C4 photosynthetic evolution : sub-types, diversity, and function within the grass tribe Paniceae

Abstract

Most plants convert sunlight into chemical energy using a process known as C[subscript 3] photosynthesis. However, some of the world's most successful plants instead use the C[subscript 4] photosynthetic pathway which allows them to more efficiently use water, nitrogen, and solar energy. In the past 30 million years, C4 photosynthesis has convergently evolved from C3 over 60 times and new lineages are in the process of evolving even today. Because of this complex evolutionary history, C[subscript 4] is not "one" uniform photosynthetic type, but a diverse collection of photosynthetic sub-types that are classically grouped according to their use of three different biochemical pathways. The grass tribe Paniceae is especially interesting in this aspect because it contains all three of these biochemical subtypes as well as important food and bioenergy crops. To better understand the evolution of C[subscript 4] photosynthesis, DNA and RNA sequencing were undertaken for various species from within the Paniceae and used for phylogenetic and comparative genomic studies. Cell type specific RNA expression profiling for the two major C4 cell types was also completed for representative species of each C[subscript 4] sub-type. Streamlined bioinformatics pipelines for both chloroplast and nuclear phylogenetics were developed for processing the data. These analyses resulted in: 1) The first "genome scale" phylogenetic tree of the grass tribe Paniceae, 2) The clearest evidence to date of the evolutionary relationships between the three classically defined C[subscript 4] sub-types, 3) The most convincing results to date that the chloroplast and nuclear phylogenies of the Paniceae are incongruent, 4) Evidence that this chloroplast nuclear incongruence is likely due to introgression and/or incomplete lineage sorting, and 5) Strong support for sub-type mixing as well as the existence of a PCK sub-type.