Abstract
There are many available reports of secondary metabolites as bioactive molecules from culturable endophytes, nevertheless, there are scarce research pertaining to the levels of metabolites in plants with respect to the incidence and colonisation of fungal endophytes in the same foliar tissues. Therefore, the study was focussed to examine whether fungal endophyte colonisation and the accumulation of secondary metabolites, such as flavonoids and phenols, in the plants are related in any way. For this reason, the study aims to analyse phenols and flavonoids from the fronds of eleven pteridophytes along with the culture-dependent isolation of fungal endophytes from the host plants subsequently assigning them to morphological category and their quantitative analysis and further resolving its identities through molecular affiliation. The results revealed that nine morpho-categories of fungal endophytes were allotted based on culture attributes, hyphal patterns and reproductive structural characters. Highest numbers of species were isolated from Adiantum capillus-veneris and least was recorded from Pteris vittata and Dicranopteris linearis. Maximum phenol content was analysed from the fronds of P. vittata and lowest was recorded in A. capillus-veneris. Highest flavonoid content was measured in D. linearis and lowest was detected in Christella dentata. Significant negative correlation was observed between phenol content of ferns and species richness of fungi. Moreover, significant positive correlation was observed with the relative abundance of Chaetomium globosum and flavonoid content of ferns and negative significant relation was found between relative abundance of Pseudopestalotiopsis chinensis and phenol content of pteridophytes. The occurrence and the quantitative aspects of endophytes in ferns and their secondary metabolites are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data available on request from the authors.
References
Alam B, Lǐ J, Ge Q, Khan MA, Gōng J et al (2021) Endophytic fungi: from symbiosis to secondary metabolite communications or vice versa? Front Plant Sci 129:1033. https://doi.org/10.3389/fpls.2021.791033
Antonovics J (2020) Pathogenic fungi in ferns and angiosperms: a comparative study. Am Fern J 110(3):79–94. https://doi.org/10.1640/0002-8444-110.3.79
Arnold AE (2008) Endophytic fungi: hidden components of tropical community ecology. In: Schnitzer S, Carson W (eds) Tropical forest community ecology. Wiley-Blackwell, Oxford, pp 254–271
Arnold AE, Lutzoni F (2007) Diversity and host range of foliar fungal endophytes: are tropical leaves biodiversity hotspots? Ecol 88(3):541–549. https://doi.org/10.1890/05-1459
Arnold AE, Maynard Z, Gilbert GS, Coley PD, Kursar TA (2000) Are tropical fungal endophytes hyperdiverse? Ecol Lett 3:267–274. https://doi.org/10.1046/j.1461-0248.2000.00159.x
Arnold AE, Maynard Z, Gilbert GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105:1502–1507. https://doi.org/10.1017/S0953756201004956
Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z et al (2003) Fungal endophytes limit pathogen damage in a tropical tree. PNAS 100:15649–15654. https://doi.org/10.1073/pnas.2533483100
Benucci GMN, Delaney B, Shepherd LD, Gregory B, Andrew MB (2020) Evidence for co-evolutionary history of early diverging Lycopodiaceae plants with fungi. Front Microbiol. https://doi.org/10.3389/fmicb.2019.02944
Bhattacharya A, Sood P, Citovsky V (2010) The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol Plant Pathol 11(5):705–719. https://doi.org/10.1111/j.1364-3703.2010.00625.x
Boratyn GM, Camacho C, Cooper PS, Coulouris G, Fong A et al (2013) BLAST: a more efficient report with usability improvements. Nucleic Acids Res 41:W29–W33. https://doi.org/10.1093/nar/gkt282
Campbell H (1908) The therapeutics of die. J R Soc Med. https://doi.org/10.1177/003591570800101314
Carvalho PLN, Oliveira Silva E, Chagas-Paula DA, Luiz JHH, Ikegaki M (2016) Importance and implications of the production of phenolic secondary metabolites by endophytic fungi: a mini-review. Mini Rev Med Chem 16:259–271. https://doi.org/10.2174/1389557515666151016123923
Chandra S, Fraser-Jenkins CR, Kumari A, Srivastava A (2008) A summary of the status of threatened pteridophytes of India. Taiwania 53(2):170–209. https://doi.org/10.6165/tai.2008.53(2).170
Chen KH, Xie QY, Chang CC, Kuo LY (2021) The mycobiome of the achlorophyllous gametophytes of Ophioderma pendulum using a high throughput metabarcoding approach. Appl Plant Sci. https://doi.org/10.1002/aps3.11461
