Dynamics of alkannin/shikonin biosynthesis in response to jasmonate and salicylic acid in Lithospermum officinale

Ahmad, Maqshoof; Alonso, Alicia Varela; Koletti, Antigoni E.; Rodić, Nebojša; Reichelt, Michael; Rödel, Philipp; Assimopoulou, Andreana N.; Paun, Ovidiu; Declerck, Stéphane; Schneider, Carolin; Sehr, Eva Maria

doi:10.1038/s41598-022-21322-0

Cited by 7 publications

(5 citation statements)

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“…For example, Wang et al (2014) demonstrated that the application of methyl jasmonate (MeJA) on shikonin-deficient A. euchroma cell lines rapidly led to the overexpression of several genes involved in the biosynthesis of A/Sd, including PGT , but was not accompanied by a significant higher production of A/Sd. In another study, Ahmad et al (2022b) showed a significantly higher expression of LePGT1 , LePGT2 , and LeGHQH1 in Lithospermum officinale L. roots treated with MeJA, but no higher accumulation of total A/Sd, after eight weeks. Conversely, the same authors ( Ahmad et al, 2022a ) demonstrated that the bacterium Chitinophaga sp.…”

Section: Discussionmentioning

confidence: 88%

“…Firstly, it is not excluded that the duration of Experiment 1 (37 days) was too short to result in a significant increased production of A/Sd, or that the timing of plant harvesting in our experiments was not optimal (i.e., gene expression behavioral oscillations due to the plant circadian cycle) ( Merrow et al, 2005 ). The PGT s regulate the first biosynthetic steps forming the basic carbon skeleton that leads to A/Sd, and therefore, it is possible that the resulting modulation of A/Sd production took longer after the upregulation of the relative expression of target PGT genes, as supported by Ahmad et al (2022b) , or that the genes oscillations were not timely targeted during our harvest times, as suggested by Wang et al (2014) ( Figure 6 ). Secondly, in a study by Andrade et al (2013) , a mismatch between alkaloid levels, another important SM group, and gene expression was reported in different Catharanthus roseus (L.) G. Don tissues.…”

Section: Discussionmentioning

confidence: 99%

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Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems

et al. 2023

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IntroductionAlkanna tinctoria Tausch. is a medicinal plant well-known to produce important therapeutic compounds, such as alkannin/shikonin and their derivatives (A/Sd). It associates with arbuscular mycorrhizal fungi (AMF), which are known, amongst others beneficial effects, to modulate the plant secondary metabolites (SMs) biosynthesis. However, to the best of our knowledge, no study on the effects of AMF strains on the growth and production of A/Sd in A. tinctoria has been reported in the literature.MethodsHere, three experiments were conducted. In Experiment 1, plants were associated with the GINCO strain Rhizophagus irregularis MUCL 41833 and, in Experiment 2, with two strains of GINCO (R. irregularis MUCL 41833 and Rhizophagus aggregatus MUCL 49408) and two native strains isolated from wild growing A. tinctoria (R. irregularis and Septoglomus viscosum) and were grown in a semi-hydroponic (S-H) cultivation system. Plants were harvested after 9 and 37 days in Experiment 1 and 9 days in Experiment 2. In Experiment 3, plants were associated with the two native AMF strains and with R. irregularis MUCL 41833 and were grown for 85 days in pots under greenhouse conditions. Quantification and identification of A/Sd were performed by HPLC-PDA and by HPLC-HRMS/MS, respectively. LePGT1, LePGT2, and GHQH genes involved in the A/Sd biosynthesis were analyzed through RT-qPCR.ResultsIn Experiment 1, no significant differences were noticed in the production of A/Sd. Conversely, in Experiments 2 and 3, plants associated with the native AMF R. irregularis had the highest content of total A/Sd expressed as shikonin equivalent. In Experiment 1, a significantly higher relative expression of both LePGT1 and LePGT2 was observed in plants inoculated with R. irregularis MUCL 41833 compared with control plants after 37 days in the S-H cultivation system. Similarly, a significantly higher relative expression of LePGT2 in plants inoculated with R. irregularis MUCL 41833 was noticed after 9 versus 37 days in the S-H cultivation system. In Experiment 2, a significant lower relative expression of LePGT2 was observed in native AMF R. irregularis inoculated plants compared to the control.DiscussionOverall, our study showed that the native R. irregularis strain increased A/Sd production in A. tinctoria regardless of the growing system used, further suggesting that the inoculation of native/best performing AMF is a promising method to improve the production of important SMs.

