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Evolutionary Aspects of Hypericin Productivity and Endogenous Phytohormone Pools Evidenced in Hypericum Species In Vitro Culture Model.

ABSTRACT: Shoot cultures of hypericin non-producing H. calycinum L. (primitive Ascyreia section), hypericin-producing H. perforatum L., H. tetrapterum Fries (section Hypericum) and H. richeri Vill. (the evolutionarily most advanced section Drosocarpium in our study) were developed and investigated for their growth, development, hypericin content and endogenous phytohormone levels. Hypericins in wild-growing H. richeri significantly exceeded those in H. perforatum and H. tetrapterum. H. richeri also had the highest hypericin productivity in vitro in medium supplemented with 0.2 mg/L N⁶-benzyladenine and 0.1 mg/L indole-3-butyric acid and H. tetrapterum-the lowest one in all media modifications. In shoot culture conditions, the evolutionarily oldest H. calycinum had the highest content of salicylic acid and total jasmonates in some of its treatments, as well as dominance of the storage form of abscisic acid (ABA-glucose ester) and lowest cytokinin ribosides and cytokinin O-glucosides as compared with the other three species. In addition, the evolutionarily youngest H. richeri was characterized by the highest total amount of cytokinin ribosides. Thus, both evolutionary development and the hypericin production capacity seemed to interact closely with the physiological parameters of the plant organism, such as endogenous phytohormones, leading to the possible hypothesis that hypericin productivity may have arisen in the evolution of Hypericum as a means to adapt to environmental changes.

SUBMITTER: Danova K

PROVIDER: S-EPMC9609395 | biostudies-literature | 2022 Oct

REPOSITORIES: biostudies-literature

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Evolutionary Aspects of Hypericin Productivity and Endogenous Phytohormone Pools Evidenced in Hypericum Species In Vitro Culture Model.

Danova Kalina K Motyka Vaclav V Trendafilova Antoaneta A Dobrev Petre I PI Ivanova Viktorya V Aneva Ina I

Plants (Basel, Switzerland) 20221018 20

Shoot cultures of hypericin non-producing H. calycinum L. (primitive Ascyreia section), hypericin-producing H. perforatum L., H. tetrapterum Fries (section Hypericum) and H. richeri Vill. (the evolutionarily most advanced section Drosocarpium in our study) were developed and investigated for their growth, development, hypericin content and endogenous phytohormone levels. Hypericins in wild-growing H. richeri significantly exceeded those in ...[more]

PMID: 36297777

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Project description:Next generation sequencing technology rapidly developed research applications in the field of plant functional genomics. Several Hypericum spp. with an aim to generate and enhance gene annotations especially for genes coding the enzymes supposedly included in biosynthesis of valuable bioactive compounds were analyzed. The first de novo transcriptome profiling of Hypericum annulatum Moris, H. tomentosum L., H. kalmianum L., and H. androsaemum L. leaves cultivated in vitro was accomplished. All four species with only limited genomic information were selected on the basis of differences in ability to synthesize hypericins and presence of dark nodules accumulating these metabolites with purpose to enrich genomic background of Hypericum spp. H. annulatum was chosen because of high number of the dark nodules and high content of hypericin. H. tomentosum leaves are typical for the presence of only 1-2 dark nodules localized in the apical part. Both H. kalmianum and H. androsaemum lack hypericin and have no dark nodules. Four separated datasets of the pair-end reads were gathered and used for de novo assembly by Trinity program. Assembled transcriptomes were annotated to the public databases Swiss-Prot and non-redundant protein database (NCBI-nr). Gene ontology analysis was performed. Differences of expression levels in the marginal tissues with dark nodules and inner part of leaves lacking these nodules indicate a potential genetic background for hypericin formation as the presumed site of hypericin biosynthesis is in the cells adjacent to these structures. Altogether 165 contigs in H. annulatum and 100 contigs in H. tomentosum were detected as significantly differentially expressed (P < 0.05) and upregulated in the leaf rim tissues containing the dark nodules. The new sequences homologous to octaketide synthase and enzymes catalyzing phenolic oxidative coupling reactions indispensable for hypericin biosynthesis were discovered. The presented transcriptomic sequence data will improve current knowledge about the selected Hypericum spp. with proposed relation to hypericin biosynthesis and will provide a useful resource of genomic information for consequential studies in the field of functional genomics, proteomics and metabolomics.

