Skip to main content

Advertisement

Log in

Auxins of microbial origin and their use in agriculture

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

To maintain the world population demand, a sustainable agriculture is needed. Since current global vision is more friendly with the environment, eco-friendly alternatives are desirable. In this sense, plant growth–promoting rhizobacteria could be the choice for the management of soil-borne diseases of crop plants. These rhizobacteria secrete chemical compounds which act as phytohormones. Indole-3-acetic acid (IAA) is the most common plant hormone of the auxin class which regulates various processes of plant growth. IAA compound, in which structure can be found a carboxylic acid attached through a methylene group to the C-3 position of an indole ring, is produced both by plants and microorganisms. Plant growth–promoting rhizobacteria and fungi secrete IAA to promote the plant growth. In this review, IAA production and mechanisms of action by bacteria and fungi along with the metabolic pathways evolved in the IAA secretion and commercial prospects are revised.

Key points

Many microorganisms produce auxins which help the plant growth promotion.

These auxins improve the plant growth by several mechanisms.

The auxins are produced through different mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahemad M, Khan MS (2011) Effects of insecticides on plant growth-promoting activities of phosphate solubilizing rhizobacterium Klebsiella sp. strain PS19. Pestic Biochem Physiol 100:51–56

    CAS  Google Scholar 

  • Ahemad M, Khan MS (2012) Ecological assessment of biotoxicity of pesticides towards plant growth promoting activities of pea (Pisum sativum)-specific Rhizobium sp. strain MRP1. Emirates J Food Agric 24:334–343

    Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ Sci 26:1–20

    Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181

    CAS  PubMed  Google Scholar 

  • Aldesuquy HS, Mansour FA, Abo-Hamed SA (1998) Effect of the culture filtrates of Streptomyces on growth and productivity of wheat plants. Folia Microbiol 43:465–470

    Google Scholar 

  • Amprayn KO, Rose M, Kecskés M, Pereg L, Nguyen H, Kennedy I (2012) Plant growth promoting characteristics of soil yeast (Candida tropicalis HY) and its effectiveness for promoting rice growth. Appl Soil Ecol 61:295–299

    Google Scholar 

  • Asghar H, Zahir Z, Arshad M, Khaliq A (2002) Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L.. Biol Fertil Soils 35:231–237

    CAS  Google Scholar 

  • Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570

    CAS  PubMed  Google Scholar 

  • Backer R, Rokem JS, Ilangumaran G, Lamont J, Praslickova D, Ricci E, Subramanian S, Smith DL (2018) Plant growth-promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Front Plant Sci 9:1473

    PubMed  PubMed Central  Google Scholar 

  • Bais HP, Park SW, Weir TL, Callaway RM, Vivanco JM (2004) How plants communicate using the underground information superhighway. Trends Plant Sci 9:26–32

    CAS  PubMed  Google Scholar 

  • Barea JM, Brown M (1974) Effects on plant growth produced by Azotobacter paspali related to synthesis of plant growth regulating substances. J Appl Bacteriol 37:583–593

    CAS  PubMed  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 diaztropicus and Herbaspirillum seropidicae in chemically defined culture media. Plant Growth Regul 24:7–11

    CAS  Google Scholar 

  • Biessy A, Novinscak A, Blom J, Léger G, Thomashow LS, Cazorla FM, Josic D, Filion M (2019) Diversity of phytobeneficial traits revealed by whole genome analysis of worldwide-isolated phenazine producing Pseudomonas spp. Environ Microbiol 21:437–455

    CAS  PubMed  Google Scholar 

  • Borriss H (1955) Über einen Krümmungstest zum spezifischen Nachweis kleinster Wuchsstoffmengen. Ber Deut Bot Ges 68:24–25

    Google Scholar 

  • Borriss H (1956) Biologische und chemische Methoden zum Nachweis pflanzlicher Streckungswuchsstoffe (Auxine). In: Beloserski AN and Proskurjakow NI (eds) Praktikum der Biochemie der Pflanzen, pp. 389-405. Deutscher Verlag der Wissenschaften Berlin

