Investigating the Role of Endophytic Fungi in Gentiana scabra bge. by Cross-Growth Period Inoculation

Original Research Article
  • 17 Downloads

Abstract

Gentiana scabra Bge. (gentian) is a Chinese medicinal plant. Endophytic fungi from the roots of gentian were isolated and cross-growth period inoculation was performed to study the roles of three Trichoderma spp. strains (F1, F2, and F9) in their original host plant. In treatments inoculated with F1, F2, and F9, gentiopicroside content increased 33.6, 23.7 and 13% than that in the control. Strains F1, F2, and F9 could also improve polysaccharide content by more than 6.6, 18.7 and 30% compared to the control. The incidence of spot blight in gentian inoculated with F1, F2, and F9 decreased by 31.2, 26.7 and 8.5%. Inconsistent changes in the activity of the three enzymes (superoxide dismutase, catalase and peroxidase) were observed when the plants were attacked by pathogens or inoculated with fungi. High enzymatic activity did not reflect mild disease. Cross-growth period inoculation, which takes into account the original living environment (gentian plant as “substrate” and different microorganisms as symbionts) of endophytic fungi, provides a new idea for studying effects of endophytes on their original hosts. This is the first research about the role of endophytic fungi in Gentiana scabra bge. in vivo.

Keywords

Endophytic fungi Gentiana scabra Bge. Growth-promoting Disease-resistant Defense enzyme 

