Genome assembly and comparative analysis reveal the imbalanced subgenomes divergence and evolutionary history of Juglans cathayensis

Abstract

Chinese walnut (Juglans cathayensis), a wild relative of Persian walnut (Juglans regia), is distinguished by its early maturation and higher resilience to abiotic stress. As a paleopolyploid species, J. cathayensis has undergone at least two whole genome duplications (WGD) and subgenome divergence, which may profoundly affect its phenotype. This study assembled a chromosome-level genome of about 553.7 Mb for J. cathayensis, with the 16 pseudochromosomes categorized into two subgenomes based on their phylogenetic relationship with potential ancestor Myrica rubra hypothesized by cytogenetics. We found that unbalanced burst insertion of long terminal repeat retrotransposons (LTR-RTs) resulted in genome expansion and subgenomic divergence. Most homoeologous gene pairings suggested subgenome-biased expression genes (SBEGs) in three organs; however, no dominant subgenome expression model was identified. The resequencing analysis of J. cathayensis and J. regia samples, along with transcriptome and metabolome results, revealed that the species-specific characteristics of J. cathayensis are directly linked to the accumulation of flavonoid metabolism. Moreover, a distinctive deletion (non-frameshift mutation) in the SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1 (SOC1) gene of J. cathayensis probably regulates the early maturation differences between J. cathayensis and other Juglans species. Our study elucidates the genetic mechanisms promoting subgenome divergence and accelerating the utilization of genetic resources in J. cathayensis.