Mikrobiol. Z. 2022; 84(2):57-72.
doi: https://doi.org/10.15407/microbiolj84.02.057

Ways of Auxin Biosynthesis in Microorganisms

T.P. Pirog1,2, D.V. Piatetska1, N.O. Klymenko1, G.O. Iutynska2

1National University of Food Technologies
68 Volodymyrska Str., Kyiv, 01601, Ukraine

2Zabolotny Institute of Microbiology and Virology, NAS of Ukraine
154 Akad. Zabolotny Str., Kyiv, 03143, Ukraine

Among plant hormones, auxins, in particular indole-3-acetic acid (IAA), are the most studied and researched. Almost all groups of soil microorganisms, both plant-associated and non-plant-associated bacteria, fungi, and phytopathogenic microorganisms are capable of producing auxins. The development of preparations for crop production is directly related to the production of bacterial strains with high auxin-synthesizing potential, which is possible only with a full understanding of the ways of regulation and synthesis of auxins in bacteria. The synthesis of auxins in microorganisms can take place in two ways: by the gradual conversion of tryptophan to IAA (tryptophan-dependent pathway) or by the use of other intermediates (tryptophan-independent pathway). The latter is poorly clarified, and in the literature available today, there is only a small amount of information on the functioning of this pathway in microorganisms. The review presents literature data on the ways of auxin biosynthesis in different groups of microorganisms, as well as approaches to the intensification of indole-3-acetic acid synthesis. The formation of IAA from tryptophan can be carried out in the following ways: through indole-3-pyruvate, through indole-3-acetamide, and through indole-3-acetonitrile. The vast majority of available publications are related to the assimilation of tryptophan through the formation of indole-3-pyruvate as this pathway is the most common among microorganisms. Thus, it functions in rhizospheric, symbiotic, endophytic, and free-living bacteria. The concentration of synthesized IAA among natural strains is in the range from 260 to 1130 μg/mL. Microorganisms in which the indole-3-acetamide pathway functions are characterized by lower auxin-synthesizing ability compared to those that assimilate tryptophan through indole-3-pyruvate. These include bacteria of the genera Streptomyces, Pseudomonas, and Bradyrhizobium and fungi of the genus Fusarium. The level of synthesis of IAA in such microorganisms is from 1.17×10−4 to 255.6 μg/mL. To date, only two strains that assimilate tryptophan via the indole-3-acetonitrile pathway and form up to 31.5 μg/mL IAA have been described in the available literature. To intensify the synthesis of indole-3-acetic acid, researchers use two main approaches: the first consists in introducing into the culture medium of exogenous precursors of biosynthesis (usually tryptophan, less often indole-3-pyruvate, indole-3-acetamide, and indole-3-acetonitrile); the second — in increasing the expression of the corresponding genes and creating recomindolebinant strains-supersynthetics of IAA. The largest number of publications is devoted to increasing the synthesis of IAA in the presence of biosynthesis precursors. Depending on the type of bacteria, the composition of the nutrient medium, and the amount of exogenously introduced precursor, the synthesis of the final product was increased by 1.2—27 times compared to that before the intensifi cation. Thus, in the presence of 11 g/L tryptophan, Enterobacter sp. DMKU-RP206 synthesized 5.56 g/L, while in a medium without the precursor, it yielded only 0.45 g/L IAA. Recombinant strains Corynebacterium glutamicum ATCC 13032 and Escherichia coli MG165 formed 7.1 and 7.3 g/L IAA, respectively, when tryptophan (10 g/L) was added to the culture medium. The level of auxin synthesis in microorganisms may be increased under stress conditions (temperature, pH, biotic and abiotic stress factors), but in this case, the IAA concentration does not exceed 100 mg/L, and therefore this method of intensification cannot compete with the others above.

Keywords: tryptophan, indole-3-pyruvate, indole-3-acetamide, indole-3-acetonitrile, indole-3-acetic acid, intensifi cation of phytohormone synthesis.

