Genome assembly of autotetraploid Actinidia arguta highlights adaptive evolution and dissects important economic traits

Actinidia arguta, the most widely distributed and the second cultivated species within Actinidia genus, has distinguished difference from current kiwifruit in biological characters like small and smooth fruit, rapid-softening and excellent cold tolerance. Knowledge of adaptive evolution of the tetraploid Actinidia species and genetic basis of its important agronomic traits is still unclear. A chromosome-scale genome assembly of an autotetraploid male A. arguta has been generated. The genome assembly was 2.77 Gb in length with a contig N50 of 9.97Mb and anchored into 116 pseudo-chromosomes. Resequencing and clustering of 101 geographically representative accessions showed they could be divided into two geographical groups, Southern and Northern Groups, which first diverged 12.9 Mya ago. A. arguta underwent two prominent expansions and one demographic bottleneck from the mid-Pleistocene climate transition (MPT) to late-Pleistocene. Population genomics study using paleoclimate data allow us to discern the evolution of the species adaptation to different historical environments. Three genes (AaCEL1, AaPME1 and AaDOF1) have been identified by multi-omics and verified their accelerating softening of flesh through transient assay. A set of genes localized in sex chromosome (Chr3), or autosomal chromosomes are biasedly expressed during stamen or carpel development, which characteristically regulate sexual dimorphism. This assembly of the autotetraploid genome at the chromosome level and detail uncover the genes related with important agronomic traits paves the way to facilitate functional genomics and improvement of A. arguta.