Chen KH, Xie QY, Chang CC, Kuo LY (2022) Mycobiome detection from a single subterranean gametophyte using metabarcoding techniques. Appl Plant Sci 10(2):e11461
Ching R-C (1988) The Chinese fern families and genera: systematic arrangement and historical origin. J Syst Evol 16:1–19
Coomes DA, Allen RB, Bentley WA, Burrows LE, Canham CD et al (2005) The hare, the tortoise, and the crocodile: the ecology of angiosperm dominance, conifer persistence and fern filtering. Ecology 93:918–935. https://doi.org/10.1111/j.1365-2745.2005.01012.x
Cui XX, WangL FHY, Zheng YG, Su CY (2022) The cultivable endophytic fungal community of Scutellaria baicalensis: diversity and relevance to flavonoid production by the host. Plant Signal Behav 17(1):2068834. https://doi.org/10.1080/15592324.2022.2068834
Das NC (2007) Ferns and fern allies of Tripura North East India. International Book Distributors, Dehradun India
Du F, Zhang F, Chen F (2011) Advances in microbial heterologous production of flavonoids. Afr J Microbiol Res 5:2566–2574
Fisher PJ, Punithalingam E (1993) Stagonospora pteridifolia sp. nov., a new endophytic coelomycete in Pteridiumaquilinum. Mycol Res 97:661–664
Fisher PJ (1996) Survival and spread of the endophyte Stagonospora pteridifolia in Pteridiumaquilinum, other ferns and some flowering plants. New Phytol 132:119–122
George LO, Bazzaz FA (1999) The fern understory as an ecological filter: emergence and establishment of canopy tree seedlings. Ecol 80:833–845. https://doi.org/10.1890/0012-9658(1999)080[0833:TFUAAE]2.0.CO;2
Higgins KL, Coley PD, Kursar TA, Arnold AE (2011) Culturing and direct PCR suggest prevalent host generalism among diverse fungal endophytes of tropical forest grasses. Mycologia 103(2):247–260. https://doi.org/10.3852/09-158
Hyde KD, Soytong K (2008) The Fungal endophyte dilemma. Fungal Divers 33:163–173
Kumar S, Pandey AK (2013) Chemistry and biological activities of flavonoids: an overview. Sci World J. https://doi.org/10.1155/2013/162750
Kumar S, Abedin MM, Singh AK, Das S (2020) Role of phenolic compounds in plant-defensive mechanisms. In: Lone R, Shuab R, Kamili A (eds) Plant phenolics in sustainable agriculture. Springer, Singapore, pp 571–532
Li Z, Wen MW, Qin YM, He D, Xu Y et al (2022) Biosynthetic mechanisms of secondary metabolites promoted by the interaction between endophytes and plant hosts. Front Microbiol 13:928967. https://doi.org/10.3389/fmicb.2022.928967
Lodge DJ, Fisher PJ, Sutton BC (1996) Endophytic fungi of Manilkara bidentata leaves in Puerto Rico. Mycology 88(5):733–738. https://doi.org/10.1080/00275514.1996.12026710
Mikulic-Petkovseka M, Schmitzera V, Schmitze FV, Stampara RF, Veberica R et al (2014) Changes in phenolic content induced by infection with Didymella applanata and Leptosphaeria coniothyrium, the causal agents of raspberry spur and cane blight. J Plant Pathol 63:185–192. https://doi.org/10.1111/ppa.12081
Oh SY, Park KH, Baldrian P, Fong J, Kwon H et al (2021) Fungal diversity living in the root and sporophore of the endemic Korean fern Mankyua chejuense. Fungal Ecol 50:101038
Olmo-Ruiz M, Arnold AE (2014) Interannual variation and host affiliations of endophytic fungi associated with ferns at La Selva. Costa Rica Mycologia 106(1):8–21. https://doi.org/10.3852/13-098
Olmo-Ruiz M, Arnold AE (2017) Community structure of fern-affiliated endophytes in three neotropical forests. J Trop Ecol 33(1):60–73. https://doi.org/10.1017/S0266467416000535
Palanichamy P, Krishnamoorthy G, Kannan S, Murugan M (2018) Bioactive potential of secondary metabolites derived from medicinal plant endophytes. Egypt J Basic Appl Sci. https://doi.org/10.1016/j.ejbas.2018.07.002
Pan F, Su TJ, Mei Cai S, Wu W (2017) Fungal endophyte-derived Fritillaria unibracteata var. wabuensis: diversity, antioxidant capacities in vitro and relations to phenolic, flavonoid or saponin compounds. Sci Rep. https://doi.org/10.1038/srep42008
Petrini O, Fisher PJ, Petrini LE (1992) Fungal endophytes of bracken (Pteridium aquilinum), with some reflections on their use in biological control. Sydowia 44:282–293
Plaszko T, Szucs Z, Cziaky Z, Acs- Szabo L, Csoma H (2022) Endophytic fungal metagenome suggests importance of various metabolite classes in community assembly in horseradish (Armoracia rusticana, Brassicaceae) roots. Front Plant Sci. https://doi.org/10.3389/fpls.2022.921008
Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Ann Rev Phytopathol 149:291–315
