Abstract
The interaction between a common soil yeast, Cryptococcus laurentii, and a slow-growing medicinal plant adapted to low-nutrient soils, Agathosma betulina (Berg.) Pillans, was studied. C. laurentii CAB 578 was isolated from the rhizosphere of wild A. betulina, and liquid chromatography-tandem mass spectrometry (LC-MS-MS) analysis revealed that the yeast was capable of producing polyamines, such as cadaverine and spermine, while growing in vitro in a chemically defined medium. Since the exogenous application of polyamines are known to impact on root growth, these findings supported the results obtained when axenic cultures of A. betulina seedlings were inoculated with C. laurentii CAB 578 and cultivated for 5 months under glasshouse conditions. The presence of the yeast increased root growth by 51%. Using soil dilution plates, it was demonstrated that yeast numbers were greater in the vicinity of the roots than in the bulk soil. In addition, fluoromicroscopy, in combination with the fluorescent probes Fungolight and Calcofluor white, revealed the presence of metabolic active yeast colonies on the rhizoplane 5 months after initiation of the experimentation. The study provided evidence for a symbiosis between C. laurentii and A. betulina.
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. Nucl Acids Res 25:3389–3402
Arena ME, Manca de Nadra MC (2001) Biogenic amine production by Lactobacillus. J Appl Microbiol 90:158–162
Bais HP, Sudha GS, Gokare AR (2000) Putrescine and silver nitrate influences shoot multiplication, in vitro flowering and endogenous titers of polyamines in Cichorium intybus L. cv. Lucknow local. J Plant Growth Regul 19:238–248
Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
Blommaert KLJ (1972) Buchu seed germination. S Afr J Bot 38:237–239
Botes AL, Lotter J, Rhode OHJ, Botha A (2005) Interspecies differences in the enantioselectivity of epoxide hydrolases in Cryptococcus laurentii (Kufferath) C.E. Skinner and Cryptococcus podzolicus (Bab’jeva & Reshetova) Golubev. Syst Appl Microbiol 28:27–33
Bryla DR, Duniway JM (1997) Growth, phosphorus uptake, and water relations of safflower and wheat infected with an arbuscular mycorrhizal fungus. New Phytol 136:581–590
Cavagnaro TR, Smith FA, Ayling SM, Smith SE (2003) Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phyt 157:127–134
Chaîneau CH, Morel JL, Oudot J (2000) Bioremediation and biodegradation: biodegradation of fuel oil hydrocarbons in the rhizosphere of maize. J Environ Qual 29:568–578
Chanway CP, Radley RA, Holl FB (1991) Inoculation of conifer seed with plant growth promoting Bacillus strains causes increased seedling emergence and biomass. Soil Biol Biochem 23:575–580
Cilliers CD, Botha A, Esler KJ, Boucher C (2005) Effects of alien plant management, fire and soil chemistry on selected soil microbial populations in the Table Mountain National Park, South Africa. S Afr J Bot 71:211–220
Cloete KJ, Valentine AJ, Blomerus LM, Botha A, Pèrez-Fernández MA (2007) Nutritional effects of indigenous arbuscular mycorrhizal associations on the sclerophyllous species Agathosma betulina. Web Ecol 77:77–86
Collins NF, Graven EH, van Beek TA, Lelyveld GP (1996) Chemotaxonomy of commercial Buchu species (Agathosma betulina and A. crenulata). J Essent Oil Res 8:229–235
Cornelissen S, Botha A, Conradie WJ, Wolfaardt GM (2003) Shifts in community composition provide a mechanism for maintenance of soil yeast activity in the presence of elevated copper levels. Can J Microbiol 49:425–432
Couée I, Hummel I, Sulmon C, Gouesbet G, El Amrani A (2004) Involvement of polyamines in root development. Plant Cell Tiss Org 76:1–10
Du Plessis KR, Botha A, Joubert L-M, Bester R, Conradie WJ, Wolfaardt GM (2005) Response of the microbial community to copper oxychloride in acidic sandy loam soil. J Appl Microbiol 98:901–909
