Abstract
The potential of mangrove-derived endophytic fungi as a promising source of diverse and structurally unprecedented bioactive natural products is unquestionable and continues to attract considerable attention. This review highlights new bioactive mangrove fungal metabolites and known compounds with hitherto unreported biological activities described during the last 10 years. The compounds are categorized according to their reported biological activities, including cytotoxic, anti-infective, in addition to a wide range of miscellaneous activities such as protein kinase, α-glucosidase, acetylcholinesterase and tyrosinase inhibitory activities, as well as antiangiogenic and neovascularisation effects, radical scavenging, DNA-binding affinity, and calcium and potassium channel blocking activity.
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Akello J, Dubois T, Gold CS, Coyne D, Nakavuma J, Paparu P (2007) Beauveria bassiana (Balsamo) Vuillemin as an endophyte in tissue culture banana (Musa spp.). J Invertebr Pathol 96:34–42
Anada K, Sridhar KR (2002) Diversity of endophytic fungi in the roots of mangrove species on the west coast of India. Can J Microbiol 48:871–878
Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 100:15649–15654
Bacon CW, White JF (2000) Microbial Endophytes. Marcel Dekker, New York, pp 341–388
Bae H, Sicher RC, Kim MS, Kim SH, Strem MD, Melnick RL, Bailey BA (2009) The beneficial endophyte Trichoderma hamatum isolate DIS 219b promotes growth and delays the onset of the drought response in Theobroma cacao. J Exp Bot 60:3279–3295
Bandaranayake WM (1998) Traditional and medicinal uses of mangroves. Mangroves Salt Marshes 2:133–148
Bandaranayake WM (2002) Bioactivities, bioactive compounds and chemical constituents of mangrove plants. Wetl Ecol Manag 10:421–452
Bialy L, Waldmann H (2005) Inhibitors of protein tyrosine phosphatases: next-generation drugs? Angew Chem Int Ed 44:3814–3839
Chokpaiboon S, Sommit D, Bunyapaiboonsri T, Matsubara K, Pudhom K (2011) Antiangiogenic effect of chamigrane endoperoxides from a Thai mangrove-derived fungus. J Nat Prod 74:2290–2294
Ebrahim W, Kjer J, El Amrani M, Wray V, Lin W, Ebel R, Lai D, Proksch P (2012a) Pullularins E and F, two new peptides from the endophytic fungus Bionectria ochroleuca isolated from the mangrove plant Sonneratia caseolaris. Mar Drugs 10:1081–1091
Ebrahim W, Aly AH, Mándi A, Totzke F, Kubbutat MHG, Wray V, Lin WH, Dai H, Proksch P, Kurtán T, Debbab A (2012b) Decalactone derivatives from Corynespora cassiicola, an endophytic fungus of the mangrove plant Laguncularia racemosa. Eur J Org Chem: 3476–3484
Giordano L, Gonthier P, Varese GC, Miserere L, Nicolotti G (2009) Mycobiota inhabiting sapwood of healthy and declining Scots pine (Pinus sylvestris L.) trees in the Alps. Fungal Divers 38:69–83
Gopal B, Chauhan M (2006) Biodiversity and its conservation in the Sundarban mangrove ecosystem. Aquat Sci 68:338–354
Huang Z, Cai X, Shao C, She Z, Xia X, Chen Y, Yang J, Zhou S, Lin Y (2008) Chemistry and weak antimicrobial activities of phomopsins produced by mangrove endophytic fungus Phomopsis sp. ZSU-H76. Phytochemistry 69:1604–1608
Huang Z, Guo Z, Yang R, Yin X, Li X, Luo W, She Z, Lin Y (2009) Chemistry and cytotoxic activities of polyketides produced by the mangrove endophytic fungus Phomopsis SP. ZSU-H76. Chem Nat Compd 45:625–628
Huang Z, Yang R, Guo Z, She Z, Lin Y (2010a) A new naphto-α-pyrone from mangrove endophytic fungus ZSU-H26. Chem Nat Compd 46:15–18
Huang Z, Yang R, Yin X, Shec Z, Lin Y (2010b) Structure elucidation and NMR assignments for two xanthone derivatives from a mangrove endophytic fungus (No. ZH19). Magn Reson Chem 48:80–82
