Cold-induced ginsenosides accumulation is associated with the alteration in DNA methylation and relative gene expression in perennial American ginseng (Panax quinquefolius L.) along with its plant growth and development process

Abstract

Background Ginsenosides accumulation responses to temperature are critical to quality formation in cold-dependent American ginseng. However, the studies on cold requirement mechanism relevant to ginsenosides have been limited in this species. Methods Two experiments were carried out: one was a multivariate linear regression analysis between the ginsenosides accumulation and the environmental conditions of American ginseng from different sites of China and the other was a synchronous determination of ginsenosides accumulation, overall DNA methylation, and relative gene expression in different tissues during different developmental stages of American ginseng after experiencing different cold exposure duration treatments. Results Results showed that the variation of the contents as well as the yields of total and individual ginsenosides Rg1, Re, and Rb1 in the roots were closely associated with environmental temperature conditions which implied that the cold environment plays a decisive role in the ginsenoside accumulation of American ginseng. Further results showed that there is a cyclically reversible dynamism between methylation and demethylation of DNA in the perennial American ginseng in response to temperature seasonality. And sufficient cold exposure duration in winter caused sufficient DNA demethylation in tender leaves in early spring and then accompanied the high expression of flowering gene PqFT in flowering stages and ginsenosides biosynthesis gene PqDDS in green berry stages successively, and finally, maximum ginsenosides accumulation occurred in the roots of American ginseng. Conclusion We, therefore, hypothesized that cold-induced DNA methylation changes might regulate relative gene expression involving both plant development and plant secondary metabolites in such cold-dependent perennial plant species.

Exogenous Putrescine Enhances Salt Tolerance and Ginsenosides Content in Korean Ginseng (Panax ginseng Meyer) Sprouts

“…As with other medicinal plants, the production of saponin-containing plants, especially their secondary metabolites, significantly depends on the geographical zone, cultivation site, and different biotic and abiotic factors in the habitat, both qualitatively and quantitatively [ 18 ]. Ginsenosides production is influenced by different abiotic stresses like temperature [ 18 ], light, [ 104 ], drought [ 105 , 106 ], and salinity [ 107 ]. The production of secondary metabolites may also be altered by environmental stresses [ 108 ].…”

“…Among them, ginsenosides, also known as triterpene glycoside saponin, are most common and well known in pharmacological and physiological fields as a remedial of anticancer, antidiabetic, immunomodulatory, neuroprotective, radioprotective, antiamnestic, and antistress [ 16 ]. Earlier it was well described that ginsenosides content in ginseng plants varies depending on factors like light, water, temperature, ionizing radiation, soil, location, plant age, and so on [ 18 , 19 , 20 ]. Salt stress is also a crucial factor that affects the growth, development and yield of ginseng plants [ 21 ].…”

ROS1 promotes low temperature-induced anthocyanin accumulation in apple by demethylating the promoter of anthocyanin-associated genes

“…Studies have also shown that ROS1 expression is promoted by DNA methylation and antagonized by DNA demethylation [ 61 ], and ROS1 expression is also inhibited in RdDM silencing and in met1 mutants [ 61 ]. Moreover, there is a cyclically reversible dynamism between DNA methylation and DNA demethylation during the temperature seasonality response in perennial American ginseng [ 62 ], which suggests that DNA methylation and demethylation are dynamic processes in plants.…”

Integration of high-throughput omics technologies in medicinal plant research: The new era of natural drug discovery

“…Developmental methylome of the medicinal plant Cape periwinkle ( Catharanthus roseus ) determined that cellular and physiological functions are likely to be impacted by tissue-specific covariations between context-dependent DNA methylation ( Dugé de Bernonville et al., 2020 ). The cold environment affected ginsenosides accumulation in perennial American ginseng ( Panax quinquefolium ), and a cyclically reversible dynamism between methylation and demethylation of DNA was also reported in response to temperature seasonality ( Hao et al., 2020 ). Further investigations of medicinal plant pan-genomes and epigenomes addressing bioactive compound metabolism are needed to improve the production of secondary metabolites for pharmaceutical applications.…”