Gene and genome duplications and the origin of C4 photosynthesis: Birth of a trait in the Cleomaceae

Abstract

C4 photosynthesis is a trait that has evolved in 66 independent plant lineages and increases the efficiency of carbon fixation. The shift from C3 to C4 photosynthesis requires substantial changes to genes and gene functions effecting phenotypic, physiological and enzymatic changes. We investigate the role of ancient whole genome duplications (WGD) as a source of new genes in the development of this trait and compare expression between paralog copies. We compare Gynandropsis gynandra, the closest relative of Arabidopsis that uses C4 photosynthesis, with its C3 relative Tarenaya hassleriana that underwent a WGD named Th-α. We establish through comparison of paralog synonymous substitution rate that both species share this paleohexaploidy. Homologous clusters of photosynthetic gene families show that gene copy numbers are similar to what would be expected given their duplication history and that no significant difference between the C3 and C4 species exists in terms of gene copy number. This is further confirmed by syntenic analysis of T. hassleriana, Arabidopsis thaliana and Aethionema arabicum, where syntenic region copy number ratios lie close to what could be theoretically expected. Expression levels of C4 photosynthesis orthologs show that regulation of transcript abundance in T. hassleriana is much less strictly controlled than in G. gynandra, where orthologs have extremely similar expression patterns in different organs, seedlings and seeds. We conclude that the Th-α and older paleopolyploidy events have had a significant influence on the specific genetic makeup of Cleomaceae versus Brassicaceae. Because the copy number of various essential genes involved in C4 photosynthesis is not significantly influenced by polyploidy combined with the fact that transcript abundance in G. gynandra is more strictly controlled, we also conclude that recruitment of existing genes through regulatory changes is more likely to have played a role in the shift to C4 than the neofunctionalization of duplicated genes. DATA: The data deposited at NCBI represents raw RNA reads for each data series mentioned: 5 leaf stages, root, stem, stamen, petal, carpel, sepal, 3 seedling stages and 3 seed stages of Tarenaya hassleriana and Gynandropsis gynandra. The assembled reads were used for all analyses of this paper where RNA was used. http://www.ncbi.nlm.nih.gov/Traces/sra/?study=SRP036637, http://www.ncbi.nlm.nih.gov/Traces/sra/?study=SRP036837

Keywords

• Plant genome evolution
• Synteny
• Cleomaceae
• Brassicaceae
• Bioinformatics
• Whole genome duplication
• Paleopolyploidy
• C4 photosynthesis