Phylogenetic spectrum and analysis of antibacterial activities of leaf extracts from plants of the genus Rhododendron

BMC Complementary and Alternative Medicine

Matthias S Ullrich³  Klaudia Brix³  Dirk C Albach²  Hartwig Schepker¹  Jennifer Nolzen²  Ahmed Rezk³ 

[1] Stiftung Bremer Rhododendronpark, Deliusweg 40, Bremen 28359, Germany;Institute for Biology and Environmental Sciences, Carl von Ossietzky University Oldenburg, Carl von Ossietzky Strasse 9-11, Oldenburg 26111, Germany;Molecular Life Science Research Center, Jacobs University Bremen, Campus Ring 1, Bremen 28759, Germany

关键词: Multidrug efflux pump;    Gram-positive bacteria;    Antimicrobial activity;    Rhododendron;   

Others  :  1138360
DOI  :  10.1186/s12906-015-0596-5

 received in 2014-10-30, accepted in 2015-02-28,  发布年份 2015

【 摘 要 】

Background

Plants are traditionally used for medicinal treatment of numerous human disorders including infectious diseases caused by microorganisms. Due to the increasing resistance of many pathogens to commonly used antimicrobial agents, there is an urgent need for novel antimicrobial compounds. Plants of the genus Rhododendron belong to the woody representatives of the family Ericaceae, which are typically used in a range of ethno-medical applications. There are more than one thousand Rhododendron species worldwide. The Rhododendron-Park Bremen grows plants representing approximately 600 of the known Rhododendron species, and thus enables research involving almost two thirds of all known Rhododendron species.

Methods

Twenty-six bacterial species representing different taxonomic clades have been used to study the antimicrobial potential of Rhododendron leaf extracts. Agar diffusion assay were conducted using 80% methanol crude extracts derived from 120 Rhododendron species.Data were analyzed using principal component analysis and the plant-borne antibacterial activities grouped according the first and second principal components.

Results

The leaf extracts of 17 Rhododendron species exhibited significant growth-inhibiting activities against Gram-positive bacteria. In contrast, only very few of the leaf extracts affected the growth of Gram-negative bacteria. All leaf extracts with antimicrobial bioactivity were extracted from representatives of the subgenus Rhododendron, with 15 from the sub-section Rhododendron and two belonging to the section Pogonanthum. The use of bacterial multidrug efflux pump mutants revealed remarkable differences in the susceptibility towards Rhododendron leaf extract treatment.

Conclusions

For the first time, our comprehensive study demonstrated that compounds with antimicrobial activities accumulate in the leaves of certain Rhododendron species, which mainly belong to a particular subgenus. The results suggested that common genetic traits are responsible for the production of bioactive secondary metabolite(s) which act primarily on Gram-positive organisms, and which may affect Gram-negative bacteria in dependence of the activity of multidrug efflux pumps in their cell envelope.

