Archives of Microbiology

, Volume 198, Issue 5, pp 429–437 | Cite as

Indole-3-acetic acid biosynthetic pathways in the basidiomycetous yeast Rhodosporidium paludigenum

  • Pumin Nutaratat
  • Nantana SrisukEmail author
  • Panarat Arunrattiyakorn
  • Savitree Limtong
Original Paper


Microorganisms produce plant growth regulators, such as auxins, cytokinins and gibberellins, to promote plant growth. Auxins are a group of compounds with an indole ring that have a positive effect on plant growth. Indole-3-acetic acid (IAA) is a plant growth hormone classified as an indole derivative of the auxin family. IAA biosynthesis pathways have been reported and widely studied in several groups of bacteria. Only a few studies on IAA biosynthesis pathways have been conducted in yeast. This study aimed to investigate IAA biosynthesis pathways in a basidiomycetous yeast (Rhodosporidium paludigenum DMKU-RP301). Investigations were performed both with and without a tryptophan supplement. Indole compound intermediates were detected by gas chromatography–mass spectrometry. Indole-3-lactic acid and indole-3-ethanol were found as a result of the enzymatic reduction of indole-3-pyruvic acid and indole-3-acetaldehyde, in IAA biosynthesis via an indole-3-pyruvic acid pathway. In addition, we also found indole-3-pyruvic acid in culture supernatants determined by high-performance liquid chromatography. Identification of tryptophan aminotransferase activity supports indole-3-pyruvic acid-routed IAA biosynthesis in R. paludigenum DMKU-RP301. We hence concluded that R. paludigenum DMKU-RP301 produces IAA through an indole-3-pyruvic acid pathway.


Basidiomycetous yeast Red yeast Rhodosporidium Indole-3-acetic acid Biosynthetic pathway 



This work was supported by a Thailand Research Fund/TRF Research Team Promotion Grant (RTA 548009) under the title “Biodiversity and ecology of endophytic and epiphytic yeasts from leaves of agronomic crops in Thailand and production of plant growth promoting auxins by the selected promising strain with the elucidation of its biosynthetic pathway” and the Higher Education Research Promotion and National Research University Project of Thailand, Office of the Higher Education Commission.

Supplementary material

203_2016_1202_MOESM1_ESM.docx (44 kb)
Supplementary material 1 (DOCX 43 kb)
203_2016_1202_MOESM2_ESM.docx (18 kb)
Supplementary material 2 (DOCX 17 kb)


