Skip to main content

Advertisement

SpringerLink
Log in

Symbiotic in vitro seed propagation of Dendrobium: fungal and bacterial partners and their influence on plant growth and development

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The genus Dendrobium is one of the largest genera of the Orchidaceae Juss. family, although some of its members are the most threatened today. The reason why many species face a vulnerable or endangered status is primarily because of anthropogenic interference in natural habitats and commercial overexploitation. The development and application of modern techniques and strategies directed towards in vitro propagation of orchids not only increases their number but also provides a viable means to conserve plants in an artificial environment, both in vitro and ex vitro, thus providing material for reintroduction. Dendrobium seed germination and propagation are challenging processes in vivo and in vitro, especially when the extreme specialization of these plants is considered: (1) their biotic relationships with pollinators and mycorrhizae; (2) adaptation to epiphytic or lithophytic life-styles; (3) fine-scale requirements for an optimal combination of nutrients, light, temperature, and pH. This review also aims to summarize the available data on symbiotic in vitro Dendrobium seed germination. The influence of abiotic factors as well as composition and amounts of different exogenous nutrient substances is examined. With a view to better understanding how to optimize and control in vitro symbiotic associations, a part of the review describes the strong biotic relations of Dendrobium with different associative microorganisms that form microbial communities with adult plants, and also influence symbiotic seed germination. The beneficial role of plant growth-promoting bacteria is also discussed.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

AMF:

Arbuscular mycorrhizal fungi

C:

Carbon

CMA:

Cornmeal agar

DW:

Dry weight

FW:

Fresh weight

GA:

Gibberellin

GA3 :

Gibberellic acid

IAA:

Indole-3-acetic acid

ITS:

Internal transcribed spacer

MH:

Mycoheterotrophy

N:

Nitrogen

OMA:

Oatmeal agar

OMF:

Orchid mycorrhizal fungi

PGPR:

Plant growth-promoting rhizobacteria

PGR:

Plant growth regulator

PLB:

Protocorm-like body

SEM:

Scanning electron microscopy

Trp:

Tryptophan

References

  • Adams DG (2000) Symbiotic interactions. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria: their diversity in time and space. Kluwer Academic Publishers, Dordrecht, pp 523–561

    Google Scholar 

  • Adams DG, Duggan PS (2008) Cyanobacteria-bryophyte symbioses. J Exp Bot 59:1047–1058

    CAS  PubMed  Google Scholar 

  • Alabouvette C, Olivain C, Migheli Q, Steinberg C (2009) Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. New Phytol 184(3):529–544

    CAS  PubMed  Google Scholar 

  • Batty AL, Dixon KW, Brundrett M, Sivasithamparam K (2001) Long-term storage of mycorrhizal fungi and seed as a tool for the conservation of endangered Western Australian terrestrial orchids. Aust J Bot 49:619–628

    Google Scholar 

  • Becker-Hapak M, Troxtel E, Hoerter J, Eisenstark A (1997) RpoS-dependent overexpression of carotenoids from Erwinia herbicola in OxyR-deficient Escherichia coli. Biochem Biophys Res Commun 239:305–309

    CAS  PubMed  Google Scholar 

  • Bernard N (1900) Sur quelques germinations dificiles. Revue Générale Bot 12:108–120

    Google Scholar 

  • Beyrle HF, Smith SE, Peterson RL, Franco CMM (1995) Colonization of Orchis morio protocorms by mycorrhizal fungus: effects of nitrogen nutrition and glyphosate in modifying the responses. Can J Bot 73:1128–1140

    Google Scholar 

  • Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ (2004) Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc R Soc London B, Biol Sci 271:1799–1806

    CAS  Google Scholar 

  • Bonnardeaux Y, Brundrett M, Batty A, Dixon K, Koch J, Sivasithamparam K (2007) Diversity of mycorrhizal fungi of terrestrial orchids: compatibility webs, brief encounters, lasting relationships and alien invasions. Mycol Res 111:51–61

    PubMed  Google Scholar 

  • Bougoure J, Ludwig M, Brundrett M, Cliff J, Clode P, Kilburn M, Grierson P (2014) High-resolution secondary ion mass spectrometry analysis of carbon dynamics in mycorrhizas formed by an obligately myco-heterotrophic orchid. Plant, Cell Env 37:1223–1230

    CAS  Google Scholar 

  • Brundrett MC (1991) Mycorrhizas in natural ecosystems. In: Macfayden A, Begon M, Fitter AH (eds) Advances in ecological research, Academic Press, London 21:171–313

  • Burgeff H (1959) Mycorrhiza of orchids. In: Withner C (ed) The orchids: a scientific survey. The Roland Press, New York, pp 361–395

  • Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycorrhizas in orchids: evidence from plant-fungus carbon and nitrogen transfers in the green-leaved terrestrial orchid Goodyera repens. New Phytol 171:405–416

    CAS  PubMed  Google Scholar 

  • Chaotham C, Pongrakhananon V, Sritularak B, Chanvorachote P (2014) A bibenzyl from Dendrobium ellipsophyllum inhibits epithelial-to-mesenchymal transition and sensitizes lung cancer cells to anoikis. Anticancer Res 34(4):1931–1938

    CAS  PubMed  Google Scholar 

  • Chen RR, Lin XG, Shi YQ (2003) Research advances of orchid mycorrhizae. Chin J Applied Env Biol 9:97–101 (in Chinese with English abstract)

    Google Scholar 

  • Chen XM, Guo SX, Meng ZX (2008) Effects of the fungal elicitors on the growth of Dendrobium candidum protocorms. Chin Trad Herb Drugs 39:423–426 (in Chinese with English abstract)

    Google Scholar 

  • Chen XM, Dong HL, Hu KX, Sun ZR, Chen J, Guo SX (2010) Diversity and antimicrobial and plant-growth-promoting activities of endophytic fungi in Dendrobium loddigesii Rolfe. Plant Growth Regul 29:328–337