  • Broadbent P, Baker KF, Waterworth Y (1977) Effect of Bacillus spp. on increased growth of seedlings in steamed and non-treated soil. Phytopathology 67:1027–1034

    Google Scholar 

  • Brown ME, Burlingham LSK (1968) Production of plant growth substances by Azotobacter chroococcum. J Gen Microbial 53:135–144

    CAS  Google Scholar 

  • Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V, Burrow AH, Beeckman T, Kepinski S, Traas J, Bennett MJ, Vernoux T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482:103–106

    CAS  PubMed  Google Scholar 

  • Bunsangiam S, Sakpuntoon V, Srisuk N, Ohashi T, Fujiyama K, Limtong S (2019) Biosynthetic pathway of indole-3-acetic acid in basidiomycetous yeast Rhodosporidiobolus fluvialis. Mycobiology 47:292–300

    PubMed  PubMed Central  Google Scholar 

  • 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 264:521–530

    CAS  PubMed  Google Scholar 

  • Chen F, Wang M, Zheng Y, Luo J, Yang X, Wang X (2010) Quantitative changes of plant defense enzymes and phytohormone in biocontrol of cucumber Fusarium wilt by Bacillus subtilis B579. World J Microbiol Biotechnol 26:675–684

    CAS  Google Scholar 

  • Cohen BA, Amsellem Z, Maor R, Sharon A, Gressel J (2002) Transgenically enhanced expression of indole-3-acetic acid confers hypervirulence to plant pathogens. Phytopathology 92:590–596

    CAS  PubMed  Google Scholar 

  • Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149:1579–1592

    CAS  PubMed  PubMed Central  Google Scholar 

  • Datta C, Basu P (2000) lndole acetic acid production by a Rhizobium species from root nodules of a leguminous shrub Cajanus cojan. Microbiol Res 155:123–127

    CAS  PubMed  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:153–162

    Google Scholar 

  • Donoso R, Leiva-Novoa P, Zúñiga A, Timmermann T, Recabarren-Gajardo G, González B (2017) Biochemical and genetic bases of indole-3-acetic acid (auxin phytohormone) degradation by the plant growth-promoting rhizobacterium Paraburkholderia phytofirmans PsJN. Appl Environ Microbiol 83:e01991–e01916

    CAS  PubMed  Google Scholar 

  • Enders TA, Strader LC (2015) Auxin activity: past, present, and future. Am J Bot 102:180–196

    CAS  PubMed  PubMed Central  Google Scholar 

  • Etemadi M, Gutjahr C, Couzigou JM, Zouine M, Lauressergues D, Timmers A, Audran C, Bouzayen M, Becard G, Combier JP (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292

    PubMed  PubMed Central  Google Scholar 

  • Etesami H, Alikhani HA, Hosseini HM (2015) Indole-3-acetic acid (IAA) production trait, a useful screening to select endophytic and rhizosphere competent bacteria for rice growth promoting agents. MethodsX 2:72–78

    PubMed  PubMed Central  Google Scholar 

  • Fan B, Blom J, Klenk HP, Borriss R (2017) Bacillus amyloliquefaciens, Bacillus velezensis and Bacillus siamensis form an ‘operational group B. amyloliquefaciens’ within the B. subtilis species complex. Front Microbiol 8:22

    PubMed  PubMed Central  Google Scholar 

  • Fan B, Wang C, Song X, Ding X, Wu L, Wu H, Gao X, Borriss R (2018) Bacillus velezensis FZB42 in 2018: the gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol 9:2491

    PubMed  PubMed Central  Google Scholar 

  • Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987

    CAS  PubMed  Google Scholar 

  • Fritze D (2004) Taxonomy of the genus Bacillus and related genera: the aerobic endospore forming bacteria. Phytopathology 94:1245–1248

