Skip to main content
Log in

Isolation of endophytic streptomycetes from above- and belowground organs of Quercus serrata

  • Original Article
  • Published:
Journal of Forest Research

Abstract

The occurrence and localization of endophytic actinomycetes within diverse organs of host plants provide ecological information that can be used to evaluate the significance of their spatial habitats. The aim of this study was to isolate and characterize endophytic actinomycetes in different organs of Quercus serrata. For this purpose, actinomycete isolates were obtained from surface-sterilized tissues of both symptomless seedlings and aged trees of Q. serrata and rhizosphere soil of the sampled seedlings. Thirty-five isolates with the ability to sporulate, including 4 from leaves of the aged trees, 10, 6, and 15 from leaves, stems, and roots of the seedlings, respectively, and 8 soil-derived isolates, were selected and characterized. The 16S rDNA nucleotide sequence analyses revealed that all of them belonged to the genus Streptomyces. According to a neighbor-joining phylogenetic tree constructed based on the results, the isolates of plant origin were divided into three major clades with high bootstrap values of 98 or 99 %, whereas eight soil-derived isolates were located at different positions from those of the endophyte isolates. Moreover, two larger clades were formed, one of which contained isolates derived only from aboveground parts, while the other contained isolates from all of the organs. These results suggest that the endophytic streptomycetes in Q. serrata may differ in their habitat positions (i.e., either above- or belowground parts).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Berg G, Krechel A, Ditz M, Sikora R, Ulrich A, Hallmann J (2005) Endophytic and ectophytic potato-associated bacterial communities differ in structure and antagonistic function against plant pathogenic fungi. FEMS Microbiol Ecol 51:215–229

    Article  PubMed  CAS  Google Scholar 

  • Bieber B, Nuske J, Ritzau M, Grafe U (1998) Alnumycin, a new naphthoqionone antibiotic, produced by Streptomyces sp. J Antibiot 51:381–382

    Article  PubMed  CAS  Google Scholar 

  • Brunckhorst J (1886) Über einige Wuerzelanschwellungen, besonders diejenigen von Alnus und den Elaeagnaceen. Unters Botan Inst Tübingen 2:151–177

    Google Scholar 

  • Cao L, Qui Z, Dai X, Tan H, Lin Y, Zhou S (2004) Isolation of endophytic actinomycetes from roots and leaves of banana (Musa acuminata) plants and their activities against Fusarium oxysporum f. sp. cubense. World J Microbiol Biotechnol 20:501–504

    Article  CAS  Google Scholar 

  • Conn VM, Franco CMM (2004) Analysis of the endophytic actinobacterial population in the roots of wheat (Triticum aestivum L.) by terminal restriction fragment length polymorphism and sequencing of 16S rRNA clones. Appl Environ Microbiol 70:1787–1794

    Article  PubMed  CAS  Google Scholar 

  • Coombs JT, Franco CMM (2003) Isolation and identification of actinobacterial from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608

    Article  PubMed  CAS  Google Scholar 

  • de Araújo JM, da Silva AC, Azevedo JL (2000) Isolation of endophytic actinomycetes from roots and leaves of maize (Zea mays L.). Braz Arch Biol Technol 43:447–451

    Article  Google Scholar 

  • Emerson R (1941) An experimental study of the life cycles and taxonomy of Allomyces. Lioydia 4:77–144

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gu Q, Zhen W, Huang Y (2007) Glycomyces sambucussp. nov., and endophytic actinomycetes isolated from the stem of Sambucus adnatawall. Int J Syst Evol Microbiol 57:1995–1998

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa S, Meguro A, Nishimuta T, Kunoh H (2004) Drought tolerance of tissue-cultured seedlings of mountain laurel (Kalmia latifolia L.) induced by an endophytic actinomycete. I. Enhancement of osmotic pressure in leaf cells. Actinomycetelogica 18:43–47

    Article  Google Scholar 

  • Hasegawa S, Meguro A, Nishimuta T, Kunoh H (2005) Drought tolerance of tissue-cultured seedlings of mountain laurel (Kalmia latifolia L.) induced by an endophytic actinomycete. II. Acceleration of callose accumulation and lignification. Actinomycetelogica 19:13–17

    Article  CAS  Google Scholar 

  • Hasegawa S, Meguro A, Shimizu M, Nishimura T, Kunoh H (2006) Endophytic actinomycetes and their interactions with host plants. Actinomycetologica 20:72–81

    Article  CAS  Google Scholar 

  • Hayakawa M, Nonomura H (1987) Humic acid–vitamin agar, a new medium for the selective isolation of soil actinomycetes. J Ferment Technol 65:501–509

    Article  CAS  Google Scholar 

  • Igarashi Y, Ogawa M, Sato Y, Saito N, Yoshida R, Kunoh H, Onaka H, Furumai T (2000) Fistupyrone, a novel inhibitor of the infection of Chinese cabbage by Alternaria brassicicola, from Streptomyces sp. TP-A0569. J Antibiot 53:1117–1122