Prakash NK, Karthick A, Poomagal D, Susithra M, Bhuvaneswari CM (2018) Fungal endophytes of an aquatic weed Marsilea minuta Linn. Curr Res Environ 8(1):86–95. https://doi.org/10.5943/cream/8/1/7
Pratyusha S (2022) Phenolic compounds in the plant development and defense: an overview. J Plant Stress Physiol. https://doi.org/10.5772/intechopen.102873
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning a laboratory manual. Cold Spring Harbor Laboratory Press, New York
Sathishkumar T, Baskar R, Shanmugam S, Rajasekaran P, Sadasivam S et al (2008) Optimization of flavonoids extraction from the leaves of Tabernaemontana heyneana wall using L16 orthogonal design. Nat Sci 6(3):10–21
Schuettpelz E, Pryer KM (2009) Evidence for a Cenozoic radiation of ferns in an angiosperm-dominated canopy. PNAS 106:11200–11205. https://doi.org/10.1073/pnas.0811136106
Singh D, Thapa S, Mahawar H, Kumar D, Geat N et al (2022) Prospecting potential of endophytes for modulations of biosynthesis of therapeutic bioactive secondary metabolites and plant growth promotion of medicinal and aromatic plants. Anton Leeuw Int J. https://doi.org/10.1007/s10482-022-01736-6
Singleton VL, Rossi JA (1965) Colorimetric of total phenolics and with phosphomolybdic-phosphotungstic acid reagents. Am J Enol 16:144–158
Socolsky C, Domínguez L, Asakawa Y, Bardon A (2012) Unusual terpenylated acylphloroglucinols from Dryopteris wallichiana. Phytochemistry 80:115–122
Suetsugu K, Nishioka T, Hogaki Y (2020) Rediscovery of Oxygenos hyodoi (Thismiaceae)in its type locality after 30 years. J Plant Taxon Plant Geogr 68:89–91
U’Ren JM, Lutzoni F, Miadlikowska J, Arnold AE (2010) Community analysis reveals close affinities between endophytic and endolichenic fungi in mosses and lichens. Microb Ecol 60(2):340–353. https://doi.org/10.1007/s00248-010-9698-2
Vasco A, Moran RC, Ambrose BA (2013) The evolution, morphology, and development of fern leaves. Front Plant Sci 4:345
Wallis C, Galarneau E (2020) Phenolic compound induction in plant-microbe and plant-insect interactions: a meta-analysis. Front Plant Sci 11:580753
Wang Y, Dai CC (2011) Endophytes: a potential resource for biosynthesis, biotransformation, and biodegradation. Ann Microbiol. https://doi.org/10.1007/s13213-010-0120-6
Wang Y, Gao S, He X, Li Y, Zhang Y et al (2020) Response of total phenols, flavonoids, minerals, and amino acids of four edible fern species to four shading treatments. Peer J. https://doi.org/10.7717/peerj.8354
Xia X, Cao J, Zheng Y (2014) Flavonoid concentrations, and bioactivity of flavonoid extracts from 19 species of ferns from China. Ind Crops Prod 58:91–98. https://doi.org/10.1016/j.indcrop.2014.04.005
Younginger BS, Ballhorn DJ (2017) Fungal endophyte communities in the temperate fern Polystichum munitum show early colonization and extensive temporal turnover. Am J Bot 104(8):1188–1194. https://doi.org/10.3732/ajb.1700149
Younginger BS, Stewart NU, Balkan MA, Ballhorn DJ (2022) Stable coexistence or competitive exclusion Fern endophytes demonstrate rapid turnover favouring a dominant fungus. Mol Ecol. https://doi.org/10.1111/mec.16732
Zhang W, Cai Y, Downum KY, Ma LQ (2004) Thiol synthesis and arsenic hyperaccumulation in Pteris vittata (Chinese brake fern). Environ Pollut 131(3):337–345
Acknowledgements
The authors are thankful to Head, Department of Botany, Tripura University for all the facilities. We are thankful to National Centre for Microbial Resource (NCMR), National Centre for Cell Science, Pune, India for molecular analysis of the fungal samples. The authors are grateful to the anonymous reviewers for their constructive comments to improve the manuscript.
Funding
The first author extends her heartfelt appreciation to University Grant Commission, New Delhi for Fellowship. We are also grateful to DBT, New Delhi, Government of India for partially supporting this work.
Author information
Authors and Affiliations
Contributions
PD and RS designed the experiment. RS and DS conducted the experiments and analysis. PD and RS analysed the data. PD, RS and AKS wrote the paper. All the authors read and finally approved the paper.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Nischitha R.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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.
About this article
Cite this article
Singha, R., Sharma, D., Saha, A.K. et al. Foliar phenols and flavonoids level in pteridophytes: an insight to culturable fungal endophyte colonisation. Arch Microbiol 206, 170 (2024). https://doi.org/10.1007/s00203-024-03880-1
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-024-03880-1