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Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots

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Abstract

A plant-growth-promoting isolate of the yeast Williopsis saturnus endophytic in maize roots was found to be capable of producing indole-3-acetic acid (IAA) and indole-3-pyruvic acid (IPYA) in vitro in a chemically defined medium. It was selected from among 24 endophytic yeasts isolated from surface-disinfested maize roots and evaluated for their potential to produce IAA and to promote maize growth under gnotobiotic and glasshouse conditions. The addition of l-tryptophan (L-TRP), as a precursor for auxins, to the medium inoculated with W. saturnus enhanced the production of IAA and IPYA severalfold compared to an L-TRP-non-amended medium. The introduction of W. saturnus to maize seedlings by the pruned-root dip method significantly (P<0.05) enhanced the growth of maize plants grown under gnotobiotic and glasshouse conditions in a soil amended with or without L-TRP. This was evident from the increases in the dry weights and lengths of roots and shoots and also in the significant (P<0.05) increases in the levels of in planta IAA and IPYA compared with control plants grown in L-TRP-amended or non-amended soil. The plant growth promotion by W. saturnus was most pronounced in the presence of L-TRP as soil amendment compared to seedlings inoculated with W. saturnus and grown in soil not amended with L-TRP. In the glasshouse test, W. saturnus was recovered from inside the root at all samplings, up to 8 weeks after inoculation, indicating that the roots of healthy maize may be a habitat for the endophytic yeast. An endophytic isolate of Rhodotorula glutinis that was incapable of producing detectable levels of IAA or IPYA in vitro failed to increase the endogenous levels of IAA and IPYA and failed to promote plant growth compared to W. saturnus, although colonization of maize root tissues by R. glutinis was similar to that of W. saturnus. Both endophytic yeasts, W. saturnus and R. glutinis, were incapable of producing in vitro detectable levels of gibberellic acid, isopentenyl adenine, isopentenyl adenoside or zeatin in their culture filtrates. This study is the first published report to demonstrate the potential of an endophytic yeast to promote plant growth. This is also the first report of the production of auxins by yeasts endophytic in plant roots.

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References

  • Abd El-Hafez AE, Shehata SF (2001) Field evaluation of yeasts as a biofertilizer for some vegetable crops. Arab Univ J Agric Sci 9:169–182

    Google Scholar 

  • Andrews JH, Buck JW (2002) Adhesion of yeasts to leaf surfaces. Phyllosphere microbiology. American Phytopathological Society, St. Paul, pp 53–68

    Google Scholar 

  • Arras G, Scherm B, Migheli Q (2002) Improving biocontrol activity of Pichia guillermondii against post-harvest decay of oranges in commercial packing-houses by reduced concentrations of fungicides. Biocontrol Sci Technol 12:547–553

    Article  Google Scholar 

  • Arsac JF, Lamothe C, Mulard D, Fages J (1990) Growth enhancement of maize (Zea mays L.) through Azospirillum lipoferum inoculation: effect of plant genotype and bacterial concentration. Agronomie 10:649–654

    Article  Google Scholar 

  • Arshad M, Frankenberger WT Jr (1998) Plant growth regulating substances in the rhizosphere: microbial production and functions. Adv Agron 62:45–151

    Article  CAS  Google Scholar 

  • Bab'eva IP, Belyanin AI (1966) Yeasts of the rhizosphere. Mikrobiologia 35:712–720

    Google Scholar 

  • Bacon CW, Hinton DM (2002) Endophytic and biological control potential of Bacillus mojavensis and related species. Biol Control 23:274–284

    Article  CAS  Google Scholar 

  • Barea JM, Navarro E, Montoya E (1976) Production of plant growth regulators by rhizosphere phosphate-solubilizing bacteria. J Appl Bacteriol 40:129–134

    PubMed  CAS  Google Scholar 

  • Bashan Y, Holguin G (1997) Azospirillum-plant relationships: environmental and physiological advances. Can J Microbiol 43:103–121