    PubMed  Google Scholar 

  • Fu S-F, Wei J-Y, Chen H-W, Liu Y-Y, Lu H-Y, Chou J-Y (2015) Indole-3-acetic acid: a widespread physiological code in interactions of fungi with other organisms. Plant Signal Behav 10:e1048052

    PubMed  PubMed Central  Google Scholar 

  • Furukawa T, Koga J, Adachi T, Kishi K, Syono K (1996) Efficient conversion of L-tryptophan to indole-3-acetic acid and/or tryptophol by some species of Rhizoctonia. Plant Cell Physiol 37:899–905

    CAS  Google Scholar 

  • Glick BR, Jacobson RB, Schwarzme MK, Pasternaj JK (1994) 1-Aminocyclopropane- I -carboxylic acid deaminase mutants of the plant growth promoting rhizobacterium. Pseudomonas putida GrlRn 12-2 do not stimulate canola root elongation. Can J Microbiol 40:911–915

    CAS  Google Scholar 

  • Glick BR, Liu C, Ghosh S, Dumbroff EB (1997) Early development of canola seedlings in the presence of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Soil Biol Biochem 29:1233–1239

    CAS  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    CAS  PubMed  Google Scholar 

  • Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500

    Google Scholar 

  • Gravel V, Antoun H, Tweddell RJ (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977

    CAS  Google Scholar 

  • Gruen HE (1959) Auxins and fungi. Annu Rev Plant Physiol 10:405–440

    CAS  Google Scholar 

  • Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting Rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. J Microbiol Biochem 7:6–102

    Google Scholar 

  • Gust AA, Willmann R, Desaki Y, Grabherr HM, Nurnberger T (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci 17:495–502

    CAS  PubMed  Google Scholar 

  • Gutierrez-Manero FJ, Ramos-Solano B, Probanza A, Mehuachi J, Tadeo FR, Talon M (2001) The plant growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant 111:206–211

    Google Scholar 

  • Haas H (2014) Fungal siderophore metabolism with a focus on Aspergillus fumigatus. Nat Prod Rep 31:1266–1276

    CAS  PubMed  PubMed Central  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    CAS  PubMed  Google Scholar 

  • Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25

    CAS  PubMed  Google Scholar 

  • Hernández-Rodríguez A, Heydrich-Pérez M, Acebo-Guerrero Y, Velazquez-del Valle MG, Hernández-Lauzardo AN (2008) Antagonistic activity of Cuban native rhizobacteria against Fusarium verticillioides (Sacc.) Nirenb. in maize (Zea mays L.). Appl Soil Ecol 39:180–186

    Google Scholar 

  • Heydarian Z, Yu M, Gruber M, Glick BR, Zhou R, Hegedus DD (2016) Inoculation of soil with plant growth promoting bacteria producing 1-aminocyclopropane-1-carboxylate deaminase or expression of the corresponding acds gene in transgenic plants increases salinity tolerance in Camelina sativa. Front Microbiol 7:1966

    PubMed  PubMed Central  Google Scholar 

  • Huddedar SB, Shete AM, Tilekar JN, Gore SD, Dhavale DD, Chopade BA (2002) Isolation, characterization, and plasmid pUPI126-mediated indole-3-acetic acid production in Acinetobacter strains from rhizosphere of wheat. Appl Biochem Biotechnol 102–103:21–39

    PubMed  Google Scholar 

  • Idris EE, Bochow H, Ross H, Borriss R (2004) Use of Bacillus subtilis as biocontrol agent. VI. Phytohormone-like action of culture filtrates prepared from plant growth promoting Bacillus amyloliquefaciens FZB24, FZB42, FZB45 and Bacillus subtilis FZB37. Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz (J Plant Dis Prot) 111:583–597

    CAS  Google Scholar 

  • Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant-Microbe Interact 20:619–626

    CAS  PubMed  Google Scholar 

  • Jameson P (2000) Cytokinins and auxins in plant-pathogen interactions-an overview. Plant Growth Regul 32:369–380