Eissenstat DM, Wells CE, Yanai RD, Whitbeck JL (2000) Building roots in a changing environment: implications for root longevity. New Phytol 147:33–42
El-Tarabily KA (2004) Suppression of Rhizoctonia solani diseases of sugar beet by antagonistic and plant growth-promoting yeasts. J Appl Microbiol 96:69–75
El-Tarabily KA, Sivasithamparam K (2006) Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Mycoscience 47:25–35
Evans PT, Malmberg RL (1989) Do polyamines have roles in plant development? Annu Rev Plant Phys Plant Mol Biol 40:235–269
Fell JW, Statzell-Tallman A (1998) Cryptococcus vuillemin. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study, fourth revised and enlarged edition. Elsevier Scientific, Amsterdam, pp 742–767
Fell JW, Boekhout T, Fonseca A, Scorzetti G, Statzell-Tallman A (2000) Biodiversity and systematics of basidiomycetous yeasts as determined by large subunit rDNA D1/D2 domain sequence analysis. Int J Syst Bacteriol 50:1351–1371
Fitter AH (1991) Characteristics and functions of root systems. In: Waisel J, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 1–27
Geneve RL, Kester ST (1991) Polyamines and adventitious root formation in the juvenile and mature phase of English ivy. J Exp Bot 42:71–75
Hewitt EJ (1966) Sand and water culture methods used in the study of plant nutrition, 2nd revised edition. Commonwealth Bureau of Horticulture and Plantation Crops, East Malling, Technical Communication No. 22, Commonwealth Agriculture Bureau, Farnham Royal, UK, pp 431–432
Hoffman CS, Winston F (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene 57:267–272
Jarvis BC, Shannon PR, Yasmin S (1983) Involvement of polyamines with adventitious root development in stem cuttings of mung bean. Plant Cell Physiol 24:677–683
Joubert L-M, Wolfaardt GM, Botha A (2006) Microbial exopolymers link predator and prey in a model yeast biofilm system. Microb Ecol 52:187–197
Kothari SK, Marschner H, George E (1990) Effect of VA mycorrhizal fungi and rhizosphere microorganisms on root and shoot morphology, growth and water relations in maize. New Phytol 116:303–311
Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: Influence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322
Kruger FJ (1979) South African heathlands. In: Specht RL (ed) Ecosystems of the world, Heathlands and related shrublands: descriptive studies, vol. 9A. Elsevier Scientific, New York, pp 19–80
Lachance MA, Starmer WT (1998) Ecology of yeasts. In: Kurtzman CP, Fell JW (eds) The yeasts, a taxonomic study. 4th edn. Elsevier Scientific, Amsterdam, pp 21–30
Linkohr BI, Williamson LC, Fitter AH, Leyser HMO (2002) Nitrogen and phosphorus availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760
Lis-Bachin M, Hart S, Simpson E (2001) Buchu (Agathosma betulina and A. crenulata, Rutaceae) essential oils: their pharmacological action on guinea-pig ileum and antimicrobial activity on microorganisms. J Pharm Pharmacol 53:579–582
López-Bucio J, Cruz-Ramýrez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287
Lubbe CM, Denman S, Lamprecht SC (2003) Fusarium wilt of Agathosma betulina newly reported in South Africa. Australas Plant Pathol 32:123–124
Lynch JP, Brown KM (2001) Topsoil foraging—an architectural adaptation of plants to low phosphorus availability. Plant Soil 237:225–237
Medina A, Vassileva M, Caravaca F, Roldán A, Azcón R (2004) Improvement of soil characteristics and growth of Dorycnium pentaphyllum by amendment with agrowastes and inoculation with AM fungi and/or the yeast Yarowia lipolytica. Chemosphere 56:449–456
Merkl N, Schultze-Kraft R, Arias M (2006) Effect of the tropical grass Brachiaria brizantha (Hochst. ex A. Rich.) Stapf on microbial population and activity in petroleum-contaminated soil. Microbiol Res 161:80–91
Mo H, Pua EC (2002) Up-regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. Physiol Plantarum 114:439–449
