Skip to main content
SpringerLink
Log in

Xylaria feejeensis, SRNE2BP a Fungal Endophyte with Biocontrol Properties to Control Early Blight and Fusarium Wilt Disease in Tomato and Plant Growth Promotion Activity

  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Over the past decade endophytic fungi have been known as a source of secondary metabolites with the ability to act as a biocontrol agents. Xylaria feejeensis, SRNE2BP a fungal endophyte isolated from a mangrove tree exhibited antagonistic activity against two fungal pathogens of tomato. Crude extract of X. feejeensis SRNE2BP significantly inhibited Fusarium oxysporum MFLUCC 19–0157 growth as shown approximately 60–75% in in vitro and in situ assays. Both assays showed that the endophyte also inhibited mycelium formation of Alternaria solani MFLUCC 19–0093 by 56% and 87%, respectively. The half maximal inhibitory concentration of X. feejeensis SRNE2BP crude extract against A. solani and F. oxysporum was approximately 7 mg/l. Crude extract and mycelium of X. feejeensis SRNE2BP showed potential in controlling early blight and fusarium wilt disease in tomato, respectively. Seedlings from seeds coated with crude extract of X. feejeensis SRNE2BP had lower disease severity (31.71%) of early blight disease compared to un-treated seeds (57.13%). Soil treated with 10% endophytic mycelium not only reduced fusarium wilt in tomato plant (55.55% severity compared with 91.66% in un-treated soil) but also promoted seed emergence and growth of tomato. Structure analysis revealed that 12 secondary metabolites, especially mellein derivatives, are major components of the crude extract of X. feejeensis SRNE2BP. These compounds could be responsible for antifungal activities; however, further study is required. Our findings strongly suggest that colonization with this fungal endophyte can be beneficial to the host plant especially with regards to plant growth promotion and broad antagonistic activity.

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

References

  1. Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x

    Article  PubMed  PubMed Central  Google Scholar 

  2. Roy CK, Akter N, Sarkar MK, Pk MU, Begum N, Zenat EA, Jahan MA (2019) Control of early blight of tomato caused by and screening of tomato varieties against the pathogen. Open Microbiol J 13:41–50. https://doi.org/10.2174/1874285801913010041

    Article  CAS  Google Scholar 

  3. Srinivas C, Nirmala Devi D, Narasimha KM, Mohan CD, Lakshmeesha TR, Singh B, Kalagatur NK, Niranjana SR, Hashem A, Alqarawi AA, Tabassum B, Abd-Allah EF, Nayaka SC, Srivastava RK (2019) Fusarium oxysporum f. sp. lycopersici causal agent of vascular wilt disease of tomato: Biology to diversity—a review. Saudi Journal of Biological Sciences 26(7):1315–1324. https://doi.org/10.1016/j.sjbs.2019.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front Public Health 4:148–156. https://doi.org/10.3389/fpubh.2016.00148

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kim KH, Kabir E, Jahan SA (2017) Exposure to pesticides and the associated human health effects. Sci Total Environ 575:525–535. https://doi.org/10.1016/j.scitotenv.2016.09.009

    Article  CAS  PubMed  Google Scholar 

  6. Toghueo RMK (2018) Anti-leishmanial and anti-inflammatory agents from endophytes: a review. Nat Prod Bioprospect. https://doi.org/10.1007/s13659-019-00220-5

    Article  Google Scholar 

  7. Larren S, Simon MR, Moreno MV, Siurana MS, Perelló A (2016) Endophytes from wheat as biocontrol agents against tan spot disease. Biol Control 92:17–23. https://doi.org/10.1016/j.biocontrol.2015.09.002

    Article  Google Scholar 

  8. Fadiji AE, Babalola OO (2020) Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front Bioeng Biotechnol 8:467. https://doi.org/10.3389/fbioe.2020.00467

    Article  PubMed  PubMed Central  Google Scholar 

  9. Hend AA, Perveen K, Tahmaz R, Alhaqbani S (2012) Evaluation of biological control potential of locally isolated antagonist fungi against Fusarium oxysporum under in vitro and pot conditions. Am J Microbiol Res 6(2):312–319. https://doi.org/10.5897/AJMR11.1367

    Article  Google Scholar 

  10. Adnan M, Alshammari E, Ashraf SA, Patel K, Lad K, Patel M (2018) Physiological and molecular characterization of biosurfactant producing endophytic fungi Xylaria regalis from the cones of Thuja plicata as a potent plant growth promoter with its potential application. Biomed Res Int. https://doi.org/10.1155/2018/7362148

