Utilization of the Plant Hormone Indole-3-Acetic Acid for Growth by Pseudomonas putida Strain 1290
Open accessAbstract
We have isolated from plant surfaces several bacteria with the ability to catabolize indole-3-acetic acid (IAA). One of them, isolate 1290, was able to utilize IAA as a sole source of carbon, nitrogen, and energy. The strain was identified by its 16S rRNA sequence as Pseudomonas putida . Activity of the enzyme catechol 1,2-dioxygenase was induced during growth on IAA, suggesting that catechol is an intermediate of the IAA catabolic pathway. This was in agreement with the observation that the oxygen uptake by IAA-grown P. putida 1290 cells was elevated in response to the addition of catechol. The inability of a catR mutant of P. putida 1290 to grow at the expense of IAA also suggests a central role for catechol as an intermediate in IAA metabolism. Besides being able to destroy IAA, strain 1290 was also capable of producing IAA in media supplemented with tryptophan. In root elongation assays, P. putida strain 1290 completely abolished the inhibitory effect of exogenous IAA on the elongation of radish roots. In fact, coinoculation of roots with P. putida 1290 and 1 mM concentration of IAA had a positive effect on root development. In coinoculation experiments on radish roots, strain 1290 was only partially able to alleviate the inhibitory effect of bacteria that in culture overproduce IAA. Our findings imply a biological role for strain 1290 as a sink or recycler of IAA in its association with plants and plant-associated bacteria.
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Microorganisms use various mechanisms for complete biodegradation (mineralization) or transformation of indole compounds into other compounds, such as catechol, indole-3-aldehyde, 3-methylindole, and indigo.
“Microorganisms use various mechanisms for complete biodegradation (mineralization) or transformation of indole compounds into other compounds, such as catechol (Leveau and Lindow 2005), indole-3-aldehyde (Arora and Bae 2014), 3-methylindole (Arora et al. 2015a, b), and indigo (Ma et al. 2018).”
From Phosphate solubilization and indole acetic acid production by rhizosphere yeast Torulaspora globosa: improvement of culture conditions for better performance in vitro (2022) · cites this paper as Leveau and Lindow 2005
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Discovery of a bacterial gene cluster for catabolism of the plant hormone indole 3-acetic acid.
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“Indole acetaldehyde can be used to support the growth of the PGPB Pseudomonas putida in a minimal medium (Leveau and Lindow 2005).”
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“IAA catabolism has been characterized in some rhizobacteria such as Pseudomonas putida, and relies on the presence of the iac locus (for IAA catabolism) constituted of 10 genes with coding similarity to enzymes acting on indole or amidated aromatics and to proteins with regulatory or unknown function [44,45].”
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“Apart from synthesizing IAA, some PGPR, such as Pseudomonas, Arthrobacter, and Bradyrhizobium, can degrade IAA and use it as a carbon and nitrogen source (10, 11).”
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“When used in seed treatment, beneficial root-colonizing microbes that secrete IAA can potentially manipulate the plant’s endogenous pool of IAA, contributing to host tolerance to the harmful effects of environmental stress [64,65].”
BackgroundSantoro, M. V., Cappellari, L. D. R., Giordano, W. F., & Banchio, E. (2015) · Plant Biology · doi:10.1111/plb.12351 · Cited by 87 · see citing works
Leveau, J. H. J. (2007) · European Journal of Plant Pathology · doi:10.1007/s10658-007-9186-9 · Cited by 68 · see citing works
“…clones can be measured using high-pressure liquid chromatography or colorimetric assays (Bric et al. 1991; Omer et al. 2004; Radwan et al. 2002; Leveau and Lindow 2005), while cytokinins and their metabolites are detectable in supernatants by e.g. immunoaffinity chromatography (Timmusk et al.…”
BackgroundMethodSelf-citationBunsangiam, S., Thongpae, N., Limtong, S., & Srisuk, N. (2021) · Scientific Reports · doi:10.1038/s41598-021-92305-w · Cited by 72 · see citing works
Biessy, A., Novinscak, A., Blom, J., Léger, G., Thomashow, L., Cazorla, F., Jošić, D., & Filion, M. (2018) · Environmental Microbiology · doi:10.1111/1462-2920.14476 · Cited by 71
Microbial Degradation of Indole and Its Derivatives
Arora, P., Sharma, A., & Bae, H. (2015) · Journal of Chemistry · doi:10.1155/2015/129159 · Cited by 70 · see citing works
“Catechol is also detected as a metabolite of indole-3-acetic acid degradation by Pseudomonas putida 1290 [81], Pseudomonas sp.”