    Article  PubMed  CAS  Google Scholar 

  • Igarashi Y, Iida T, Yoshida R, Furumai T (2002) Pteridic acids A and B, novel plant growth promoters with auxin-like activity from Streptomyces hygroscopicus TP-A0451. J Antibiot 55:764–767

    Article  PubMed  CAS  Google Scholar 

  • Inderiati S, Muliani S (2008) Isolation and characterization of endophytic actinomycetes of tobacco plants. J Agrisistem 4:82–100

    Google Scholar 

  • Ishiyama D, Vujaklija D, Davies J (2004) Novel pathway of salicylate degradation by Streptomyces sp. strain WA46. Appl Environ Microbiol 70:1297–1306

    Article  PubMed  CAS  Google Scholar 

  • Ito S, Kawasato H (1978) Distribution of secondary forests in Japan. In: Paper on plant ecology to the memory of Dr. Kuniji Yoshioka. Group of plant ecology in Tohoku, Sendai, pp 281–284 (in Japanese)

  • Kunoh H (2002) Endophytic actinomycetes: attractive biocontrol agents. J Gen Plant Pathol 68:249–252

    Article  CAS  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichester, pp 115–175

    Google Scholar 

  • Loria R, Bukhalid A, Fry AB, King PR (1997) Plant pathogenicity in the genus Streptomyces. Plant Dis 81:836–846

    Article  Google Scholar 

  • Mano H, Morisaki H (2008) Endophytic bacteria in the rice plant. Microbes Environ 23:109–117

    Article  PubMed  Google Scholar 

  • Matsukuma S, Okuda T, Watanabe J (1994) Isolation of actinomycetes from pine litter layers. Actinomycetologica 8:57–65

    Article  Google Scholar 

  • Meguro A, Ohmura Y, Hasegawa S, Shimizu M, Nishimura T, Kunoh H (2006) An endophytic actinomycete, Streptomyces sp. MBR-52, that accelerates emergence and elongation of plant adventitious roots. Actinomycetologica 20:1–9

    Article  CAS  Google Scholar 

  • Miyadoh S (2001) Identification protocols of the genera of actinomycetes. In: The Society for Actinomycetes Japan (ed) Identification manual of actinomycetes. Business Center for Academic Societies Japan, Tokyo, pp 9–35 (in Japanese)

  • Nishimura T, Meguro A, Hasegawa S, Nakagawa Y, Shimizu M, Kunoh H (2002) An endophytic actinomycete, Streptomyces sp. AOK-30, isolated from mountain laurel and its antifungal activity. J Gen Plant Pathol 68:390–397

    Article  Google Scholar 

  • Okazaki T (2003) Studies on actinomycetes isolated from plant leaves. In: Kurtboke I (ed) Selective isolation of rare actinomycetes. National Library of Australia, Queensland, pp 102–121

    Google Scholar 

  • Petit JR, Jouzel J, Raynaud D, Barkov NI, Barnola JM, Basile I, Benders M, Chappellaz J, Davis M, Delaygue G, Delmotte M, Kotlyakov VM, Legrand M, Lipenkov VY, Lorius C, Pepin L, Ritz C, Saltzman E, Stievenard M (1999) Climate and atmospheric history of the past 420,000 years from the Vostock ice core, Antarctica. Nature 399:429–436

    Article  CAS  Google Scholar 

  • Polsinelli M, Mazza PG (1984) Use of membrane filters for selective isolation of actinomycetes from soil. FEMS Microbiol Lett 22:79–83

    Article  Google Scholar 

  • Sardi P, Saracchi M, Ouaroni S, Petrolini B, Borgonovoli GE, Merli S (1992) Isolation of endophytic Streptomycetes from surface-sterilized roots. Appl Environ Microbiol 58:2691–2693

    PubMed  CAS  Google Scholar 

  • Sasaki T, Igarashi Y, Saito N, Furumai T (2001a) TPU-0031-A and B, new antibiotics of the novobiocingroup produced by Streptomyces sp. TP-A0556. J Antibiot 54:441–447

    Article  PubMed  CAS  Google Scholar 

  • Sasaki T, Igarashi Y, Saito N, Furumai T (2001b) Cedamycins A and B, new antimicrobial antibiotics from Streptomyces sp. TP-A0456. J Antibiot 54:567–572

    Article  PubMed  CAS  Google Scholar 

  • Seo MY, Matsuda Y, Nakashima C, Ito S (2011) Taxonomic re-evaluation of Raffaelea quercivora isolates collected from mass mortality of oak trees in Japan. Mycoscience. doi:10.1007/s10267-011-0154-z