    Google Scholar 

  • Chen J, Hu KX, Hou XQ, Guo SX (2011) Endophytic fungi assemblages from 10 Dendrobium medicinal plants (Orchidaceae). World J Microbiol Biotechnol 27:1009–1016

    Google Scholar 

  • Chen J, Wang H, Guo SX (2012) Isolation and identification of endophytic and mycorrhizal fungi from seeds and roots of Dendrobium (Orchidaceae). Mycorrhiza 22:297–307

    PubMed  Google Scholar 

  • Chen CA, Chen CC, Shen CC, Chang HH, Chen YJ (2013a) Moscatilin induces apoptosis and mitotic catastrophe in human esophageal cancer cells. J Med Food 16(10):869–877

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Zhang LC, Xing YM, Wang YQ, Xing XK, Zhang DW, Liang HQ, Guo SX (2013b) Isolation and identification of endophytic and mycorrhizal fungi from seeds and roots of Dendrobium (Orchidaceae). PLoS One 8:e58268

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Qi H, Li JB, Yi YQ, Chen D, Hu XH, Wang ML, Sun XL, Wei XY (2014) Experimental study on Dendrobium candidum polysaccharides on promotion of hair growth. Zhongguo Zhong Yao Za Zhi 39(2):291–295 (in Chinese)

    PubMed  Google Scholar 

  • Clements MA (1988) Orchid mycorrhizal associations. Lindleyana 3:73–86

  • Cockburn W, Goh CJ, Avadhani PN (1985) Photosynthetic carbon assimilation in a shootless orchid, Chiloschista usneoides (Don) LDL: a variant on crassulacean acid metabolism. Plant Physiol 77:83–86

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dan Y, Meng ZX, Guo SX (2012) Effects of forty strains of Orchidaceae mycorrhizal fungi on growth of protocorms and plantlets of Dendrobium candidum and D. nobile. Afr J Microbiol Res 6:34–39

    Google Scholar 

  • Dearnaley J (2007) Further advances in orchid mycorrhizal research. Mycorrhiza 17:475–486

    PubMed  Google Scholar 

  • Dressler RL (1993) Phylogeny and classification of the orchid family. Deoscorides Press, Oregon

    Google Scholar 

  • Dressler RL (2005) How many orchid species? Selbyana 26:155–158

    Google Scholar 

  • Dycus A, Knudson L (1957) The role of the velamen of the aerial roots of orchids. Bot Gazette 119:78–87

    Google Scholar 

  • Ehling-Schulz M, Bilger W, Scherer S (1997) UV-B-induced synthesis of photoprotective pigments and extracellular polysaccharides in the terrestrial cyanobacterium Nostoc commune. J Bacteriol 179:1940–1945

    CAS  PubMed Central  PubMed  Google Scholar 

  • Faria DC, Dias AC, Melo IS, de Carvalho Costa FE (2013) Endophytic bacteria isolated from orchid and their potential to promote plant growth. World J Microbiol Biotechnol 29(2):217–221

    PubMed  Google Scholar 

  • Fay MF, Chase MW (2009) Orchid biology: from Linnaeus via Darwin to the 21st century. Ann Bot 104:359–364

    PubMed Central  PubMed  Google Scholar 

  • Fonnesbech M (1972) Growth hormones and propagation of Cymbidium in vitro. Physiol Plant 27:310–316

    CAS  Google Scholar 

  • Forsyth LM, Smith LJ, Aitken EA (2006) Identification and characterization of non-pathogenic Fusarium oxysporum capable of increasing and decreasing Fusarium wilt severity. Mycol Res 110:929–935

    PubMed  Google Scholar 

  • Galdiano Júnior RF, Pedrinho EAN, Castellane TCL, Lemos EGM (2011) Auxin-producing bacteria isolated from the roots of Cattleya walkeriana, an endangered Brazilian orchid, and their role in acclimatization. Rev Bras Ciência Solo 35:729–737

    Google Scholar 

  • Galdiano Júnior RF, Lemos EGM, Faria RT, Vendrame WA (2012) Cryopreservation of Dendrobium hybrid seeds and protocorms as affected by phloroglucinol and Supercool X1000. Sci Hortic 148:154–160

    Google Scholar 

  • Gebauer G, Meyer M (2003) 15N and 13C natural abundance of autotrophic and myco-heterotrophic orchids provides insights into nitrogen and carbon gain from fungal association. New Phytol 160:209–223

    CAS  Google Scholar 

  • Gong CY, Yu ZY, Lu B, Yang L, Sheng YC, Fan YM, Ji LL, Wang ZT (2014) Ethanol extract of Dendrobium chrysotoxum Lindl ameliorates diabetic retinopathy and its mechanism. Vascul Pharmacol 62(3):134–142

    CAS  PubMed  Google Scholar 

  • Guo SX, Xu JT (1990) Effects of fungi and its liquid extract on seed germination of Dendrobium hancockii Rolf. J Chin Mat Med 15(7397–7399):445 (in Chinese with English abstract)

    Google Scholar 

  • He XH, Duan YH, Chen YL, Xu MG (2010) A 60-year journey of mycorrhizal research in China: past, present and future directions. Sci China Life Sci 53:1374–1398

    PubMed  Google Scholar 

  • Henskens FL, Green TG, Wilkins A (2012) Cyanolichens can have both cyanobacteria and green algae in a common layer as major contributors to photosynthesis. Ann Bot 110:555–563

    CAS  PubMed Central  PubMed  Google Scholar 

  • Homolka L (2013) Methods of cryopreservation in fungi. In: Gupta VK, Tuohy MG, Ayyachamy M, Turner KM, O’Donovan A (eds) Laboratory protocols in fungal biology current methods in fungal biology. Springer, NY, p 604

