Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis

The evolution of C-4 photosynthesis provides one of the most interesting examples of evolutionary novelty in plants. As an adaptation that enhances plant carbon gain in warm climates with high light and relatively low atmospheric CO2 concentration, the complex interactions between C-4 anatomy and biochemistry appear to have evolved over thirty times independently within the angiosperms. Past theories have explained the multiple appearances of C-4 photosynthesis solely on the basis of global decreases in atmospheric CO2 concentration during the past 50 million years. The premise of such theories is that the C-4 pathway provides selective advantages in terms of plant carbon gain in an atmosphere of low CO2 concentration. These carbon balance theories, however, are limited in their ability to explain why or how C-4 photosynthesis evolved so many times independently and why certain patterns in the taxonomic distribution of C-4 photosynthesis exist; e. g., the absence of C-4 photosynthesis in canopy-forming forest tree species and the paucity of C-4 species within eudicots compared to monocots. In this review, I present the case that one of the most often overlooked aspects of C-4 evolution is the potential for genetic limitation, specifically that associated with gene duplication and subsequent modification, which is crucial to the evolution of C-4 biochemistry. I describe the research to date that provides insight into the origins of C-4 genes, and I derive the conclusion that the evolution of C-4 photosynthesis is largely a story of gene duplication while plants are still in the ancestral, C-3 state. Once a reservoir of key, duplicated, and preserved C-3 genes is present, a small amount of subsequent modification within gene promoter regions is all that is necessary to transform certain C-3 patterns of gene expression to C-4 patterns. Quantitative theory predicts that the most likely factors to be associated with the accumulation of a reservoir of duplicated C-3 genes are large population size, short generation time, and frequent recruitment of sexually produced individuals. When combined with the selective pressures of reduced atmospheric CO2 concentration, consideration of population and life history factors, and the genetic constraints that they impose, could help explain certain patterns of C-4 distribution.