A near-complete genome assembly of the allotetrapolyploid Cenchrus fungigraminus (JUJUNCAO) provides insights into its evolution and C4 photosynthesis

JUJUNCAO (Cenchrus fungigraminus; 2n=4x=28) is a Cenchrus grass with the highest productive biomass among cultivated plants, and could be used for the cultivation of mushrooms, animal feed and biofuel production. Here, we reported a near completely assembled genome of JUJUNCAO and discovered that JUJUNCAO was an allopolyploid originated ∼2.7 MYA. Its genome consisted of two subgenomes, with subgenome A sharing a high collinear synteny with pearl millet. We also investigated the genome evolution of JUJUNCAO and suggested that the ancestral karyotype of Cenchrus split into the A and B ancestral karyotypes of JUJUNCAO. Comparative transcriptome and DNA methylome analyses revealed a functional divergence of the homeologous gene pairs between the two subgenomes, which was a further indication of asymmetric DNA methylation. The three types of centromeric repeats in the JUJUNCAO genome (CEN137, CEN148 and CEN156) may have evolved independently within each subgenome, with some introgressions of CEN156 from B subgenome into A subgenome. We further investigated the photosynthetic characteristics of JUJUNCAO which revealed a typical C4 Kranz anatomy and a high photosynthetic efficiency. Moreover, NADP-ME and PEPCK in JUJUNCAO very likely have co-operated in the major C4 decarboxylation reaction, which is different from other C4 photosynthetic subtypes reported and may contribute to the high photosynthetic efficiency and consequently high biomass yield of JUJUNCAO. Taken together, our results provide insights into the highly efficient photosynthetic mechanism in JUJUNCAO and are a valuable reference genome for future genetic and evolutionary studies, as well as the genetic improvement of the Cenchrus grasses.