    Google Scholar 

  • Hossain MM, Kant R, Van PT, Winarto B, Zeng SJ, Teixeira da Silva JA (2013) The application of biotechnology to orchids. Critical Rev Plant Sci 32(2):69–139

    CAS  Google Scholar 

  • Hsu JL, Lee YJ, Leu WJ, Dong YS, Pan SL, Uang BJ, Guh JH (2014) Moniliformediquinone induces in vitro and in vivo antitumor activity through glutathione involved DNA damage response and mitochondrial stress in human hormone refractory prostate cancer. J Urol 191(5):1429–1438

    CAS  PubMed  Google Scholar 

  • Hynson NA, Madsen TP, Selosse MA, Adam IKU, Ogura-Tsujita Y, Roy M, Gebauer G (2013) The physiological ecology of mycoheterotrophy in mycoheterotrophy. In: Merckx VSFT (ed) The biology of plants living on fungi. Springer Science + Business Media, New York, pp 297–343

    Google Scholar 

  • Jin H, Xu ZX, Chen JH, Han SF, Ge S, Luo YB (2009) Interaction between tissue-cultured seedlings of Dendrobium officinale and mycorrhizal fungus (Epulorhiza sp.) during symbiotic culture. Chin J Plant Ecol 33:433–441 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Kamemoto H, Kuehnle AR, Amore TD (1999) Breeding Dendrobium orchids in Hawaii. University of Hawai‘i Press, Honolulu, p 166

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant-Microbe Interact 19:250–256

    CAS  PubMed  Google Scholar 

  • Kang ZH, Han SF, Han ZM (2007) Effects of orchidaceous Rhizoctonias on the growth of Dendrobium candidum. J Nanjing For Univ (Nat Sci) 31:49–52

    Google Scholar 

  • Katiyar RS, Sharma GD, Mishra RR (1986) Mycorrhizal infections of epiphytic orchids in tropical forests of Meghalaya (India). J Ind Bot Soc 65:329–334

    Google Scholar 

  • Kavroulakis N, Ntougias S, Zervakis GI, Ehaliotis C, Haralampidis K, Papadopoulou KK (2007) Role of ethylene in the protection of tomato plants against soil-borne fungal pathogens conferred by an endophytic Fusarium solani strain. J Exp Bot 58:3853–3864

    CAS  PubMed  Google Scholar 

  • Kew (Royal Botanic Gardens) (2011) World checklist of selected plant families. http://apps.kew.org/wcsp/incfamilies.do. Accessed 26 April 2015

  • Kharitonova IP (1999) Phytoncidal activity of prchids. Okhorona i kul’tivuvannya orkhidei (Preservation and Cultivation of Orchids). Kiev: Nauk. Dumka, pp. 131–133 (in Russian)

  • Kim JH, Oh SY, Han SB, Uddin GM, Kim CY, Lee JK (2014) Anti-inflammatory effects of Dendrobium nobile derived phenanthrenes in LPS-stimulated murine macrophages. DOI, Arch Pharm Res. doi:10.1007/s12272-014-0511-5

    Google Scholar 

  • Knudson L (1921) La germinación simbiótica de las semillas de orquideas. Bol Real Soc Española Hist Nat 21:250–260

    Google Scholar 

  • Knudson L (1922) Nonsymbiotic germination of orchid seeds. Bot Gazette 73:1–25

    Google Scholar 

  • Knudson L (1925) Physiological study of the symbiotic germination of orchid seeds. Bot Gazette 79:345–379

    CAS  Google Scholar 

  • Knudson L (1946) A new nutrient solution for germination of orchid seed. Am Orch Soc Bull 15:214–217

    CAS  Google Scholar 

  • Kolomeitseva GL, Tsavkelova EA, Gusev EM, Malina NE (2002) On symbiosis of orchids and active isolate of the bacterium Bacillus pumilus in culture in vitro. Bull GBS Russian Acad Sci 183:117–126 (in Russian with English abstract)

    Google Scholar 

  • Kolomeitseva GL, Antipina VA, Shirokov AI, Khomutovskiy MI, Babosha AV, Riabchenko AS (2012) The orchid seeds: development, structure, germination. Geos, Moscow, p 352 (in Russian)

  • Kowitdamrong A, Chanvorachote P, Sritularak B, Pongrakhananon V (2013) Moscatilin inhibits lung cancer cell motility and invasion via suppression of endogenous reactive oxygen species. Biomed Res Int 2013:765–894

    Google Scholar 

  • Kravchenko LV, Azarova TS, Makarova NM, Tikhonovich IA (2004) The effect of tryptophan of plant root metabolites on the phytostimulating activity of rhizobacteria. Mikrobiologiia 73:156–158 (in English) and 195–198 (in Russian)

  • Kuga Y, Sakamoto N, Yurimoto H (2014) Stable isotope cellular imaging reveals that both live and degenerating fungal pelotons transfer carbon and nitrogen to orchid protocorms. New Phytol 202:594–605

    CAS  PubMed  Google Scholar 

  • Kumar P, Rawat GS, Wood HP (2011) Diversity and ecology of Dendrobiums (Orchidaceae) in Chotanagpur plateau. India. Taiwania 56(1):23–36

    Google Scholar 

  • Li GJ, Sun P, Wang Q, Qian Y, Zhu K, Zhao X (2014) Dendrobium candidum Wall. ex Lindl. attenuates CCl4-induced hepatic damage in imprinting control region mice. Exp Ther Med 8(3):1015–1021

    PubMed Central  PubMed  Google Scholar 

  • Liebel HT, Bidartondo MI, Preiss K, Segreto R, Stöckel M, Rodda M, Gebauer G (2010) C and N stable isotope signatures reveal constraints to nutritional modes in orchids from the Mediterranean and Macaronesia. Am J Bot 97:903–912