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  1. Yashchuk I, Shlonchak G. [Experience of growing pine seedlings with the use of plant growth regulators in SE "Klavdievske Forestry"]. Forestry and agroforestry. 2019; 134: 43—46. Ukrainian. https://doi.org/10.33220/1026-3365.134.2019.43
  2. Tsygankova V, Galkina L, Musatenko L, Sytnik K. [Genetic and epigenetic control of plant growth and development. Auxin biosynthesis genes and auxin-regulated genes that control plant cell division and stretching]. Biopolymers and cell. 2005; 21(2):107—133. Russian. https://doi.org/10.7124/bc.0006E2
  3. Imada E, Rolla Dos Santos A, Oliveira A, Hungria M, Rodrigues E. Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Microbiol Res. 2017; 168(3):283—292. https://doi.org/10.1016/j.resmic.2016.10.010
  4. Lin HR, Shu HY, Lin GH. Biological roles of indole-3-acetic acid in Acinetobacter baumannii. Microbiol Res. 2018; 216:30—39. https://doi.org/10.1016/j.micres.2018.08.004
  5. Molina R, Rivera D, Mora V, López G, Rosas S, Spaepen S, et al. Regulation of indole-3-acetic acid biosynthesis in Azospirillum brasilense under environmental stress conditions. Curr Microbiol. 2018; 75(10):1408—1418. https://doi.org/10.1007/s00284-018-1537-6
  6. Ouyang L, Pei H, Xu Z. Low nitrogen stress stimulating the indole-3-acetic acid biosynthesis of Serratia sp. ZM is vital for the survival of the bacterium and its plant growth-promoting characteristic. Arch Microbiol. 2017; 199(3):425—432. https://doi.org/10.1007/s00203-016-1312-7
  7. Ghosh PK, Sen SK, Maiti TK. Production and metabolism of indole-3-acetic acid by Enterobacter spp. (Gammaproteobacteria) isolated from root nodules of a legume Abrus precatorius L. Biocatal Agric Biotechnol. 2015; 4(3):296—303. https://doi.org/10.1016/j.bcab.2015.04.002
  8. Rodrigues EP, Soares CP, Galvão PG, Imada EL, Simões-Araújo JL, Rouws LF, et al. Identification of genes involved in indole-3-acetic acid biosynthesis by Gluconacetobacter diazotrophicus PAL5 strain using transposon mutagenesis. Front Microbiol. 2016; 7:1572. https://doi.org/10.3389/fmicb.2016.01572
  9. Estenson K, Hurst GB, Standaert RF, Bible AN, Garcia D, Chourey K, et al. Characterization of indole-3-acetic acid biosynthesis and the effects of this phytohormone on the proteome of the plant-associated microbe Pantoea sp. YR343. J Proteome Res. 2018; 17(4):1361—1374. https://doi.org/10.1021/acs.jproteome.7b00708
  10. Rivera D, Mora V, Lopez G, Rosas S, Spaepen S, Vanderleyden J, et al. New insights into indole-3-acetic acid metabolism in Azospirillum brasilense. J Appl Microbiol. 2018; 125(6):1774—1785. https://doi.org/10.1111/jam.14080
  11. Sun SL, Yang WL, Fang WW, Zhao YX, Guo L, Dai YJ. Th e plant growth-promoting rhizobacterium Variovorax boronicumulans CGMCC 4969 regulates the level of indole-3-acetic acid synthesized from indole-3-acetonitrile. Appl Environ Microbiol. 2018; 84(16):e00298-18. https://doi.org/10.1128/AEM.00298-18
  12. McClerklin SA, Lee SG, Harper CP, Nwumeh R, Jez JM, Kunkel BN. Indole-3-acetaldehyde dehydrogenasedependent auxin synthesis contributes to virulence of Pseudomonas syringae strain DC3000. PLoS Pathog. 2018; 14(1):e1006811. https://doi.org/10.1371/journal.ppat.1006811
  13. Aragón IM, Pérez-Martínez I, Moreno-Pérez A, Cerezo M, Ramos C. New insights into the role of indole-3-acetic acid in the virulence of Pseudomonas savastanoi pv. savastanoi. FEMS Microbiol Lett. 2014; 356(2):184—192. https://doi.org/10.1111/1574-6968.12413
  14. Methabolism of tryprophan in Agrobacterium tumefaciens Ach5. KEGG: Kyoto encyclopedia of genes and genomes [Electronic resource]. Access mode: https://www.kegg.jp/kegg-bin/highlight_pathway?scale=1.0&map=atf00380&keyword=