Notes

Acknowledgements

We are grateful to the National Natural Science Foundation of China (NSFC No. 31400441).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Dolatabad HK, Javan-Nikkhah M, Shier WT (2017) Evaluation of antifungal, phosphate solubilisation, and siderophore and chitinase release activities of endophytic fungi from Pistacia vera. Mycol Progress 16:777–790CrossRefGoogle Scholar
  2. 2.
    Surono KN (2017) The dark septate endophytic fungus Phialocephala fortinii is a potential decomposer of soil organic compounds and a promoter of Asparagus officinalis growth. Fungal Ecol 28:1–10CrossRefGoogle Scholar
  3. 3.
    Waqas M, Khan AL, Hamayun M, Shahzad R, Kim YH, Choi KS, Lee IJ (2015) Endophytic infection alleviates biotic stress in sunflower through regulation of defence hormones, antioxidants and functional amino acids. Eur J Plant Pathol 141:803–824CrossRefGoogle Scholar
  4. 4.
    Clay K, Schardl C (2002) Evolutionary origins and ecological consequences of endophyte symbiosis with grasses. Am Nat 160:S99–S127CrossRefPubMedGoogle Scholar
  5. 5.
    Kleczewski NM, Bauer JT, Bever JD, Clay K, Reynolds HL (2012) A survey of endophytic fungi of switchgrass (Panicum virgatum) in the Midwest, and their putative roles in plant growth. Fungal Ecol 5:521–529CrossRefGoogle Scholar
  6. 6.
    Yuan Z, Zhang C, Lin F (2010) Role of diverse non-systemic fungal endophytes in plant performance and response to stress: progress and approaches. J Plant Growth Regul 29:116–126CrossRefGoogle Scholar
  7. 7.
    Jasim B, Anisha C, Rohini S, Kurian JM, Jyothis M, Radhakrishnan EK (2014) Phenazine carboxylic acid production and rhizome protective effect of endophytic Pseudomonas aeruginosa isolated from Zingiber officinale. World J Microb Biot 30:1649–1654CrossRefGoogle Scholar
  8. 8.
    Pérez LI, Gundel PE, Ghersa CM, Omacini M (2013) Family issues: fungal endophyte protects host grass from the closely related pathogen Claviceps purpurea. Fungal Ecol 6:379–386CrossRefGoogle Scholar
  9. 9.
    Yang XQ, Peng TF, Yang YB, Li W, Xiong J, Zhao LX, Ding ZT (2015) Antimicrobial and antioxidant activities of a new benzamide from endophytic Streptomyces sp. YIM 67086. Nat Prod Res 29:331–335CrossRefPubMedGoogle Scholar
  10. 10.
    Qian YX, Kang JC, Luo YK, Zhao JJ, He J, Geng K (2016) A bilobalide-producing endophytic fungus, Pestalotiopsis uvicola from medicinal plant Ginkgo biloba. Curr Microbiol 73:280–286CrossRefPubMedGoogle Scholar
  11. 11.
    Ding CH, Wang QB, Guo S, Wang ZY (2018) The improvement of bioactive secondary metabolites accumulation in Rumex gmelini Turcz through co-culture with endophytic fungi. Braz J Microbiol 49:362–369CrossRefPubMedGoogle Scholar
  12. 12.
    Bhagat J, Kaur A, Sharma M, Saxena AK, Chadha BS (2012) Molecular and functional characterization of endophytic fungi from traditional medicinal plants. World J Microbiol Biotechnol 28:963–971CrossRefPubMedGoogle Scholar
  13. 13.
    Song YL, Wu P, Li YF, Tong XX, Zheng YF, Chen ZH, Wang LL, Xiang TH (2017) Effect of endophytic fungi on the host plant growth, expression of expansin gene and flavonoid content in Tetrastigma hemsleyanum Diels and Gilg ex Diels. Plant Soil 417:393–402CrossRefGoogle Scholar
  14. 14.
    Cao FH, Li C (2008) New advantages in research of chemical constituents and pharmacological activities of genus Gentiana. Chin J New Drugs 17:27–29, 32Google Scholar
  15. 15.
    Yang SB, Wang C (2005) Research progress in chemical constituents and pharmacological activities of Radix gentianae. Acta Chin Med Pharm 33:54–56Google Scholar
  16. 16.
    Jiang WX, Zhao X (2008) Study on anticoagulant function of gentian polysaccharides. J Heilongjiang Med 5:31–32Google Scholar
  17. 17.
    Wang JH (2012) Research about the effects of gentian polysaccharides on liver protection, lipid decrease and immune regulation. M.S. thesis. College of Harbin Commerce University, HarbinGoogle Scholar
  18. 18.
    Du XW, Zhou YT (2010) Experimental research about antagonistic action of endophytic fungi in Gentiana manshurica on Gentian leaf blight. In: Abstract: 2nd national traditional Chinese medicine commodity conference. China Society of Commodity Science, pp 104–105Google Scholar
  19. 19.
    Song YQ, Liu WH (2017) Isolation and antimicrobial activity of endophytic fungi from Yunnan Gentiana. J Qujing Normal Univ 36:33–36Google Scholar
  20. 20.
    Rybakova D, Schmuck M, Wetzlinger U, Varo-Suarez A, Murgu O, Müller H, Berg G (2016) Kill or cure? The interaction between endophytic Paenibacillus and Serratia strains and the host plant is shaped by plant growth conditions. Plant Soil 405:65–79CrossRefGoogle Scholar
