Skip to main content
SpringerLink
Log in

Metabolites of zearalenone and phytohormones secreted by endophytic fungus strain TH15 regulating the root development in Tetrastigma hemsleyanum

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

This article has been updated

Abstract

Tetrastigma hemsleyanum is a traditional Chinese herb plant. The endophytic fungus strain TH15 isolated from root of T. hemsleyanum has been reported to significantly promote the growth of T. hemsleyanum. In this study, we combined HPLC–MS and ELISA to analyze the composition of TH15’s fermentation broth. We also explored the effects of zearalenone, a metabolite of strain TH15, on the growth of T. hemsleyanum seedlings and expansin gene expression in root. Metabolomic analysis revealed that TH15 metabolites contained 5 phytohormones [indole-3-acetic acid (IAA), methyl indole-3-acetate (MeIAA), jasmonic acid (JA), jasmonoyl-l-isoleucine (JA-ILE) and salicylic acid (SA)], amino acids, sugar and vitamins. ELISA test indicated that TH15 metabolites contained zearalenone (ZEN). Supplement 0.1–0.5 mg/L ZEN into the culture medium promoted the growth of seedlings of T. hemsleyanum. Besides, ZEN treatment significantly promoted expression of the expansin gene in the root of T. hemsleyanum. The endophytic fungus strain TH15 secretes phytohormones like IAA, JA and SA, as well as other metabolites like ZEN. TH15’s growth-promoting effects are realized by these secreted molecules’ coordinated action. The endophytic fungal metabolite ZEN participates in the regulation of T. hemsleyanum’s growth, which is an important molecular mechanism for the plant growth-promoting effects of the endophytic fungi strain TH15.

Key message

The endophytic fungus strain TH15 isolated from root of T. hemsleyanum secrets zearalenone and phytohormones (IAA, JA and SA), which have the effect on regulating root development of T. hemsleyanum.

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

Similar content being viewed by others

Change history

  • 05 June 2022

    The original version of this article has been revised: The Funding section has been corrected.

Abbreviations

ELISA:

Enzyme-linked immunosorbent assay

FB:

Fermentation broth

FC:

Fold change

GA:

Gibberellic acid

HPLC–MS:

High-performance liquid chromatography with tandem mass spectrometry

IAA:

Indole-3-acetic acid

ICA:

Indole-3-carboxaldehyde

ITS:

Internally transcribed spacer

JA:

Jasmonic acid

JA-ILE:

Jasmonoyl-l-isoleucine

MeIAA:

Methyl indole-3-acetate

OD:

Optical density

OPLS-DA:

Orthogonal partial least squares discriminant analysis

PCA:

Principal component analysis

PLS-DA:

Partial least squares discriminant analysis

QC:

Quality control

RSD:

Relative standard deviation

SA:

Salicylic acid

TIC:

Total ion chromatography

VIP:

Variable important in projection

ZEN:

Zearalenone

References

  • Álvarez-Fernández MA, Carafa I, Vrhovsek U, Arapitsas P (2020) Modulating wine aromatic amino acid catabolites by using Torulaspora delbrueckii in sequentially inoculated fermentations or Saccharomyces cerevisiae alone. Microorganisms 8:1349

    Article  PubMed Central  CAS  Google Scholar 

  • Bowya T, Balachandar DJ (2020) Basic Microbiol. Harnessing PGPR inoculation through exogenous foliar application of salicylic acid and microbial extracts for improving rice growth. J Basic Microbiol 60:950–961

    Article  CAS  PubMed  Google Scholar 

  • Chaiwanon J, Wang W, Zhu J-Y, Oh E, Wang Z-Y (2016) Information integration and communication in plant growth regulation. Cell 164:1257–1268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chanway CP (1996) Endophytes: they’re not just fungi! Can J Bot 74:321–322

    Article  Google Scholar 

  • Chen X, Liu H, Meng F (1989) Direct enzyme-linked immunoassay for zearalenone. Plant Physiol Commun 25:61–63 (in Chinese)

    CAS  Google Scholar 

  • Compant S, Saikkonen K, Mitter B, Campisano A, Mercado-Blanco J (2016) Editorial special issue: soil, plants and endophytes. Plant Soil 405:1–11

    Article  CAS  Google Scholar 

  • Du S, Xiang T, Song Y, Huang L, Sun Y, Han Y (2015) Transgenic hairy roots of Tetrastigma hemsleyanum: induction, propagation, genetic characteristics and medicinal components. Plant Cell Tissue Org Cult 122:373–382

