Skip to main content
SpringerLink
Log in

Callus of East Indian sandalwood co-cultured with fungus Colletotrichum gloeosporioides accumulates santalenes and bisabolene

  • Short Communication
  • Published:
Trees Aims and scope Submit manuscript

Abstract

The inducible accumulation of desired products via in vitro cultures provides an experimental system for researching secondary metabolism in woody plants. This system is convenient, because environmental conditions can be strictly controlled. This is particularly important for East Indian sandalwood (Santalum album L.), a tree with desired sandal oil products that are restricted to the heartwood. In this study, we established a method to induce and proliferate callus from sandalwood shoot explants. Thidiazuron (TDZ) (0.2–1.5 mg/l) could induce the formation of callus, which proliferated rapidly within a month following three successive subcultures in liquid shake culture on Murashige and Skoog (MS) basal medium supplemented with 0.8–1.0-mg/l TDZ. Callus cultured in this liquid medium for 7 days was co-cultured with fungi, either Colletotrichum gloeosporioides or Penidiella kurandae. Gas chromatography–mass spectrometry (GC–MS) analysis of the solvent extract by chemical anhydrous diethyl ether of callus co-cultured with C. gloeosporioides showed the presence of santalenes and bisabolene, which are the precursors of santalol. However, another fungus, P. kurandae, could not induce santalenes or bisabolene. This study provides an opportunity to further studies on the santalene and bisabolene biosynthetic signaling pathway and the fungal endophyte–plant interaction in sandalwood.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Baldi A, Jain A, Gupta N, Srivastava AK, Bisaria VS (2008) Co-culture of arbuscular mycorrhiza-like fungi (Piriformospora indica, and Sebacina vermifera) with plant cells of Linum album, for enhanced production of podophyllotoxins: a first report. Biotechnol Lett 30:1671–1677

    Article  CAS  PubMed  Google Scholar 

  • Celedon JM, Chiang A, Yuen M, Diaz-Chavez ML, Madilao LL, Finnegan PM, Barbour EL, Bohlmann J (2016) Heartwood-specific transcriptome and metabolite signatures of tropical sandalwood (Santalum album) reveal the final step of (Z)-santalol fragrance biosynthesis. Plant J 86:289–299

    Article  CAS  PubMed  Google Scholar 

  • Choi D, Bostock RM, Avdiushko S, Hildebrand DF (1994) Lipid-derived signals that discriminate wound-and pathogen-responsive isoprenoid pathways in plants: methyl jasmonate and the fungal elicitor arachidonic acid induce different 3-hydroxy-3-methylglutaryl-coenzyme A reductase genes and antimicrobial isoprenoids in Solanum tuberosum L. Proc Nat Acad Sci USA 91:2329–2333

    Article  CAS  PubMed  Google Scholar 

  • Crovadore J, Schalk M, Lefort F (2012) Selection and mass production of Santalum album L. calli for induction of sesquiterpenes. Biotechnol Biotechnol Equip 26:2870–2874

    Article  CAS  Google Scholar 

  • Das S, Pal S, Mujib A, Sahoo SS, Ponde NR, Gupta S, Dey S (1999) A novel process for rapid mass propagation of the aromatic plant Santalum album in liquid media and bioreactor. Acta Hortic 502:281–288

    Article  Google Scholar 

  • Diaz-Chavez ML, Moniodis J, Madilao LL, Jancsik S, Keeling CI, Barbour EL, Ghisalberti EL, Plummer JA, Jones CG, Bohlmann J (2013) Biosynthesis of sandalwood oil: Santalum album CYP76F cytochromes P450 produce santalols and bergamotol. PLoS One 8:e75053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dornenburg IH, Knorr D (1995) Strategies for the improvement of secondary metabolite production in plant cell cultures. Enzyme Microb Technol 17:674–684

    Article  Google Scholar 

  • Howes MJR, Simmonds MSJ, Kite GC (2004) Evaluation of the quality of sandalwood essential oils by gas chromatography-mass spectrometry. J Chromatog A 1028:307–312