  15. Huang YY, Cho S, Lo WS, Wang YC, Lai E, Kuo CH. Complete genome sequence of Agrobacterium tumefaciens Ach5. Genome Announc. 2015; 3(3):e00570-15. https://doi.org/10.1128/genomeA.00570-15
  16. Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y, Tudzynski B, et al. Identifi cation and functional characterization of indole-3-acetamide-mediated indole-3-acetic acid biosynthesis in plant-associated Fusarium species. Fungal Genet Biol. 2012; 49(1):48—57. https://doi.org/10.1016/j.fgb.2011.10.005
  17. Legault GS, Lerat S, Nicolas P, Beaulieu C. Tryptophan regulates thaxtomin A and indole-3-acetic acid production in Streptomyces scabiei and modifies its interactions with radish seedlings. Phytopathology. 2011; 101(9):1045—1051. https://doi.org/10.1094/PHYTO-03-11-0064
  18. Luo K, Rocheleau H, Qi PF, Zheng YL, Zhao HY, Ouellet T. Indole-3-acetic acid in Fusarium graminearum: identification of biosynthetic pathways and characterization of physiological effects. Fungal Biol. 2016; 120(9):1135—1145. https://doi.org/10.1016/j.funbio.2016.06.002
  19. Duca DR, Rose DR, Glick BR. Indole acetic acid overproduction transformants of the rhizobacterium Pseudomonas sp. UW4. Anton Leeuwe. 2018; 111(9):1645—1660. https://doi.org/10.1007/s10482-018-1051-7
  20. Lehmann T, Hoff mann M, Hentrich M, Pollmann S. Indole-3-acetamide-dependent auxin biosynthesis: a widely distributed way of indole-3-acetic acid production? Eur J Cell Biol. 2010; 89(12):895—905. https://doi.org/10.1016/j.ejcb.2010.06.021
  21. Olanrewaju OS, Glick BR, Babalola OO. Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol. 2017; 33(11):197. https://doi.org/10.1007/s11274-017-2364-9
  22. Cerboneschi M, Decorosi F, Biancalani C, Ortenzi MV, Macconi S, Giovannetti L, et al. Indole-3-acetic acid in plant-pathogen interactions: a key molecule for in planta bacterial virulence and fitness. Res Microbiol. 2016; 167(9—10):774—787. https://doi.org/10.1016/j.resmic.2016.09.002
  23. Guo D, Kong S, Chu X, Li X, Pan H. De novo biosynthesis of indole-3-acetic acid in engineered Escherichia coli. J Agric Food Chem. 2019; 67(29):8186—8190. https://doi.org/10.1021/acs.jafc.9b02048
  24. Duca D, Lorv J, Patten CL, Rose D, Glick BR. Indole-3-acetic acid in plant-microbe interactions. Anton Leeuwe. 2014; 106(1):85—125. https://doi.org/10.1007/s10482-013-0095-y
  25. Zhang B, Wang YY, Hu X. Highly efficient biosynthesis of indole-3-acetic acid by Enterobacter xiangfangensis BHW6. Research square. 2020. https://doi.org/10.21203/rs.3.rs-54635/v1
  26. Luziatelli F, Ficca AG, Bonini P, Muleo R, Gatti L, Meneghini M, et al. A genetic and metabolomic perspective on the production of indole-3-acetic acid by Pantoea agglomerans and use of their metabolites as biostimulants in plant nurseries. Front Microbiol, 2020; 11:1475. https://doi.org/10.3389/fmicb.2020.01475
  27. Pan L, Chen J, Ren S, Shen H, Rong B, Liu W, et al. Complete genome sequence of Mycobacterium Mya-zh01, an endophytic bacterium, promotes plant growth and seed germination isolated from flower stalk of Doritaenopsis. Arch Microbiol. 2020; 202:1965—1976. https://doi.org/10.1007/s00203-020-01924-w
  28. Torres D, Benavidez I, Donadio F, Mongiardini E, Rosas S, Spaepen S, et al. New insights into auxin metabolism in Bradyrhizobium japonicum. Res Microbiol. 2018; 169(6):313—323. https://doi.org/10.1016/j.resmic.2018.04.002
  29. Upadhyay A, Srivastava S. Characterization of a new isolate of Pseudomonas fluorescens strain Psd as a potential biocontrol agent. Lett Appl Microbiol. 2008; 47(2):98—105. https://doi.org/10.1111/j.1472-765X.2008.02390.x
  30. Upadhyay A, Srivastava S. Evaluation of multiple plant growth promoting traits of an isolate of Pseudomonas fluorescens strain Psd. Indian J Exp Biol. 2010; 48(6):601—609.
