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      Improving large-scale biomass and total alkaloid production of Dendrobium nobile Lindl. using a temporary immersion bioreactor system and MeJA elicitation

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          Abstract

          Background

          Dendrobium nobile Lindl. is an important pharmacopeial plant with medicinal and ornamental value. This study sought to provide a technical means for the large-scale production of total alkaloid in D. nobile. Seedlings were cultured in vitro using a temporary immersion bioreactor system (TIBS). The four tested immersion frequencies (min/h; 5/2, 5/4, 5/6, and 5/8) influenced the production of biomass and total alkaloid content. In addition, to compare the effects of different concentrations of the phytohormone methyl jasmonate (MeJA) and treatment time on biomass and total alkaloid accumulation, MeJA was added to the TIBS medium after 50 days. Finally, total alkaloid production in semi-solid system (SSS), TIBS, and TIBS combined with the MeJA system (TIBS-MeJA) were compared.

          Results

          The best immersion frequency was found to be 5/6 (5 min every 6 h), which ensured appropriate levels of biomass and total alkaloid content in plantlets. The alkaloid content and production level of seedlings were the highest after treatment with 10 μM MeJA separately for 20 and 30 days using TIBS. The maximum content (7.41 mg/g DW) and production level (361.24 mg/L) of total alkaloid on use of TIBS-MeJA were 2.32- and 4.69-fold, respectively, higher in terms of content, and 2.07- and 10.49-fold, respectively, higher in terms of production level than those on using of TIBS (3.20 mg/g DW, 174.34 mg/L) and SSS (1.58 mg/g DW, 34.44 mg/L).

          Conclusions

          Our results show TIBS-MeJA is suitable for large-scale production of total alkaloid in in vitro seedlings. Therefore, this study provides a technical means for the large-scale production of total alkaloid in D. nobile.

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          Most cited references65

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          A downstream mediator in the growth repression limb of the jasmonate pathway.

          Wounding plant tissues initiates large-scale changes in transcription coupled to growth arrest, allowing resource diversion for defense. These processes are mediated in large part by the potent lipid regulator jasmonic acid (JA). Genes selected from a list of wound-inducible transcripts regulated by the jasmonate pathway were overexpressed in Arabidopsis thaliana, and the transgenic plants were then assayed for sensitivity to methyl jasmonate (MeJA). When grown in the presence of MeJA, the roots of plants overexpressing a gene of unknown function were longer than those of wild-type plants. When transcript levels for this gene, which we named JASMONATE-ASSOCIATED1 (JAS1), were reduced by RNA interference, the plants showed increased sensitivity to MeJA and growth was inhibited. These gain- and loss-of-function assays suggest that this gene acts as a repressor of JA-inhibited growth. An alternative transcript from the gene encoding a second protein isoform with a longer C terminus failed to repress jasmonate sensitivity. This identified a conserved C-terminal sequence in JAS1 and related genes, all of which also contain Zim motifs and many of which are jasmonate-regulated. Both forms of JAS1 were found to localize to the nucleus in transient expression assays. Physiological tests of growth responses after wounding were consistent with the fact that JAS1 is a repressor of JA-regulated growth retardation.
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            Jasmonic acid promotes degreening via MYC2/3/4- and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes.

            Degreening caused by rapid chlorophyll (Chl) degradation is a characteristic event during green organ senescence or maturation. Pheophorbide a oxygenase gene (PAO) encodes a key enzyme of Chl degradation, yet its transcriptional regulation remains largely unknown. Using yeast one-hybrid screening, coupled with in vitro and in vivo assays, we revealed that Arabidopsis MYC2/3/4 basic helix-loop-helix proteins directly bind to PAO promoter. Overexpression of the MYCs significantly enhanced the transcriptional activity of PAO promoter in Arabidopsis protoplasts, and methyl jasmonate (MeJA) treatment greatly induced PAO expression in wild-type Arabidopsis plants, but the induction was abolished in myc2 myc3 myc4. In addition, MYC2/3/4 proteins could promote the expression of another Chl catabolic enzyme gene, NYC1, as well as a key regulatory gene of Chl degradation, NYE1/SGR1, by directly binding to their promoters. More importantly, the myc2 myc3 myc4 triple mutant showed a severe stay-green phenotype, whereas the lines overexpressing the MYCs showed accelerated leaf yellowing upon MeJA treatment. These results suggest that MYC2/3/4 proteins may mediate jasmonic acid (JA)-induced Chl degradation by directly activating these Chl catabolic genes (CCGs). Three NAC family proteins, ANAC019/055/072, downstream from MYC2/3/4 proteins, could also directly promote the expression of a similar set of CCGs (NYE1/SGR1, NYE2/SGR2 and NYC1) during Chl degradation. In particular, anac019 anac055 anac072 triple mutant displayed a severe stay-green phenotype after MeJA treatment. Finally, we revealed that MYC2 and ANAC019 may interact with each other and synergistically enhance NYE1 expression. Together, our study reveals a hierarchical and coordinated regulatory network of JA-induced Chl degradation.
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              Elicitation: A Tool for Enriching the Bioactive Composition of Foods

              Elicitation is a good strategy to induce physiological changes and stimulate defense or stress-induced responses in plants. The elicitor treatments trigger the synthesis of phytochemical compounds in fruits, vegetables and herbs. These metabolites have been widely investigated as bioactive compounds responsible of plant cell adaptation to the environment, specific organoleptic properties of foods, and protective effects in human cells against oxidative processes in the development of neurodegenerative and cardiovascular diseases and certain types of cancer. Biotic (biological origin), abiotic (chemical or physical origin) elicitors and phytohormones have been applied alone or in combinations, in hydroponic solutions or sprays, and in different selected time points of the plant growth or during post-harvest. Understanding how plant tissues and their specific secondary metabolic pathways respond to specific treatments with elicitors would be the basis for designing protocols to enhance the production of secondary metabolites, in order to produce quality and healthy fresh foods.
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                Author and article information

                Contributors
                dingxynjj@163.com
                Journal
                Plant Methods
                Plant Methods
                Plant Methods
                BioMed Central (London )
                1746-4811
                22 January 2022
                22 January 2022
                2022
                : 18
                : 10
                Affiliations
                GRID grid.260474.3, ISNI 0000 0001 0089 5711, College of Life Sciences, , Nanjing Normal University, ; Nanjing, 210023 China
                Author information
                http://orcid.org/0000-0003-3836-3395
                Article
                843
                10.1186/s13007-022-00843-9
                8783522
                35065671
                c9ae0694-835c-4d90-8f1d-21839146402f
                © The Author(s) 2022

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 18 May 2021
                : 12 January 2022
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100012431, Jiangsu Agricultural Science and Technology Independent Innovation Fund;
                Award ID: (No. CX(18)3063).
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2022

                Plant science & Botany
                dendrobium nobile lindl.,temporary immersion bioreactor system,immersion frequency,meja,bioactive compound

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