    CAS  Google Scholar 

  • Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577

    Article  PubMed  CAS  Google Scholar 

  • Bastian F, Cohen A, Piccoli P, Luna V, Baraldi R, Bottini R (1998) Production of indole-3-acetic acid and gibberellins A1 and A3 by Acetobacter diazotrophicus and Herbaspirillum seropedicae in chemically-defined culture media. Plant Growth Regul 24:7–11

    Article  CAS  Google Scholar 

  • Bressan W, Borges MT (2004) Delivery methods for introducing endophytic bacteria into maize. Biocontrol 49:315–322

    Article  Google Scholar 

  • Buck JW, Lachance MA, Traquair JA (1998) Mycoflora of peach bark: population dynamics and composition. Can J Bot 76:345–354

    Article  Google Scholar 

  • Cao LX, You JL, Zhou SN (2002) Endophytic fungi from Musa acuminata leaves and roots in south China. World J Microbiol Biotechnol 18:169–171

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cleland RE (1990) Auxin and cell elongation. In: Davies PJ (ed) Plant hormones and their role in plant growth and development. Kluwer, Dordrecht, pp 132–148

    Google Scholar 

  • di Menna ME (1957) The isolation of yeasts from soil. J Gen Microbiol 17:678–688

    PubMed  Google Scholar 

  • El-Abyad MS, El-Sayed MA, El-Shanshoury AR, Farid M (1994) Optimization of culture conditions for indole-3-pyruvic acid production by Streptomyces griseoflavus. Can J Microbiol 40:754–760

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • El-Tarabily KA, Hardy GEStJ, Sivasithamparam K, Kurtböke ID (1996) Microbiological differences between limed and unlimed soils and their relationship with cavity spot disease of carrots (Daucus carota L.) caused by Pythium coloratum in Western Australia. Plant Soil 183:279–290

    Article  CAS  Google Scholar 

  • El-Tarabily KA, Nassar AH, Hardy GEStJ, Sivasithamparam K (2003) Fish emulsion as a food base for rhizobacteria promoting growth of radish (Raphanus sativus L. var sativus) in a sandy soil. Plant Soil 252:397–411

    Article  CAS  Google Scholar 

  • Fallik E, Okon Y, Epstein E, Goldman A, Fischer M (1989) Identification and quantification of IAA and IBA in Azospirillum brasilense-inoculated maize roots. Soil Biol Biochem 21:147–153

    Article  CAS  Google Scholar 

  • Fisher PJ, Petrini O, Scott HM (1992) The distribution of some fungal and bacterial endophytes in maize (Zea mays L.). New Phytol 122:299–305

    Article  Google Scholar 

  • Floch G, Rey P, Benizri E, Benhamou N, Tirilly Y (2003) Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant Soil 257:459–470

    Article  Google Scholar 

  • Frankenberger WT Jr, Poth M (1987) Biosynthesis of indole-3-acetic acid by the pine ectomycorrhizal fungus, Pisolithus tinctorius. Appl Environ Microbiol 53:2908–2913

    PubMed  CAS  Google Scholar 

  • Frankenberger WT Jr, Chang AC, Arshad M (1990) Response of Raphanus sativus to the auxin precursor, l-tryptophan applied to soil. Plant Soil 129:235–241

    CAS  Google Scholar 

  • Gomes NCM, Fagbola O, Costa R, Rumjanek NG, Buchner A, Mendona-Hagler L, Smalla K (2003) Dynamics of fungal communities in bulk and maize rhizosphere soil in the tropics. Appl Environ Microbiol 69:3758–3766

    Article  PubMed  CAS  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195

    PubMed  CAS  Google Scholar 

  • Guinn G, Brummett DL, Beier RC (1986) Purification and measurement of abscisic acid and indole-acetic acid by high performance liquid chromatography. Plant Physiol 81:997–1002

    PubMed  CAS  Google Scholar 

  • Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914

    CAS  Google Scholar 

  • Kaldorf M, Ludwig-Muller J (2000) AM fungi might affect the root morphology of maize by increasing indole-3-butyric acid biosynthesis. Physiol Plant 109:58–67

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Larran S, Monaco C, Alippi HE (2001) Endophytic fungi in leaves of Lycopersicon esculentum Mill. World J Microbiol Biotechnol 17:181–184