    CAS  PubMed  Google Scholar 

  • Lin X, Shaw PC, Sze SC, Tong Y, Zhang Y (2011) Dendrobium officinale polysaccharides ameliorate the abnormality of aquaporin 5, pro-inflammatory cytokines and inhibit apoptosis in the experimental Sjögren’s syndrome mice. Int Immunopharmacol 11(12):2025–2032

    CAS  PubMed  Google Scholar 

  • Lin J, Chang YJ, Yang WB, Yu AL, Wong CH (2014) The multifaceted effects of polysaccharides isolated from Dendrobium huoshanense on immune functions with the induction of interleukin-1 receptor antagonist (IL-1ra) in monocytes. PLoS One 9(4):e94040

    PubMed Central  PubMed  Google Scholar 

  • Lin X, Liu J, Chung W, Sze SC, Li H, Lao L, Zhang Y (2015) Polysaccharides of Dendrobium officinale induce aquaporin 5 translocation by activating M3 muscarinic receptors. Planta Med 81(2):130–137

    CAS  PubMed  Google Scholar 

  • Lindblad P (2009) Cyanobacteria in symbiosis with cycads. In: Pawlowski K (ed) Prokaryotic symbionts in plants: microbiological monographs, vol 8. Springer, Dordrecht, pp 225–233

    Google Scholar 

  • Liu HX, Luo YB, Liu H (2010) Studies of mycorrhizal fungi of Chinese orchids and their role in orchid conservation in China—a review. Bot Rev 76:241–262

    Google Scholar 

  • Liu XF, Zhu J, Ge SY, Xia LJ, Yang HY, Qian YT, Ren FZ (2011) Orally administered Dendrobium officinale and its polysaccharides enhance immune functions in BALB/c mice. Nat Prod Commun 6(6):867–870

    CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    CAS  PubMed  Google Scholar 

  • Lv GY, Xia CQ, Chen SH, Su J, Liu XP, Li B, Gao JL (2013) Effect of Dendrobium officinale granule on long-term-alcohol-induced hypertension rats. Zhongguo Zhong Yao Za Zhi 38(20):3560–3565 (in Chinese)

    PubMed  Google Scholar 

  • Maor R, Haskin S, Levi-Kedmi H, Sharon A (2004) In planta production of indole-3-acetic acid by Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 70:852–854

    Google Scholar 

  • Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse MA (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Mol Ecol 21(20):5098–5109

    PubMed  Google Scholar 

  • Mehdipour Moghaddam MJ, Emtiazi G, Salehi Z (2012) Enchanced auxin production by Azospirillum pure cultures from plant root exudates. J Agr Sci Technol 14:985–994

    Google Scholar 

  • Merckx VS, Janssens SB, Hynson NA, Specht CD, Bruns TD, Smets EF (2012) Mycoheterotrophic interactions are not limited to a narrow phylogenetic range of arbuscular mycorrhizal fungi. Mol Ecol 21(6):1524–1532

    PubMed  Google Scholar 

  • Miyazawa M, Shimamura H, Nakamura S, Sugiura W, Kosaka H, Kameoka H (1999) Moscatilin from Dendrobium nobile, a naturally occurring bibenzyl compound with potential antimutagenic activity. J Agric Food Chem 47:2163–2167

    CAS  PubMed  Google Scholar 

  • Mohanty P, Das MC, Kumaria S, Tandon P (2012) High-efficiency cryopreservation of the medicinal orchid Dendrobium nobile Lindl. Plant Cell Tissue Organ Cult 109:297–305

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ng TB, Liu JY, Wong JH, Ye XJ, Sze SCW, Tong Y, Zhang KY (2012) Review of research on Dendrobium, a prized folk medicine. Appl Microbiol Biotechnol 93:1795–1803

    CAS  PubMed  Google Scholar 

  • Noel ARA (1974) Aspects of cell wall structure and development of velamen in Ansellia gigantean Reichb F. Ann Bot 38:495–504

    Google Scholar 

  • Nogueira RE, Pereira OL, Kasuya MCM, Lanna MCS, Mendonça MP (2005) Fungos micorrízicos associados a orquídeas em campos rupestres na região do Quadrilátero Ferrífero, MG, Brazil. Acta Bot Bras 19(3):417–424 (in Portuguese)

    Google Scholar 

  • Nontachaiyapoom S, Sasirat S, Manoch L (2010) Isolation and identification of Rhizoctonia-like fungi from roots of three orchid genera, Paphiopedilum, Dendrobium and Cymbidium, collected in Chiang Rai and Chiang Mai provinces of Thailand. Mycorrhiza 20:459–471

    PubMed  Google Scholar 

  • Nontachaiyapoom S, Sasirat S, Manoch L (2011) Symbiotic seed germination of Grammatophyllum speciosum Blume and Dendrobium draconis Rchb. f., native orchids of Thailand. Sci Hortic 130:303–308

    Google Scholar 

  • Nurfadilah S, Swarts ND, Dixon KW, Lambers H, Merritt DJ (2013) Variation in nutrient-acquisition patterns by mycorrhizal fungi of rare and common orchids explains diversification in a global biodiversity hotspot. Ann Bot 111:1233–1241

    CAS  PubMed Central  PubMed  Google Scholar 

  • Olivain C, Alabouvette C (1997) Colonization of tomato by a non-pathogenic strain of Fusarium oxysporum. New Phytol 137:481–494

    Google Scholar 

  • Otero JT, Ackerman JD, Bayman P (2002) Diversity and host specificity of endophytic Rhizoctonia-like fungi from tropical orchids. Am J Bot 89(11):1852–1858

    CAS  Google Scholar 

  • Otero JT, Mosquera TA, Flanagan NS (2013) Tropical orchid mycorrhizae: potential applications in orchid conservation, commercialization, and beyond. Lankesteriana 13(1–2):57–63