  31. Lin L, Xu X. Indole-3-acetic acid production by endophytic Streptomyces sp. En-1 isolated from medicinal plants. Curr Microbiol. 2013; 67(2):209—217. https://doi.org/10.1007/s00284-013-0348-z
  32. Liu D, Yan R, Fu Y, Wang X, Zhang J, Xiang W. Antifungal, plant growth-promoting, and genomic properties of an endophytic Actinobacterium Streptomyces sp. NEAU-S7GS2. Front Microbiol. 2019; 10:2077. https://doi.org/10.3389/fmicb.2019.02077
  33. Lacroix B, Gizatullina DI, Babst BA, Giff ord AN, Citovsky V. Agrobacterium T-DNA-encoded protein Atu6002 interferes with the host auxin response. Mol Plant Pathol. 2014; 15(3):275—283. https://doi.org/10.1111/mpp.12088
  34. Kochar M, Upadhyay A, Srivastava S. Indole-3-acetic acid biosynthesis in the biocontrol strain Pseudomonas fluorescens Psd and plant growth regulation by hormone overexpression. Res Microbiol. 2011; 162(4):426—435. https://doi.org/10.1016/j.resmic.2011.03.006
  35. Manulis S, Shafrir H, Epstein E, Lichter A, Barash I. Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology. 1994; 140(5):1045—1050. https://doi.org/10.1099/13500872-140-5-1045
  36. Sousa JAJ, Olivares FL. Plant growth promotion by Streptomycetes: ecophysiology, mechanisms and applications. Chem Biol Technol Agric. 2016; 3(24):1—12. https://doi.org/10.1186/s40538-016-0073-5
  37. Spaepen S, Vanderleyden J, Remans R. indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev. 2007; 31(4):425—448. https://doi.org/10.1111/j.1574-6976.2007.00072.x
  38. Kim YM, Kwak MH, Kim HS, Lee JH. Production of indole-3-acetate in Corynebacterium glutamicum by heterologous expression of the indole-3-pyruvate pathway genes. Microbiol Biotechnol Lett. 2019; 47(2):242—249. https://doi.org/10.4014/mbl.1901.01013
  39. Wu H, Yang J, Shen P, Li Q, Wu W, Jiang X, et al. High-level production of indole-3-acetic acid in the metabolically engineered Escherichia coli. J Agric Food Chem. 2021; 69(6):1916—1924. https://doi.org/10.1021/acs.jafc.0c08141
  40. Cosracurta A, Vanderleyden J. Synthesis of phytohormones by plant-associated bacteria. Cri Rev Microbiol. 1995; 21(1):1—18. https://doi.org/10.3109/10408419509113531
  41. Ambawade MS, Pathade GR. Production of IAA (indole-3-acetic acid) by Stenotrophomonas maltophilia BE25 isolated from roots of banana (Musa spp). Int J Sci Res. 2015; 4(1):2644—2650.
  42. Jeyanthi V, Ganesh P. Production, optimization and characterization of phytohormone indole acetic acid by Pseudomonas fluorescence. Int J Pharm Bio Arch. 2013; 4(2):514—520.
  43. Bose A, Kher MM, Nataraj M, Keharia H. Phytostimulatory effect of indole-3-acetic acid by Enterobacter cloacae SN19 isolated from Teramnus labialis (L.f.) spreng rhizosphere. Biocatal Agric Biotech. 2016; 6:128—137. https://doi.org/10.1016/j.bcab.2016.03.005
  44. Ozdal M, Ozdal OG, Sezen A, Algur OF, Kurbanoglu EB. Continuous production of indole-3-acetic acid by immobilized cells of Arthrobacter agilis. 3 Biotec. 2017; 7(1):23. https://doi.org/10.1007/s13205-017-0605-0
  45. Nutaratat P, Monprasit A, Srisuk N. High-yield production of indole-3-acetic acid by Enterobacter sp. DMKURP206, a rice phyllosphere bacterium that possesses plant growth-promoting traits. 3 Biotech. 2017; 7(5):305. https://doi.org/10.1007/s13205-017-0937-9
  46. Mon Myo E, Ge B, Ma J, Cui H, Liu B, Shi L, et al. Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiol. 2019; 19(1):1—14. https://doi.org/10.1186/s12866-019-1528-1
  47. Chandra S, Askari K, Kumari M. Optimization of indole acetic acid production by isolated bacteria from Stevia rebaudiana rhizosphere and its effects on plant growth. J Gen Eng Biotechnol. 2018; 16(2):581—586. https://doi.org/10.1016/j.jgeb.2018.09.001
  48. Hasuty A, Choliq A, Hidayat I. Production of IAA (indole-3-acetic acid) by Serratia marcescens subsp. marcescens and Rhodococcus aff. qingshengii. Int J Agric Technol. 2018; 14(3):299—312.
