Skip to main content
SpringerLink
Log in

Induction and metabolomic analysis of hairy roots of Atractylodes lancea

  • Methods and Protocols
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Atractylodes lancea is an important source of traditional Chinese medicines. Sesquiterpenoids are the key active compounds in A. lancea, and their presence determines the quality of the material. Hairy hoot (HR) culture is a potential method to produce medicinally active compounds industrially; however, the induction and metabolic profiling of A. lancea HR have not been reported. We found that optimal induction of A. lancea HR was achieved by Agrobacterium rhizogenes strain C58C1 using the young leaves of tissue culture seedlings in the rooting stage as explants. Ultra-performance liquid chromatography-tandem mass spectrometric analyses of the chemical compositions of HR and normal root (NR) led to the annotation of 1046 metabolites. Over 200 differentially accumulated metabolites were identified, with 41 found to be up-regulated in HR relative to NR and 179 down-regulated in HR. Specifically, atractylodin levels were higher in HR, while the levels of β-eudesmol and hinesol were higher in NR. Metabolic pathway analyses showed a significant difference in metabolites of the shikimate acid pathway between HR and NR. Five A. lancea compounds are potential biomarkers for evaluation of HR and NR quality. This study provides an important reference for the application of HR for the production of medicinally active compounds.

Key points

• We established an efficient protocol for the induction of HR in A. lancea

• HR was found to have a significantly higher amount of atractylodin than did NRs

• Metabolic pathway analyses showed a significant difference in metabolites of the shikimate acid pathway between HR and NR

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The authors declare that the data supporting the findings of this study are available within the article and its supplementary information file.

References

  • Aboul-Maaty NAF, Oraby HAS (2019) Extraction of high-quality genomic DNA from different plant orders applying a modified CTAB-based method. Bull Nat Res Centre 43:1–10

    Google Scholar 

  • Amani S, Mohebodini M, Khademvatan S, Jafari M (2020) Agrobacterium rhizogenes mediated transformation of Ficus carica L. for the efficient production of secondary metabolites. J Sci Food Agric 100:2185–2197

    CAS  PubMed  Google Scholar 

  • Bai C, Xu J, Cao B, Li X, Li G (2018) Transcriptomic analysis and dynamic expression of genes reveal flavonoid synthesis in Scutellaria viscidula. Acta Physiol Plant 40:1–11

    Google Scholar 

  • Bailly C (2021) Medicinal properties and anti-inflammatory components of Phytolacca (Shanglu). DCM 4(3):159–169

    CAS  Google Scholar 

  • Bais HP, Loyola-Vargas VM, Flores HE, Vivanco JM (2001) Root-specific metabolism: the biology and biochemistry of underground organs. In Vitro Cell Dev-Pl 37:730–741

    CAS  Google Scholar 

  • Brijwal L, Pandey A, Tamta S (2015) In vitro propagation of the endangered species berberis aristata DC. via leaf-derived callus. In Vitro Cell Dev-Pl 51:637–647

    CAS  Google Scholar 

  • Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395

    CAS  Google Scholar 

  • Chen L, Yang J, Zhao S, Li T, Qing R, Kong L (2021) Atractylodis rhizome water extract attenuates fructose-induced glomerular injury in rats through anti-oxidation to inhibit TRPC6/p-CaMK4 signaling. Phytomedicine 91:153643

    CAS  PubMed  Google Scholar 

  • Cho H, Kim U, Suh J, Eom H, Kim J, Lee S, Han S (2016) Classification of the medicinal plants of the genus Atractylodes using high-performance liquid chromatography with diode array and tandem mass spectrometry detection combined with multivariate statistical analysis. J Sep Sci 39(7):1286–1294

    CAS  PubMed  Google Scholar 

  • Deng C, Hao X, Shi M, Fu R, Wang Y, Zhang Y, Kai G (2019) Tanshinone production could be increased by the expression of SmWRKY2 in Salvia miltiorrhiza hairy roots. Plant Sci 284:1–8

