Arbuscular mycorrhiza facilitates the accumulation of glycyrrhizin and liquiritin in Glycyrrhiza uralensis under drought stress

Abstract

Liquorice (Glycyrrhiza uralensis) is an important medicinal plant for which there is a huge market demand. It has been reported that arbuscular mycorrhizal (AM) symbiosis and drought stress can stimulate the accumulation of the active ingredients, glycyrrhizin and liquiritin, in liquorice plants, but the potential interactions of AM symbiosis and drought stress remain largely unknown. In the present work, we investigated mycorrhizal effects on plant growth and accumulation of glycyrrhizin and liquiritin in liquorice plants under different water regimes. The results indicated that AM plants generally exhibited better growth and physiological status including stomatal conductance, photosynthesis rate, and water use efficiency compared with non-AM plants. AM inoculation up-regulated the expression of an aquaporin gene PIP and decreased root abscisic acid (ABA) concentrations under drought stress. In general, AM plants displayed lower root carbon (C) and nitrogen (N) concentrations, higher phosphorus (P) concentrations, and therefore, lower C:P and N:P ratios but higher C:N ratio than non-AM plants. On the other hand, AM inoculation increased root glycyrrhizin and liquiritin concentrations, and the mycorrhizal effects were more pronounced under moderate drought stress than under well-watered condition or severe drought stress for glycyrrhizin accumulation. The accumulation of glycyrrhizin and liquiritin in AM plants was consistent with the C:N ratio changes in support of the carbon-nutrient balance hypothesis. Moreover, the glycyrrhizin accumulation was positively correlated with the expression of glycyrrhizin biosynthesis genes SQS1, β-AS, CYP88D6, and CYP72A154. By contrast, no significant interaction of AM inoculation with water treatment was observed for liquiritin accumulation, while we similarly observed a positive correlation between liquiritin accumulation and the expression of a liquiritin biosynthesis gene CHS. These results suggested that AM inoculation in combination with proper water management potentially could improve glycyrrhizin and liquiritin accumulation in liquorice roots and may be practiced to promote liquorice cultivation.

Arbuscular Mycorrhizal Fungi Can Compensate for the Loss of Indigenous Microbial Communities to Support the Growth of Liquorice (Glycyrrhiza uralensis Fisch.)

“…AM symbiosis can improve plant mineral nutrition, especially P, and regulate the biosynthesis of secondary metabolites to enhance plant resistance [47]. In the current study, AM inoculation markedly improved plant growth and facilitated the accumulations of glycyrrhizin and liquiritin compared with the non-AM plants in sterilized soil, which has been proven in our previous studies [28,30]. However, we observed no significant difference in plant growth, including plant height, plant dry weights, nutrient concentrations, photosynthesis traits, and accumulations of glycyrrhizin and liquiritin between the AM plants in sterilized soil and non-AM plants in unsterilized soil, suggesting that AM symbiosis could take over the role of indigenous soil microbial communities to a certain extent to support plant growth and biosynthesis of secondary metabolites.…”

“…In this study, plants grown in sterilized soil showed significant reductions in glycyrrhizin and liquiritin concentrations, indicating the importance of soil microorganisms in plant secondary metabolism. Nutrient level, especially those of P, essentially affects the accumulation of glycyrrhizin and liquiritin through direct involvement in the biosynthesis of secondary metabolites, regulation of C:N:P ratios and expression of the related genes [30]. Our results indicated that the non-AM plants grown in unsterilized soil had higher levels of root P and C:N ratios and higher concentrations of glycyrrhizin and liquiritin compared with those in sterilized soil.…”

“…While the role of microbial communities in ecosystem functioning is unequal, there exist some specific microbial group, such as AM fungi, being key drivers of many ecosystem processes, including soil nutrient cycling, water uptake and plant growth [14,15]. Our previous studies have proven that AM fungi play important roles in promoting plant growth [28,30], however, the relative importance and effectiveness of indigenous soil microbial communities and the key beneficial microorganisms, such as AM fungi, are rarely considered [37]. In this study, we used liquorice as the host plant to test the hypotheses that soil indigenous microorganisms are indispensable for plant growth, and that AM fungi may compensate for the loss of indigenous microbial communities to support plant growth.…”

“…In general, secondary metabolite biosynthesis in plants can be facilitated either by increasing precursors in the related biosynthetic pathways or by regulating the expression of metabolite synthase genes [47,60]. Improved photosynthetic efficiency and nutrient status, especially P, could provide substrates for secondary metabolite biosynthesis [30,46,47]. In this study, AM plants in sterilized and unsterilized soils showed chlorophyll concentrations, photosynthetic efficiency, and plant nutrients similar to those of non-AM plants cultivated in unsterilized soil, which may also provide similar substrates to the biosynthesis pathway of secondary metabolites and determine the accumulation of glycyrrhizin and liquiritin in liquorice plants.…”

“…(1) Rhizophagus has a global distribution and could be successfully adapted to different environment conditions [31][32][33][34]. (2) Our previous studies verified that R. irregularis shows excellent promoting effects on liquorice growth and active ingredient accumulation in sterilized soil [28,30]. However, the importance of the roles of R. irregularis in promoting plant performance relative to that of soil indigenous microbes remains largely unclear.…”