    CAS  Google Scholar 

  • Jogaiah S, Abdelrahman M, Tran LS, Shin-ichi I (2013) Characterization of rhizosphere fungi that mediate resistance in tomato against bacterial wilt disease. J Exp Bot 64:3829–3842

    CAS  PubMed  Google Scholar 

  • Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B (2005) Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environ Microbiol 7:1809–1817

    CAS  PubMed  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant-Microbe Interact 19:250–256

    CAS  PubMed  Google Scholar 

  • Kamoun S (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10:358–365

    CAS  PubMed  Google Scholar 

  • Karnwal A (2009) Production of indole acetic acid by fluorescent Pseudomonas in the presence of l-tryptophan and rice root exudates. J Plant Pathol 91:61–63

    CAS  Google Scholar 

  • Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307

    CAS  Google Scholar 

  • Keswani C, Mishra S, Sarma BK, Singh SP, Singh HB (2014) Unravelling the efficient applications of secondary metabolites of various Trichoderma spp. Appl Microbiol Biotechnol 98:533–544

    CAS  PubMed  Google Scholar 

  • Keswani C, Singh HB, Vinale F, Hermosa R, García-Estrada C, Caradus J, He Y-W, Mezaache-Aichour S, Glare TR, Borriss R, Sansinenea E (2019a) Antimicrobial secondary metabolites from agriculturally important fungi as next biocontrol agents. Appl Microbiol Biotechnol 103:9287–9303

    CAS  PubMed  Google Scholar 

  • Keswani C, Prakash O, Bharti N, Vílchez JI, Sansinenea E, Lally RD, Borriss R, Singh SP, Gupta VK, Fraceto LF, de Lima R (2019b) Re-addressing the biosafety issues of plant growth promoting rhizobacteria. Sci Total Environ 690:841–852

    CAS  PubMed  Google Scholar 

  • Keswani C, Singh HB, García-Estrada C, Caradus J, He YW, Mezaache-Aichour S, Glare TR, Borriss R, Sansinenea E (2020) Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides. Appl Microbiol Biotechnol 104:1013–1034

    CAS  PubMed  Google Scholar 

  • Khalid A, Tahir S, Arshad M, Zahir ZA (2004) Relative efficiency of rhizobacteria for auxin biosynthesis in rhizosphere and non-rhizosphere soils. Aust J Soil Res 42:921–926

    CAS  Google Scholar 

  • Kobayashi M, Suzuki T, Fujita T, Masuda M, Shimizu S (1995) Occurrence of enzymes involved in biosynthesis of indole-3-acetic acid from indole-3-acetonitrile in plant-associated bacteria, Agrobacterium and Rhizobium. Proc Natl Acad Sci U S A 92:714–718

    CAS  PubMed  PubMed Central  Google Scholar 

  • Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krause K, Henke C, Asiimwe T, Ulbricht A, Klemmer S, Schachtschabel D, Boland W, Kothe E (2015) Biosynthesis and secretion of indole-3-acetic acid and its morphological effects on Tricholoma vaccinum-spruce ectomycorrhiza. Appl Environ Microbiol 81:7003–7011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kulkarni GB, Nayak AS, Sajjan SS, Oblesha A, Karegoudar TB (2013a) Indole-3-acetic acid biosynthetic pathway and aromatic amino acid aminotransferase activities in Pantoea dispersa strain GPK. Lett Appl Microbiol 56:340–347

    CAS  PubMed  Google Scholar 

  • Kulkarni GB, Sanjeevkumar S, Kirankumar B, Santoshkumar M, Karegoudar TB (2013b) Indole-3-acetic acid biosynthesis in Fusarium delphinoides strain GPK, a causal agent of Wilt in Chickpea. Appl Biochem Biotechnol 169:1292–1305

    CAS  PubMed  Google Scholar 

  • Kumla J, Suwannarach N, Matsui K, Lumyong S (2020) Biosynthetic pathway of indole-3-acetic acid in ectomycorrhizal fungi collected from northern Thailand. PLoS One 15:e0227478

