Evolutionary history of magnoliid genomes and benzylisoquinoline alkaloid biosynthesis.

Abstract

Benzylisoquinoline alkaloids (BIAs) are important metabolites synthesized in early-diverging eudicots and magnoliids, yet the genetic basis of BIA biosynthesis in magnoliids remains unclear. Here, we decode the genomes of two magnoliid species, Saruma henryi and Aristolochia manshuriensis, and reconstruct the ancestral magnoliid karyotype and infer the chromosomal rearrangement history following magnoliid diversification. Metabolomic, transcriptomic, and phylogenetic analyses reveal the intermediate chemical components and genetic basis of BIA biosynthesis in A. manshuriensis. Although the core enzymes involved in BIA synthesis appear to be largely conserved between early-diverging eudicots and magnoliids, the biosynthetic pathways in magnoliids seem to exhibit greater flexibility. Significantly, our investigation of the evolutionary history of BIA biosynthetic genes revealed that almost all were duplicated before the emergence of extant angiosperms, with only early-diverging eudicots and magnoliids preferentially retaining these duplicated genes, thereby enabling the biosynthesis of BIAs in these groups.