    Article  CAS  Google Scholar 

  • Eagles EJ, Benstead R, MacDonald S, Handy R, Hutchinson TH (2019) Impacts of the mycotoxin zearalenone on growth and photosynthetic responses in laboratory populations of freshwater macrophytes (Lemna minor) and microalgae (Pseudokirchneriella subcapitata). Ecotoxicol Environ Saf 169:225–231

    Article  CAS  PubMed  Google Scholar 

  • Eagles EJ, Benstead R, MacDonald S, Handy RD, Hutchinson TH (2021) Environmental risks to freshwater organisms from the mycotoxins deoxynivalenol and zearalenone using Species Sensitivity Distributions. Chemosphere 267:129279

    Article  CAS  PubMed  Google Scholar 

  • Filek M, Sieprawska A, Kościelniak J, Oklestkova J, Jurczyk B, Telk A, Biesaga-Kościelniak J, Janeczko A (2019) The role of chloroplasts in the oxidative stress that is induced by zearalenone in wheat plants—the functions of 24-epibrassinolide and selenium in the protective mechanisms. Plant Physiol Biochem 137:84–92

    Article  CAS  PubMed  Google Scholar 

  • Fu Y-F, Meng F-J (1993) The effects of zearalenone on the growth and development of Lemna Gibba G3. Acta Phytophysiol Sin 29:395–398 (in Chinese)

    Google Scholar 

  • Fu Y-F, Meng F-J (1994) Zearalenone in growth and development of winter wheat. Acta Agron Sin 20:271–276 (in Chinese)

    Google Scholar 

  • Fu Y-F, Han Y-Z, Zhao D-G, Meng F-J (2000) Zearalenone and flower bud formation in thin-cell layers of Nicotiana tabacum L. Plant Growth Regul 30:271–274

    Article  CAS  Google Scholar 

  • Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:E311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact 22:763–772

    Article  CAS  PubMed  Google Scholar 

  • Hardoim P, van Overbeek L, Berg G, Pirttilä A, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Kesting J, Olsen L, Staerk D, Tejesvi M, Kini K, Prakash H, Jaroszewski J (2011) Production of unusual dispiro metabolites in Pestalotiopsis virgatula endophyte cultures: HPLC-SPE-NMR, electronic circular dichroism, and time-dependent density-functional computation study. J Nat Prod 74:2206–2215

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Lee IJ (2013) Endophytic Penicillium funiculosum LHL06 secretes gibberellin that reprograms Glycine max L. growth during copper stress. BMC Plant Biol 13:86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AL, Hamayun M, Kang SM, Kim YH, Jung HY, Lee J, Lee IJ (2012) Endophytic fungal association via gibberellins and indole acetic acid can improve plant growth under abiotic stress: an example of Paecilomyces formosus LHL10. BMC Microbiol 12:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan AL, Hussain J, Al-Harrasi A, Al-Rawahi A, Lee IJ (2015) Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit Rev Biotechnol 3:62–74

    Article  CAS  Google Scholar 

  • Kościelniak J, Biesaga-Kościelniak J, Janeczko A, Filek W, Kalaji HM (2010) Can the Giberella zeae toxin zearalenone affect the photosynthetic productivity and increase yield formation in spring wheat and soybean plants? Photosynthetica 47:586–594

    Article  CAS  Google Scholar 

  • Kościelniak J, Ostrowska A, Biesaga-Kościelniak J, Filek W, Janeczko A, Kalaji HM, Stalmach K (2011) The effect of zearalenone on PSII photochemical activity and growth in wheat and soybean under salt (NaCl) stress. Acta Physiol Plant 33:2329–2338

    Article  CAS  Google Scholar 

  • Leitão AL, Enguita FJ (2016) Gibberellins in Penicillium strains: challenges for endophyte-plant host interactions under salinity stress. Microbiol Res 183:8–18

    Article  PubMed  CAS  Google Scholar 

  • Li J, Zhu T, Zhang C, Li B, Deng ZY, Meng F (1980) Study on zearalenone. J Beijing Agric Univ 1:13–28 (in Chinese)

    Google Scholar 

  • Liao X, Lovett B, Fang W, St Leger RJ (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163:980–991

    Article  CAS  PubMed  Google Scholar 

  • Lofgren LA, LeBlanc NR, Certano AK, Nachtigall J, LaBine KM, Riddle J, Broz K, Dong Y, Bethan B, Kafer CW, Kistler HC (2018) Fusarium graminearum: pathogen or endophyte of North American grasses? New Phytol 217:1203–1212

    Article  CAS  PubMed  Google Scholar 

  • Ma Y, Prasad MNV, Rajkumar M, Freitas H (2011) Plant growth promoting rhizobacteria and endophytes accelerate phytoremediation of metalliferous soils. Biotechnol Adv 29:248–258

