The Genome of Eleocharis vivipara Elucidates the Genetics of C3-C4 Photosynthetic Plasticity and Karyotype Evolution in the Cyperaceae.

Eleocharis vivipara, an amphibious plant in Cyperaceae family, was reported to have numerous valuable biological traits, particularly its adaptive photosynthesis plasticity that employing C3 type underwater and C4 type on land. However, the evolutionary and genetic studies of it have been hampered due to lack of genomes. Here we assembled a high-quality genome of E. vivipara, the first chromosome-level genome of Eleocharis genus, with its size ~965.22 Mb and contains 10 chromosomes. Its diagonal Hi-C pattern for adjacent chromosomes, and its 1-to-1 genome synteny relationship for two subgroups suggested it is a tetraploid with n = 2x = 10. Phylogeny result displayed the Eleocharis diverged with Cyperus genus ~23.11 Mya, a closer relationship than others in Cyperaceae. Interestingly, the well 1-to-1 genome synteny result for the subgenome 2 of E. vivipara (x = 5), the genomes of Cyperus esculentus (n = 54) and Rhynchospora tenuis (n = 2), displayed twice chromosomes fusion events resulted to their number reduction from 54 to 5 and then to 2. Compared with its close relative Juncus effusus which has monocentromeres, we found E. vivipara showed characteristics of holocentromeres that can maintain the stability of its fusion chromosomes. Strikingly, transplanting experiment displayed its culms anatomy gradually presented Proto-Kranz structure with increased number of chloroplasts in BS cells in terrestrial culms. Further comparison results not only displayed most of its C4 photosynthesis related genes showed higher expression, but also identified 2,602 up-DEGs that mainly functional in response to water deprivation and ABA, revealed the drought inducted transition of C4 photosynthesis in E. vivipara. Briefly, our results not only shed light on the karyotype evolution of Cyperaceae, but also provided new valuable insights into C3 and C4 transformation that will benefit for crop improvement and breeding.