    CAS  PubMed  Google Scholar 

  • Dhakulkar S, Ganapathi TR, Bhargava S, Bapat VA (2005) Induction of hairy roots in Gmelina arborea Roxb. and production of verbascoside in hairy roots. Plant Sci 169:812–818

    CAS  Google Scholar 

  • Díaz-Quiroz D, Cardona-Félix C, Viveros-Ceballos J, Reyes-González M, Bolívar F, Ordoñez M, Escalante A (2018) Synthesis, biological activity and molecular modelling studies of shikimic acid derivatives as inhibitors of the shikimate dehydrogenase enzyme of Escherichia coli. J Enzym Inhib Med Ch 33(1):397–404

    Google Scholar 

  • Dupre P, Lacoux J, Neutelings G, Mattar-Laurain D, Fliniaux M, David A, Jacquin-Dubreuil A (2000) Genetic transformation of Ginkgo biloba by Agrobacterium tumefaciens. Physiol Plant 108:413–419

    CAS  Google Scholar 

  • Foresto E, Gilardi P, Ibarra L, Cogno I (2021) Light-activated green drugs: how we can use them in photodynamic therapy and mass-produce them with biotechnological tools. Phytomedicine Plus 1(3):100044

    Google Scholar 

  • Fu C, Zhao D, Xue X, Jin Z, Ma F (2005) Transformation of Saussurea involucrata by agrobacterium rhizogenes: hairy root induction and syringin production. Process Biochem 40:3789–3794

    CAS  Google Scholar 

  • Gabr AM, Sytar O, Ghareeb H, Brestic M (2019) Accumulation of amino acids and flavonoids in hairy root cultures of common buckwheat (Fagopyrum esculentum). Physiol Mol Biol Plants 25:787–797

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghimire B, Thiruvengadam M, Chung I (2019) Identification of elicitors enhances the polyphenolic compounds and pharmacological potential in hairy root cultures of aster scaber. S Afr J Bot 125:92–101

    CAS  Google Scholar 

  • Giri A, Narasu M (2000) Transgenic hairy roots: recent trends and applications. Biotechnol Adv 18(1):1–22

    CAS  PubMed  Google Scholar 

  • Goel M, Mehrotra S, Kukreja A (2011) Elicitor-induced cellular and molecular events are responsible for productivity enhancement in hairy root cultures: an insight study. Appl Biochem Biotechnol 165:1342–1355

    CAS  PubMed  Google Scholar 

  • Guimaraes L, Pereira B, Araujo A, Guimaraes P, Brasileiro A (2017) Ex vitro hairy root induction in detached peanut leaves for plant-nematode interaction studies. Plant Methods 13:1–10

    Google Scholar 

  • Gurel S (2021) Sand-wounding of shoot and petiole explants enhances transformation efficiency in sugar beet (Beta vulgaris L.) by Agrobacterium-mediated transformation. Sugar Tech 23:415–427

    CAS  Google Scholar 

  • Gurunani S, Yeole M, Gholse Y, Chaple D (2015) Hairy root culture: an experimental system for secondary metabolite production. RJPT 8(6):728–730

    Google Scholar 

  • Ha L, Pawlicki-Jullian N, Pillon-Lequart M, Boitel-Conti M, Duong H, Gontier E (2016) Hairy root cultures of Panax vietnamensis, a promising approach for the production of ocotillol-type ginsenosides. Plant Cell Tiss Org 126:93–103

    CAS  Google Scholar 

  • Halder M, Sarkar S, Jha S (2019) Elicitation: a biotechnological tool for enhanced production of secondary metabolites in hairy root cultures. Eng Life Sci 19(12):880–895

    CAS  PubMed  PubMed Central  Google Scholar 

  • Han X, Wang B, Lin X, Jia J (2006) Study on efficient somatic embryogenesis and plant regeneration of coronilla varia. J Nor Univer (Natural Science Edition) 36:420–423