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems

et al. 2023

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“…Studies have shown a consistent promotional effect for shikonin biosynthesis in L. erythorhizon, A. euchroma [21], L. officinale [62], and O. paniculatum [63]. Exogenous MeJA promoted the accumulation of shikonin derivatives, shikonofuran derivatives, and rosmarinic acid in the shikonin-proficiency cells, and caused a rapid and massive increase in the expression of genes involved in the shikonin biosynthesis pathway, such as HMGR and PGT [21].Zhao et al [16,31] overexpressed LeMYB1 in hairy roots of L. erythorhizon.…”

Section: 4shikonin Synthesis Of Aehr Under Nh4+ Toxicity and Its Poss...mentioning

confidence: 87%

Ammonium/Nitrate Ratio Affects the Growth and Shikonin Accumulation in <em>Arnebia euchroma</em>

Shi¹,

Liang²,

Wang³

et al. 2023

Preprint

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Nitrogen (N) strongly affects plant growth and metabolism. For shikonin biosynthesis, although the ammonium toxicity phenomenon has been reported, the effects of nitrogen on the shikonin synthesis remains obscure. In this study, we carried out four different concentrations of NH4+ treatments on Arnebia euchroma hairy roots (AEHR) to clarify the influence of NH4+ on the growth and shikonin accumulation in A. euchroma and the possible mechanism. The results showed that compared with the 0% NH4+ treatment (only nitrate as nitrogen source), 10% NH4+ treatment increased the fresh weight and the dry weight of AEHR, and promoted the synthesis of shikonins; 20% NH4+ treatment started to show the inhibition effects on growth and shikonin accumulation of AEHR and 30% NH4+ treatment exhibited the strongest inhibition effects. With increased percentage of NH4+, AEHRs became shorter and thicker with more branches. To further elucidate the mechanism, we analyzed the time-course of nitrogen assimilation, gene expression level of key enzymes involved in the shikonin biosynthesis pathway, and contents of various endogenous hormones under NH4+ toxicity condition. Results indicated that auxin and cytokinin might regulate the growth and architecture of AEHR under NH4+ toxicity, and jasmonate level was reduced along with the inhibition of shikonin biosynthesis. This first comprehensive investigation into the effects of ammonium/nitrate ratio on shikonin biosynthesis not only provided valuable data for optimizing the in vitro culture and shikonin production in A. euchroma, but also suggested potential fertilizer strategies for its cultivation.

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“…Studies have shown a consistent promotional effect of shikonin biosynthesis in L. erythorhizon, A. euchroma [21], L. officinale [62], and O. paniculatum [63]. Exogenous MeJA promoted the accumulation of shikonin derivatives, shikonofuran derivatives, and rosmarinic acid in shikonin-proficiency cells and caused a rapid and massive increase in the expression of genes involved in the shikonin biosynthesis pathway, such as HMGR and PGT [21].…”

Section: Shikonin Synthesis In Aehr Under Nh 4 + Toxicity and Its Pos...mentioning

confidence: 90%

The Ammonium/Nitrate Ratio Affects the Growth and Shikonin Accumulation in Arnebia euchroma

Shi,

Liang,

Wang

et al. 2023

Agronomy

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Nitrogen (N) strongly affects plant growth and metabolism. Although ammonium toxicity has been reported, the effects of nitrogen on shikonin biosynthesis remain obscure. In this study, we tested four different concentrations of NH4+ on Arnebia euchroma hairy roots (AEHR) to clarify the influence of NH4+ on the growth of AEHR and on shikonin accumulation in them and the possible mechanisms. The results showed that compared with the 0% NH4+ treatment (only nitrate as a nitrogen source), the 10% NH4+ treatment increased the fresh weight and the dry weight of AEHR and promoted the synthesis of shikonins. In contrast, the 20% NH4+ treatment started to show inhibition effects on the growth of and shikonin accumulation in AEHR, and the 30% NH4+ treatment exhibited the strongest inhibition effects. With an increased percentage of NH4+, the AEHR became shorter and thicker, with more branches. To further elucidate the mechanisms, we analyzed the time course of nitrogen assimilation, the gene expression level of key enzymes involved in shikonin biosynthesis pathway, and the content of various endogenous hormones in the presence of toxic NH4+ concentrations. The results indicated that auxin and cytokinin might regulate the growth and architecture of AEHR under NH4+ toxicity and revealed that the jasmonate level was reduced along with the inhibition of shikonin biosynthesis. This first comprehensive investigation of the effects of the ammonium/nitrate ratio on shikonin biosynthesis not only provides valuable data for optimizing the in vitro culture of A. euchroma and its shikonin production, but also suggests potential fertilizing strategies for its cultivation.

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Dynamics of alkannin/shikonin biosynthesis in response to jasmonate and salicylic acid in Lithospermum officinale

Cited by 7 publications

References 86 publications

Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems

Arbuscular mycorrhizal fungi impact the production of alkannin/shikonin and their derivatives in Alkanna tinctoria Tausch. grown in semi-hydroponic and pot cultivation systems

Ammonium/Nitrate Ratio Affects the Growth and Shikonin Accumulation in <em>Arnebia euchroma</em>

The Ammonium/Nitrate Ratio Affects the Growth and Shikonin Accumulation in Arnebia euchroma

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