Huang HB, Feng XJ, Liu L, Chen B, Lu YJ, Ma L, She ZG, Lin YC (2010c) Three dimeric naphtho-γ-pyrones from the mangrove endophytic fungus Aspergillus tubingensis isolated from Pongamia pinnata. Planta Med 76:1888–1891
Huang HB, Xiao ZE, Feng XJ, Huang CH, Zhu X, Ju JH, Li MF, Lin YC, Liu L, She ZG (2011a) Cytotoxic naphtho-g-pyrones from the mangrove endophytic fungus Aspergillus tubingensis (GX1-5E). Helv Chim Acta 94:1732–1740
Huang CH, Pan JH, Chen B, Yu M, Huang HB, Zhu X, Lu YJ, She ZG, Lin YC (2011b) Three bianthraquinone derivatives from the mangrove endophytic fungus Alternaria sp. ZJ9-6B from the south China sea. Mar Drugs 9:832–843
Huang H, Feng X, Xiao Z, Liu L, Li H, Ma L, Lu Y, Ju J, She Z, Lin Y (2011c) Azaphilones and p-terphenyls from the mangrove endophytic fungus Penicillium chermesinum (ZH4-E2) isolated from the South China Sea. J Nat Prod 74:997–1002
Huang X, Huang H, Li H, Sun X, Huang H, Lu Y, Lin Y, Long Y, She Z (2013) Asperterpenoid A, a new sesterterpenoid as an inhibitor of Mycobacterium tuberculosis protein tyrosine phosphatase B from the culture of Aspergillus sp. 16-5c. Org Lett 15:721–723
Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173
Jones G, Stanley SJ, Pinruan U (2008) Marine endophyte sources of new chemical natural products: a review. Bot Mar 51:163–170
Kjer J, Wray V, Edrada-Ebel RA, Ebel R, Pretsch A, Lin WH, Proksch P (2009) Xanalteric acids I and II and related phenolic compounds from an endophytic Alternaria sp. isolated from the mangrove plant Sonneratia alba. J Nat Prod 72:2053–2057
Klaiklay S, Rukachaisirikul V, Phongpaichit S, Pakawatchai C, Saithong S, Buatong J, Preedanon S, Sakayaroj J (2012a) Anthraquinone derivatives from the mangrove-derived fungus Phomopsis sp. PSU-MA214. Phytochem Lett 5:738–742
Klaiklay S, Rukachaisirikul V, Tadpetch K, Sukpondma Y, Phongpaichit S, Buatong J, Sakayaroj J (2012b) Chlorinated chromone and diphenyl ether derivatives from the mangrove-derived fungus Pestalotiopsis sp. PSU-MA69. Tetrahedron 68:2299–2305
Klaiklay S, Rukachaisirikul V, Phongpaichit S, Buatong J, Preedanon S, Sakayaroj J (2012c) Flavodonfuran: a new difuranylmethane derivative from the mangrove endophytic fungus Flavodon flavus PSU-MA201. Nat Prod Res 1–5
Klaiklay S, Rukachaisirikul V, Sukpondma Y, Phongpaichit S, Buatong J, Bussaban B (2012d) Metabolites from the mangrove-derived fungus Xylaria cubensis PSU-MA34. Arch Pharm Res 35:1127–1131
Kogel KH, Franken P, Hückelhoven R (2006) Endophyte or parasite – what decides? Curr Opin Plant Biol 9:358–363
Kohlmeyer J, Volkmann-Kohlmeyer B (1993) Two new genera of Ascomycotina from saltmarsh Juncus. Systema Ascomycetum 11:95–106
Li MY, Xiao Q, Pan JY, Wu J (2009a) Natural products from semi-mangrove flora: source, chemistry and bioactivities. Nat Prod Rep 26:281–298
Li DL, Li XM, Wang BG (2009b) Natural anthraquinone derivatives from a marine mangrove plant-derived endophytic fungus Eurotium rubrum: structural elucidation and DPPH radical scavenging activity. J Microbiol Biotechnol 19:675–680
Li KK, Lu YJ, Song XH, She ZG, Wuc XW, An LK, Ye CX, Lin YC (2010) The metabolites of mangrove endophytic fungus Zh6-B1 from the South China Sea. Bioorg Med Chem Lett 20:3326–3328
Li H, Huang H, Shao C, Huang H, Jiang J, Zhu X, Liu Y, Liu L, Lu Y, Li M, Lin Y, She Z (2011a) Cytotoxic norsesquiterpene peroxides from the endophytic fungus Talaromyces flavus isolated from the mangrove plant Sonneratia apetala. J Nat Prod 74:1230–1235