  21. 21.
    Wali P, Helander M, Saloniemi I, Ahlholm J, Saikkonen K (2009) Variable effects of endophytic fungus on seedling establishment of fine fescues. Oecologia 159:49–57CrossRefPubMedGoogle Scholar
  22. 22.
    Rodriguez RJ, JrJF W, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles: Tansley review. New Phytol 182:314–330CrossRefPubMedGoogle Scholar
  23. 23.
    Molinamontenegro MA, Oses R, Torresdíaz C, Atala C, Núnez MA, Armas C (2015) Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem. Perspect Plant Ecol Evol Syst 17:218–226CrossRefGoogle Scholar
  24. 24.
    Wang XM, Yam TW, Meng QW, Zhu J, Zhang P, Wu HF, Wang J, Zhao Y, Song XQ (2016) The dual inoculation of endophytic fungi and bacteria promotes seedlings growth in Dendrobium catenatum (Orchidaceae) under in vitro culture conditions. Plant Cell Tissue Organ Cult 126:523–531CrossRefGoogle Scholar
  25. 25.
    Gundel P, Helander M, Casas C, Hamilton C, Faeth S, Saikkonen K (2013) Neotyphodium fungal endophyte in tall fescue (Schedonorus phoenix): a comparison of three Northern European wild populations and the cultivar Kentuky-31. Fungal Divers 1:15–24CrossRefGoogle Scholar
  26. 26.
    Krauss J, Harri DA, Bush L, Power SA, Muller CB (2007) Fungal grass endophytes, grass cultivars, nitrogen deposition and the associations with colonizing insects. In: 6th international symposium on fungal endophytes of grasses, “From Lab To Farm”, Christchurch, pp 53–57Google Scholar
  27. 27.
    White TJ, Bruns T, Lee S, Taylor J (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gefland DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  28. 28.
    Chinese Pharmacopoeia Commission (2015) Pharmacopoeia of the People’s Republic of China part 1. Medical Science and Technology Press, Beijing, p 96Google Scholar
  29. 29.
    Duan Y, Wang DM, Pan YN, Lu Y, Wu XL, Liu XQ (2014) Correlation between the accumulation of polysaccharide and gentiopicroside in Gentianae Radix et Rhizoma and soil factors from Liaoning GAP base. J Shenyang Pharm Univ 31:998–1002Google Scholar
  30. 30.
    Liu JH, Li J, Zhang YQ (2010) Germination characteristics and secondary metabolism regulation of Scutellaria baicalensis Georgi seeds under different temperatures. Agric Sci Technol 11:213–216Google Scholar
  31. 31.
    Bai R, Ma FW, Liang D, Zhao X (2009) Phthalic acid induces oxidative stress and alters the activity of some antioxidant enzymes in roots of Malus prunifolia. J Chem Ecol 35:488–497CrossRefPubMedGoogle Scholar
  32. 32.
    Sofo A, Dichio B, Xiloynnis C, Masia A (2004) Effects of different irradiance levels on some antioxidant enzymes and on malondialdehyde content during rewatering in olive tree. Plant Sci 166:293–302CrossRefGoogle Scholar
  33. 33.
    Hosseyni-Moghaddam MS, Soltani J (2014) Bioactivity of endophytic Trichoderma fungal species from the plant family Cupressaceae. Ann Microbiol 64:753–761CrossRefGoogle Scholar
  34. 34.
    Samuels GJ (1996) Trichoderma: a review of biology and systematics of the genus. Mycol Res 100:923–935CrossRefGoogle Scholar
  35. 35.
    Hahm MS, Sumayo M, Hwang YJ, Jeon SA, Park SJ, Lee JY, Ahn JH, Kim BS, Ryu CM, Ghim SY (2012) Biological control and plant growth promoting capacity of rhizobacteria on pepper under greenhouse and field conditions. J Microbiol 50:380–385CrossRefPubMedGoogle Scholar
  36. 36.
    Martins SJ, Medeiros FHV, Souza RM, Resende MLV, Ribeiro JPM (2013) Biological control of bacterial wilt of common bean by plant growth-promoting rhizobacteria. Biol Control 66:65–71CrossRefGoogle Scholar
  37. 37.
    Cho UH, Seo NH (2005) Oxidative stress in Arabidopsis thaliana exposed to cadmium is due to hydrogen peroxide accumulation. Plant Sci 168:113–120CrossRefGoogle Scholar
  38. 38.
    Asada K (1992) Ascorbate peroxidase—a hydrogen peroxide scavenging enzyme in plants. Physiol Plant 85:235–241CrossRefGoogle Scholar
  39. 39.
    Liu T, Greenslade A, Yang SC (2017) Levels of rhizome endophytic fungi fluctuate in Paris polyphylla var. yunnanensis as plants age. Plant Divers 39:60–64CrossRefGoogle Scholar

Copyright information

© Association of Microbiologists of India 2018

Authors and Affiliations

  1. 1.School of PharmacyShenyang Pharmaceutical UniversityShenyangPeople’s Republic of China
  2. 2.School of Traditional Chinese MedicineShenyang Pharmaceutical UniversityShenyangPeople’s Republic of China

Personalised recommendations