Abstract
Germination of orchid seeds is a complex process. In this paper we focus on interactions between the host-plant and its bacterial partners via indole-3-acetic acid (IAA). Originally isolated from the roots of the epiphytic orchid Dendrobium moschatum, the strains of Rhizobium, Microbacterium, Sphingomonas, and Mycobacterium genera were among the most active IAA producers. Addition of exogenous tryptophan significantly enhanced auxin formation both in mineral and complex media. The presence of IAA and indole-3-acetaldehyde was confirmed by HPLC. Indole-3-pyruvic and indole-3-lactic acids were also detected in supernatants of culture filtrates of Sphingomonas sp., Rhizobium sp., and Microbacterium sp., while indole-3-acetamide was identified only in Mycobacterium sp. Some concentration- and strain-dependent effects of exogenous IAA on bacterial development were also established. Treatment of the cultures with 10 and 100 μg/ml of auxin resulted in an increase in microbial yield. None of the investigated strains was able to utilize IAA as a source of carbon and energy. Furthermore, inoculation of D. moschatum seeds with Sphingomonas sp. and Mycobacterium sp. resulted in considerable enhancement of orchid seeds germination. This growth-promoting activity was observed in the absence of any plant growth stimulators or mycorrhizal fungi, usually required for orchid germination.
Similar content being viewed by others
References
Arditti J (1967) Niacin biosynthesis in germinating Laeliocattleya orchid embryos and young seedlings. Am J Bot 54:291–298
Ayyadurai N, Ravindra Naik P, Sreehari Rao M, Sunish Kumar R, Samrat SK, Manohar M, Sakthivel N (2006) Isolation and characterization of a novel banana rhizosphere bacterium as fungal antagonist and microbial adjuvant in micropropagation of banana. J Appl Microbiol 100:926–937
Bar T, Okon Y (1993) Tryptophan conversion via indole-3-acetamide in Azospirillum brasilense Sp7. Can J Microbiol 39:81–86
Barea JM, Navarro E, Montoya E (1981) Production of plant growth regulators by rhizosphere phosphate-solubilizing bacteria. J Appl Bact 40:129–134
Berliner MD (1981) Hormone effects on Cosmarium botrytis cell division. Cytobios 30:89–99
Brandl MT, Lindow SE (1996) Cloning and characterization of a locus encoding an indolepyruvate decarboxylase involved in indole-3-acetic acid synthesis in Erwinia herbicola. Appl Environ Microbiol 62:4121–4128
Burgeff H (1959) Mycorrhiza of orchids. In: Withner C (ed) The orchids: a scientific survey. The Roland Press, New York, pp 361–395
Cacciari I, Lippi D, Pietrosanti T, Pietrosanti W (1989) Phytohormone-like substances produced by single and mixed diazotrophic cultures of Azospirillum and Arthrobacter. Plant Soil 115:151–153
Clements MA (1988) Orchid mycorrhizal associations. Lindleyana 3:73–86
Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant associated bacteria. Crit Rev Microbiol 21:1–18
Davies PJ (1995) The plant hormone concept: concentration, sensitivity, and transport. In: Davies PJ (ed) Plant hormones: physiology, biochemistry, and molecular biology. Kluwer Academic Publishers, Dordrecht, pp 13–18
Egebo LA, Nielsen SVS, Jochimsen B (1991) Oxygen-dependent catabolism of indole-3-acetic acid in Bradyrhizobium japonicum. J Bacteriol 173:4897–4901
Faria RT, Valle Rego L, Bernardi A, Molinari H (2001) Performance of differents genotyps of Brazilian orchid cultivation in alternative substrates. Brazil Archiv Biol Technol 44:337–342
Fonnesbech M (1972) Growth hormones and propagation of Cymbidium in vitro. Physiol Plant 27:310–316
Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796
Glickmann E, Gardan L, Jacquet S, Hussain S, Elasri M, Petit A, Dessaux Y (1998) Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol Plant Microbe Interact 11:156–162
Hadley G, Harvais G (1968) The effect of certain growth substances on asymbiotic germination and development of Orchis purpurella. New Phytol 67:441–445
Halda-Alija L (2003) Identification of indole-3-acetic acid producing freshwater wetland rhizosphere bacteria associated with Juncus effuses L. Can J Microbiol 49:781–787
Hill DS, Stein JI, Torkewitz NR, Morse AM, Howell CR, Pachlatko JP, Becker JO, Ligon JM (1994) Cloning of genes involved in the synthesis of pyrrolnitrin from Pseudomonas fluorescens and role of pyrrolnitrin synthesis in biological control of plant disease. Appl Environ Microbiol 60:78–85
Ivanova EG, Doronina NV, Trotsenko IuA (2001) Aerobic methylobacteria are capable of synthesizing auxins. Mikrobiologia 70:452–458
Jaeger CH, Lindow SE, Miller W, Clark E, Firestone MK (1999) Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Appl Environ Microbiol 65:2685–2690
Jensen JB, Egsgaard H, Van Onckelen H, Jochimsen BU (1995) Catabolism of indole-3-acetic acid and 4- and 5-chloroindole-3-acetic acid in Bradyrhizobium japonicum. J Bacteriol 177:5762–5766
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
Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480
Knudson L (1922) Nonsymbiotic germination of orchid seeds. Bot Gazette 73:1–25
Knudson L (1946) A new nutrient solution for germination of orchid seed. Am Orch Soc Bull 15:214–217
Koga J, Syono K, Ichikawa T, Adachi T (1994) Involvement of L-tryptophan aminotransferase in indole-3-acetic acid biosynthesis in Enterobacter cloacae. Biochim Biophys Acta 1209:241–247