【 授权许可】

   
2015 Rezk et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Hill AF: Economic botany: a textbook of useful plants and plant products. McGraw-Hill, New York; 1952.
• [2]Sofowora A: Medicinal plants and traditional medicine in Africa. Wiley, New York; 1982.
• [3]Popescu R, Kopp B: The genus Rhododendron: an ethnopharmacological and toxicological review. J Ethnopharmacol 2013, 147(1):42-62.
• [4]WHO: WHO traditional medicine strategy 2002–2005. WHO, Geneva; 2002.
• [5]Farnsworth NR, Soejarto DD: The conservation of medicinal plants. In Global importance of medicinal plants. Cambridge University Press, Cambridge; 1991:25-51.
• [6]Kim H-S: Do not put too much value on conventional medicines. J Ethnopharmacol 2005, 100(1–2):37-9.
• [7]Sydnor ERM, Perl TM: Hospital epidemiology and infection control in acute-care settings. Clin Microbiol Rev 2011, 24(1):141-73.
• [8]Acar JF: Consequences of bacterial resistance to antibiotics in medical practice. Clin Infect Dis 1997, 24(1):17-8.
• [9]Valentin Bhimba B, Meenupriya J, Joel EL, Naveena DE, Kumar S, Thangaraj M: Antibacterial activity and characterization of secondary metabolites isolated from mangrove plant Avicennia officinalis. Asian Pac J Trop Med 2010, 3(7):544-6.
• [10]Hunter MD, Hull LA: Variation in concentrations of phloridzin and phloretin in apple foliage. Phytochem 1993, 34(5):1251-4.
• [11]Omulokoli E, Khan B, Chhabra SC: Antiplasmodial activity of four Kenyan medicinal plants. J Ethnopharmacol 1997, 56(2):133-7.
• [12]Demain AL, Fang A: The natural functions of secondary metabolites. Adv Biochem Eng Biotechnol 2000, 69:1-39.
• [13]Bennett RN, Wallsgrove RM: Secondary metabolites in plant defence mechanisms. New Phytol 1994, 127(4):617-33.
• [14]Chamberlain DF, Hyam R, Argent G, Fairweather G, Walter KS: The genus Rhododendron. Its classification and synonymy. Royal Botanical Garden, Edinburgh; 1996.
• [15]Innocenti G, Dall’ Acqua S, Scialino G, Banfi E, Sosa S, Gurung K, et al.: Chemical composition and biological properties of rhododendron anthopogon essential oil. Mol 2010, 15(4):2326-38.
• [16]Kim M-H, Nugroho A, Choi J, Park J, Park H-J: Rhododendrin, an analgesic/anti-inflammatory arylbutanoid glycoside, from the leaves of Rhododendron aureum. Arch Pharm Res 2011, 34(6):971-8.
• [17]Dampc A, Luczkiewicz M: Rhododendron tomentosum (Ledum palustre). A review of traditional use based on current research. Fitoterapia 2013, 85:130-43.
• [18]Rehman SU, Khan R, Bhat KA, Raja AF, Shawl AS, Alam MS: Isolation, characterisation and antibacterial activity studies of coumarins from Rhododendron lepidotum Wall. ex G. Don, Ericaceae. Revista Brasileira de Farmacognosia 2010, 20:886-90.
• [19]Dorman HJ, Deans SG: Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol 2000, 88(2):308-16.
• [20]Wang W, Li N, Luo M, Zu Y, Efferth T: Antibacterial activity and anticancer activity of rosmarinus officinalis L. Essential oil compared to that of its main components. Mol 2012, 17(3):2704-13.
• [21]Jaiswal R, Jayasinghe L, Kuhnert N: Identification and characterization of proanthocyanidins of 16 members of the Rhododendron genus (Ericaceae) by tandem LC-MS. J Mass Spectrom: JMS 2012, 47(4):502-15.
• [22]Sambrook J, Russell DW: Molecular cloning: a laboratory manual. Cold Spring Habor Laboratory Press, New York, USA; 2001.
• [23]Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, et al.: The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 2003, 100(18):10181-6.
• [24]Morita Y, Kodama K, Shiota S, Mine T, Kataoka A, Mizushima T, et al.: NorM, a putative multidrug efflux protein, of Vibrio parahaemolyticus and its homolog in Escherichia coli. Antimicrob Agents Chemother 1998, 42(7):1778-82.
• [25]Al-Karablieh N, Weingart H, Ullrich MS: Genetic exchange of multidrug efflux pumps among two enterobacterial species with distinctive ecological Niches. Int J Mol Sci 2009, 10(2):629-45.
• [26]Burse A, Weingart H, Ullrich MS: The phytoalexin-inducible multidrug efflux pump AcrAB contributes to virulence in the fire blight pathogen, Erwinia amylovora. Mol Plant-Microbe Interact: MPMI 2004, 17(1):43-54.
• [27]Al-Karablieh N, Weingart H, Ullrich MS: The outer membrane protein TolC is required for phytoalexin resistance and virulence of the fire blight pathogen Erwinia amylovora. J Microbial Biotechnol 2009, 2(4):465-75.
• [28]Stoitsova SO, Braun Y, Ullrich MS, Weingart H: Characterization of the RND-type multidrug efflux pump MexAB-OprM of the plant pathogen Pseudomonas syringae. Appl Environ Microbiol 2008, 74(11):3387-93.
• [29]Nathan P, Law EJ, Murphy DF, MacMillan BG: A laboratory method for selection of topical antimicrobial agents to treat infected burn wounds. Burns Incl Therm Inj 1978, 4:176-87.
• [30]Jolliffe IT: Principal component analysis. Springer, New York, USA; 2002.
• [31]Frodin DG: History and concepts of big plant genera. Taxon 2004, 53(3):753-76.
• [32]Ghamba PE, Agbo EB, Umar AF, Bukbuk DN, Goje LJ: In vitro antibacterial activity of crude ethanol, acetone and aqueous Garcinia kola seed extracts on selected clinical isolates. Afr J Biotechnol 2012, 11(6):1473-83.
• [33]Zgurskaya HI, Nikaido H: Multidrug resistance mechanisms: drug efflux across two membranes. Mol Microbiol 2000, 37(2):219-25.
• [34]Nikaido H: Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 1996, 178(20):5853-9.
• [35]Kirk H, Cheng D, Choi Y, Vrieling K, Klinkhamer PL: Transgressive segregation of primary and secondary metabolites in F2 hybrids between Jacobaea aquatica and J. vulgaris. Metabolomics 2012, 8(2):211-9.
• [36]Orians CM: The effects of hybridization in plants on secondary chemistry: implications for the ecology and evolution of plant-herbivore interactions. Am J Bot 2000, 87(12):1749-56.
• [37]Strauss SY: Levels of herbivory and parasitism in host hybrid zones. Trends Ecol Evol 1994, 9(6):209-14.
• [38]Chhetri HP, Yogol NS, Sherchan J, Anupa KC, Mansoor S, Thapa P: Phytochemical and antimicrobial evaluations of some medicinal plants of Nepal. Kathmandu Univ J Sci Eng Technol 2008, 4(1):49-54.
• [39]Paudel A, Panthee S, Shakya S, Amatya S, Shrestha TM, Amatya MP: Phytochemical and antibacterial properties of Rhododendron campanulatum from Nepal. J Tradit Med 2011, 6(6):252-8.
• [40]Ertürk O, Karakaş FP, Pehli̇van D, Nas N: The antibacterial and antifungal effects of Rhododendron derived mad honey and extracts of four Rhododendron species. Turk J Biol 2009, 33(2):151-8.
• [41]Nisar M, Ali S, Qaisar M: Antibacterial and cytotoxic activities of the methanolic extracts of Rhododendron arboreum. J Med Plants Res 2013, 7(8):398-403.
• [42]Ramakrishna A, Ravishankar GA: Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 2011, 6(11):1720-31.
• [43]Xu Z, Zhou G, Shimizu H: Plant responses to drought and rewatering. Plant Signal Behav 2010, 5(6):649-54.
• [44]Wu J, Wang C, Mei X: Stimulation of taxol production and excretion in Taxus spp cell cultures by rare earth chemical lanthanum. J Biotechnol 2001, 85(1):67-73.
• [45]Peñaflor M, Bento JMS: Herbivore-induced plant volatiles to enhance biological control in agriculture. Neotrop Entomol 2013, 42(4):331-43.
• [46]Ribera AE, Zuñiga G: Induced plant secondary metabolites for phytopatogenic fungi control: a review. J Soil Sci Plant Nutr 2012, 12:893-911.