    CAS  Google Scholar 

  • Hao C, Wang S, Wang Y, Hou X, Jiang Y, Jiang B, Xue Z (2021) Technology and application of hairy root culture in Monocotyledons. Cur Bio Eng 7:31–37

    Google Scholar 

  • Hao X, Shi M, Cui L, Xu C, Zhang Y, Kai G (2015) Effects of methyl jasmonate and salicylic acid on tanshinone production and biosynthetic gene expression in transgenic Salvia miltiorrhiza hairy roots. Biotech Bioch 62:24–31

    CAS  Google Scholar 

  • Ibañez S, Talano M, Ontañon O, Suman J, Medina M, Macek T, Agostini E (2016) transgenic plants and hairy roots: exploiting the potential of plant species to remediate contaminants. N Biotechnol 33(5):625–635

    PubMed  Google Scholar 

  • Jiao P, Tseng-Crank J, Corneliusen B, Yimam M, Hodges M, Hong M, Jia Q (2014) Lipase inhibition and antiobesity effect of Atractylodes lancea. Planta Med 80(07):577–582

    CAS  PubMed  Google Scholar 

  • Jin S, Hyun TK (2020) Ectopic expression of production of anthocyanin pigment 1 (PAP1) improves the antioxidant and anti-melanogenic properties of ginseng (Panax ginseng CA Meyer) hairy roots. Antioxidants 9:922

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jun X, Fu P, Lei Y, Cheng P (2018) Pharmacological effects of medicinal components of Atractylodes lancea (Thunb.) DC. Chinas Med 13:1–10

    Google Scholar 

  • Kang M, Fu R, Zhang P, Lou S, Yang X, Chen Y, Liu J (2021) A chromosome-level camptotheca acuminata genome assembly provides insights into the evolutionary origin of camptothecin biosynthesis. Nat Commun 12:3531

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kim O, Bang K, Shin Y, Lee M, Jung S, Hyun D, Hwang B (2007) Enhanced production of asiaticoside from hairy root cultures of Centella asiatica (L.) Urban elicited by methyl jasmonate. Plant Cell Rep 26:1941–1949

    CAS  PubMed  Google Scholar 

  • Kochan E, Szymczyk P, Kuźma Ł, Szymańska G (2016) Nitrogen and phosphorus as the factors affecting ginsenoside production in hairy root cultures of Panax quinquefolium cultivated in shake flasks and nutrient sprinkle bioreactor. Acta Physiol Plant 38:1–13

    CAS  Google Scholar 

  • Li C, Wang M (2021) Application of hairy root culture for bioactive compounds production in medicinal plants. Curr Pharm Biotechnol 22(5):592–608

    CAS  PubMed  Google Scholar 

  • Li H, Liu J, Pei T, Bai Z, Han R, Liang Z (2019) Overexpression of SmANS enhances anthocyanin accumulation and alters phenolic acids content in Salvia miltiorrhiza and Salvia miltiorrhiza Bge f. alba plantlets. Int J Mol Sci 20:2225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin H, Kwok K, Doran P (2003) Development of Linum flavum hairy root cultures for production of coniferin. Biotechnol Lett 25:521–525

    CAS  PubMed  Google Scholar 

  • Liu Y, Qi X, Liu Y, Cai Q, Liu S, Sun J, Lv X (2020) Investigation on the urinary excretion kinetics of three atractylenolides from crude and processed Atractylodis rhizoma extracts in rats by UPLC-MS/MS. Pak J Pharm Sci 33(3):953–960

    CAS  PubMed  Google Scholar 

  • Lokhande V, Kudale S, Nikalje G, Desai N, Suprasanna P (2015) Hairy root induction and phytoremediation of textile dye, Reactive green 19A-HE4BD, in a halophyte, sesuvium portulacastrum (L.) L. Biotechnol Rep 8:56–63

