Integrated genomic, transcriptomic, and metabolomic analyses provide novel insights into high cadmium accumulation in Phytolacca icosandra L

The evolutionary features and molecular basis of the conserved abilities of Phytolacca species to accumulate cadmium (Cd) and manganese (Mn) are poorly understood. In this study, the chromosomal-level genome of P. icosandra (2n = 2x = 36) was sequenced and assembled. The genome has a size of 1042.86 Mb, with a contig N50 of 52.37 Mb and a GC content of 38.17%. Genomic evaluation revealed that the P. icosandra genome contains 98.95% of BUSCO and achieves an LAI score of 15.45. Genome annotation indicated that the P. icosandra genome encompasses 25,756 protein-coding genes. Evolutionary analysis identified one recent whole genome duplication event and showed that the unique, significantly expanded, and positive selection genes in P. icosandra were markedly enriched in various functional categories (e.g., zinc ion binding, Mn ion binding, nicotianamine biosynthetic process) associated with metal (e.g., Cd and Mn) responses. Furthermore, several of these evolution-related genes were significantly upregulated by 25 and 100 μM Cd stress. Among them, an expanded gene PiNAS-l significantly improved Cd tolerance in the Δycf1 yeast strain. These results indicate that the high-Cd-accumulating characteristics of P. icosandra may be driven by evolutionary selection. Integrated physiological, transcriptomic, and metabolomic analyses revealed that several key processes, including Cd transport, signal transduction, lignin- and flavonoid-biosynthesis, and carbohydrate metabolism, contributed to Cd detoxification in P. icosandra roots. These processes were likely regulated by multiple transcription factor networks involving in WRKY, ERF, MYB, bHLH, bZIP, and several other families. This study provides the first chromosomal-level genome of Phytolaccaceae species and offers novel insights into Cd tolerance and accumulation in plants from evolutionary and molecular perspectives.