    Article  Google Scholar 

  • Larran S, Perello A, Simon MR, Moreno V (2002) Isolation and analysis of endophytic microorganisms in wheat (Triticum aestivum L.) leaves. World J Microbiol Biotechnol 18:683–686

    Article  CAS  Google Scholar 

  • Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151:67–73

    Article  CAS  Google Scholar 

  • Maria GL, Sridhar KR (2003) Endophytic fungal assemblage of two halophytes from west coast mangrove habitats, India. Czech Mycol 55:241–251

    Google Scholar 

  • Millonig G (1976) Laboratory manual of biological electron microscopy. Saviolo M (ed) Vercelli, Italy

    Google Scholar 

  • Mucciarelli M, Scannerini S, Bertea C, Maffei M (2003) In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol 158:579–591

    Article  Google Scholar 

  • Musson G, McInroy JA, Kloepper JW (1995) Development of delivery systems for introducing endophytic bacteria into cotton. Biocontrol Sci Technol 5:407–416

    Article  Google Scholar 

  • Nakamura T, Murakami T, Saotome M, Tomita K, Kitsuwa T, Meyers SP (1991) Identification of indole-3-acetic acid in Pichia spartinae, an ascosporogenous yeast from Spartina alterniflora marshland environments. Mycologia 83:662–664

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Nieto KF, Frankenberger WT Jr (1989) Biosynthesis of cytokinins in soil. Soil Sci Soc Am J 53:735–740

    CAS  Google Scholar 

  • Normanly J, Cohen JD, Fink GR (1993) Arabidopsis thaliana auxotrophs reveal a tryptophan-independent biosynthetic pathway for indole-3-acetic acid. Proc Natl Acad Sci U S A 90:10355–10359

    Article  PubMed  CAS  Google Scholar 

  • Payne C, Bruce A (2001) The yeast Debaryomyces hansenii as a short-term biological control agent against fungal spoilage of sawn Pinus sylvestris timber. Biol Control 22:22–28

    Article  Google Scholar 

  • Perondi NL, Luz WC, Thomas R (1996) Microbiological control of Gibberella in wheat. Fitopatol Bras 21:243–249

    Google Scholar 

  • Petersson S, Jonsson N, Schnürer J (1999) Pichia anomala as a biocontrol agent during storage of high-moisture feed grain under airtight conditions. Postharvest Biol Technol 15:175–184

    Article  Google Scholar 

  • Petrini O (1991) Fungal endophytes of tree leaves. In: Andrews JH, Hirano SS (eds) Microbial ecology of leaves. Springer, Berlin Heidelberg New York, pp 179–197

    Google Scholar 

  • Prikryl Z, Vancura V, Wurst M (1985) Auxin formation by rhizosphere bacteria as a factor of root growth. Biol Plant 27:159–163

    Article  CAS  Google Scholar 

  • Rennie RJ, De Freitas JR, Ruschel AP, Vose PB (1982) Isolation and identification of N2-fixing bacteria associated with sugar cane (Saccharum sp.). Can J Microbiol 28:462–467

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Sarwar M, Frankenberger WT Jr (1994) Influence of l-tryptophan and auxins applied to the rhizosphere on the vegetative growth of Zea mays L. Plant Soil 160:97–104

    Article  CAS  Google Scholar 

  • Sivasithamparam K (1998) Root cortex—the final frontier for the biocontrol of root-rot with fungal antagonists: a case study on a sterile red fungus. Annu Rev Phytopathol 36:439–452

    Article  PubMed  CAS  Google Scholar 

  • Srinivasan M, Petersen DJ, Holl FB (1996) Influence of indoleacetic-acid-producing Bacillus isolates on the nodulation of Phaseolus vulgaris by Rhizobium etli under gnotobiotic conditions. Can J Microbiol 42:1006–1014

    Article  CAS  Google Scholar 

  • Stone JK, Bacon CW, White JF Jr (2000) An overview of endophytic microbes: endophytism defined. In: Bacon CW, White JF Jr (eds) Microbial endophytes. Marcel Dekker, New York, USA, pp 3–29

