vein density represents a potential "precondition" contributing to lower ratios of photosynthetic tissues (mesophyll, bundle sheath) and precedes further anatomical and biochemical modifications observed in derived C₃–C₄ intermediates. In derived Flaveria species, bundle sheath volume is modified through cell expansion, whereas mesophyll volume is altered through mesophyll cell expansion, reductions in the number of ground tissue layers, and increased vein density. Results demonstrated that key anatomical features of C₄ plants are also required for C₃–C₄ biochemical intermediacy, and anatomical and biochemical alterations acquired during evolution of intermediacy may predispose a species for evolution of C₄ photosynthesis. C₄-like species are similar to C₄ species, demonstrating that Kranz anatomy is fully evolved before complete C₄ biochemistry is achieved.

Key Words: bundle sheath • C₃–C₄ photosynthesis • C₄ photosynthesis • C₄-like photosynthesis • interveinal distance • mesophyll • parallel evolution • vein density

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