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ortega HE, Torres-Mendoza D, Cubilla-Rios L (2020) Patents on endophytic fungi for agriculture and bio-and phytoremediation applications. Microorganisms 8:1237. https://doi.org/10.3390/microorganisms8081237

    Article  CAS  PubMed Central  Google Scholar 

  12. Aamir MR, Zehra K, Dubey A, Kumar M, Shukla S, Ram VU (2020). Microbial Endophytes: Microbial bioformulation-based plant biostimulants: a plausible approach toward next generation of sustainable agriculture. Woodhead publishing, Cambridge. https://doi.org/10.1016/B978-0-12-819654-0.00008-9

  13. Simberloff D (2012) Risks of biological control for conservation purposes. Biocontrol 57:263–276. https://doi.org/10.1007/s10526-011-9392-4

    Article  Google Scholar 

  14. Carbone I, Kohn LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553–556. https://doi.org/10.1080/00275514.1999.12061051

    Article  CAS  Google Scholar 

  15. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246. https://doi.org/10.1128/jb.172.8.4238-4246.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Glass NL, Donaldson GC (1995) Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl Environ Microbiol 61:1323–1330. https://doi.org/10.1128/aem.61.4.1323-1330.1995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. National Center for Biotechnology Information. Available from http://www.ncbi.nlm.nih.gove. Accessed April 11, 2021.

  18. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usa-bility. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics (Oxford, England) 14:817–818. https://doi.org/10.1093/bioinformatics/14.9.817

    Article  CAS  Google Scholar 

  21. Silvestro D, Michalak I (2012) raxmlGUI: a graphical front-end for RAxML. Org Divers Evol 12:335–337. https://doi.org/10.1007/s13127-011-0056-0

    Article  Google Scholar 

  22. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180

    Article  CAS  PubMed  Google Scholar 

  23. Adobe Illustrator | Graphic Design Software. Available from https://www.adobe.com/cn/products/illustrator.html. Accessed March 1, 2021.

  24. Akhtar KU, Najeeb S, Muhammad I, Qumer AM, Khan A (2019) Evaluation of tomato genotypes for early blight disease resistance caused by Alternaria solani in Pakistan. J of Plant Pathol. https://doi.org/10.1007/s42161-019-00304-8

    Article  Google Scholar 

  25. Arici E, Çaltili O, Soy Ö (2018) Determination of sensitivities of some tomato varieties to Fusarium oxysporum f.sp. lycopersici (FOL). Int J Envron Trends 1:44–52

    Google Scholar 

  26. Sichaem J, Ruksip T, Sawasdee P, Khumkratok S, Tip-pyang S (2018) Chemical constituents of the stems of Spatholobus parviflorus and their cholinesterase inhibitory activity. Chem Nat Compd 54:356–357. https://doi.org/10.1007/s10600-018-2344-9

    Article  CAS  Google Scholar 

  27. Fujimoto Y, Yokoyama E, Takahashi T, Uzawa J, Morooka N, Tsunoda H, Tsunoda T (1986) Studies on the metabolics of Penicillium diversum var. aureum. Chem Pharm Bull 34:1497–1500. https://doi.org/10.1021/jf202089y

    Article  CAS  Google Scholar 

  28. Talapatra SK, Karmacharya B, De SC, Talapatra B (1988) Regiolone, and α-tetralone from Juglans regia: structure, stereochem-istry and configuration. Phytochemistry 27:3929–3932. https://doi.org/10.1016/0031-9422(88)83047-4

    Article  CAS  Google Scholar 

  29. Li W, Wiesenfeldt MP, Glorius F (2017) Ruthenium-NHC-diamine catalyzed enantioselective hydrogenation of isocoumarins. Am Chem Soc 139:2585–2588. https://doi.org/10.1021/jacs.6b13124

    Article  CAS  Google Scholar 

  30. Okuno T, Oikawa S, Goto T, Sawai K, Shirahama H, Matsumoto T (1986) Structures and phytotoxicity of metabolites from Valsa ceratosperma. Agric Biol Chem 50:997–1001. https://doi.org/10.1080/00021369.1986.10867484

    Article  CAS  Google Scholar 

  31. Borgschulte K, Rebuffat S, Kienast WT, Schomburg D, Pinon J, Bodo B (1991) Isolation and structure elucidation of hymatoxins B-E and other phytotoxins from Hypoxylon mammatum fungal pathogen of leuce poplars. Tetrahedron 39:8351–8360. https://doi.org/10.1016/S0040-4020(01)96176-9

