Siberian plants: untapped repertoire of bioactive endosymbionts

Abstract

BACKGROUND: Endosymbionts are microorganisms present in all plant species, and constitute the subject of interest among the scientific community. These symbionts have gained considerable attention in recent years, owing to their emerging biological roles. Global challenges, such as antimicrobial resistance, treatment of infectious diseases such as HIV and tuberculosis, cancer, and many genetic disorders, exist. Endosymbionts can help address these challenges by secreting value-added bioactive compounds with various activities.

OBJECTIVE: Herein, we describe the importance of plants inhabiting Siberian niches. These plants are considered to be among the least studied organisms in the plant kingdom worldwide. Barcoding these plants can be of interest for exploring bioactive endosymbionts possessing myriad biological properties.

METHODS: A systematic survey of relevant scientific reports was conducted using the PubMed search engine. The reports were analyzed, and compiled to draft this review.

RESULTS: The literature survey on Siberian plants regarding endosymbionts included a few reports, since extremely few exploratory studies have been conducted on the plants in these regions. Studies on the endosymbionts of these plants are highly valuable, as they report potent endosymbionts possessing numerous biological properties. Based on these considerations, this review aims to create awareness among the global scientific community working on related areas.

CONCLUSION: This review could provide the basis for barcoding novel endosymbionts of Siberian plants and their ecological importance, which can be exploited in various sectors. The main purpose of this review is to create awareness of Siberian plants, which are among the least studied organisms in the plant kingdom, with respect to endosymbionts, among the scientific community.

Keywords

endosymbiont / endophyte / siberian plant / bioactive metabolite / novel compound

References

[1] Abdou R, Scherlach K, Dahse H M, Sattler I, Hertweck C (2010). Botryorhodines A-D, antifungal and cytotoxic depsidones from Botryosphaeria rhodina, an endophyte of the medicinal plant Bidens pilosa. Phytochemistry, 71(1): 110–116

[2] Abhijeet Singh Y M (2014). Understanding the biodiversity and biological applications of endophytic fungi. J Microb Biochem Technol, s8(01): 004

[3] Alm T (2004). Ethnobotany of Rhodiola rosea (Crassulaceae) in Norway. SIDA Contrib Bot, 21: 321–344

[4] Amna T, Puri S C, Verma V, Sharma J P, Khajuria R K, Musarrat J, Spiteller M, Qazi G N (2006). Bioreactor studies on the endophytic fungus Entrophospora infrequens for the production of an anticancer alkaloid camptothecin. Can J Microbiol, 52(3): 189–196

[5] Arnold A E (2005). Diversity and ecology of fungal endophytes in tropical forests. 49–68. In: Deshmukh S (Ed.). Current Trends in Mycological Research. New Delhi, Oxford & IBH Publishing Co. Pvt. Ltd.

[6] Azevedo J L, Maccheroni W Jr, Pereira J O, De Araújo W L (2000). Endophytic microorganisms: A review on insect control and recent advances on tropical plants. Electron J Biotechnol, 3(1): 40–65

[7] Baker S, Kavitha K S, Chinnappa H, Rao Y, Rakshith D, Harini B P, Kumar K, Satish S (2015). Bacterial endo-symbiont inhabiting Tridax procumbens L. and their antimicrobial potential. Zhongguo Shengwuzhipinxue Zazhi, 2015(2): 1473–1476

[8] Baker S, Rakshith D, Kavitha K S, Santosh P, Kavitha H U, Rao Y, Satish S (2013). Plants: Emerging as nanofactories towards facile route in synthesis of nanoparticles. Bioimpacts, 3: 111–117

[9] Baker S, Satish S (2012). Endophytes: Natural warehouse of bioactive compounds. Drug Invent Today, 4: 548–553

[10] Baker S, Satish S (2015). Biosynthesis of gold nanoparticles by Pseudomonas veronii AS41G inhabiting Annona squamosa L. Spectrochim Acta A Mol Biomol Spectrosc, 150: 691–695

[11] Banerjee D, Strobel G A, Booth E, Geary B, Sears J, Spakowicz D, Busse S (2010). An endophytic Myrothecium inundatum producing volatile organic compounds. Mycosphere, 1: 229–240

[12] Bangera M G, Thomashow L S (1999). Identification and characterization of a gene cluster for synthesis of the polyketide antibiotic 2,4-diacetylphloroglucinol from Pseudomonas fluorescens Q2-87. J Bacteriol, 181(10): 3155–3163

[13] Bayoumi M T, Shaer H M E (1994). Impact of halophytes on animal health and nutrition. Halophytes as a resource for livestock and for rehabilitation of degraded lands Tasks for vegetation science, 267–272.