Li C, Zhang J, Shao C, Ding W, She Z, Lin Y (2011b) A new xanthone derivative from the co-culture broth of two marine fungi (strain No. E33 and K38). Chem Nat Compd 47:382–384
Li S, Wei M, Chen G, Lin Y (2012) Two new dihydroisocoumarins from the endophytic fungus Aspergillus sp. collected from the South China Sea. Chem Nat Compd 48:371–373
Lin Z, Zhu T, Fang Y, Gu Q (2008a) 1Hand 13C NMR assignments of two new indolic enamide diastereomers from a mangrove endophytic fungus Aspergillus sp. Magn Reson Chem 46:1212–1216
Lin Z, Zhu T, Fang Y, Gu Q, Zhu W (2008b) Polyketides from Penicillium sp. JP-1, an endophytic fungus associated with the mangrove plant Aegiceras corniculatum. Phytochemistry 69:1273–1278
Lin Z, Zhang GJ, Zhu TJ, Liu R, Wei HJ, Gu QQ (2009) Bioactive cytochalasins from Aspergillus flavipes, an endophytic fungus associated with the mangrove plant Acanthus ilicifolius. Helv Chim Acta 92:1538–1544
Liu F, Cai X-L, Yang H, Xia X-K, Guo Z-Y, Yuan J, Li M-F, She Z-G, Lin Y-C (2010) The bioactive metabolites of the mangrove endophytic fungus Talaromyces sp. ZH-154 isolated from Kandelia candel (L.). Planta Med 76:185–189
Liu D, Li XM, Meng L, Li CS, Gao SS, Shang Z, Proksch P, Huang CG, Wang BG (2011) Nigerapyrones A-H, α-pyrone derivatives from the marine mangrove-derived endophytic fungus Aspergillus niger MA-132. J Nat Prod 74:1787–1791
Lu Z, Zhu H, Fu P, Wang Y, Zhang Z, Lin H, Liu P, Zhuang Y, Hong K, Zhu W (2010) Cytotoxic polyphenols from the marine-derived fungus Penicillium expansum. J Nat Prod 73:911–914
Mei WL, Zheng B, Zhao YX, Zhong HM, Chen XL, Zeng YB, Dong WH, Huang JL, Proksch P, Dai HF (2012) Meroterpenes from endophytic fungus A1 of mangrove plant Scyphiphora hydrophyllacea. Mar Drugs 10:1993–2001
Pang KL, Vrijmoed LLP, Goh TK, Plaingam N, Jones GEB (2008) Fungal endophytes associated with Kandelia candel (Rhizophoraceae) in Mai Po nature reserve, Hong Kong. Bot Mar 51:171–178
Redman RS, Dunigan DD, Rodriguez RJ (2001) Fungal symbiosis: from mutualism to parasitism, who controls the outcome, host or invader? New Phytol 151:705–716
Redman RS, Sheehan KB, Stout TG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581
Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114
Rukachaisirikul V, Rodglin A, Sukpondma Y, Phongpaichit S, Buatong J, Sakayaroj J (2012) Phthalide and isocoumarin derivatives produced by an Acremonium sp. isolated from a mangrove Rhizophora apiculata. J Nat Prod 75:853–858
Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343
Sengputa A, Chaudhuri S (2002) Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174
Shang Z, Li XM, Li CS, Wang BG (2012) Diverse secondary metabolites produced by marine-derived fungus Nigrospora sp. MA75 on various culture media. Chem Biodivers 9:1338–1348
Shao C, Wang C, Wei M, Gu Y, Xia X, She Z, Lin Y (2008) Structure elucidation of two new xanthone derivatives from the marine fungus Penicillium sp. (ZZF 32#) from the South China Sea. Magn Reson Chem 46:1066–1069
Shao SL, Wang CY, Gu YC, Wei MY, Pan JH, Deng DS, She ZG, Lin YC (2010) Penicinoline, a new pyrrolyl 4-quinolinone alkaloid with an unprecedented ring system from an endophytic fungus Penicillium sp. Bioorg Med Chem Lett 20:3284–3286
Shearer CA, Descals E, Kohlmeyer B, Kohlmeyer J, Marvanova L, Padgett D, Porter D, Raja HA, Schmit JP, Thorton HA, Voglymayr H (2007) Fungal diversity in aquatic habitats. Biodivers Conserv 16:49–67
Song Y, Wang J, Huang H, Ma L, Wang J, Gu Y, Liu L, Lin Y (2012) Four eremophilane sesquiterpenes from the mangrove endophytic fungus Xylaria sp. BL321. Mar Drugs 10:340–348
Sridhar KR (2004) Mangrove fungi in India. Curr Sci 86:1586–1587