    Article  Google Scholar 

  32. Ayer WA, Trifonov LS, Hutchison LJ, Chakravarty P (2000) Metabolites from a wood inhabiting cup fungus, Urnula craterium. Nat Prod Res 16:405–410. https://doi.org/10.1080/10575630008043776

    Article  Google Scholar 

  33. Krohn K, Kock I, Elsasser B, Florke U, Schulz B, Draeger S, Pescitelli G, Antus S, Kurtán T (2007) Bioactive natural products from the endophytic fungus Ascochyta sp. from Meliotus dentatus configurational assignment by solid-state CD and TDDFT calculations. Eur J Org Chem 7:1123–1129. https://doi.org/10.1002/ejoc.200600907

    Article  CAS  Google Scholar 

  34. Kumura Y, Tamura S (1972) Isolation and structure of pestalotin, a gibberellin synergist from Pestalotia cryptomeriaecola. Agric Biol Chem 36:19251930. https://doi.org/10.1080/00021369.1972.10860489

    Article  Google Scholar 

  35. Gehrt A, Erkel G, Anke H, Anke T, Sterner O (1997) New hexaketide inhibitors of eukaryotic signal transduction. Nat Prod Lett 9:259–264. https://doi.org/10.1080/10575639708043637

    Article  CAS  Google Scholar 

  36. Tang WT, Wang WG, Li A, Yan BC, Chen R, Li XN, Du X, Sun HD, Pu JX (2017) Polyketides from the endophytic fungus Phomopsis sp. sh917 by using the one strain/many compounds strategy. Tetrahedron 73:3577–3584. https://doi.org/10.1016/j.tet.2017.02.019

    Article  CAS  Google Scholar 

  37. Jones EG, Stanley SJ, Pinruan U (2008) Marine endophyte sources of new chemical natural products: a review. Bot Mar 51:163–170. https://doi.org/10.1515/BOT.2008.028

    Article  Google Scholar 

  38. Jones EG, Pang KL, Abdel-Wahab MA, Scholz B, Hyde KD, Boekhout T, Suetrong S (2019) An online resource for marine fungi. Fungal Divers 96:347–433. https://doi.org/10.1007/s13225-019-00426-5

    Article  Google Scholar 

  39. Wang Y, Zhu H, Nora NFY (2014) Polyphenols, tannins and antioxidant activities of eight true mangrove plant species in South China. Plant Soil 374:549–563. https://doi.org/10.1007/s11104-013-1912-9

    Article  CAS  Google Scholar 

  40. Xu J, Kjer J, Sendker J (2009) Cytosporones, coumarins, and an alkaloid from the endophytic fungus Pestalotiopsis sp. isolated from the Chinese mangrove plant Rhizophora mucronata. Bioorgan Med Chem 17:7362–7367. https://doi.org/10.1016/j.bmc.2009.08.031

    Article  CAS  Google Scholar 

  41. Suwannasai P, Mongkolthanaruk N, Senawong W, Prawat T, Moontragoon P, Jaursup B, Youmgme S, McCloskey S (2019) Chemical constituents and cytotoxic activity from Xylaria spp. fungi. Planta Med 85(18):1387. https://doi.org/10.1055/s-0039-3399866

    Article  Google Scholar 

  42. Zhang Q, Xiao J, Sun QQ, Qin JC, Pescitelli G, Gao JM (2014) Characterization of cytochalasins from the endophytic Xylaria sp. and their biological functions. J Agr food Chem 62:10962–10969. https://doi.org/10.1021/jf503846z

    Article  CAS  Google Scholar 

  43. Sopalun K, Laosripaiboon W, Wachirachaikarn A, Iamtham S (2021) Biological potential and chemical composition of bioactive compounds from endophytic fungi associated with thai mangrove plants. South African J of Bot 141:66–76. https://doi.org/10.1016/j.sajb.2021.04.031

    Article  CAS  Google Scholar 

  44. Wang J, Xu CC, Tang H, Su L, Chou Y, Soong K, Li J, Zhuang CL, Luo YP, Zhang W (2018) Osteoclastogenesis inhibitory polyketides from the sponge-associated fungus Xylaria feejeensis. Chem. Biodiver. 15(12):e1800358. https://doi.org/10.1002/cbdv.201800358