[14] Bertozzi S, Padian N S, Wegbreit J, DeMaria L M, Feldman B, Gayle H, Gold J, Grant R, Isbell M T (2006). HIV/AIDS Prevention and Treatment. In: Dis Control Priorities Dev Ctries. 331–370.

[15] Castillo U F, Strobel G A, Ford E J, Hess W M, Porter H, Jensen J B, Albert H, Robison R, Condron M A M, Teplow D B, Stevens D, Yaver D (2002). Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562, endophytic on Kennedia nigriscans. Microbiology, 148(Pt 9): 2675–2685

[16] Chikhi I, Allali H, El Amine Dib M, Medjdoub H, Tabti B (2014). Antidiabetic activity of aqueous leaf extract of Atriplex halimus L. (Chenopodiaceae) in streptozotocin-induced diabetic rats. Asian Pac J Trop Dis, 4(3): 181–184

[17] Compant S, Reiter B, Sessitsch A, Nowak J, Clément C, Ait Barka E (2005). Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol, 71(4): 1685–1693

[18] Deshmukh S K, Mishra P D, Kulkarni-Almeida A, Verekar S, Sahoo M R, Periyasamy G, Goswami H, Khanna A, Balakrishnan A, Vishwakarma R (2009). Anti-inflammatory and anticancer activity of ergoflavin isolated from an endophytic fungus. Chem Biodivers, 6(5): 784–789

[19] Dhankhar S, Dhankhar S, Yadav J P (2013). Investigations towards new antidiabetic drugs from fungal endophytes associated with Salvadora oleoides Decne. Med Chem, 9(4): 624–632

[20] Ding L, Münch J, Goerls H, Maier A, Fiebig H H, Lin W H, Hertweck C (2010). Xiamycin, a pentacyclic indolosesquiterpene with selective anti-HIV activity from a bacterial mangrove endophyte. Bioorg Med Chem Lett, 20(22): 6685–6687

[21] Dompeipen E J, Srikandace Y, Suharso W P, Cahyana H, Simanjuntak P (2011). Potential endophytic microbes selection for antidiabetic bioactive compounds production. Asian J Biochem, 6(6): 465–471

[22] Dragoeva A P, Koleva V P, Nanova Z D, Georgiev B P (2015). Allelopathic effects of Adonis vernalis L.: Root growth inhibition and cytogenetic alterations. J Agric Chem Environ, 4: 48–55

[23] Ezra D, Castillo U F, Strobel G A, Hess W M, Porter H, Jensen J B, Condron M A, Teplow D B, Sears J, Maranta M, Hunter M, Weber B, Yaver D (2004). Coronamycins, peptide antibiotics produced by a verticillate Streptomyces sp. (MSU-2110) endophytic on Monstera sp. Microbiology, 150(Pt 4): 785–793

[24] Farrar K, Bryant D, Cope-Selby N (2014). Understanding and engineering beneficial plant-microbe interactions: plant growth promotion in energy crops. Plant Biotechnol J, 12(9): 1193–1206

[25] Franke D, Hinz K, Reichert C (2004). Geology of the East Siberian Sea, Russian Arctic, from seismic images: Structures, evolution, and implications for the evolution of the Arctic Ocean Basin. J Geophys Res B Solid Earth, 109(7): 1–19

[26] Gaiero J R, McCall C A, Thompson K A, Day N J, Best A S, Dunfield K E (2013). Inside the root microbiome: bacterial root endophytes and plant growth promotion. Am J Bot, 100(9): 1738–1750

[27] Govindappa M, Channabasava R, Sowmya D V, Meenakshi J, Shreevidya M R, Lavanya A, Santoyo G, Sadananda T S (2011). Phytochemical screening, antimicrobial and in vitro anti-inflammatory activity of endophytic extracts from Loranthus sp. Pharmacogn J, 3(25): 82–90

[28] Guan S, Grabley S, Groth I, Lin W, Christner A, Guo D, Sattler I (2005). Structure determination of germacrane-type sesquiterpene alcohols from an endophyte Streptomyces griseus subsp. Magn Reson Chem, 43(12): 1028–1031