Moawad H, Salem SH, Badr El-Din SMS, Khater T, Iskandar M (1986) Yeasts in soils of Egypt. Zentralbl Mikrobiol 141:431–435
Nassar AH, El-Tarabily KA, Sivasithamparam K (2003) Growth promotion of bean (Phaseolus vulgaris L.) by a polyamine-producing isolate of Streptomyces griseoluteus. Plant Growth Regul 40:97–106
Nassar AH, El-Tarabily KA, Sivasithamparam K (2005) Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fert Soils 42:97–108
Price NS, Roncadori RW, Hussey RS (1989) Cotton root growth as influenced by phosphorus nutrition and vesicular-arbuscular mycorrhizas. New Phytol 111:61–66
Rajasekaran LR, Blake TJ (1998) Early growth invigoration of Jack pine seedlings by natural plant growth regulators. Trees-Struct Funct 12:420–423
Schefler WC (1979) Statistics for the biological sciences, 2nd edn. Addison-Wesley, Philippines
Sharma ML, Ali M (1998) Polyamines as modulators of soybean productivity. J Agron Crop Sci 181:189–191
Slocum RD, Flores HE (1991) Uncommon polyamines in plants and other organisms. In: Slocum RD, Flores HE (eds) Biochemistry and physiology of polyamines in plants. CRC, Boca Raton, pp 121–136
Spreeth AD (1976) A revision of the commercially important Agathosma species. S Afr J Bot 42:109–119
Stock WD, Allsopp N (1992) Functional perspective of ecosystems. In: Cowling RM (ed) The ecology of Fynbos: nutrients, fire and diversity. Oxford University Press, Cape Town, SA, pp 241–259
Takashima M, Sugita T, Shinoda T, Nakase T (2003) Three new combinations from the Cryptococcus laurentii complex: Cryptococcus aureus, Cryptococcus carnescens and Cryptococcus peneaus. Int J Syst Evol Micr 53:1187–1194
Tiburcio AF, Campos JL, Figueras X, Besford RT (1993) Recent advances in the understanding of polyamine functions during plant development. Plant Growth Regul 12:331–340
Todorov D, Alexieva V, Karanov E (1998) Effect of putrescine, 4-PU-30, and abscisic acid on maize plants grown under normal, drought and rewatering conditions. J Plant Growth Regul 17:197–203
Van Rooyen G, Steyn H, de Villiers R (1999) Cederberg: Clanwilliam and Biedouw Valley, South African wild flower guide 10. Botanical Society of South Africa, Cape Town, SA
Van Wyk BE, van Oudtshoorn B, Gericke N (1997) Medicinal plants of South Africa. Briza, Pretoria, SA
Vreulink J, Esterhuyse A, Jacobs K, Botha A (2007) Soil properties that impact on yeast and actinomycete numbers in sandy low nutrient soils. Can J Microbiol 53:1369–1374
Watt M, Silk WK, Passioura JB (2006) Rates of root and organism growth, soil conditions, and temporal and spatial development of the rhizosphere. Ann Bot 97:839–855
Wen-Quan S (1989) Path analysis of relationship between the endogenous polyamines and lateral root initiation in apple seedlings. Acta Phytophysiol Sin 15:388–392
Wickerham LJ (1951) Taxonomy of yeasts, Technology Bulletin No. 1029
Yonghong X, An S, Yao X, Xiao K, Zhang C (2005) Short-time response in root morphology of Vallisneria natans to sediment type and water-column nutrient. Aquat Bot 81:85–96
Zheleva D, Tsonev T, Sergiev I, Karanov E (1994) Protective effect of exogenous polyamines against atrazine in pea plants. J Plant Growth Regul 13:203–211
Acknowledgments
We hereby acknowledge the financial assistance of the Department of Labor of the South African Government and The South African National Research Foundation.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(PPT 3.07 MB)
Rights and permissions
About this article
Cite this article
Cloete, K.J., Valentine, A.J., Stander, M.A. et al. Evidence of Symbiosis Between the Soil Yeast Cryptococcus laurentii and a Sclerophyllous Medicinal Shrub, Agathosma betulina (Berg.) Pillans. Microb Ecol 57, 624–632 (2009). https://doi.org/10.1007/s00248-008-9457-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-008-9457-9