    Google Scholar 

  • Lott A, Freed C, Dickinson C, Whitehead S, Collakova E, Jelesko J (2020) Poison Ivy Hairy Root Cultures Enable A Stable Transformation System Suitable For Detailed Investigation Of Urushiol Metabolism. Plant Direct 4(8):E00243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mahendran G, Verma N, Singh S, Parveen S, Singh M, Luqman S, Rahman L (2022) Isolation, and characterization of a novel xanthone from the hairy root cultures of swertia chirayita (Roxb.) H. Karst. and its biological activity. Ind Crop Prod 176:114369

    CAS  Google Scholar 

  • Matveeva T, Sokornova S, Lutova L (2015) Influence of Agrobacterium oncogenes on secondary metabolism of plants. Phytochem Rev 14:541–554

    CAS  Google Scholar 

  • Mi Y, Zhu Z, Qian G, Li Y, Meng X, Xue J, Shi Y (2020) Inducing hairy roots by agrobacterium rhizogenes-mediated transformation in tartary buckwheat (Fagopyrum tataricum). JoVE 157:e60828

    Google Scholar 

  • Nigutová K, Kusari. S, Sezgin. S, Petijová. L, Henzelyová. J, Bálintová. M, Čellárová  (2019) Chemometric evaluation of hypericin and related phytochemicals in 17 in vitro cultured Hypericum species, hairy root cultures and hairy root-derived transgenic plants. J Pharm Pharmacol 71:46-57

  • Nourozi E, Hosseini B, Hassani A (2016) Influences of various factors on hairy root induction in Agastache foeniculum (Pursh) Kuntze. Acta Agriculturae Slovenica 107:45–54

    Google Scholar 

  • Ooi C, Syahida A, Stanslas J, Maziah M (2013) Efficiency of different Agrobacterium rhizogenes strains on hairy roots induction in Solanum mammosum. World J Microbiol Biotechnol 29:421–430

    CAS  PubMed  Google Scholar 

  • Takeda O, Miki E, Terabayashi S, Okada M, Lu Y, He HS, He SA (1996) A Comparative study on essential oil components of wild and cultivated Atractylodes lancea and A. chinensis. Planta Med (62):444–449

  • Pandey N, Rai K, Pandey-Rai S (2021) Heterologous expression of cyanobacterial PCS confers augmented arsenic and cadmium stress tolerance and higher artemisinin in Artemisia annua hairy roots. Plant Biotechnol Rep 15:317–334

    CAS  PubMed  PubMed Central  Google Scholar 

  • Petit A, David C, Dahl GA, Ellis JG, Guyon P, Casse-Delbart F, Tempé J (1983) Further extension of the opine concept: plasmids in Agrobacterium rhizogenes cooperate for opine degradation. MGG 190:204–214

    CAS  Google Scholar 

  • Povydysh M, Titova M, Ivkin D, Krasnova M, Vasilevskaya E, Fedulova L, Nosov A (2023) The Hypoglycemic and hypocholesterolemic activity of Dioscorea deltoidea, tribulus terrestris and Panax japonicus cell cultures in rats with high-fat diet-induced obesity. Nutrients 15:656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes-Pérez R, Herrera-Ruiz M, Perea-Arango I, Martínez-Morales F, Arellano DJ, García J, Nicasio-Torres P (2022) Anti-inflammatory compounds produced in hairy roots culture of Sphaeralcea angustifolia. Pctoc 149:351–361

    Google Scholar 

  • Sandhya S, Giri A (2022) Development of efficient Agrobacterium rhizogenes-mediated hairy root system in Curcuma longa L. and elicitation driven enhanced production of pharmaceutically important curcuminoids. In Vitro Cell Dev-Pl 58:794–805

    CAS  Google Scholar 

  • Sarkar J, Misra A, Banerjee N (2020) Genetic transfection, hairy root induction and solasodine accumulation in elicited hairy root clone of Solanum erianthum D. Don J Biotechnol 323:238–245

    CAS  PubMed  Google Scholar 

  • Sazegari S, Niazi A, Shahriari-Ahmadi F, Afsharifar A (2022) CrMYC1 contributes to catharanthine and ajmalicine accumulation by regulating the TIA pathway in catharanthus roseus hairy roots. Hortic Environ Biote 63:709–717

