Gene duplication, neofunctionalization, and the evolution of C₄ photosynthesis

The evolution of C₄ 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 C₄ anatomy and biochemistry appear to have evolved over thirty times independently within the angiosperms. Past theories have explained the multiple appearances of C₄ 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 C₄ 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 C₄ photosynthesis evolved so many times independently and why certain patterns in the taxonomic distribution of C₄ photosynthesis exist; e.g., the absence of C₄ photosynthesis in canopy-forming forest tree species and the paucity of C₄ species within eudicots compared to monocots. In this review, I present the case that one of the most often overlooked aspects of C₄ evolution is the potential for genetic limitation, specifically that associated with gene duplication and subsequent modification, which is crucial to the evolution of C₄ biochemistry. I describe the research to date that provides insight into the origins of C₄ genes, and I derive the conclusion that the evolution of C₄ photosynthesis is largely a story of gene duplication while plants are still in the ancestral, C₃ state. Once a reservoir of key, duplicated, and preserved C₃ genes is present, a small amount of subsequent modification within gene promoter regions is all that is necessary to transform certain C₃ patterns of gene expression to C₄ patterns. Quantitative theory predicts that the most likely factors to be associated with the accumulation of a reservoir of duplicated C₃ 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 C₄ distribution.