    Google Scholar 

  • Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39:23–32

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M (2011) Endophytic actinomycetes: biocontrol agents and growth promoters. In: Maheshwari DK (ed) Bacteria in agrobiology (plant growth responses). Springer, Dordrecht, pp 201–220

    Chapter  Google Scholar 

  • Shimizu M, Nakagawa T, Sato Y, Furumai T, Igarashi Y, Onaka H, Yoshida R, Kunoh H (2000) Studies on endophytic actinomycetes (1). Streptomyces sp. isolated from rhododendron and its antifungal activity. J Gen Plant Pathol 66:360–366

    Article  CAS  Google Scholar 

  • Shimizu M, Furumai T, Igarashi Y, Onaka H, Nishimura T, Yoshida R, Kunoh H (2001) Association of induced disease resistance of rhododendron seedlings with inoculation of Streptomyces sp. R-5 and treatment with actinomycin D and amphotericin B to the tissue-culture medium. J Antibiot 54:501–505

    Article  PubMed  CAS  Google Scholar 

  • Shimizu M, Meguro A, Hasegawa S, Nishimuta T, Kunoh H (2006) Disease resistance induced by nonantagonistic endophytes Streptomyces spp. on tissue-cultured seedlings of rhododendron. J Gen Plant Pathol 72:351–354

    Article  Google Scholar 

  • Shimizu M, Yazawa S, Ushijima Y (2009) A promising strain of endophytic Streptomyces sp. for biological control of cucumber anthracnose. J Gen Plant Pathol 75:27–36

    Article  Google Scholar 

  • Shirling EB, Gottlieb D (1966) Methods for characterization of Streptomyces species. Int J Syst Bacteriol 16:313–340

    Article  Google Scholar 

  • Taechowisan T, Peberdy JF, Lumyong S (2003) Isolation of endophytic actinomycetes from selected plants and their antifungal activity. World J Microbiol Biotechnol 19:381–385

    Article  CAS  Google Scholar 

  • Takahashi Y, Omura S (2003) Isolation of new actinomycete strains for the screening of new bioactive compounds. J Gen Appl Microbiol 49:141–154

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Thakur D, Yadav A, Gogoi BK, Bora TC (2007) Isolation and screening of Streptomyces in soil of protected forest areas from the state of Assam and Tripura, India, for antimicrobial metabolites. J Mycol Med 17:242–249

    Article  Google Scholar 

  • Tian XL, Cao LX, Tan HM, Han WQ, Chen M, Liu YH, Zhou SN (2007) Diversity of cultivated and uncultivated actinobacterial endophytes in the stems and roots of rice. Microb Ecol 53:700–707

    Article  PubMed  Google Scholar 

  • Ulrich K, Ulrich A, Ewald D (2008) Diversity of endophytic bacterial communities in poplar grown under field conditions. FEMS Microbiol Ecol 63:169–180

    Article  PubMed  CAS  Google Scholar 

  • van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • Verma VC, Gond SK, Kumar A, Mishra A, Kharwar RN, Gange AC (2009) Endophytic actinomycetes from Azadirachta indica A. Juss: isolation, diversity, and anti-microbial activity. Microb Ecol 57:749–756

    Article  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed  CAS  Google Scholar 

  • Williams ST, Sharpe ME, Holt JG, Murray GE, Brener DJ, Krieg NR, Mouldar JW, Pfenning NP, Sneath HA, Staley JT (1989) Bergey’s manual of systematic bacteriology, vol 4. Williams and Wilkins, Baltimore

    Google Scholar 

  • Zin NM, Sarmin NIM, Ghadin N, Basri DF, Sidik NM, Hess WM, Strobel GA (2007) Bioactive endophytic streptomycetes from the Malay Peninsula. FEMS Microbiol Lett 274:83–88

    Article  PubMed  CAS  Google Scholar 

  • Zinniel DK, Lambrecht P, Harris NB, Feng Z, Kuczmarski D, Higley P, Ishimaru CA, Arunakumari A, Barletta RG, Vidaver AK (2002) Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl Environ Microbiol 68:2198–2208

    Google Scholar 

Download references

Acknowledgments

We are grateful to the late Dr. K. Nakanishi of Mie University for his valuable suggestions. We are also grateful to Ms. T. Chikada (Life Science Research Center, Center for Molecular Biology and Genetics, Mie University) for sequencing the samples, and to Dr. H. Shimada (Mie Prefectural Research Institute) and the members of the Laboratory of Forest Pathology and Mycology, Mie University, for their field assistance. This research was partly supported by a Grant-in-Aid for Exploratory Research from JSPS to SI (22658048).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yosuke Matsuda.

About this article

Cite this article

Thongsandee, W., Matsuda, Y., Shimizu, M. et al. Isolation of endophytic streptomycetes from above- and belowground organs of Quercus serrata . J For Res 18, 179–189 (2013). https://doi.org/10.1007/s10310-012-0337-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10310-012-0337-2

Keywords

Navigation