    Google Scholar 

  • Pan LH, Li XF, Wang MN, Zha XQ, Yang XF, Liu ZJ, Luo YB, Luo JP (2014) Comparison of hypoglycemic and antioxidative effects of polysaccharides from four different Dendrobium species. Int J Biol Macromol 64:420–427

    CAS  PubMed  Google Scholar 

  • Pant B (2013) Medicinal orchids and their uses: tissue culture a potential alternative for conservation. African J Plant Sci 7(10):448–467

    Google Scholar 

  • Parthibhan S, Senthil Kumar T, Rao MV (2015) Phenology and reintroduction strategies for Dendrobium aqueum Lindley—an endemic, near threatened orchid. J Nature Conserv 24:68–71

    Google Scholar 

  • Pereira MC, Pereira OL, Costa MD, Rocha RB, Kasuya MCM (2009) Diversidade de fungos micorrízicos Epulorhiza spp. isolados de Epidendrum secundum (Orchidaceae). Rev Bras Ciên Solo 33(5):1187–1197 (in Portuguese)

  • Peterson RL, Currah RS (1990) Synthesis of mycorrhizae between protocorms of Goodyera repens (Orchidaceae) and Ceratobasidium cereale. Can J Bot 68:1117–1125

    Google Scholar 

  • Pridgeon AM (1986) Anatomical adaptations in Orchidaceae. Lindleyana 1:96–101

    Google Scholar 

  • Pritchard HW (1984) Liquid nitrogen preservation of terrestrial and epiphytic orchid seed. CryoLetters 5:295–300

    Google Scholar 

  • Qian XP, Zha XQ, Xiao JJ, Zhang HL, Pan LH, Luo JP (2014) Sulfated modification can enhance antiglycation abilities of polysaccharides from Dendrobium huoshanense. Carbohydr Polym 101:982–989

    CAS  PubMed  Google Scholar 

  • Rai A, Bergman B (2002) Creation of new nitrogen-fixing cyanobacterial associations. Biol Env Proc Royal Irish Acad 102:65–68

    Google Scholar 

  • Rasmussen HN (1995) Terrestrial orchids: from seed to mycotrophic plant. Cambridge University Press, Cambridge

    Google Scholar 

  • Rasmussen HN, Rasmussen FN (2014) Seedling mycorrhiza: a discussion of origin and evolution in Orchidaceae. Bot J Linn Soc 175:313–327

    Google Scholar 

  • Rasmussen HN, Whigham DF (1993) Seed ecology of dust seeds in situ: a new study technique and its application in terrestrial orchids. Amer J Bot 80:1374–1378

    Google Scholar 

  • Rasmussen HN, Whigham DF (2002) Phenology of roots and mycorrhiza in orchid species differing in phototrophic strategy. New Phytol 154:797–807

    Google Scholar 

  • Rikkinen J (2013) Molecular studies on cyanobacterial diversity in lichen symbioses. MycoKeys 6:3–32

    Google Scholar 

  • Roberts DL, Dixon KW (2008) Orchids. Curr Biol 18:R325–R329

    CAS  PubMed  Google Scholar 

  • Roy A, Tripathy P, Adhikary SP (1998) UV protecting pigment of epilithic cyanobacteria occuring on the various regions of India. In: Subramanian G, Kaushik BD, Venkataraman GS (eds) Cyanobacterial Biotechnology, Proceedings of an International Symposium, Sep 18-21. ISBN 81-204-1269-9, Oxford & IBH publishing, New Delhi, pp 439–447

  • Ryan MJ, Smith D (2007) Cryopreservation and freeze-drying of fungi employing centrifugal and shelf freeze-drying. Methods Mol Biol 368:127–140

    CAS  PubMed  Google Scholar 

  • Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res 2011:1–21

    Google Scholar 

  • Sandmann G, Kuhn S, Boger P (1998) Evaluation of structurally different carotenoids in Escherichia coli transformants as protectants against UV-B radiation. Appl Environ Microbiol 64:1972–1974

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sanford WW, Adanlawo I (1973) Velamen and exodermis characters of West African epiphytic orchids in relation to taxonomic grouping and habitat tolerance. Bot J Linn Soc 66:307–321

    Google Scholar 

  • Sattayasai N, Sudmoon R, Nuchadomrong S, Chaveerach A, Kuehnle AR, Mudalige-Jayawickrama RG, Bunyatratchata W (2009) Dendrobium findleyanum agglutinin: production, localization, anti-fungal activity and gene characterization. Plant Cell Rep 28:1243–1252

    CAS  PubMed  Google Scholar 

  • Selosse MA, Martos F, Perry BA, Padamsee M, Roy M, Pailler T (2010) Saprotrophic fungal symbionts in tropical achlorophyllous orchids: finding treasures among the ‘molecular scraps’? Plant Signal Behav 5:349–353

    PubMed Central  PubMed  Google Scholar 

  • Selosse MA, Boullard B, Richardson D (2011) Noël Bernard (1874–1911): orchids to symbiosis in a dozen years, one century ago. Symbiosis 54:61–68

    Google Scholar 

  • Singh A, Duggal S (2009) Medicinal orchids: an overview. Ethnobotanical Leaflets 13:351–363

    Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, New York

    Google Scholar 

  • Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York

    Google Scholar 

  • Song JY, Guo SX (2001) Effects of fungus on the growth of Dendrobium candidum and D. nobile in vitro culture. Acta Acad Med Sin 23(6):547–551 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Song JI, Kang YJ, Yong HY, Kim YC, Moon A (2012) Denbinobin, a phenanthrene from Dendrobium nobile, inhibits invasion and induces apoptosis in SNU-484 human gastric cancer cells. Oncol Rep 27(3):813–818