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lambrecht M, Okon Y, Vande Broek A, Vanderleyden J (2000) Indole-3-acetic acid: a reciprocal signalling molecule in bacteria–plant interactions. Trends Microbiol 8:298–230

    CAS  PubMed  Google Scholar 

  • Lebuhn M, Heulin T, Hartmann A (1997) Production of auxin and other indolic and phenolic compounds by Paenibacillus polymyxa strains isolated from different proximity to plant roots. FEMS Microbiol Ecol 22:325–334

    CAS  Google Scholar 

  • Lee M, Breckenridge C, Knowles DR (1970) Effect of some culture conditions on the production of indole-3-acetic acid and a gibberellin-like substance by Azotobacter vinelandii. Can J Microbiol 16:1325–1330

    CAS  PubMed  Google Scholar 

  • Li M, Guo R, Yu F, Chen X, Zhao H, Li H, Wu J (2018) Indole-3-acetic acid biosynthesis pathways in the plant-beneficial bacterium Arthrobacter pascens ZZ21. Int J Mol Sci 2018:443

    Google Scholar 

  • Libbert E, Kaiser W, Kunert R (2006) Interactions between plants and epiphytic bacteria regarding their auxin metabolism VI. The influence of the epiphytic bacteria on the content of extractable auxin in the plant. Physiol Plant 22:432–439

    Google Scholar 

  • Limtong S, Koowadjanakul N (2012) Yeasts from phylloplane and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 28:3323–3335

    CAS  PubMed  Google Scholar 

  • Liu YP, Chen L, Zhang N, Li Z, Zhang G, Xu Y, Shen Q, Zhang R (2016a) Plant-microbe communication enhances auxin biosynthesis by a root-associated bacterium Bacillus amyloliquefaciens SQR9. Mol Plant-Microbe Interact 29:324–330

    CAS  PubMed  Google Scholar 

  • Liu YY, Chen HW, Chou JY (2016b) Variation in indole-3-acetic acid production by wild Saccharomyces cerevisiae and S. paradoxus strains from diverse ecological sources and its effect on growth. PLoS One 11:e0160524–e0160524

    PubMed  PubMed Central  Google Scholar 

  • Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872

    CAS  PubMed  Google Scholar 

  • Manulis S, Shafrir H, Epstein E, Lichter A, Barash I (1994) Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology 140:1045–1050

    CAS  PubMed  Google Scholar 

  • Maor R, Haskin S, Levi-Kedmi H, Sharon A (2004) In planta production of indole-3-acetic acid by Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 70:1852–1854

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Pařezová M, Petrášek J, Friml J, Kleine-Vehn J, Benková E (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21:796–804

    PubMed  Google Scholar 

  • MarketWhatch (2020) Indole-3-acetic acid (IAA) market size forecast report 2020

  • Mendoza-Hernández JC, Perea-Vélez YS, Arriola-Morales J, Martínez-Simón SM, Pérez-Osorio (2016) Assessing the effects of heavy metals in ACC deaminase and IAA production on plant growth-promoting bacteria. Microbiol Res 188-189:53–61

    Google Scholar 

  • Mezaache-Aichour S, Guechi A, Nicklin J, Drider D, Prevost H, Strange RN (2012) Isolation, identification and antimicrobial activity of pseudomonads isolated from the rhizosphere of potatoes growing in Algeria. J Plant Pathol 94:89–98

    Google Scholar 

  • Mishra PK, Mishra S, Bisht SC, Selvakumar G, Kundu S, Bisht JK, Gupta HS (2009) Isolation, molecular characterization and growth-promotion activities of a cold tolerant bacterium Pseudomonas sp. NARs9 (MTCC9002) from the Indian Himalayas. Biol Res 42:305–313

    CAS  PubMed  Google Scholar 

  • Mohite B (2013) Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. J Soil Sci Plant Nutr 13:638–649

    Google Scholar 

  • Mole BM, Baltrus DA, Dangl JL, Grant SR (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol 15:363–371

