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 CO(2) 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 vein-development-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 C(4) CO(2) 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.