Project description:Hypericin, an extract from St John's Wort (Hypericum perforatum L.), is a promising photosensitizer in the context of clinical photodynamic therapy due to its excellent photosensitizing properties and tumoritropic characteristics. Hypericin-PDT induced cytotoxicity elicits tumor cell death by various mechanisms including apoptosis, necrosis and autophagy-related cell death. However, limited reports on the efficacy of this photomedicine for the treatment of melanoma have been published. Melanoma is a highly aggressive tumor due to its metastasizing potential and resistance to conventional cancer therapies. The aim of this study was to investigate the response mechanisms of melanoma cells to hypericin-PDT in an in vitro tissue culture model. Hypericin was taken up by all melanoma cells and partially co-localized to the endoplasmic reticulum, mitochondria, lysosomes and melanosomes, but not the nucleus. Light activation of hypericin induced a rapid, extensive modification of the tubular mitochondrial network into a beaded appearance, loss of structural details of the endoplasmic reticulum and concomitant loss of hypericin co-localization. Surprisingly the opposite was found for lysosomal-related organelles, suggesting that the melanoma cells may be using these intracellular organelles for hypericin-PDT resistance. In line with this speculation we found an increase in cellular granularity, suggesting an increase in pigmentation levels in response to hypericin-PDT. Pigmentation in melanoma is related to a melanocyte-specific organelle, the melanosome, which has recently been implicated in drug trapping, chemotherapy and hypericin-PDT resistance. However, hypericin-PDT was effective in killing both unpigmented (A375 and 501mel) and pigmented (UCT Mel-1) melanoma cells by specific mechanisms involving the externalization of phosphatidylserines, cell shrinkage and loss of cell membrane integrity. In addition, this treatment resulted in extrinsic (A375) and intrinsic (UCT Mel-1) caspase-dependent apoptotic modes of cell death, as well as a caspase-independent apoptotic mode that did not involve apoptosis-inducing factor (501 mel). Further research is needed to shed more light on these mechanisms.

Project description:Background and aimsIn Central Europe Hypericum perforatum and Hypericum maculatum show significant hybridization and introgression as a consequence of Pleistocene range fluctuations, and their gene pools are merging on higher ploidy levels. This paper discusses whether polyploid hybrid gene pools are trapped in the ecological climatic niche space of their diploid ancestors, and tests the idea of geographical parthenogenesis.MethodsDNA sequence information of nuclear ribosomal DNA and plastid loci, ploidy level estimates and ecological niche modelling are used to characterize the various diploid and polyploid gene pools and unravel spatio-temporal patterns of gene flow among them.Key resultsOn the diploid level, the three gene pools are clearly distinct between and within species of H. perforatum (two gene pools) and H. maculatum, and their divergence dates back to the first half of the Pleistocene. All polyploids in Central Europe show high levels of past and contemporary gene flow between all three gene pools. The correlation of genetic and geographical distances breaks down if the latter is larger than 250 km, indicating recent and ongoing gene flow. The two species are ecologically differentiated, but in particular hybrids among all three gene pools do not show significant niche differences compared to their parental gene pools, except for some combinations with H. maculatum.ConclusionsInter- and intraspecific gene flow between inter- and intra-species gene pools is limited on the diploid level, and the geographical distribution of the diploids largely reflects Pleistocene evolutionary history. Secondary contact promoted hybridization and introgression on the polyploid level, enabling offspring to escape the diploid gene pools. However, the hybrid polyploids do not show significant niche differences compared to their diploid progenitors. It is concluded that the observed absence of niche divergence has precluded further differentiation and geographical partitioning of new polyploid lineages being effectively separated from the parental lines. The predominantly apomictic reproducing polyploids are trapped in the polyploid gene pool and the ecological climatic niche space of their diploid ancestors.

Dataset Information

Evolutionary Aspects of Hypericin Productivity and Endogenous Phytohormone Pools Evidenced in Hypericum Species In Vitro Culture Model.

Publications

Evolutionary Aspects of Hypericin Productivity and Endogenous Phytohormone Pools Evidenced in <i>Hypericum</i> Species In Vitro Culture Model.

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