    CAS  PubMed  Google Scholar 

  • Mukherjee S, Sen SK (2015) Exploration of novel rhizospheric yeast isolate as fertilizing soil inoculant for improvement of maize cultivation. J Sci Food Agric 95:1491–1499

    CAS  PubMed  Google Scholar 

  • Myo EM, Ge B, Ma J, Cui H, Liu B, Shi L, Jiang M, Zhang K (2019) Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiol 19:155

    PubMed  PubMed Central  Google Scholar 

  • Oberhansli T, Defago G, Haas D (1991) Indole-3-acetic acid (IAA) synthesis in the biocontrol strain CHA0 of Pseudomonas fluorescens: role of tryptophan side chain oxidase. J Gen Microbiol 137:2273–2279

    CAS  PubMed  Google Scholar 

  • Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197

    PubMed  PubMed Central  Google Scholar 

  • Ortiz-Castro R, Contreras-Cornejo HA, Macias-Rodriguez L, Lopez-Bucio J (2009) The role of microbial signals in plant growth and development. Plant Signal Behav 4:701–712

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ozimek E, Jaroszuk-Scisel J, Bohacz J, Kornillowicz-Kowalska T, Tyskiewicz R, Slomka A, Nowak A, Hanaka A (2018) Synthesis of indoleacetic acid, gibberellic acid and ACC-deaminase by Mortierella strains promotea winter wheat seedlings growth under different conditions. In J Mol Sci 19:3218

    Google Scholar 

  • Parsek M, Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33

    CAS  PubMed  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    CAS  PubMed  Google Scholar 

  • Pérez-Montaño F, Alías-Villegas C, Bellogín R, Del Cerro P, Espuny M, Jiménez-Guerrero I, Lopez-Baena FJ, Ollero FJ, Cubo T (2014) Plant growth promotion in cereal and leguminous agricultural important plants: from microorganism capacities to crop production. Microbiol Res 169:325–336

    PubMed  Google Scholar 

  • Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant–rhizobacteria interactions. Plant Cell Environ 26:189–199

    CAS  Google Scholar 

  • Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    PubMed  Google Scholar 

  • Phi QT, Park YM, Ryu CM, Park SH, Ghim SY (2008) Functional identification and expression of indole-3-pyruvate decarboxylase from Paenibacillus polymyxa E681. J Microbiol Biotechnol 18:1235–1244

    CAS  PubMed  Google Scholar 

  • Phi QT, Park YM, Seul KJ, Ryu CM, Park SH, Kim JG, Ghim SY (2010) Assessment of root-associated Paenibacillus polymyxa groups on growth promotion and induced systemic resistance in pepper. J Microbiol Biotechnol 20:1605–1613

    CAS  PubMed  Google Scholar 

  • Picard C, Bosco M (2003) Soil antimony pollution and plant growth stage affect the biodiversity of auxin-producing bacteria isolated from the rhizosphere of Achillea ageratum L. FEMS Microbiol Ecol 46:73–80

    CAS  PubMed  Google Scholar 

  • Piotrowska-Niczyporuk A, Bajguz A (2014) The effect of natural and synthetic auxins on the growth, metabolite content and antioxidant response of green alga Chlorella vulgaris (Trebouxiophyceae). Plant Growth Regul 73:57–66

    CAS  Google Scholar 

  • Pliego C, Cazorla FM, Gonzalez-Sanchez MA, Perez-Jimenez RM, de Vicente A, Ramos C (2007) Selection for biocontrol bacteria antagonistic toward Rosellinia necatrix by enrichment of competitive avocado root tip colonizers. Res Microbiol 158:463–470

    CAS  PubMed  Google Scholar 

  • Pokorny R (1941) New compounds. Some chlorophenoxyacetic acids. J Am Chem Soc 63:1768

    CAS  Google Scholar 

  • Prinsen E, Costacura A, Michiels K, Vanderleyden J, Van Onckelen H (1993) Azospirillum brasilense indole-3-acetic acid biosynthesis: evidence for a non-tryptophan dependent pathway. Mol Plant-Microbe Interact 6:609–615