[29] Guimarães D O, Borges W S, Kawano C Y, Ribeiro P H, Goldman G H, Nomizo A, Thiemann O H, Oliva G, Lopes N P, Pupo M T (2008). Biological activities from extracts of endophytic fungi isolated from Viguiera arenaria and Tithonia diversifolia. FEMS Immunol Med Microbiol, 52(1): 134–144

[30] Guo B, Dai J R, Ng S, Huang Y, Leong C, Ong W, Carté B K (2000). Cytonic acids A and B: novel tridepside inhibitors of hCMV protease from the endophytic fungus Cytonaema species. J Nat Prod, 63(5): 602–604

[31] Hale I L, Broders K, Iriarte G (2014). A Vavilovian approach to discovering crop-associated microbes with potential to enhance plant immunity. Front Plant Sci, 5: 492

[32] Hardoim P R, van Overbeek L S, Berg G, Pirttilä A M, 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(3): 293–320

[33] Hilarino M P A, Silveira F A O, Oki Y, Rodrigues L, Santos J C, Correa-Junior A, Fernandes G W, Rosa C A (2011). Distribution of the endophytic fungi community in leaves of Bauhinia brevipes (Fabaceae). Acta Bot Bras, 25(4): 815–821

[34] Inahashi Y, Iwatsuki M, Ishiyama A, Namatame M, Nishihara-Tsukashima A, Matsumoto A, Hirose T, Sunazuka T, Yamada H, Otoguro K, Takahashi Y, Ōmura S, Shiomi K (2011). Spoxazomicins A-C, novel antitrypanosomal alkaloids produced by an endophytic actinomycete, Streptosporangium oxazolinicum K07-0460(T). J Antibiot (Tokyo), 64(4): 303–307

[35] Karmakar R, Kumar S, Prakash H S (2013). Fungal endophytes from Garcinia species. Int J Pharm Pharm Sci, 5: 889–897

[36] Kavitha K, Baker S, Rakshith D, Kavitha H, Yashwantha Rao H, Harini B, Satish S (2013). Plants as Green source towards synthesis of nanoparticles. Int Res J Biol Sci, 2: 66–76

[37] Kharwar R N, Verma V C, Strobel G, Ezra D (2008). The endophytic fungal complex of Catharanthus roseus (L.) G. Don. Curr Sci, 95: 228–233

[38] Kim D M, Nam B W (2006). Extracts and essential oil of Ledum palustre L. leaves and their antioxidant and antimicrobial activities. Prev Nutr Food Sci, 11(2): 100–104

[39] Kokoska L, Janovska D (2009). Chemistry and pharmacology of Rhaponticum carthamoides: a review. Phytochemistry, 70(7): 842–855

[40] Kokoska L, Polesny Z, Rada V, Nepovim A, Vanek T (2002). Screening of some Siberian medicinal plants for antimicrobial activity. J Ethnopharmacol, 82(1): 51–53

[41] Kusari S, Hertweck C, Spiteller M (2012). Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol, 19(7): 792–798

[42] Li J Y, Harper J K, Grant D M, Tombe B O, Bashyal B, Hess W M, Strobel G A (2001). Ambuic acid, a highly functionalized cyclohexenone with antifungal activity from Pestalotiopsis spp. and Monochaetia sp. Phytochemistry, 56(5): 463–468

[43] Liang J, Chen J, Tan Z, Peng J, Zheng X, Nishiura K, Ng J, Wang Z, Wang D, Chen Z, Liu L (2013). Extracts of medicinal herb Sanguisorba officinalisinhibit the entry of human immunodeficiency virus type one. Yao Wu Shi Pin Fen Xi, 21(4): S52–S58

[44] Lotocka B, Geszprych A (2004). Anatomy of the vegetative organs and secretory structures of Rhaponticum carthamoides (Asteraceae). Bot J Linn Soc, 144(2): 207–233

[45] Maji A, Banerji P (2015). Chelidonium majus L.(Greater celandine)–A review on its phytochemical and therapeutic perspectives. Int J Herb Med, 3(1): 10–27

[46] Marchev A S, Dinkova-Kostova A T, Gyrgy Z, Mirmazloum I, Aneva I Y, Georgiev M I (2016). Rhodiola rosea L.: from golden root to green cell factories. Phytochem Rev, 15(4): 515–536

