Whole-Genome Duplication Facilitated the Evolution of C-4 Photosynthesis in Gynandropsis gynandra

In higher plants, whole-genome duplication (WGD) is thought to facilitate the evolution of C-4 photosynthesis from C-3 photosynthesis. To understand this issue, we used new and existing leaf-development transcriptomes to construct two coding sequence databases for C-4 Gynandropsis gynandra and C-3 Tarenaya hassleriana, which shared a WGD before their divergence. We compared duplicated genes in the two species and found that the WGD contributed to four aspects of the evolution of C-4 photosynthesis in G. gynandra. First, G. gynandra has retained the duplicates of ALAAT (alanine aminotransferase) and GOGAT (glutamine oxoglutarate aminotransferase) for nitrogen recycling to establish a photorespiratory CO2 pump in bundle sheath (BS) cells for increasing photosynthesis efficiency, suggesting that G. gynandra experienced a C-3-C-4 intermediate stage during the C-4 evolution. Second, G. gynandra has retained almost all known veindevelopment-related paralogous genes derived from the WGD event, likely contributing to the high vein complexity of G. gynandra. Third, the WGD facilitated the evolution of C-4 enzyme genes and their recruitment into the C-4 pathway. Fourth, several genes encoding photosystem I proteins were derived from the WGD and are upregulated in G. gynandra, likely enabling the NADH dehydrogenase-like complex to produce extra ATPs for the C4CO2 concentration mechanism. Thus, the WGD apparently played an enabler role in the evolution of C-4 photosynthesis in G. gynandra. Importantly, an ALAAT duplicate became highly expressed in BS cells in G. gynandra, facilitating nitrogen recycling and transition to the C-4 cycle. This study revealed how WDG may facilitate C-4 photosynthesis evolution.