Gene Duplication, Neofunctionalization, and the Evolution of C4Photosynthesis

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.