[47] Miller C M, Miller R V, Garton-Kenny D, Redgrave B, Sears J, Condron M M, Teplow D B, Strobel G A (1998). Ecomycins, unique antimycotics from Pseudomonas viridiflava. J Appl Microbiol, 84(6): 937–944

[48] Nadeem M, Ram M, Alam P, Ahmad M M, Mohammad A, Al-Qurainy F, Khan S, Abdin M Z (2012). Fusarium solani, P1, a new endophytic podophyllotoxin-producing fungus from roots of Podophyllum hexandrum. Afr J Microbiol Res, 6: 2493–2499

[49] Nair D N, Padmavathy S (2014). Impact of endophytic microorganisms on plants, environment and humans. Sci World J, 2014: 250693

[50] Newman D J, Cragg G M (2015). Endophytic and epiphytic microbes as “sources” of bioactive agents. Front Chem, 3: 34

[51] Opletal L, Sovova M, Dittrich M, Solich P, Dvorak J, Kratky F, Cerovsky J, Hofbauer J (1997). Phytotherapeutic aspects of diseases of the circulatory system. 6. Leuzea carthamoides (WILLD.).

[52] Pan J H, Chen Y, Huang Y H, Tao Y W, Wang J, Li Y, Peng Y, Dong T, Lai X M, Lin Y C (2011). Antimycobacterial activity of fusaric acid from a mangrove endophyte and its metal complexes. Arch Pharm Res, 34(7): 1177–1181

[53] Panossian A, Wikman G, Sarris J (2010). Rosenroot (Rhodiola rosea): traditional use, chemical composition, pharmacology and clinical efficacy. Phytomedicine, 17(7): 481–493

[54] Partida-Martínez L P, Heil M (2011). The microbe-free plant: fact or artifact? Front Plant Sci, 2: 100

[55] Popov S V, Popova G Y, Nikolaeva S Y, Golovchenko V V, Ovodova R G (2005). Immunostimulating activity of pectic polysaccharide from Bergenia crassifolia (L.) Fritsch. Phytother Res, 19(12): 1052– 1056

[56] Powledge T M (2011). Behavioral epigenetics: how nurture shapes Nature. Bioscience, 61(8): 588–592

[57] Qin J C, Zhang Y M, Gao J M, Bai M S, Yang S X, Laatsch H, Zhang A L (2009). Bioactive metabolites produced by Chaetomium globosum, an endophytic fungus isolated from Ginkgo biloba. Bioorg Med Chem Lett, 19(6): 1572–1574

[58] Raiklin E (2008). The Chinese challenge to Russia in Siberia and the Russian Far East. J Soc Polit Econ Stud, 33: 145–204

[59] Rather M A, Mansoor S, Bhat Z S, Amin S (2016). Evaluation of antimicrobial and antioxidant activities of Swertia petiolata. Adv Biomed Pharma, 5: 272–279

[60] Rodrigues-Heerklotz K F, Drandarov K, Heerldotz J, Hesse M, Werner C (2001). Guignardic acid, a novel type of secondary metabolite produced by the endophytic fungus Guignardia sp.: isolation, structure elucidation, and asymmetric synthesis. Helv Chim Acta, 84(12): 3766–3772

[61] Rodriguez R J, White J F J Jr, Arnold A E, Redman R S (2009). Fungal endophytes: diversity and functional roles. New Phytol, 182(2): 314–330

[62] Saikkonen K, Wäli P, Helander M, Faeth S H (2004). Evolution of endophyte-plant symbioses. Trends Plant Sci, 9(6): 275–280

[63] Satish S, Raveesha K A, Janardhana G R (1999). Antibacterial activity of plant extracts on phytopathogenic Xanthomonas campestris pathovars. Lett Appl Microbiol, 28(2): 145–147

[64] Schulz B, Boyle C (2006). What are Endophytes? 9:1–14.