  1. Bau YS (1981) Indole compounds in Saccharomyces cerevisiae and Aspergillus niger. Bot Bull Acad Sin 22:123–130Google Scholar
  2. Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107CrossRefPubMedGoogle Scholar
  3. Brown HM, Purves WK (1980) Indoleacetaldehyde reductase of Cucumis sativus L: kinetic properties and role in auxin biosynthesis. Plant Physiol 65:107–113CrossRefPubMedPubMedCentralGoogle Scholar
  4. Carreno-Lopez R, Campos-Reales N, Elmerich C, Baca BE (2000) Physiological evidence for differently regulated tryptophan dependent pathways for indole-3-acetic acid synthesis in Azospirillum brasilense. Mol Gen Genet 264:521–530CrossRefPubMedGoogle Scholar
  5. Chung KR, Tzeng DD (2004) Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustilago esculenta. J Biol Sci 4:744–750CrossRefGoogle Scholar
  6. Cohen JD, Bandurski RS (1982) Chemistry and physiology of the bound auxins. Annu Rev Plant Physiol 33:403–430CrossRefGoogle Scholar
  7. Deslandes B, Gariépy C, Houde A (2001) Review of microbiological and biochemical effects of skatole on animal production. Livest Prod Sci 71:193–200CrossRefGoogle Scholar
  8. Duca D, Lorv J, Patten CL, Rose D, Glick BR (2014) Indole-3-acetic acid in plant–microbe interactions. Antonie Van Leeuwenhoek 106:85–125CrossRefPubMedGoogle Scholar
  9. Ebenau-Jehle C, Thomas M, Scharf G, Kockelkorn D, Knapp B, Schühle K, Heider J, Fuchs G (2012) Anaerobic metabolism of indoleacetate. J Bacteriol 194:2894–2903CrossRefPubMedPubMedCentralGoogle Scholar
  10. Ernstsen A, Sandberg G, Crozier A, Wheeler C (1987) Endogenous indoles and the biosynthesis and metabolism of indole-3-acetic acid in cultures of Rhizobium phaseoli. Planta 171:422–428CrossRefPubMedGoogle Scholar
  11. Evidente A, Iacobellis NS, Sisto A (1993) Isolation of indole-3-acetic acid methyl ester, a metabolite of indole-3-acetic acid from Pseudomonas amygdali. Experientia 49:182–183CrossRefGoogle Scholar
  12. Fell JW, Statzell-Tallman A (1980) Rhodosporidium paludigenum sp. nov., a basidiomycetous yeast from intertidal waters of South Florida. Int J Syst Bacteriol 30:658–659CrossRefGoogle Scholar
  13. Glass NL, Kosuge T (1988) Role of indoleacetic acid lysine synthetase in regulation of indoleacetic acid pool size and virulence of Pseudomonas syringae subsp savastanoi. J Bacteriol 170:2367–2373PubMedPubMedCentralGoogle Scholar
  14. Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol 196:520–534CrossRefPubMedGoogle Scholar
  15. Inácio J, Pereira P, Carvalho M, Fonseca A, Amaral-Collaço MT, Spencer-Martins I (2002) Estimation and diversity of phylloplane mycobiota on selected plants in a Mediterranean-type ecosystem in Portugal. Microb Ecol 44:344–353CrossRefPubMedGoogle Scholar
  16. Jia SR, Cui JD, Li Y, Sun AY (2008) Production of l-phenylalanine from transcinnamic acids by high-level expression of phenylalanine ammonia lyase gene from Rhodosporidium toruloides in Escherichia coli. Biochem Eng J 42:193–197CrossRefGoogle Scholar
  17. Kumavath RN, Ramana ChV, Sasikala Ch (2010) l-Tryptophan catabolism by Rubrivivax benzoatilyticus JA2 occurs through indole 3-pyruvic acid pathway. Biodegradation 21:825–832CrossRefPubMedGoogle Scholar
  18. Leveau JHJ, Lindow SE (2005) Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Appl Environ Microbiol 71:2365–2371CrossRefPubMedPubMedCentralGoogle Scholar
  19. Mujahid Md, Sasikala Ch, Ramana ChV (2011) Production of indole-3-acetic acid and related indole derivatives from l-tryptophan by Rubrivivax benzoatilyticus JA2. Appl Microbiol Biotechnol 89:1001–1008CrossRefPubMedGoogle Scholar
  20. Nagia MM, Shaaban M, Abdel-Aziz MS, El-Zalabani SM, Hanna AG (2012) Secondary metabolites and bioactivity of two fungal strains. Egypt Pharm J 11:16–21Google Scholar
  21. 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 Fertil Soils 42:97–108CrossRefGoogle Scholar
  22. Normanly J, Sovin J, Cohen J (2004) Auxin metabolism in plant hormones: biosynthesis, signal transduction, action. Kluwer, DordrechtGoogle Scholar
  23. Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S (2014) Plant growth-promoting traits of epiphytic and endophytic yeasts isolated from rice and sugar cane leaves in Thailand. Fungal Biol 118:683–694CrossRefPubMedGoogle Scholar