BackgroundThe birth of a giant: evolutionary insights into the origin of auxin responses in plants
Carrillo‐Carrasco, V. P., Hernández‐García, J., Mutte, S. K., & Weijers, D. (2023) · The EMBO Journal · doi:10.15252/embj.2022113018 · Cited by 79 · see citing works
“Yet, these responses may also be part of a more general metabolic homeostasis system, which would agree with the idea of IAA being used as a carbon source for bacteria (Jensen et al , 1995; Leveau & Lindow, 2005; Donoso et al , 2016; Conway et al , 2022).”
Biological roles of indole-3-acetic acid in Acinetobacter baumannii.
Lin, H.-R., Shu, H.-Y., & Lin, G.-H. (2018) · Microbiology Research · doi:10.1016/j.micres.2018.08.004 · Cited by 67
Scott, J. C., Greenhut, I. V., & Leveau, J. H. J. (2013) · Journal of Chemical Ecology · doi:10.1007/s10886-013-0324-x · Cited by 67 · see citing works
“This bacterium originally was isolated from pear tree foliage and it efficiently exploits IAA as a nutrient source (Leveau and Lindow 2005).”
InfluentialSelf-citationDonoso, R., Leiva-Novoa, P., Zúñiga, A., Timmermann, T., Recabarren‐Gajardo, G., & González, B. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01991-16 · Cited by 63
“An anaerobic auxin degradation pathway has been proposed in Azoarcus evansii and Aromatoleum aromaticum (8), and complete aerobic degradation of this auxin has been reported in Bradyrhizobium (9, 10); Pseudomonas (11); Burkholderia, Rhodococcus, and Sphingomonas (12); and Acinetobacter (13) species.”
BackgroundInfluentialGrapevine (Vitis vinifera) Crown Galls Host Distinct Microbiota
Faist, H., Keller, A., Hentschel, U., & Deeken, R. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.01131-16 · Cited by 62 · see citing works
Li, L., Mohamad, O., Ma, J.-B., Friel, A. D., Su, Y.-G., Wang, Y., Musa, Z., Liu, Y.-H., Hedlund, B., & Li, W.-J. (2018) · Antonie van Leeuwenhoek · doi:10.1007/s10482-018-1062-4 · Cited by 61
“Some studies have reported that endophytic bacteria isolated from medicinal plants produced indole-3-acetic acid (IAA) (Khan et al. 2014), which is involved in stimulation of plant growth by stimulating cell enlargement, division, differentiation, and gene regulation (Leveau and Lindow 2005).”
BackgroundBasu, S., Rabara, R., & Negi, S. (2017) · Plant Gene · doi:10.1016/j.plgene.2017.07.004 · Cited by 65 · see citing works
Attia, M. S., Salem, M., & Abdelaziz, A. (2022) · Biomass Conversion and Biorefinery · doi:10.1007/s13399-022-03607-6 · Cited by 59
“The ability of fungi to create indole acetic acid (IAA) was established by the technique described by Leveau and Lin-dow [39].”
Bacterial catabolism of indole-3-acetic acid
Laird, T. S., Flores, N., & Leveau, J. (2020) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-020-10938-9 · Cited by 58 · see citing works
Self-citationBahroun, A., Jousset, A., Mhamdi, R., Mrabet, M., & Mhadhbi, H. (2017) · doi:10.1016/j.apsoil.2017.10.025 · Cited by 54
Panichikkal, J., Thomas, R., John, J. C., & Radhakrishnan, E. (2019) · Current Microbiology · doi:10.1007/s00284-019-01649-0 · Cited by 53
Significance of microbial interactions in the mycorrhizosphere.