[65] Schulz B, Haas S, Junker C, Andree N, Schobert M (2015). Fungal endophytes are involved in multiple balanced antagonisms. Curr Sci, 109: 39–45

[66] Shikov A N, Pozharitskaya O N, Makarova M N, Makarov V G, Wagner H (2014). Bergenia crassifolia (L.) Fritsch--pharmacology and phytochemistry. Phytomedicine, 21(12): 1534–1542

[67] Singh S B, Jayasuriya H, Dewey R, Polishook J D, Dombrowski A W, Zink D L, Guan Z, Collado J, Platas G, Pelaez F, Felock P J, Hazuda D J (2003). Isolation, structure, and HIV-1-integrase inhibitory activity of structurally diverse fungal metabolites. J Ind Microbiol Biotechnol, 30(12): 721–731

[68] Song Y C, Li H, Ye Y H, Shan C Y, Yang Y M, Tan R X (2004). Endophytic naphthopyrone metabolites are co-inhibitors of xanthine oxidase, SW1116 cell and some microbial growths. FEMS Microbiol Lett, 241(1): 67–72

[69] Srobel G, Li J Y, Sugawara F, Koshino H, Harper J, Hess W M (1999). Oocydin A, a chlorinated macrocyclic lactone with potent anti-oomycete activity from Serratia marcescens. Microbiology, 145(Pt 12): 3557–3564

[70] Stadler M, Schulz B (2009). High energy biofuel from endophytic fungi? Trends Plant Sci, 14(7): 353–355

[71] Stierle A, Strobel G, Stierle D, Grothaus P, Bignami G (1995). The search for a taxol-producing microorganism among the endophytic fungi of the Pacific yew, Taxus brevifolia. J Nat Prod, 58(9): 1315–1324

[72] Strobel G, Daisy B (2003). Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev, 67(4): 491–502

[73] Strobel G, Daisy B, Castillo U, Harper J (2004). Natural products from endophytic microorganisms. J Nat Prod, 67(2): 257–268

[74] Svidén G A, Tham K, Borell L (2010). Involvement in everyday life for people with a life threatening illness. Palliat Support Care, 8(3): 345–352

[75] Syed B, Nagendra Prasad M N, Mohan Kumar K, Dhananjaya B L, Satish S (2017). Endo-symbiont mediated synthesis of gold nanobactericides and their activity against human pathogenic bacteria. Environ Toxicol Pharmacol, 52: 143–149

[76] Syed B, Nagendra Prasad M N, Satish S (2016). Synthesis and characterization of silver nanobactericides produced by Aneurinibacillus migulanus 141, a novel endophyte inhabiting Mimosa pudica L. Arab J Chem,

[77] Tchebakova N M, Kuzmina N A, Parfenova E I, Senashova V A, Kuzmin S R (2016). Potential climate-induced distributions of Lophodermium needle cast across central Siberia in the 21 century. Web Ecol, 16(1): 37–39

[78] Turner J, Bracegirdle T J, Phillips T, Marshall G J, Hosking J S (2012). An initial assessment of antarctic sea ice extent in the CMIP5 models. J Clim, 26(5): 1473–1484

[79] Vdovitchenko M Y, Kuzovkina I N, Paetz C, Schneider B (2007). Formation of phenolic compounds in the roots of Hedysarum theinum cultured in vitro. Russ J Plant Physiol, 54(4): 536–544

[80] Xia Y, DeBolt S, Dreyer J, Scott D, Williams M A (2015). Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Front Plant Sci, 6: 490

[81] Xue S Y, Li Z Y, Zhi H J, Sun H F, Zhang L Z, Guo X Q, Qin X M (2012). Metabolic finger printing investigation of Tussilago farfara L. by GC-MS and multivariate data analysis. Biochem Syst Ecol, 41: 6–12

[82] Yashina S, Gubin S, Maksimovich S, Yashina A, Gakhova E, Gilichinsky D (2012). Regeneration of whole fertile plants from 30,000-y-old fruit tissue buried in Siberian permafrost. Proc Natl Acad Sci USA, 109(10): 4008–4013

[83] You Y H, Yoon H, Kang S M, Shin J H, Choo Y S, Lee I J, Lee J M, Kim J G (2012). Fungal diversity and plant growth promotion of endophytic fungi from six halophytes in Suncheon Bay. J Microbiol Biotechnol, 22(11): 1549–1556

[84] Zabalgogeazcoa (2008). Fungal endophytes and their interactions with plant pathogens. Span J Agric Res 6: 138–146

Acknowledgments

The authors are grateful to the Ministry of Education and Science of the Russian Federation for providing funding under the 5–100: Russian Academic Excellence Project. The authors are grateful for the facilities provided by the Siberian Federal University.

Compliance with ethics guidelines

Syed Baker, Svetlana V. Prudnikova and Tatiana Volova declare that they no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

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