Carbonic anhydrase and the molecular evolution of C4 photosynthesis

Abstract

C4 photosynthesis, a biochemical CO2-concentrating mechanism (CCM), evolved more than 60 times within the angiosperms from C3 ancestors. The genus Flaveria, which contains species demonstrating C3, C3-C4, C4-like or C4 photosynthesis, is a model for examining the molecular evolution of the C4 pathway. Work with carbonic anhydrase (CA), and C3 and C4Flaveria congeners has added significantly to the understanding of this process. The C4 form of CA3, a β-CA, which catalyses the first reaction in the C4 pathway by hydrating atmospheric CO2 to bicarbonate in the cytosol of mesophyll cells (mcs), evolved from a chloroplastic C3 ancestor. The molecular modifications to the ancestral CA3 gene included the loss of the sequence encoding the chloroplast transit peptide, and mutations in regulatory regions that resulted in high levels of expression in the C4 mesophyll. Analyses of the CA3 proteins and regulatory elements from Flaveria photosynthetic intermediates indicated C4 biochemistry very likely evolved in a specific, stepwise manner in this genus. The details of the mechanisms involved in the molecular evolution of other C4 plant β-CAs are unknown; however, comparative genetics indicate gene duplication and neofunctionalization played significant roles as they did in Flaveria. The current knowledge of carbonic anhydrase multigene families in plants using C4 photosynthesis is reviewed, and the novel insights this enzyme has given into the molecular evolution of this photosynthetic pathway are highlighted. Work with members of the genus Flaveria is described as a case study, and consideration is also given to carbonic anhydrases from C4 plants for which there is whole genome sequence information. With the current interest in C4 plants as sustainable sources of fuel, the transfer of the C4 pathway into C3 crops, and the evolution of angiosperms, the information presented is of interest to plant physiologists and molecular and evolutionary biologists. © 2011 Blackwell Publishing Ltd.