Bending, G., Aspray, T., & Whipps, J. (2006) · Advances in Applied Microbiology · doi:10.1016/s0065-2164(06)60004-x · Cited by 53
“However, as the ECM fungus L. bicolor also produces IAA, it is not clear what contribution bacterially produced IAA has on enhancing this symbiosis.”
BackgroundInfluentialSasirekha, B., & Shivakumar, S. (2012) · doi:10.4067/s0718-95162012005000038 · Cited by 51
“The IAA produced by bacteria colonizing the rhizosphere of the plants is proposed to act in conjunction with endogenous IAA in plant to stimulate cell proliferation, elongation, and enhancement of host’s uptake of minerals and nutrients from the soil (Suzuki and Oyaizu, 2003; Leveau and Lindow, 2005).”
BackgroundDiverse MarR bacterial regulators of auxin catabolism in the plant microbiome
Conway, J., Walton, W., Salas-González, I., Law, T. F., Lindberg, C., Crook, L., Kosina, S., Fitzpatrick, C. R., Lietzan, A., Northen, T., et al. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01244-3 · Cited by 50
Stout, L., Dodova, E. N., Tyson, J., & Nüsslein, K. (2010) · Water Research · doi:10.1016/j.watres.2010.07.073 · Cited by 50
Raddadi, N., Cherif, A., Ouzari, H., Marzorati, M., Brusetti, L., Boudabous, A., & Daffonchio, D. (2007) · Annals of Microbiology · doi:10.1007/bf03175344 · Cited by 50 · see citing works
“…al., 2003b), autolysins (Raddadi et al., 2004, 2005), lactonases (Dong et al., 2002), siderophores, β-1,3-glucanase, chitinases, antibiotics and hydrogene cyanide and to the ability to degrade indole-3-acetic acid (IAA) (protect the plant from high-IAA-producing bacteria) (Leveau and Lindow, 2005).”
BackgroundBoopathi, T., Balamurugan, V., Gopinath, S., & Sundararaman, M. (2013) · Journal of Plant Growth Regulation · doi:10.1007/s00344-013-9342-8 · Cited by 48
“Chlorophyll content and production of IAA were quantitatively analyzed at 24-h intervals using the Salkowski method (Leveau and Lindow 2005).”
MethodDaigham, G. E., Mahfouz, A. Y., Abdelaziz, A., Nofel, M. M., & Attia, M. S. (2023) · Biomass Conversion and Biorefinery · doi:10.1007/s13399-023-04510-4 · Cited by 45
“The efficacy of isolates for (IAA) production was determined by the colorimetric technique according to Leveau and Lin-dow [22].”
Nishu, S. D., No, J., & Lee, T. (2022) · Microbiology spectrum · doi:10.1128/spectrum.00979-22 · Cited by 45
“elongation, cell division, and enlargement under drought stress (15).”
BackgroundFarhaoui, A., Adadi, A., Tahiri, A., Alami, N. E., Khayi, S., Mentag, R., Ezrari, S., Nabil, R., Mokrini, F., Belabess, Z., et al. (2022) · Physiological and molecular plant pathology · doi:10.1016/j.pmpp.2022.101829 · Cited by 45
Navarro-Ródenas, A., Berná, L., Lozano-Carrillo, C., Andrino, A., & Morte, A. (2016) · Mycorrhiza · doi:10.1007/s00572-016-0711-6 · Cited by 44
“For this, the isolates were cultivated in a NB medium supplemented with 3 g/l of tryptophan (Ahmad et al. 2005; Leveau and Lindow 2005) at 28 °C for 2 days in a shaking incubator, at 100 rpm. Bacterial cells were removed from the culture broth by centrifugation (1.5 ml of bacterial suspension).”
MethodInfluentialNoreen, S., Ali, B., & Hasnain, S. (2012) · Annals of Microbiology · doi:10.1007/s13213-011-0277-7 · Cited by 43
“It has been previously reported that bacteria produced the highest concentrations of IAA during stationary phase cultures (Leveau and Lindow 2005).”