    CAS  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. Microbiol Rev 31:425–448

    CAS  Google Scholar 

  • Stewart SL, Zettler LW (2002) Symbiotic germination of three semiaquatic rein orchids (Habenaria repens, H. quinquiseta, H. macroceratitis) from Florida. Aquat Bot 72:25–35

    Google Scholar 

  • Stöckel M, Tesitelova T, Jersakova J, Bidartondo MI, Gebauer G (2014) Carbon and nitrogen gain during the growth of orchid seedlings in nature. New Phytol 202:606–615

    PubMed  Google Scholar 

  • Stoessl A, Arditti J (1984) Orchid phytoalexins. In: Arditti J (ed) Orchid biology: reviews and perspectives. Cornell University Press, New York, pp 151–175

    Google Scholar 

  • Sukphan P, Sritularak B, Mekboonsonglarp W, Lipipun V, Likhitwitayawuid K (2014) Chemical constituents of Dendrobium venustum and their antimalarial and anti-herpetic properties. Nat Prod Commun 9(6):825–827

    CAS  PubMed  Google Scholar 

  • Sun J, Zhang F, Yang M, Zhang J, Chen L, Zhan R, Li L, Chen Y (2014) Isolation of α-glucosidase inhibitors including a new flavonol glycoside from Dendrobium devonianum. Nat Prod Res 28(21):1900–1905

    CAS  PubMed  Google Scholar 

  • Sundin GW, Jacobs JL (1999) Ultraviolet radiation (UVR) sensitivity analysis and UVR survival strategies of a bacterial community from the phyllosphere of field-grown peanut (Arachis hypogeae L.). Microb Ecol 38:27–38

    PubMed  Google Scholar 

  • Swangmaneecharern P, Serivichyaswat P, Nontachaiyapoom S (2012) Promoting effect of orchid mycorrhizal fungi Epulorhiza isolates on seed germination of Dendrobium orchids. Sci Hortic 148:55–58

    Google Scholar 

  • Swarts ND, Dixon KW (2009) Terrestrial orchid conservation in the age of extinction. Ann Bot 104:543–556

    PubMed Central  PubMed  Google Scholar 

  • Tan XM, Wang CL, Chen XM, Zhou YQ, Wang YQ, Luo AX, Liu ZH, Guo SX (2014) In vitro seed germination and seedling growth of an endangered epiphytic orchid, Dendrobium officinale, endemic to China using mycorrhizal fungi (Tulasnella sp.). Sci Hortic 165:62–68

    Google Scholar 

  • Teixeira da Silva JA, Kerbauy GB, Zeng SJ, Chen ZL, Duan J (2014a) In vitro flowering of orchids. Crit Rev Biotechnol 34:56–76

    PubMed  Google Scholar 

  • Teixeira da Silva JA, Zeng SJ, Dobránszki J, Galdiano R Jr, Cardoso JC, Vendrame WA (2014b) In vitro conservation of Dendrobium germplasm. Plant Cell Rep 33(9):1413–1423

    CAS  PubMed  Google Scholar 

  • Teixeira da Silva JA, Zeng SJ, Dobránszki J, Cardoso JC, Kerbauy GB (2014c) In vitro flowering of Dendrobium. Plant Cell Tiss Org Cult 119:447–456

    CAS  Google Scholar 

  • Teixeira da Silva JA, Dobránszki J, Cardoso JC, Zeng SJ (2015) Dendrobium micropropagation: a review. Plant Cell Rep 34:671–704

    CAS  Google Scholar 

  • Tian CC, Zha XQ, Pan LH, Luo JP (2013) Structural characterization and antioxidant activity of a low-molecular polysaccharide from Dendrobium huoshanense. Fitoterapia 91:247–255

    CAS  PubMed  Google Scholar 

  • Touchell DH, Dixon KW (1993) Cryopreservation of seed of Western Australian native species. Biodiversity Conserv 2:594–602

    Google Scholar 

  • Tsai AC, Pan SL, Liao CH, Guh JH, Wang SW, Sun HL, Liu YN, Chen CC, Shen CC, Chang YL, Teng CM (2010) Moscatilin, a bibenzyl derivative from the India orchid Dendrobrium loddigesii, suppresses tumor angiogenesis and growth in vitro and in vivo. Cancer Lett 292(2):163–170

    CAS  PubMed  Google Scholar 

  • Tsavkelova EA (2011) Bacteria associated with orchid roots. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin, pp 221–259

    Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Lobakova ES, Kolomeitseva GL, Netrusov AI (2001) Microbiota of orchid rhizoplane. Microbiology 70:492–497 (in English) and 567–573 (in Russian)

  • Tsavkelova EA, Alexandrova AV, Cherdyntseva TA, Kolomeitseva GL, Netrusov AI (2003a) Fungi associated with orchid roots in greenhouse conditions. Mycol Phytopathol 37:57–63 (in Russian with English abstract)

    Google Scholar 

  • Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2003b) Phytohormones production by the fungi associated with orchids. Mycol Phytopathol 37:75–83 (in Russian with English abstract)

    CAS  Google Scholar 

  • Tsavkelova EA, Lobakova ES, Kolomeitseva GL, Cherdyntseva TA, Netrusov AI (2003c) Localization of associative cyanobacteria in the roots of epiphytic orchids. Microbiology 86:91–104 (in English) and 99–104 (in Russian)

  • Tsavkelova EA, Lobakova ES, Kolomeitseva GL, Cherdyntseva TA, Netrusov AI (2003d) Associative cyanobacteria, isolated from the roots of epiphytic orchids. Microbiology 72:92–97 (in English) and 105–110 (in Russian)

  • Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2004) Bacteria associated with the roots of epiphytic orchids. Microbiology 73:710–715 (in English) and 825–831 (in Russian)