    Google Scholar 

  • Strzelczyk E, Pokojska-Burdziej A (1984) Production of auxins and gibberellin-like substances by mycorrhizal fungi, bacteria and actinomycetes isolated from soil and the mycorrhizosphere of pine (Pinus silvestris L.). Plant Soil 81:185–194

    Article  CAS  Google Scholar 

  • Sturz AV, Christie BR, Matheson BG (1998) Associations of bacterial endophyte populations from red clover and potato crops with potential for beneficial allelopathy. Can J Microbiol 44:162–167

    Article  CAS  Google Scholar 

  • Sturz AV, Christie BR, Nowak J (2000) Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19:1–30

    Article  Google Scholar 

  • Suslow TV, Schroth MN (1982) Rhizobacteria of sugar beets: effects of seed application and root colonization on yield. Phytopathology 72:199–206

    Google Scholar 

  • Tian XL, Cao LX, Tan HM, Zeng QG, Jia YY, Han WQ, Zhou SN (2004) Study on the communities of endophytic fungi and endophytic actinomycetes from rice and their antipathogenic activities in vitro. World J Microbiol Biotechnol 20:303–309

    Article  Google Scholar 

  • Tien TM, Gaskings 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

    PubMed  CAS  Google Scholar 

  • Urquhart EJ, Punja ZK (2002) Hydrolytic enzymes and antifungal compounds produced by Tilletiopsis species, phyllosphere yeasts that are antagonists of powdery mildew fungi. Can J Microbiol 48:219–229

    Article  PubMed  CAS  Google Scholar 

  • Varma A, Verma S, Sudha, Sahay N, Butehorn B, Franken P (1999) Piriformospora indica, a cultivable plant-growth-promoting root endophyte. Appl Environ Microbiol 65:2741–2744

    PubMed  CAS  Google Scholar 

  • Wellington EMH, Williams ST (1978) Preservation of actinomycete inoculum in frozen glycerol. Microbios Lett 6:151–157

    Google Scholar 

  • Wickerham LJ (1951) Taxonomy of yeasts. Tech Bull No 1029. US Department of Agriculture, Washington, DC, pp 1–56

    Google Scholar 

  • Zahir ZA, Arshad M, Azam M, Hussain A (1997) Effect of an auxin precursor tryptophan and Azotobacter inoculation on yield and chemical composition of potato under fertilized conditions. J Plant Nutr 20:745–752

    CAS  Google Scholar 

  • Zakharova EA, Shcherbakov AA, Brudnik VV, Skripko NG, Bulkhin NS, Ignatov VV (1999) Biosynthesis of indole-3-acetic acid in Azospirillum brasilense: insights from quantum chemistry. Eur J Biochem 259:572–576

    Article  PubMed  CAS  Google Scholar 

  • Zinniel DK, Lambrecht P, Harris NB, Feng ZY, 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank the United Arab Emirates University Research Council for financial support (grant number 03-04-2-11/04). We would like to thank the laboratory and field staff at the University of United Arab Emirates for their valuable assistance. We would like also to thank A. Gbewonyo and S. Tariq from the Electron Microscopy Unit, Faculty of Medicine and Health Sciences, United Arab Emirates University, for their assistance in the preparation of transmission electron microscope specimens.

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, United Arab Emirates University, 17551, Al-Ain, United Arab Emirates

    Amr H. Nassar & Khaled A. El-Tarabily

  2. Department of Botany, Faculty of Science, University of Ain Shams, Cairo, 11566, Egypt

    Amr H. Nassar

  3. Soil Science and Plant Nutrition, School of Earth and Geographical Sciences, Faculty of Natural and Agricultural Sciences, University of Western Australia, 35 Stirling Highway, Crawley, Western Australia, 6009, Australia

    Krishnapillai Sivasithamparam

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  1. Amr H. Nassar
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Nassar, A.H., El-Tarabily, K.A. & Sivasithamparam, K. Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fertil Soils 42, 97–108 (2005). https://doi.org/10.1007/s00374-005-0008-y

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