Strobel G, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502
Tan N, Tao Y, Pan J, Wang S, Xu F, She Z, Lin Y, Gareth Jones EB (2008) Isolation, structure elucidation, and mutagenicity of four alternariol derivatives produced by the mangrove endophytic fungus No. 2240. Chem Nat Compd 44:296–300
Tao Y, Zeng X, Mou C, Li J, Cai X, She Z, Zhoub S, Lin Y (2008) 1H and 13C NMR assignments of three nitrogen containing compounds from the mangrove endophytic fungus (ZZF08). Magn Reson Chem 46:501–505
Unterseher M, Schnittler M (2010) Species richness analysis and ITS rDNA phylogeny revealed the majority of cultivable foliar endophytes from beech (Fagus sylvatica). Fungal Ecol 3:366–378
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, Von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391
Wen L, Chen G, She Z, Yan C, Cai J, Mua L (2010) Two new paeciloxocins from a mangrove endophytic fungus Paecilomyces sp. Russ Chem B 59:1656–1659
Wu XY, Liu XH, Lin YC, Luo JH, She ZG, Houjin L, Chan WL, Antus S, Kurtan T, Elsässer B, Krohn K (2005) Xyloketal F: a strong L-calcium channel blocker from the mangrove fungus Xylaria sp. (#2508) from the South China Sea coast. Eur J Org Chem: 4061–4064
Xia XK, Huang HR, She ZG, Cai JW, Lan L, Zhang JY, Fuc LW, Vrijmoed LLP, Lin YC (2007) Structural and biological properties of vermistatin and two new vermistatin derivatives isolated from the marine-mangrove endophytic fungus Guignardia sp. No. 4382. Helv Chim Acta 90:1925–1931
Xu M, Gessner G, Groth I, Lange C, Christner A, Bruhn T, Deng Z, Li X, Heinemann SH, Grabley S, Bringmann G, Sattler I, Lin W (2007) Shearinines D-K, new indole triterpenoids from an endophytic Penicillium sp. (strain HKI0459) with blocking activity on large-conductance calcium-activated potassium channels. Tetrahedron 63:435–444
Xu J, Kjer J, Sendker J, Wray V, Guan H, Edrada RA, Lin WH, Wu J, Proksch P (2009a) Chromones from the endophytic fungus Pestalotiopsis sp. Isolated from the Chinese Mangrove plant Rhizophora mucronata. J Nat Prod 72:662–665
Xu F, Pang J, Lu B, Wang J, Zhang Y, She Z, Vrijmoed LLP, Gareth Jones EB, Lin Y (2009b) Two metabolites with DNA-binding affinity from the mangrove fungus Xylaria sp. (#2508) from the South China Sea coast. Chin J Chem 27:365–368
Yan HJ, Lia XM, Lia CS, Wang BG (2012) Alkaloid and anthraquinone derivatives produced by the marine-derived endophytic fungus Eurotium rubrum. Helv Chim Acta 95:163–168
Yang J, Xu F, Huang C, Li J, She Z, Pei Z, Lin Y (2010) Metabolites from the mangrove endophytic fungus Phomopsis sp. (#zsu-H76). Eur J Org Chem, 3692–3695
Zeng YB, Wang H, Zuo WJ, Zheng B, Yang T, Dai HF, Mei WL (2012) A fatty acid glycoside from a marine-derived fungus isolated from mangrove plant Scyphiphora hydrophyllacea. Mar Drugs 10:598–603
Zhang G, Sun S, Zhu T, Lin Z, Gu J, Li D, Gu Q (2011) Antiviral isoindolone derivatives from an endophytic fungus Emericella sp. associated with Aegiceras corniculatum. Phytochemistry 72:1436–1442
Zhou H, Zhu T, Cai S, Gu Q, Li D (2011) Drimane sesquiterpenoids from the mangrove-derived fungus Aspergillus ustus. Chem Pharm Bull 59:762–766
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Financial support to P.P. and A.D. by BMBF is gratefully acknowledged.
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Debbab, A., Aly, A.H. & Proksch, P. Mangrove derived fungal endophytes – a chemical and biological perception. Fungal Diversity 61, 1–27 (2013). https://doi.org/10.1007/s13225-013-0243-8
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DOI: https://doi.org/10.1007/s13225-013-0243-8