    Article  CAS  PubMed  Google Scholar 

  • Mally A, Solfrizzo M, Degen GH (2016) Biomonitoring of the mycotoxin zearalenone: current state-of-the art and application to human exposure assessment. Arch Toxicol 90:1281–1292

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Rodríguez J, De la Mora-Amutio M, Plascencia-Correa LA, Audelo-Regalado E, Guardado FR, Hernández-Sánchez E, Peña-Ramírez YJ, Escalante A, Beltrán-García MJ, Ogura T (2015) Cultivable endophytic bacteria from leaf bases of Agave tequilana and their role as plant growth promoters. Braz J Microbiol 45:1333–1339

    Article  PubMed Central  Google Scholar 

  • Masunaka A, Hyakumachi M, Takenaka S (2011) Plant growth-promoting fungus, Trichoderma koningi suppresses isoflavonoid phytoalexin vestitol production for colonization on/in the roots of Lotus japonicus. Microbes Environ 26:128–134

    Article  PubMed  Google Scholar 

  • Mayer E, Dörr de Quadros P, Fulthorpe R (2019) Plantibacter flavus, Curtobacterium herbarum, Paenibacillus taichungensis, and Rhizobium selenitireducens endophytes provide host-Specific growth promotion of Arabidopsis thaliana, Basil, Lettuce, and Bok Choy plants. Appl Environ Microbiol 85:e00383-e419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng F-J, Que Y-M, Zhang S-Q (1986) Zearalenone-like substance in winter plants and its relation to vernalization. Acta Bot Sin 28:622–627 (in Chinese)

    CAS  Google Scholar 

  • Meng F-J, Que Y-M, Han Y-Z, Li H-X, Wang Z-C (1989) Isolation of zearalenone from shoot apices of overwintering winter wheat. Sci China Ser B 32:1100–1105

    Google Scholar 

  • Meng FJ, Han YZ, Que YM, Wang H (1992) Zearalenone, a key substance controlling plant development. In: Karssen CM, van Loon LC, Vreugdenhil D (eds) Progress in plant growth regulation. Current plant science and biotechnology in agriculture, vol 13. Springer, Dordrecht, pp 291–297

    Chapter  Google Scholar 

  • Nieva AS, Vilas JM, Gárriz A, Maiale SJ, Menéndez AB, Erban A, Kopka J, Ruiz OA (2019) The fungal endophyte Fusarium solani provokes differential effects on the fitness of two Lotus species. Plant Physiol Biochem 144:100–109

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richardson KE, Hagler WM Jr, Campbell CL, Hamilton PB (1985) Production of zearalenone, T-2 toxin, and deoxynivalenol by Fusarium spp. isolated from plant materials grown in North Carolina. Mycopathologia 90:155–160

    Article  CAS  PubMed  Google Scholar 

  • Righetti L, Rolli E, Galaverna G, Suman M, Bruni R, Dall’Asta C (2017) Plant organ cultures as masked mycotoxin biofactories: Deciphering the fate of zearalenone in micropropagated durum wheat roots and leaves. PLoS ONE 12:e0187247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rolli E, Righetti L, Galaverna G, Suman M, Dall’Asta C, Bruni R (2018) Zearalenone uptake and biotransformation in micropropagated Triticum durum Desf. Plants: a xenobolomic approach. J Agric Food Chem 66:1523–1532

    Article  CAS  PubMed  Google Scholar 

  • Song Y, Wu P, Li Y, Tong X, Zheng Y, Chen Z, Wang L, Xiang T (2017) Effect of endophytic fungi on the host plant growth, expression of expansin gene and flavonoid content in Tetrastigma hemsleyanum Diels & Gilg ex Diels. Plant Soil 417:393–402

    Article  CAS  Google Scholar 

  • Sun L, Lei P, Wang Q, Ma J, Zhan Y, Jiang K, Xu Z, Xu H (2020) The endophyte Pantoea alhagi NX-11 alleviates salt stress damage to rice seedlings by secreting exopolysaccharides. Front Microbiol 10:3112

    Article  PubMed  PubMed Central  Google Scholar 

  • Tiwari R, Kalra A, Darokar MP, Chandra M, Aggarwal N, Singh AK, Khanuja SPS (2010) Endophytic Bacteria from Ocimum sanctum and their yield enhancing capabilities. Curr Microbiol 60:167–171

    Article  CAS  PubMed  Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    Article  CAS  PubMed  Google Scholar 

  • Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Han L, Wu P, Feng C, Zhao J, Li Y (2013) Development of ELISA kit for rapid detection of zenralenone residues. Jiangsu J Agric Sci 29:659–663 (in Chinese)