Kravchenko LV, Azarova TS, Makarova NM, Tikhonovich IA (2004) The effect of tryptophan of plant root metabolites on the phytostimulating activity of rhizobacteria. Mikrobiologia 73:195–198
Leblond-Bourget N, Philippe H, Mangin I, Decaris B (1996) 16S rRNA and 16S to 23S internal transcribed spacer sequence analyses reveal inter- and intraspecific Bifidobacterium phylogeny. Int J Syst Bacteriol 46:102–111
Leveau JH, Lindow S E (2005) Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Appl Environ Microbiol 71:2365–2371
Libbert E, Risch H (1969) Interactions between plants and epiphytic bacteria regarding their auxin metabolism. V. Isolation and identification of the IAA-producing and destroying bacteria from pea plants. Physiol Plantarum 22:51–58
Liu P, Nester EW (2006) Indoleacetic acid, a product of transferred DNA, inhibits vir gene expression and growth of Agrobacterium tumefaciens C58. Proc Natl Acad Sci USA 103:4658–4662
Ma W, Zalec K, Glick BR (2001) Biological activity and colonization pattern of the bioluminescence-labeled plant growth-promoting bacterium Kluyvera ascorbata SUD165/26. FEMS Microbiol Ecol 35:137–144
Magie AR, Wilson EE, Kosuge T (1963) Indoleacetamide as an intermediate in the synthesis of indoleacetic acid in Pseudomonas savastanoi. Science 141:1281–1282
Manulis S, Haviv-Chesner A, Brandl MT, Lindow SE, Barash I (1998) Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol Plant Microbe Interact 11:634–642
Manulis S, Shafrir H, Epstein E, Lichter A, Barash I (1994) Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology 140:1045–1050
Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335
Mordukhova EA, Skvortsova NP, Kochetkov VV, Dubeikovskii AN, Boronin AM (1991) Synthesis of the phytohormone indole-3-acetic acid by rhizosphere bacteria of the genus Pseudomonas. Mikrobiologiia 60:494–500
Noel TC, Sheng C, Yost CK, Pharis RP, Hynes MF (1996) Rhizobium leguminosarum as a plant growth-promoting rhizobacterium: direct growth promotion of canola and lettuce. Can J Microbiol 42:279–283
Ona O, Van Impe J, Prinsen E, Vanderleyden J (2005) Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol Lett 246:125–132
Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220
Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801
Sergeeva E, Liaimer A, Bergman B (2002) Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215:229–238
Sessitsch A, Reiter B, Berg G (2004) Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can J Microbiol 50:239–249
Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.). Appl Environ Microbiol 37:1016–1024
Tsavkelova EA, Cherdyntseva TA, Botina SG, Netrusov AI (2007) Bacteria associated with orchid roots and microbial production of auxin. Microbiol Res 162:69–76
Tsavkelova EA, Cherdyntseva TA, Netrusov AI (2005) Auxin production by bacteria associated with orchid roots. Mikrobiologiia 74:46–53
Tsavkelova EA, Lobakova ES, Kolomeitseva GL, Cherdyntseva TA, Netrusov AI (2003) Localization of associative cyanobacteria on the roots of epiphytic orchids. Mikrobiologiia 72:86–91
Unno Y, Okubo K, Wasaki J, Shinano T, Osaki M (2005) Plant growth promotion abilities and microscale bacterial dynamics in the rhizosphere of Lupin analysed by phytate utilization ability. Environ Microbiol 7:396–404
Vande Broek A, Lambrecht M, Eggermont K, Vanderleyden J (1999) Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense. J Bacteriol 181:1338–1342
Weiler E, Schröder J (1987) Hormone genes and the crown gall disease. Trends Biochem Sci 12:271–275
White R (1987) Indole-3-acetic acid and 2-(indol-3-ylmethyl)indol-3-yl acetic acid in the thermophilic archaebacterium Sulfolobus acidocaldarius. J Bacteriol 169:5859–5860
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
Wilkinson KG, Dixon KW, Sivasithamparam K, Ghisalberti EL (1994a) Effect of IAA on symbiotic germination of an Australian orchid and its production by orchid-associated bacteria. Plant Soil 159:291–295
Wilkinson KG, Sivasithamparam K, Dixon KW, Fahy PC, Bradley JK (1994b) Identification and characterization of bacteria associated with western Australian orchids. Soil Biol Biochem 26:137–142
Williams MN, Signer ER (1990) Metabolism of tryptophan and tryptophan analogs by Rhizobium meliloti. Plant Physiol 92:1009–1013
Woodward AW, Bartel B (2005) Auxin: regulation, action and interaction. Ann Bot 95:707–735
Yasmin S, Rahman Bakar MA, Malik KA, Hafeez FY (2004) Isolation, characterization and beneficial effects of rice associated plant growth promoting bacteria from Zanzibar soils. J Basic Microbiol 44:241–252
Young JM, Kuykendall LD, Martinez-Romero E, Kerr A, Sawada H (2001) A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis Int J Syst Evol Microbiol 51:89–103
Acknowledgments
We are grateful to Dr. Elena Popova for helpful discussions and encouragement and to Dr. Gary Sawers, MPI-Marburg (Germany) for valuable commentary and critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Erko Stackebrandt.
Rights and permissions
About this article
Cite this article
Tsavkelova, E.A., Cherdyntseva, T.A., Klimova, S.Y. et al. 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 (2007). https://doi.org/10.1007/s00203-007-0286-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-007-0286-x