  • Tsavkelova EA, Klimova YS, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:133–143 (in English) and 133–143 (in Russian)

  • Tsavkelova EA, Cherdyntseva TA, Klimova SYu, Shestakov AI, Botina SG, Netrusov AI (2007) Orchid-associated bacteria produce indole-3-acetic acid, promote seed germination, and increase their microbial yield in response to exogenous auxin. Arch Microbiol 188:655–664

    CAS  PubMed  Google Scholar 

  • Tsavkelova EA, Bömke C, Netrusov AI, Weiner J, Tudzynski B (2008) Production of gibberellic acids by an orchid-associated Fusarium proliferatum strain. Fung Gen Biol 45:1393–1403

    CAS  Google Scholar 

  • Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y, Tudzynski B, Sharon A (2012) Identification and functional characterization of the genes for indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fung Gen Biol 49:48–57

    CAS  Google Scholar 

  • Tudzynski B, Sharon A (2002) Biosynthesis, biological role and application of fungal hormones. In: Osiewacz HD (ed) The Mycota X: industrial applications. Springer-Verlag, Berlin, pp 183–211

    Google Scholar 

  • Vakhrameeva MG, Tatarenko IV, Varlygina TI, Torosyan GK, Zagulskii MN (2008) Orchids of Russia and Adjacent Countries (within the Borders of the Former USSR). A.R.G Ganter Verlag, Ruggell 690 pp

    Google Scholar 

  • Vendrame WA, Carvalho VS, Dias JMM, Maguire I (2008) Pollination of Dendrobium hybrids using cryopreserved pollen. HortScience 43(1):264–267

    Google Scholar 

  • Venkateswarlu S, Raju MS, Subbaraju GV (2002) Synthesis and biological activity of isoamoenylin, a metabolite of Dendrobium amoenum. Biosci Biotechnol Biochem 66:2236–2238

    CAS  PubMed  Google Scholar 

  • Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma–plant–pathogen interactions. Soil Biol Biochem 40:1–10

    CAS  Google Scholar 

  • Vujanovic V, St-Arnaud M, Barabé D, Thibeault G (2000) Viability testing of orchid seed and the promotion of coloration and germination. Ann Bot 86:79–86

    Google Scholar 

  • Wang J, Ge J, Liu F, Bian H, Huang C (1998) Cryopreservation of seeds and protocorms of Dendrobium candidum. CryoLetters 19:123–128

    Google Scholar 

  • Wang H, Fang H, Wang Y, Duan L, Guo S (2011) In situ seed baiting techniques in Dendrobium officinale Kimuraet Migo and Dendrobium nobile Lindl.: the endangered Chinese endemic Dendrobium (Orchidaceae). World J Microbiol Biotechnol 27:2051–2059

    Google Scholar 

  • Wang Q, Sun P, Li G, Zhu K, Wang C, Zhao X (2014) Inhibitory effects of Dendrobium candidum Wall ex Lindl. on azoxymethane- and dextran sulfate sodium-induced colon carcinogenesis in C57BL/6 mice. Oncol Lett 7(2):493–498

    PubMed Central  PubMed  Google Scholar 

  • Warcup J (1981) The mycorrhizal relationships of Australian orchids. New Phytol 87:371–381

    Google Scholar 

  • Waterman RJ, Bidartondo MI (2008) Deception above, deception below: linking pollination and mycorrhizal biology of orchids. J Exp Bot 59:1085–1096

    CAS  PubMed  Google Scholar 

  • Wilkinson KG, Dixon KW, Sivasithamparam K (1989) Interaction of soil bacteria, mycorrhizal fungi and orchid seed in relation to germination of Australian orchids. New Phytol 112:429–435

    Google Scholar 

  • Wilkinson KG, Dixon KW, Sivasithamparam K, Ghisalberti EL (1994) Effect of IAA on symbiotic germination of an Australian orchid and its production by orchid-associated bacteria. Plant Soil 159:291–295

    CAS  Google Scholar 

  • Wu JP, Qian J, Zheng SZ (2002) A preliminary study on ingredient of secretion from fungi of orchid mycorrhizal. Chin J Applied Ecol 13(7):845–848

    CAS  Google Scholar 

  • Wu HF, Song XQ, Liu HX (2012) Ex-situ symbiotic seed germination of Dendrobium catenatum. Acta Ecol Sin 32(8):2491–2497 (in Chinese with English abstract)

    Google Scholar 

  • Xing YM, Chen J, Cui JL, Chen XM, Guo SX (2011) Antimicrobial activity and biodiversity of endophytic fungi in Dendrobium devonianum and Dendrobium thyrsiflorum from Vietman. Curr Microbiol 62:1218–1224

    CAS  PubMed  Google Scholar 

  • Xiong L, Cao ZX, Peng C, Li XH, Xie XF, Zhang TM, Zhou QM, Yang L, Guo L (2013) Phenolic glucosides from Dendrobium aurantiacum var. denneanum and their bioactivities. Molecules 18(6):6153–6160

    CAS  PubMed  Google Scholar 

  • Yang YL, Liu ZY, Zhu GS (2008) Study on symbiotic seed germination of Pleione bulbocodioides (Franch) Rolfe. Microbiology 35(6):909–912 (in Chinese with English abstract)

    Google Scholar 

  • Yang H, Lee PJ, Jeong EJ, Kim HP, Kim YC (2012) Selective apoptosis in hepatic stellate cells mediates the antifibrotic effect of phenanthrenes from Dendrobium nobile. Phytother Res 26:974–980

    PubMed  Google Scholar 

  • Yang LC, Lu TJ, Hsieh CC, Lin WC (2014a) Characterization and immunomodulatory activity of polysaccharides derived from Dendrobium tosaense. Carbohydr Polym 111:856–863