    Article  CAS  Google Scholar 

  • Jones CG, Moniodis J, Zulak KG, Scaffidi A, Plummer JA, Ghisalberti EL, Barbour E, Bohlmann J (2011) Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase TPS-a and TPS-b subfamilies, including santalene synthases. J Biol Chem 286:17445–17454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolewe ME, Gaurav V, Roberts SC (2008) Pharmaceutically active natural product synthesis and supply via plant cell culture technology. Mol Pharm 5:243–256

    Article  CAS  PubMed  Google Scholar 

  • Külheim C, Jones CG, Plummer JA, Ghisalberti EL, Barbour L, Bohlmann J (2014) Foliar application of methyl jasmonate does not increase terpenoid accumulation, but weakly elicits terpenoid pathway genes in sandalwood (Santalum album L.) seedlings. Plant Biotechnol 31:585–591

    Article  CAS  Google Scholar 

  • Kuramae-Izioka EE (1997) A rapid, easy and high yield protocol for total genomic DNA isolation from Colletotrichum gloeosporioides and Fusarium oxysporum for RAPD. Rev Unimar 19:683–689

    Google Scholar 

  • Liu WY, Chen SH, Li J, Yang XM, Yan C, Liu HJ (2018) A new β-tetralonyl glucoside from the Santalum album derived endophytic fungus Colletotrichum sp. GDMU-1. Nat Prod Res. https://doi.org/10.1080/14786419.2018.1452003

    Article  PubMed  Google Scholar 

  • Misra BB, Dey S (2013) Developmental variations in sesquiterpenoid biosynthesis in East Indian sandalwood tree (Santalum album L.). Trees 27:1071–1086

    Article  CAS  Google Scholar 

  • Misra BB, Dey S (2014) Immunolocalization of α-santalol in sandalwood. J Essen Oil Res 26:238–246

    Article  CAS  Google Scholar 

  • Misra BB, Dey S (2015) Biological activities of East Indian sandalwood tree, Santalum album. PeerJ 1. https://doi.org/10.7287/peerj.preprints.96v1

  • Misra BB, Dey S (2016) Culture of East Indian sandalwood tree somatic embryos in air-lift bioreactors for production of santalols, phenolics and arabinogalactan proteins. AoB Plants S5:plt025

    Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Ochi T, Shibata H, Higuti T, Kodama K, Kusumi T, Takaishi Y (2005) Anti Helicobacter pylori compounds from Santalum album. J Nat Prod 68:819–824

    Article  CAS  PubMed  Google Scholar 

  • Peeris M, Senarath W (2015) In vitro propagation of Santalum album L.. Eur J Biochem 213:743–748

    Google Scholar 

  • Phillips MA, Walter MH, Ralph SG, Dabrowska P, Luck K, Urós EM, Boland W, Strack D, Rodríguez-Concepción M, Bohlmann J, Gershenzon J (2007) Functional identification and differential expression of 1-deoxy-d-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies). Plant Mol Biol 65:243–257

    Article  CAS  PubMed  Google Scholar 

  • Roberts S, Kolewe ME (2010) Plant natural products from cultured multi potent cells. Nature Biotechnol 28:1175–1176

    Article  CAS  Google Scholar 

  • Rugkhla A, Jones MGK (1998) Somatic embryogenesis and plantlet formation in Santalum album and S. spicatum. J Exp Bot 49:563–571

    Article  CAS  Google Scholar 

  • Singh CK, Raj SR, Patil VR, Jaiswal PS, Subhash N (2013) Plant regeneration from leaf explants of mature sandalwood (Santalum album L.) trees under in vitro conditions. In Vitro Cell Dev Biol Plant 49:216–222

    Article  CAS  Google Scholar 

  • Smith BJ, Black LL (1990) Morphological, cultural, and pathogenic variation among Colletotrichum species isolated from strawberry. Plant Dis 74:69–76