  24. Nutaratat P, Amsri W, Srisuk N, Arunrattiyakorn P, Limtong S (2015) Indole-3-acetic acid production by newly isolated red yeast Rhodosporidium paludigenum. J Gen Appl Microbiol 61:1–9CrossRefPubMedGoogle Scholar
  25. Prinsen E, Costacurta A, Michiels K, Vanderleyden J, Onckelen HV (1993) Azospirillum brasilense indole-3-acetic acid biosynthesis: evidence for a non-tryptophan dependent pathway. Mol Plant-Microbe Interact 6:609–615CrossRefGoogle Scholar
  26. Rao RP, Hunter A, Kashpur O, Normanly J (2010) Aberrant synthesis of indole-3-acetic acid in Saccharomyces cerevisiae triggers morphogenic transition, a virulence trait of pathogenic fungi. Genet Soc Am 185:211–220Google Scholar
  27. Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9:339–355CrossRefPubMedGoogle Scholar
  28. Robinson M, Riov J, Sharon A (1998) Indole-3-acetic acid biosynthesis in Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 64:5030–5032PubMedPubMedCentralGoogle Scholar
  29. Seidel C, Walz A, Park S, Cohen JD, Ludwig-Muller J (2006) Indole-3-acetic acid protein conjugates: novel players in auxin homeostasis. Plant Biol 8:340–345CrossRefPubMedGoogle Scholar
  30. Spaepen S, Vanderleyden J (2011) Auxin and plant-microbe interactions. Cold Spring Harb Perspect Biol. doi: 10.1101/cshperspect.a001438 PubMedPubMedCentralGoogle Scholar
  31. Szkop M, Bielawski W (2013) A simple method for simultaneous RP-HPLC determination of indolic compounds related to bacterial biosynthesis of indole-3-acetic acid. Antonie Van Leeuwenhoek 103:683–691CrossRefPubMedGoogle Scholar
  32. Teale WD, Paponov IA, Palme K (2006) Auxin in action: signaling, transport and the control of plant growth and development. Mol Cell Biol 7:847–859Google Scholar
  33. Tromas A, Perrot-Rechenmann C (2010) Recent progress in auxin biology. C R Biol 333:297–306CrossRefPubMedGoogle Scholar
  34. Tsavkelova EA, Klimova SYu, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42:117–126CrossRefGoogle Scholar
  35. Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y, Tudzynski B, Sharon A (2012) Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fungal Genet Biol 49:48–57CrossRefPubMedGoogle Scholar
  36. Wang Y, Yu T, Li Y, Cai D, Liu X, Lu H, Zheng XD (2009) Postharvest biocontrol of Alternaria alternata in Chinese winter jujube by Rhodosporidium paludigenum. J Appl Microbiol 107:1492–1498CrossRefPubMedGoogle Scholar
  37. Wiebe MG, Koivuranta K, Penttilä M, Ruohonen L (2012) Lipid production in batch and fed-batch cultures of Rhodosporidium toruloides from 5 and 6 carbon carbohydrates. BMC Biotechnol 12:1–10CrossRefGoogle Scholar
  38. Woodward AW, Barte B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wu S, Zhao X, Shen H, Wang Q, Zhao ZK (2011) Microbial lipid production by Rhodosporidium toruloides under sulfate-limited conditions. Bioresour Technol 102:1803–1807CrossRefPubMedGoogle Scholar
  40. Xin G, Glawe D, Doty SL (2009) Characterization of three endophytic, indole-3-acetic acid producing yeasts occurring in Populus trees. Mycol Res 113:973–980CrossRefPubMedGoogle Scholar
  41. Yang Y, Xu R, Ma C, Vlot AC, Klessig DF, Pichersky E (2008) Inactive methyl indole-3-acetic acid ester can be hydrolyzed and activated by several esterases belonging to the AtMES esterase family of Arabidopsis. Plant Physiol 147:1034–1045CrossRefPubMedPubMedCentralGoogle Scholar
  42. Yimyoo T, Yongmanitchai W, Limtong S (2011) Carotenoid production by Rhodosporidium paludigenum DMKU3-LPK4 using glycerol as the carbon source. Kasetsart J (Nat Sci) 45:90–100Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Pumin Nutaratat
    • 1
    • 2
  • Nantana Srisuk
    • 1
    • 2
    Email author
  • Panarat Arunrattiyakorn
    • 3
  • Savitree Limtong
    • 1
    • 2
  1. 1.Department of Microbiology, Faculty of ScienceKasetsart UniversityChatuchak, BangkokThailand
  2. 2.Center for Advanced Studies in Tropical Natural Resources, NRU-KUKasetsart UniversityChatuchak, BangkokThailand
  3. 3.Department of Chemistry, Faculty of ScienceSrinakharinwirot UniversityBangkokThailand

Personalised recommendations