BackgroundSharma, P., Kumar, V., Khosla, R., & Guleria, P. (2020) · 3 Biotech · doi:10.1007/s13205-020-02428-6 · Cited by 41 · see citing works
A dynamic rhizosphere interplay between tree roots and soil bacteria under drought stress
Oppenheimer‐Shaanan, Y., Jakoby, G., Starr, M. L., Karliner, R., Eilon, G., Itkin, M., Malitsky, S., & Klein, T. (2022) · eLife · doi:10.7554/elife.79679 · Cited by 71 · see citing works
Nascimento, F., Glick, B. R., & Rossi, M. (2019) · Access Microbiology · doi:10.1099/acmi.0.000053 · Cited by 40
Ely, C., & Smets, B. (2017) · International journal of phytoremediation · doi:10.1080/15226514.2017.1303805 · Cited by 40 · see citing works
Mahdi, I., Fahsi, N., Hafidi, M., Benjelloun, S., Allaoui, A., & Biskri, L. (2021) · doi:10.3390/su13063307 · Cited by 39
Isolation, identification and characterization of phenolic acid‐degrading bacteria from soil
Wang, Y., Zhang, W., Zhang, Z.-F., Wang, W.-H., Xu, S.-F., & He, X.-F. (2020) · Journal of Applied Microbiology · doi:10.1111/jam.14956 · Cited by 39
“…these, Pseudomonas sp., including P. putida, P. fluorescens, P. syringae, P. mendocina and P. aeruginosa, are considered to be the best bacterial agents for enhancing plant growth and yield (Patten and Glick 1996; Leveau and Lindow 2005; Kohler et al. 2010; Kochar et al. 2011; Goswami et al. 2015).”
BackgroundContinuous production of indole-3-acetic acid by immobilized cells of Arthrobacter agilis
Ozdal, M., Ozdal, O. G., Sezen, A., Algur, O. F., & Kurbanoglu, E. B. (2017) · 3 Biotech · doi:10.1007/s13205-017-0605-0 · Cited by 39 · see citing works
“Leveau and Lindow (2005) reported degradation of IAA to catechol by Pseudomonas putida.”
BackgroundArora, P. K., & Bae, H. (2014) · International Journal of Analytical Chemistry · doi:10.1155/2014/239641 · Cited by 38 · see citing works
“Leveau and Lindow [22] studied catabolism of indole-3-acetic acid by Pseudomonas putida strain 1290 that degraded indole-3-acetic acid via formation of catechol.”
BackgroundMahdi, I., Hafidi, M., Allaoui, A., & Biskri, L. (2021) · Agriculture · doi:10.3390/agriculture11030224 · Cited by 38 · see citing works
“5% of L-tryptophan and incubated at 28 ± 2 ◦C for 11 days under shaking of 150 rpm [55].”
MethodGenomics as a potential tool to unravel the rhizosphere microbiome interactions on plant health
Priya, P., Aneesh, B. P., & Harikrishnan, K. (2021) · Journal of Microbiological Methods · doi:10.1016/j.mimet.2021.106215 · Cited by 55 · see citing works
- Authors
- Leveau, J. H. J., & Lindow, S. E.
- Affiliations
- Netherlands Institute of Ecology (NL)
- University of California, Berkeley (US)
- Venue
- Applied and Environmental Microbiology
- Publisher
- American Society for Microbiology
- Published
- 2005-05
- Volume
- 71
- Issue
- 5
- Pages
- 2365-2371
- ISSN
- 0099-2240 (ISSN-L)
- 1098-5336
- OpenAlex
- W2143648038
- Cited by
- 286
- References
- 58
- Citations by year
- 2026: 4 · 2025: 11 · 2024: 21 · 2023: 15 · 2022: 25 · 2021: 22 · 2020: 20 · 2019: 21 · 2018: 13 · 2017: 22 · 2016: 15 · 2015: 13 · 2014: 11 · 2013: 16 · 2012: 9
- FWCI
- 8.82
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Applied and Environmental Microbiology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (submittedVersion)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (863.03.005)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Legume Nitrogen Fixing Symbiosis
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
- Keywords
- indole-3-acetic acid, Pseudomonas putida, catechol 1,2-dioxygenase, root elongation, radish, plant growth-promoting bacteria, plant-associated bacteria
- MeSH terms
- Base Sequence, Culture Media, Indoleacetic Acids, Molecular Sequence Data, Phylogeny, RNA, Ribosomal, 16S, Pseudomonas putida, Plant Roots
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