The mixed auto-/allooctoploid genome of Japanese knotweed (Reynoutria japonica) provides insights into its polyploid origin and invasiveness

Abstract

Reynoutria japonica Houtt. (Polygonaceae), a traditional Chinese medicine, is one of the top 100 most destructive invasive species worldwide due to its aggressive growth and strong adaptability. Here, we report an 8.04 Gb chromosome-scale assembly of R. japonica with 88 chromosomes across eight homologous sets. Through a combined phylogenetic and genomic analysis, we demonstrate that R. japonica is a mixed auto-/allooctoploid (AAAABBBB). Subgenome A (SubA) exhibited a close phylogenetic relationship with the related species Fallopia multiflora. We also unveiled the origin and evolutionary history of octoploid R. japonica based on resequencing data from Reynoutria species with different ploidy. Comparative genomics analysis revealed the genetic basis of R. japonica's invasivity and adaptability. The auxin response factor (ARF) gene family was significantly expanded in R. japonica, and these genes were highly expressed in rhizomes. We also investigated the collaboration and differentiation of the duplicated genes resulting from auto- and allo-polyploidization at the genomic variation, gene family evolution, and gene expression levels in R. japonica. Transcriptomic analysis of stem internodes and apices at different developmental stages revealed that the octuplication and significant expansion of the SAUR19 and SAUR63 subfamilies due to tandem replication in SubA, and the high expression of these genes in stems, likely contribute to the rapid growth of R. japonica. Our study provides important clues into adaptive evolution and polyploidy dominant traits in invasive plants, and will also provide important guidance for the breeding of polyploid crops.