    CAS  Google Scholar 

  • Prusty R, Grisafi P, Fink GR (2004) The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 101:4153–4157

    CAS  PubMed  PubMed Central  Google Scholar 

  • Radhakrishnan R, Shim KB, Lee BW, Hwang CD, Pae SB, Park CH, Kim SU, Lee CK, Baek IY (2013) IAA-producing Penicillium sp. NICS01 triggers plant growth and suppresses Fusarium sp.-induced oxidative stress in sesame (Sesamum indicum L.). J Microbiol Biotechnol 23:856–863

    CAS  PubMed  Google Scholar 

  • Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842

    CAS  PubMed  Google Scholar 

  • Rajkumar M, Nagendran R, Lee KJ, Lee WH, Kim SZ (2006) Influence of plant growth promoting bacteria and Cr6+ on the growth of Indian mustard. Chemosphere 62:741–748

    CAS  PubMed  Google Scholar 

  • 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. Genetics 185:211–220

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raut V, Shaikh I, Naphade B, Prashar K, Adhapure N (2017) Plant growth promotion using microbial IAA producers in conjunction with azolla: a novel approach. Chem Biol Technol Agric 4:1

    Google Scholar 

  • 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 9:339–355

    CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson M, Riov J, Sharon A (1998) Indole-3-acetic acid biosynthesis in Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 64:5030–5032

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ruanpanun P, Tangchitsomkid N, Hyde K, Lumyong S (2010) Actinomycetes and fungi isolated from plant-parasitic nematode infested soils: Screening of the effective biocontrol potential, indole-3-acetic acid and siderophore production. World J Microbiol Biotechnol 26:1569–1578

    CAS  Google Scholar 

  • Rubin RL, Van Groenigen KJ, Hungate BA (2017) Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis. Plant Soil 416:309–323

    CAS  Google Scholar 

  • Ruzzi M, Aroca R (2015) Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci Hortic 196:124–134

    CAS  Google Scholar 

  • San-Francisco S, Houdusse F, Zamarreno AM, Garnica M, Casanova E, García-Mina JM (2005) Effects of IAA and IAA precursors on the development, mineral nutrition, IAA content and free polyamine content of pepper plants cultivated in hydroponic conditions. Sci Hortic 106:38–52

    CAS  Google Scholar 

  • Selvakumar G, Mohan M, Kundu S, Gupta AD, Joshi P, Nazim S, Gupta HS (2008) Cold tolerance and plant growth promotion potential of Serratia marcescens strain SRM (MTCC 8708) isolated from flowers of summer squash (Cucurbita pepo). Lett Appl Microbiol 46:171–175

    CAS  PubMed  Google Scholar 

  • Shaharoona B, Naveed M, Arshad M, Zahir ZA (2008) Fertilizer-dependent efficiency of Pseudomonads for improving growth, yield, and nutrient use efficiency of wheat (Triticum aestivum L.). Appl Microbiol Biotechnol 79:147–155

    CAS  PubMed  Google Scholar 

  • Shao J, Li S, Zhang N, Cui X, Zhou X, Zhang G, Shen Q, Zhang R (2015) Analysis and cloning of the synthetic pathway of the phytohormone indole-3-acetic acid in the plant-beneficial Bacillus amyloliquefaciens SQR9. Microb Cell Factories 14:130

    Google Scholar 

  • Singh HB, Sarma BK, Keswani C (2016) Agriculturally important microorganisms: commercialization and regulatory requirements in Asia. Springer, Singapore, 336 pages

    Google Scholar 

  • Singh HB, Sarma BK, Keswani C (2017) Advances in PGPR Research. CABI, UK, 408 pages

    Google Scholar 

  • Singh HB, Keswani C, Reddy MS, Sansinenea E, García-Estrada C (2019) Secondary metabolites of plant growth promoting rhizomicroorganisms: discovery and applications. Springer-Nature, Singapore, 392 pages

    Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant – microbe interactions. Cold Spring Harb Perspect Biol 3:a001438