    CAS  Google Scholar 

  • Sharafi A, Sohi HH, Azadi P, Sharafi AA (2014) Hairy root induction and plant regeneration of medicinal plant Dracocephalum kotschyi. Physiol Mol Biol Pla 20:257–262

    CAS  Google Scholar 

  • Shi M, Liao P, Nile S, Georgiev M, Kai G (2021) Biotechnological exploration of transformed root culture for value-added products. Trends Biotechnol 39:137–149

    CAS  PubMed  Google Scholar 

  • Song G, Xu Y, Shi J, Xie Z (2018) Establishment of large-scale tissue culture and rapid propagation system for Atractylodes lancea. Acta Agriculturae Jiangxi 30(9):63–67

    Google Scholar 

  • Song W, Zhuang Y, Liu T (2020) Potential role of two cytochrome P450s obtained from lithospermum erythrorhizon in catalyzing the oxidation of geranylhydroquinone during Shikonin biosynthesis. Phytochemistry 175:112375

    CAS  PubMed  Google Scholar 

  • Sudha C, Reddy B, Ravishankar G, Seeni S (2003) Production of ajmalicine and ajmaline in hairy root cultures of Rauvolfia micrantha Hook f., a rare and endemic medicinal plant. Biotechnol Lett 25:631–636

    CAS  PubMed  Google Scholar 

  • Sujatha G, Zdravković-Korać S, Ćalić D, Flamini G, Kumari BR (2013) High-efficiency Agrobacterium rhizogenes-mediated genetic transformation in Artemisia vulgaris: hairy root production and essential oil analysis. Ind Crop Prod 44:643–652

    CAS  Google Scholar 

  • Thwe A, Kim J, Bok Kim Y, Romij Uddin M, Kim SJ, Park SU (2013) Metabolomic analysis and phenylpropanoid biosynthesis in hairy root culture of tartary buckwheat cultivars. PloS One 8:e65349

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tu J, Xie Y, Xu K, Qu L, Lin X, Ke C, Liu Y (2020) Treatment of spleen-deficiency syndrome with atractyloside A from bran-processed Atractylodes lancea by protection of the intestinal mucosal barrier. Front Pharmacol 11:583160

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsusaka T, Makino B, Ohsawa R, Ezura H (2019) Genetic and environmental factors influencing the contents of essential oil compounds in Atractylodes lancea. PloS One 14(5):e0217522

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vinterhalter B, Savić J, Zdravković-Korać S, Banjac N, Vinterhalter D, Krstić-Milošević D (2019) Agrobacterium rhizogenes-mediated transformation of gentiana utriculosa L. and xanthones decussatin-1-O-primeveroside and decussatin accumulation in hairy roots and somatic embryo-derived transgenic plants. Ind Crop Prod 130:216–229

    CAS  Google Scholar 

  • Volk GM, Bonnart R, Oliveira ACA, Henk AD (2022) Minimizing the deleterious effects of endophytes in plant shoot tip cryopreservation. Appl in Plant Sci 10:e11489

    CAS  Google Scholar 

  • Wen S, Ge XL, Wang R, Yang H, Bai Y, Guo Y, Wang L (2022) An efficient agrobacterium-mediated transformation method for hybrid poplar 84K (Populus alba × P. glandulosa) using calli as explants. Int J Mol Sci 23:2216

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Zheng L, Yuan H, Wang J (2013) Propagation of Salvia miltiorrhiza from hairy root explants via somatic embryogenesis and tanshinone content in obtained plants. Ind Crop Prod 50:648–653

    CAS  Google Scholar 

  • Wu S, Chen W, Lu S, Zhang H, Yin L (2022) Metabolic engineering of shikimic acid biosynthesis pathway for the production of shikimic acid and its branched products in microorganisms: advances and prospects. Molecules 27(15):4779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu R, Lu J, Wu J, Yu D, Chu S, Guan F, Zha L (2022) Comparative analysis in different organs and tissue-specific metabolite profiling of Atractylodes lancea from four regions by GC–MS and laser microdissection. J Sep Sci 45:1067–1079

