Whole-genome, transcriptome, and methylome analyses provide insights into the evolution of platycoside biosynthesis in Platycodon grandiflorus, a medicinal plant

Triterpenoid saponins (TSs) are common plant defense phytochemicals with potential pharmaceutical properties. <i>Platycodon grandiflorus</i> (Campanulaceae) has been traditionally used to treat bronchitis and asthma in East Asia. The oleanane-type TSs, platycosides, are a major component of the <i>P. grandiflorus</i> root extract. Recent studies show that platycosides exhibit anti-inflammatory, antiobesity, anticancer, antiviral, and antiallergy properties. However, the evolutionary history of platycoside biosynthesis genes remains unknown. In this study, we sequenced the genome of <i>P. grandiflorus</i> and investigated the genes involved in platycoside biosynthesis. The draft genome of <i>P. grandiflorus</i> is 680.1 Mb long and contains 40,017 protein-coding genes. Genomic analysis revealed that the <i>CYP716</i> family genes play a major role in platycoside oxidation. The <i>CYP716</i> gene family of <i>P. grandiflorus</i> was much larger than that of other Asterid species. Orthologous gene annotation also revealed the expansion of <i>β-amyrin synthases</i> (<i>bASs</i>) in <i>P. grandiflorus</i>, which was confirmed by tissue-specific gene expression. In these expanded gene families, we identified key genes showing preferential expression in roots and association with platycoside biosynthesis. In addition, whole-genome bisulfite sequencing showed that <i>CYP716</i> and <i>bAS</i> genes are hypomethylated in <i>P. grandiflorus</i>, suggesting that epigenetic modification of these two gene families affects platycoside biosynthesis. Thus whole-genome, transcriptome, and methylome data of <i>P. grandiflorus</i> provide novel insights into the regulation of platycoside biosynthesis by <i>CYP716</i> and <i>bAS</i> gene families.