    Article  CAS  Google Scholar 

  45. Pourmoghaddam MJ, Lambert C, Surup F, Khodaparast SA, Krisai-Greilhuber I, Voglmayr H, Stadler M (2020) Discovery of a new species of the Hypoxylon rubiginosum complex from Iran and antagonistic activities of Hypoxylon spp. against the Ash Dieback pathogen, Hymenoscyphus fraxineus, in dual culture. MycoKeys 66:105–133. https://doi.org/10.3897/mycokeys.66.50946

    Article  PubMed  PubMed Central  Google Scholar 

  46. Reveglia P, Masi M, Evidente A (2020) Mellins-intriguing natural compounds. Biomolecules 10:772. https://doi.org/10.3390/biom10050772

    Article  CAS  PubMed Central  Google Scholar 

  47. Evidente A, Masi M, Linaldeddu BT, Franceschini A, Scanu B, Cimmino A, Andolfi A, Motta A, Maddau L (2012) Afritoxinones A and B, dihydrofuropyran-2-ones produced by Diplodia africana the causal agent of branch dieback on Juniperus phoenicea. Phytochemistry 77:245–250. https://doi.org/10.1016/j.phytochem.2012.01.011

    Article  CAS  PubMed  Google Scholar 

  48. Patjana T, Jantaharn P, Katrun P, Mongkolthanaru W, Suwannasai N, Senawong T, Tontapha S, Amornkitbumrung V, McCloskey S (2019) Anti-inflammatory and cytotoxic agents from Xylaria sp. SWUF09-62 fungus. Nat Prod Res 24:1–10. https://doi.org/10.1080/14786419.2019.1652292

    Article  CAS  Google Scholar 

  49. Singh VK, Singh HB, Upadhyay RS (2017) Role of fusaric acid in the development of ‘Fusarium wilt’ symptoms in tomato: physiological, biochemical and proteomic perspectives. Plant Physiol Biochem 118:320–332. https://doi.org/10.1016/j.plaphy.2017.06.028

    Article  CAS  PubMed  Google Scholar 

  50. Niño-Sánchez J, Tello V, Casado-del Castillo V, Thon MR, Benito EP, Díaz-Mínguez JM (2015) Gene expression patterns and dynamics of the colonization of common bean (Phaseolus vulgaris L.) by highly virulent and weakly virulent strains of Fusarium oxysporum. Front Microbiol 6:234. https://doi.org/10.3389/fmicb.2015.00234

    Article  PubMed  PubMed Central  Google Scholar 

  51. Li X, Guo Z, Deng Z, Yang J, Zou K (2015) A new [alpha]-pyrone derivative from endophytic fungus Pestalotiopsis microspora. Records of Natural Products 9:503

    CAS  Google Scholar 

  52. Moriyama M, Nakata K, Fujiwara T, Tanabe Y (2020) Divergent asymmetric total synthesis of all four Pestalotin diastereomers from (R)-Glycidol. Molecules 25:394. https://doi.org/10.3390/molecules25020394

    Article  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by a grant from Mae Fah Luang University with grant number 611B01002 and Agricultural Research Development Agency (Public Organization) with grant number CRP6105020320. We also would like to thank Associate Professor Surat Laphookhieo for his support on the chemical analysis in this study.

Author information

Authors and Affiliations

  1. School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Siraprapa Brooks, Anthikan Klomchit & Surangkana Chimthai

  2. Medicinal Plant Innovation Center of Mae Fah, Luang University, Mae Fah Luang University, Chiang Rai, 57100, Thailand

    Wuttichai Jaidee

  3. College of Agriculture and Life Science, University of Wisconsin-Madison, Madison, WI, USA

    Aaron Christopher Bastian

Authors
  1. Siraprapa Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthikan Klomchit
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Surangkana Chimthai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wuttichai Jaidee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Aaron Christopher Bastian
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by SB, AK, SC, WJ, and ACB. The first draft of the manuscript was written by SB and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. All authors agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Siraprapa Brooks.

Ethics declarations

Conflict of interest

The authors declare that they have no issue of competing interest.

Additional information

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brooks, S., Klomchit, A., Chimthai, S. et al. Xylaria feejeensis, SRNE2BP a Fungal Endophyte with Biocontrol Properties to Control Early Blight and Fusarium Wilt Disease in Tomato and Plant Growth Promotion Activity. Curr Microbiol 79, 108 (2022). https://doi.org/10.1007/s00284-022-02803-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-022-02803-x

Search

Navigation