Spatial and temporal patterns of secoiridoid and xanthone biosynthetic pathways during early development of Centaurium erythraea Rafn, as altered by ploidy level

Abstract

Centaurium erythraea, used as medical plant from the earliest times, is an immense depot of quite rare bioactive compounds. Secoiridoids (sweroside, swertiamarin, and gentiopicrin) and xanthones (methylbellidifolin and decussatin) are predominant bioactive compounds in C. erythraea. The present study aims at providing new insights into how the content of these bioactive principles can be related with plant ploidy level by characterizing possible differences in their biosynthesis and accumulation between diploid and tetraploid genotypes from both spatial and temporal aspects. In general, shoots are determined as the major site of secoiridoids’ and xanthones’ accumulation, whose ratio vary during the development. Genes involved in iridoid and xanthone metabolic pathways were found to be coordinately regulated at the transcriptional level both during the development and among organs. Biosynthetic gene expression levels were found highly correlated with the content of major compounds from these two classes. Diversification in chemical profiles between tetraploid and diploid genotypes may result from the expression difference between homologous loci correspondent to several key biosynthetic genes, which trigger changes in the two metabolic routes. Thus, enhanced expression of genes coding for geraniol synthase (GES), 8-hydroxygeraniol oxidoreductase (8HGO), and 7-deoxyloganic acid hydrolase (7DLH2) is strongly associated with intensive production of iridoids. Interestingly, transcript levels of beta-glucosidase (CebGLU), a candidate to catalyze the first step in the secoiridoid catabolism, is significantly positively correlated with the content of major secoiridoids. Elevated expression of genes coding for benzophenone synthase (BS) and 3-hydroxybenzoate:CoA ligase (3HBL) appear to account for enhanced production of hexa-substituted xanthones. Regarding content of iridoids and xanthones, a diploid genotype appeared to be more productive than a tetraploid genotype under controlled in vitro conditions, therewithal displaying significantly higher biomass.