Haplotype-resolved genome assembly provides insights into the evolutionary origin of waterlogging-tolerant Actinidia valvata hexaploid

Abstract Kiwifruit plants are much damaged by several days of waterlogging stress. The effect can be a serious problem for the growers in the lowlands or plain areas where floods cannot be drained timely. Actinidia valvata is a polyploid species that has been widely used as waterlogging resistant rootstock in kiwifruit cultivation. Here we report haplotype-resolved chromosome-scale assemblies of an A. valvata male plant ‘DE’, defining two subgenomes, a diploid closely related to Actinidia polygama and an autotetraploid closely related to Actinidia macrosperma as their ancestral contributors, respectively, together to form an allohexaploid. Genome-wide comparisons of the assembled 174 pseudochromosomes with nine distinct Actinidia species revealed the genomic structure, phylogeny and duplication history of ‘DE’ genome. Evolutionary analyses suggest that it was formed ~0.44 to 0.88 Mya and evolved by a recent alloploid addition to an autotetraploid ancestor. Annotation of sex determining genes (SyGl and FrBy) on Y chromosome unraveled that the chromosomal location and organization of sex determining region (SDR) are conserved to and share an identical lineage with A. polygama, the diploid ancestor. Comprehensive transcriptome analysis indicates that its enhanced waterlogging tolerance is due to the restricted activation of anaerobic survival genes and the consequence with prolonged carbohydrate supply to keep the root system quiescently alive under hypoxia. Our study provides valuable genomic resources and offers insights into the evolution and the underlying mechanism of enhanced waterlogging tolerance of A. valvata hexaploid.