    CAS  PubMed  Google Scholar 

  • Yao S, Bai L, Lan Z, Tang M, Zhai Y, Huang H, Wei R (2016) Hairy root induction and polysaccharide production of medicinal plant Callerya speciosa Champ. Plant Cell Tiss Org 126(1):177–186

    CAS  Google Scholar 

  • Zeng L, Dehesh K (2021) The eukaryotic MEP-pathway genes are evolutionarily conserved and originated from chlaymidia and cyanobacteria. BMC Genomics 22:1–12

    Google Scholar 

  • Zhang C, Jiang Y, Liu C, Shi L, Li J, Zeng Y, Wang S (2022a) Identification of medicinal compounds of Fagopyri Dibotryis rhizome from different origins and its varieties using UPLC-MS/MS-Based metabolomics. Metabolites 12(9):790

    PubMed  PubMed Central  Google Scholar 

  • Zhang H, Cao Y, Zhang H, Xu Y, Zhou C, Liu W, Sun D (2020a) Efficient generation of CRISPR/Cas9-mediated homozygous/biallelic Medicago truncatula mutants using a hairy root system. Front Plant Sci 11:294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Liu R, Li H, Yang Y, Zhou F (2022b) Isoflavonoids from Astragalus membranaceus hairy roots. Chem Nat Compd 58:541–544

    CAS  Google Scholar 

  • Zhang W, Ouyang Z, Zhao M, Wei Y, Peng H, Wang Q, Guo L (2015) The influences of inorganic elements in soil on the development of famous-region Atractylodes lancea (Thunb.) DC. Pharmacogn Mag 11(42):337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Zhao Z, Chang L, Cao Y, Wang S, Kang C, Wang H, Zhou L, Huang L, Guo L (2020b) Atractylodis Rhizoma: a review of its traditional uses, phytochemistry, pharmacology, toxicology, and quality control. J Ethnopharmacol 266:113415

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was financially supported by National Natural Science Foundation of China (No: 81891014), Scientific and technological innovation project of China Academy of Chinese Medical Sciences (CI2021A03903, CI2021A03905, CI2021B013), Innovation Team and Talents Cultivation Program of National Administration of Traditional Chinese Medicine (No: ZYYCXTD-D-202005), China Agriculture Research System of MOF and MARA (CARS-21), and Key Project at Central Government level: the ability establishment of sustainable use for valuable Chinese medicine resources (2060302).

Author information

Author notes

  1. Chengcai Zhang and Xiuzhi Guo contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, 100700, People’s Republic of China

    Chengcai Zhang, Xiuzhi Guo, Hongyang Wang, Binbin Yan, Sheng Wang & Lanping Guo

  2. Dexing Research and Training Center of Chinese Medical Sciences, Dexing, 334220, People’s Republic of China

    Xiaoyu Dai, Binbin Yan & Sheng Wang

Authors
  1. Chengcai Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiuzhi Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongyang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoyu Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Binbin Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sheng Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Lanping Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conception and design, S.W. and L.G.; sample collection, X.D. and B.Y.; sample preparation and measurement, C.Z., H.W., and X.G; data analysis, C.Z. and S.W.; writing: preparation of the original draft, C.Z. and X.G.; writing: review and editing, C.Z.; and funding acquisition, S.W. and L.G. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Sheng Wang or Lanping Guo.

Ethics declarations

Ethics approval

Not applicable.

Conflicts of interest

The authors declare competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(PDF 492 kb)

ESM 2

(XLS 1254 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, C., Guo, X., Wang, H. et al. Induction and metabolomic analysis of hairy roots of Atractylodes lancea. Appl Microbiol Biotechnol 107, 6655–6670 (2023). https://doi.org/10.1007/s00253-023-12735-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-023-12735-6

Keywords

Search

Navigation