    CAS  PubMed  Google Scholar 

  • Yang S, Gong Q, Wu Q, Li F, Lu Y, Shi J (2014b) Alkaloids enriched extract from Dendrobium nobile Lindl. attenuates tau protein hyperphosphorylation and apoptosis induced by lipopolysaccharide in rat brain. Phytomedicine 21(5):712–716

    CAS  PubMed  Google Scholar 

  • Yang S, Zhang X, Cao Z, Zhao K, Wang S, Chen M, Hu X (2014c) Growth-promoting Sphingomonas paucimobilis ZJSH1 associated with Dendrobium officinale through phytohormone production and nitrogen fixation. Microb Biotechnol 7(6):611–620

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu J, Zhou XF, Yang SJ, Liu WH, Hu XF (2013) Design and application of specific 16S DNA-targeted primers for assessing endophytic diversity in Dendrobium officinale using nested PCR DGGE. Appl Microbiol Biotechnol 97:9825–9836

    CAS  PubMed  Google Scholar 

  • Yuan ZL, Chen YC, Yang Y (2009a) Diverse non-mycorrhizal fungal endophytes inhabiting an epiphytic, medicinal orchid (Dendrobium nobile): estimation and characterization. World J Microbiol Biotechnol 25:295–303

    Google Scholar 

  • Yuan ZQ, Zhang JY, Liu T (2009b) Phylogenetic relationship of China Dendrobium species based on the sequence of the internal transcribed spacer of ribosomal DNA. Biol Plant 53:155–158

    CAS  Google Scholar 

  • Zainuddin M, Julkifle AL, Pobathy R, Sinniah UR, Khoddamzadeh A, Antony JJ, Pavallekoodi J, Subramaniam S (2011) Preliminary analysis of cryopreservation of Dendrobium Bobby Messina orchid using an encapsulation dehydration technique with Evans blue assay. Afr J Biotechnol 10:11870–11878

    CAS  Google Scholar 

  • Zeng SJ, Wu KL, Teixeira da Silva JA, Zhang JX, Chen ZL, Xia NH, Duan J (2012) Asymbiotic seed germination, seedling development and reintroduction of Paphiopedilum wardii Sumerh., an endangered terrestrial orchid. Sci Hortic 138:198–209

    Google Scholar 

  • Zeng SJ, Zhang Y, Teixeira da Silva JA, Wu KL, Zhang JX, Duan J (2014) Seed biology and in vitro seed germination of Cypripedium. Crit Rev Biotechnol 34:358–371

    CAS  PubMed  Google Scholar 

  • Zhang L, Chen J, Lv Y, Gao C, Guo S (2012) Mycena sp., a mycorrhizal fungus of the orchid Dendrobium officinale. Mycol Progress 11(2):395–401

    Google Scholar 

  • Zhao MM, Zhang G, Zhang DW, Hsiao YY, Guo SX (2013) ESTs analysis reveals putative genes involved in symbiotic seed germination in Dendrobium officinale. PLoS One 8(8):e72705

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu GS, Yu ZN, Gui Y, Liu ZY (2008) A novel technique for isolating orchid mycorrhizal fungi. Fungal Div 33:123–137

    Google Scholar 

  • Zi XM, Sheng CL, Goodale UM, Shao SC, Gao JY (2014) In situ seed baiting to isolate germination-enhancing fungi for an epiphytic orchid Dendrobium aphyllum (Orchidaceae). Mycorrhiza 24:487–499

    CAS  PubMed  Google Scholar 

  • Zotz G, Winkler U (2013) Aerial roots of epiphytic orchids: the velamen radicum and its role in water and nutrient uptake. Oecologia 171:733–741

    PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank Dr. Meesawat Upatham (Prince of Songkla University, Thailand) for comments and opinions on an earlier version of the manuscript.

Conflict of interest

The authors declare no conflicts of interest.

Author information

Author notes

    Authors and Affiliations

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

      Jaime A. Teixeira da Silva

    2. Department of Microbiology, Faculty of Biology, Lomonosov Moscow State University, Leninskie gory 1-12, 119234, Moscow, Russia

      Elena A. Tsavkelova

    3. Key Laboratory of South China Agricultural Plant Molecular Analysis and Gene Improvement, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China

      Songjun Zeng

    4. School of Biomedical Sciences, Faculty of Medicine, The Chinese University of Hong Kong, Hong Kong, China

      Tzi Bun Ng

    5. Shenzhen Research Institute, The Chinese University of Hong Kong, Shenzhen, China

      Tzi Bun Ng

    6. Department of Plant Science, Bharathidasan University, Tiruchirappalli, 620 024, Tamil Nadu, India

      S. Parthibhan & M. V. Rao

    7. Research Institute of Nyíregyháza, University of Debrecen, Nyíregyháza, P.O. Box 12, 4400, Hungary

      Judit Dobránszki

    8. Department of Rural Development, Centro de Ciências Agrárias, UFSCar, Via Anhanguera, km 174, CP 153, Araras, CEP 13.600-970, Brazil

      Jean Carlos Cardoso

    Authors
    1. Jaime A. Teixeira da Silva
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Elena A. Tsavkelova
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Songjun Zeng
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Tzi Bun Ng
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. S. Parthibhan
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Judit Dobránszki
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Jean Carlos Cardoso
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. M. V. Rao
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Jaime A. Teixeira da Silva, Elena A. Tsavkelova, Songjun Zeng, Tzi Bun Ng, S. Parthibhan, Judit Dobránszki, Jean Carlos Cardoso or M. V. Rao.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Teixeira da Silva, J.A., Tsavkelova, E.A., Zeng, S. et al. Symbiotic in vitro seed propagation of Dendrobium: fungal and bacterial partners and their influence on plant growth and development. Planta 242, 1–22 (2015). https://doi.org/10.1007/s00425-015-2301-9

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00425-015-2301-9

    Keywords

    Search

    Navigation