Apomixis in Saccharina japonica: Parthenogenesis in male and apogamy in female gametophytes

Apomixis, an asexual reproduction process that does not involve meiosis and fertilization, has shown great potential in accelerating crop breeding by producing offspring with genotypes identical to those of the parental plants. In brown algae, parthenogenesis and apogamy are types of apomixis observed in gametophytes. Saccharina japonica is a widely cultivated and highly productive marine brown algae “crop”. Previously, parthenogenesis was reported in female gametophytes and apogamy in male gametophytes, respectively. However, in this study, we observed apogamy in female gametophytes and parthenogenesis in male gametophytes during S. japonica gametophyte development. Apogamy in females occurred later than parthenogenesis, with apogamous sporophytes forming occasionally and being easily overlooked due to the prevalence of partheno-sporophytes. Some male gametophytes developed into partheno-sporophytes by producing smaller egg-like cells. The reproductive ability of male gametophytes through parthenogenesis was positively correlated with the formation ability of egg-like cells. These results suggest that parthenogenesis-related reproductive traits of S. japonica are not only linked to sex traits, but are complex traits regulated by multiple genes. Gene expression analysis revealed that early feminization in male gametophytes was associated with the combined down-regulation of male-biased genes and the up-regulation of female-biased genes. Twenty-two male-biased genes and 14 female-biased genes were further identified as parthenogenesis-related candidate genes, potentially playing crucial roles in the early feminization of male gametophytes. This study deepens our understanding of the regulation of parthenogenesis and apomixis in gametophytes of S. japonica. It lays the foundations for further research on the molecular mechanism of apomixis and its applications in S. japonica breeding.