  49. Wagi S, Ahmed A. Bacillus spp.: potent microfactories of bacterial indole-3-acetic acid. Peer J. 2019; 7:e7258. https://doi.org/10.7717/peerj.7258
  50. Kumari S, Prabha C, Singh A, Kumari S, Kiran S. Optimization of indole-3-acetic acid production by diazotrophic B. subtilis DR2 (KP455653), isolated from rhizospere of Eragrostis cynosuroides. Int J Pharm Med Bio Sci. 2018; 7(2):20—27. https://doi.org/10.18178/ijpmbs.7.2.20-27
  51. Naveed M, Qureshi MA, Zahir ZA. L-Tryptophan-dependent biosynthesis of IAA (indole-3-acetic acid) improves plant growth and colonization of maize by Burkholderia phytofirmans PsJN. Ann Microbiol. 2015; 65:1381—1389. https://doi.org/10.1007/s13213-014-0976-y
  52. Shim J, Kim JW, Shea PJ, Oh BT. Indole-3-acetic acid production by Bacillus sp. JH 2-2 promotes Indian mustard growth in the presence of hexavalent chromium. J Basic Microbiol. 2015; 55(5):652—658. https://doi.org/10.1002/jobm.201400311
  53. Lebrazi S, Niehaus K, Bednarz H, Fadil M, Chraibi M, Fikri-Benbrahi K. Screening and optimization of indole-3-acetic acid production and phosphate solubilization by rhizobacterial strains isolated from Acacia cyanophylla root nodules and their effects on its plant growth. J Gen Eng Biotechnol. 2020; 18(1):1—12. https://doi.org/10.1186/s43141-020-00090-2
  54. Dasri K, Kaewharn J, Kanso S, Sangchanjirader S. Optimization of IAA (indole-3-acetic acid) production by rhizobacteria isolated from epiphytic orchids. KKU Res J. 2014; 19:268—275.
  55. Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S. Indole-3-acetic acid biosynthetic pathways in the basidiomycetous yeast Rhodosporidium paludigenum. Arch Microbiol. 2016; 198(5):429—437. https://doi.org/10.1007/s00203-016-1202-z
  56. Fu S-F, Sun P-F, Lu H-Y, Wei J-Y, Xiao H-S, Fang W-T, et al. Plant growth-promoting traits of yeasts isolated from the phyllosphere and rhizosphere of Drosera spatulata Lab. Fungal Biol. 2016; 120:433—448. https://doi.org/10.1016/j.funbio.2015.12.006
  57. Bunsangiam S, Sakpuntoon V, Srisuk N, Ohashi T, Fujiyama K, Limtong S. Biosynthetic pathway of indole-3-acetic acid in basidiomycetous yeast Rhodosporidiobolus fluvialis. Mycobiology. 2019; 47(3):292—300. https://doi.org/10.1080/12298093.2019.1638672
  58. Feoktistova NV, Mardanova AM, Khadieva GF, Sharipova MR. [Rhizospheric bacteria]. Scientists records of Kazan University. Natural sciences series. 2016; 158 (2):207—224. Russian.
  59. Kudoyarova G, Arkhipova T, Korshunova T, Bakaeva M, Loginov O, Dodd IC. Phytohormone mediation of interactions between plants and non-symbiotic growth promoting bacteria under edaphic stresses. Front Plant Sci. 2019; 10:1368. https://doi.org/10.3389/fpls.2019.01368
  60. Kolupaev YE, Karpets YV, Yastreb TO, Lugovaya AA. [Signaling mediators in the realization of the physiological effects of stress phytohormones]. Journal of Kharkov National Agrarian University. Biology series. 2016; 1(37):42—62. Russian.