Manipulating Unisexual-Sexual Reproduction Transition to Engineer Genome-Reconstructed Polyploids

Both unisexuality and polyploidy are significant in agriculture, exhibiting revolutionary biotechnology potential, as their coupling has been demonstrated to enable the design of polyploid genomes in crops. However, their applicability to animals has remained a challenge. Herein, the first case of engineering polyploid genomes with desirable traits via unisexual-sexual reproduction transition is provided. First, a group of genome-reconstructed amphitriploids (GR-A3n) is generated involving unisexual gynogenetic Carassius gibelio, sexual C. auratus, and sexual C. cuvieri. Then, we found that the gynogenesis ability have transferred from C. gibelio to some of the GR-A3n females. This study subsequently established three GR-A3n clones with distinct herpesvirus resistance and in which differential transcriptome profiles are characterized in two main hematopoietic organs. Most genes of the hemoglobin metabolism pathway is found to exhibit high expression levels, as in C. cuvieri, which led to efficient hemoglobin biosynthesis and blood oxygen homeostasis during infection, thereby resulting in strong herpesvirus resistance. Furthermore, this study determined the resistant and susceptible haplotypes derived from chromosome 12B of C. cuvieri, which should be responsible for resistance differences between GR-A3n clones. Overall, this study establishes an approach for genetic improvement through polyploid genome design in animals.