    CAS  Google Scholar 

  • White JF, Kingsley KL, Zhang Q, Verma R, Obi N, Dvinskikh S, Elmore MT, Verma SK, Gond SK, Kowalski KP (2019) Review: endophytic microbes and their potential applications in crop management. Pest Manag Sci 75:2558–2565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woitek S, Unkles SE, Kinghorn JR, Tudzynski B (1997) 3-Hydroxy-3-methylglutaryl-CoA reductase gene of Gibberella fujikuroi: isolation and characterization. Curr Genet 31:38–47

    Article  CAS  PubMed  Google Scholar 

  • Wonglom P, Ito SI, Sunpapao A (2020) Volatile organic compounds emitted from endophytic fungus Trichoderma asperellum T1 mediate antifungal activity, defense response and promote plant growth in lettuce (Lactuca sativa). Fungal Ecol 43:20–26

    Article  Google Scholar 

  • Xiang T, Li J, Bao S, Xu Z, Wang L, Long F, He C (2021) Digital RNA-seq transcriptome plus tissue anatomy analyses reveal the developmental mechanism of the calabash-shaped root in Tetrastigma hemsleyanum. Tree Physiol 41:1729–1748

    Article  CAS  PubMed  Google Scholar 

  • Xiong Y, Wu X, Rao L (2015) Tetrastigma hemsleyanum (Sanyeqing) root tuber extracts induces apoptosis in human cervical carcinoma HeLa cells. J Ethnopharmacol 165:46–53

    Article  CAS  PubMed  Google Scholar 

  • Yan L, Zhu J, Zhao X, Shi J, Jiang C, Shao D (2019) Beneficial effects of endophytic fungi colonization on plants. Appl Microbiol Biotechnol 103:3327–3340

    CAS  PubMed  Google Scholar 

  • Yao K, Zhang F, Meng F (1991) Biological effects of zearalenone in tissue culture (Bulletin). Plant Physiol Commun 27:29–31 (in Chinese)

    Google Scholar 

  • Yuan LX, Wu H, Peng X, Qiu D, Tao ZF, Qiu WY (2020) Reference genes selection and system establishment for RT-qPCR of T. hemsleyanum in root development stages. Mol Plant Breed 18:6785–6792 (in Chinese)

    Google Scholar 

  • Zaher AM, Moharram AM, Davis R, Panizzi P, Makboul MA, Calderón AI (2015) Characterisation of the metabolites of an antibacterial endophyte Botryodiplodia theobromae Pat. of Dracaena draco L. by LC-MS/MS. Nat Prod Res 29:2275–2281

    Article  CAS  PubMed  Google Scholar 

  • Zhao DG, Meng FJ (1999) Involvement of zearalenone in short-day vernalization in winter wheat. Acta Phytophysiol Sin 25:66–72 (in Chinese)

    CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Shanghai Bioprofile Technology Company Ltd. for assistance in test of metabolomics.

Funding

This research was supported by grants from the National Natural Science Foundation of China (Grant No. 31872181).

Author information

Author notes

  1. Leizhen Wang, Xiaoping Huang and Jiangshan Li have contributed equally to this article.

Authors and Affiliations

  1. College of Life and Environmental Sciences, Hangzhou Normal University, Hangzhou, 311121, China

    Leizhen Wang, Xiaoping Huang, Jiangshan Li, Jinxin Huang, Shuying Bao, Chenjin He, Mengmeng Zhang & Taihe Xiang

  2. Zhejiang Provincial Key Laboratory for Genetic Improvement and Quality Control of Medicinal Plants, Hangzhou, 311121, China

    Xiaoping Huang & Taihe Xiang

Authors
  1. Leizhen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoping Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jiangshan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jinxin Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shuying Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chenjin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mengmeng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Taihe Xiang
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TX and XH conceived the study and designed the experiment; XH, LW, JL and TX performed the analysis of HPLC–MS; LW and SB carried out ELISA analysis; LW and JL performed the statistical analysis. JL, XH and JH carried out qRT-PCR. LW, SB, CH, MZ performed plant culture. TX, XH and LW wrote the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Taihe Xiang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Sergio J. Ochatt.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 618 kb)

Supplementary file2 (DOC 832 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Huang, X., Li, J. et al. Metabolites of zearalenone and phytohormones secreted by endophytic fungus strain TH15 regulating the root development in Tetrastigma hemsleyanum. Plant Cell Tiss Organ Cult 150, 683–694 (2022). https://doi.org/10.1007/s11240-022-02321-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-022-02321-5

Keywords

Search

Navigation