    Article  Google Scholar 

  • Teixeira da Silva JA, Kher MM, Soner D, Page T, Zhang XH, Nataraj M, Ma GH (2016) Sandalwood: basic biology, tissue culture, and genetic transformation. Planta 243:847–887

    Article  CAS  PubMed  Google Scholar 

  • Valluri J (2009) Bioreactor production of secondary metabolites from cell cultures of periwinkle and sandalwood. In: Jain SM, Saxena PK (eds) Protocols for in vitro cultures and secondary metabolite analysis of aromatic and medicinal plants. Methods in molecular biology (methods and protocols), vol 547. Humana Press, Totowa, pp 325–335

    Google Scholar 

  • Weathers PJ, Towler MJ, Xu J (2010) Bench to batch: advances in plant cell culture for producing useful products. Appl Microbiol Biotechnol 85:1339–1351

    Article  CAS  Google Scholar 

  • Wei Y, Ming QL, Lin B, Rahman K, Zheng CJ, Han T, Qin LP (2016) Medicinal plant cell suspension cultures: pharmaceutical applications and high-yielding strategies for the desired secondary metabolites. Crit Rev Biotechnol 36:215–332

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc., New York, pp 315–322

    Google Scholar 

  • Wilson SA, Roberts SC (2012) Recent advances towards development and commercialization of plant cell culture processes for the synthesis of biomolecules. Plant Biotech J 10:249–268

    Article  CAS  Google Scholar 

  • Xu J, Ge X, Dolan MC (2011) Towards high-yield production of pharmaceutical proteins with plant cell suspension cultures. Biotechnol Adv 29:278–299

    Article  CAS  Google Scholar 

  • Xu M, He R, Peng Y, Zeng CB, Liu Y, Tang GH, Tang H (2017) Isolation and molecular identification of Colletotrichum gloeosporioides causing brown spot disease of Camellia oleifera in Hainan of China. J Phytopathol 165:380–386

    Article  CAS  Google Scholar 

  • Zhang YY, Yan HF, Niu MY, Cheng QW, Zhang XH, Teixeira da Silva JA, Ma GH (2018) Multiple strategies for increasing yields of essential oil and obtaining sandalwood terpenoids by biotechnological methods in sandalwood. Trees 32:21–29

    Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant numbers 31470685, 31270720, and 31100498), the Natural Science Foundation of Guangdong Province (S2012010009025), and a Guangdong Science and Technology project (2015B020231008).

Author information

Authors and Affiliations

  1. Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical Garden, The Chinese Academy of Sciences, Guangzhou, 510650, China

    Qingwei Cheng, Yuping Xiong, Meiyun Niu, Yueya Zhang, Haifeng Yan, Hanzhi Liang, Beiyi Guo, Xinhua Zhang & Guohua Ma

  2. University of Chinese Academy of Sciences, Beijing, 100039, China

    Qingwei Cheng, Yuping Xiong, Meiyun Niu, Yueya Zhang, Haifeng Yan & Beiyi Guo

  3. College of Horticulture and Landscape Architecture, Zhongkai University of Agriculture and Engineering, Guangzhou, 510225, China

    Hanzhi Liang & Youhua Xiong

  4. P.O. Box 7, Miki-cho Post Office, Miki-cho, 3011-2, Ikenobe, Kagawa-ken, 761-0799, Japan

    Jaime A. Teixeira da Silva

Authors
  1. Qingwei Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuping Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Meiyun Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yueya Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haifeng Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hanzhi Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Beiyi Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xinhua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jaime A. Teixeira da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Youhua Xiong
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Guohua Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Youhua Xiong or Guohua Ma.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Additional information

Communicated by Merkle.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, Q., Xiong, Y., Niu, M. et al. Callus of East Indian sandalwood co-cultured with fungus Colletotrichum gloeosporioides accumulates santalenes and bisabolene. Trees 33, 305–312 (2019). https://doi.org/10.1007/s00468-018-1758-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-018-1758-0

Keywords

Search

Navigation