    PubMed  PubMed Central  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    CAS  PubMed  Google Scholar 

  • Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9:737–748

    CAS  PubMed  Google Scholar 

  • Sudha M, Gowri S, Prabhavathi R, Astapriya P, Devi PY, Saranya A (2012) Production and optimization of indole acetic acid by indigenous micro flora using agro-waste as substrate. Pak J Biol Sci 15:39–43

    CAS  PubMed  Google Scholar 

  • Sun PF, Fang WT, Shin LY, Wei JY, Fu SF, Chou JY (2014) Indole-3-acetic acid-producing yeasts in the phyllosphere of the carnivorous plant Drosera indica L. PLoS One 9:e114196

    PubMed  PubMed Central  Google Scholar 

  • Tanimoto E (2005) Regulation of root growth by plant hormones—roles for auxin and gibberellin. CRC Crit Rev Plant Sci 24:249–265

    CAS  Google Scholar 

  • Teale WD, Paponov IA, Palme K (2006) Auxin in action: signaling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 7:847–859

    CAS  PubMed  Google Scholar 

  • Templeman WG, Marmoy CJ (2008) The effect upon the growth of plants of watering with solutions of plant-growth substances and of seed dressings containing these materials. Ann Appl Biol 27:453–471

    Google Scholar 

  • Thomashow LS, Reeves S, Thomashow MF (1984) Crown gall oncogenesis: evidence that a T-DNA gene from the Agrobacterium Ti plasmid pTiA6 encodes an enzyme that catalyzes synthesis of indoleacetic acid. Proc Natl Acad Sci U S A 81:5071–5075

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tien TM, Gaskins 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852

    CAS  Google Scholar 

  • Tivendale ND, Ross JJ, Cohen JD (2014) The shifting paradigms of auxin biosynthesis. Trends Plant Sci 19:44–51

    CAS  PubMed  Google Scholar 

  • Tzeng D (2004) Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustilago esculenta. J Biol Sci 4:744–750

    Google Scholar 

  • Ulrich J (2006) Auxin production by mycorrhizal fungi. Physiol Plant 13:429–443

    Google Scholar 

  • Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moënne-Loccoz Y, Muller D, Legendre L, Wisniewski-Dyé F, Prigent-Combaret C (2013) Plant growth-promoting rhizobacteria and root system functioning. Front Plant Sci 4:356

    PubMed  PubMed Central  Google Scholar 

  • Vandeputte O, Öden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E (2005) Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infect plant tissues. Appl Environ Microbiol 71:1169–1177

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vediyappan G, Dumontet V, Pelissier F, d'Enfert C (2013) Gymnemic acids inhibit hyphal growth and virulence in Candida albicans. PLoS One 8:e74189

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verma VC, Singh SK, Prakash S (2011) Biocontrol and plant growth promotion potential of siderophore producing endophytic Streptomyces from Azadirachta indica A. Juss J Basic Microbiol 51:550–556

    CAS  PubMed  Google Scholar 

  • Vivas A, Biro B, Ruiz-Lozano JM, Barea JM, Azcon R (2006) Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn toxicity. Chemosphere 52:1523–1533

    Google Scholar 

  • Wani PA, Khan MS (2010) Bacillus species enhance growth parameters of chickpea (Cicer arietinum L.) in chromium stressed soils. Food Chem Toxicol 48:3262–3267

    CAS  PubMed  Google Scholar 

  • Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163

    CAS  PubMed  Google Scholar 

  • Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    CAS  PubMed  Google Scholar 

  • Wong WS, Tan SN, Ge L, Chen X, Yong JWH (2015) The importance of phytohormones and microbes in biofertilizers. In: Maheshwari D (ed) Bacterial metabolites in sustainable agroecosystem, Sustainable Development and Biodiversity, vol 12. Springer, Cham, pp 105–158

  • Wright AD, Sampson MB, Neuffer MG, Michalczuk L, Slovin JP, Cohen JD (1991) Indole-3-acetic acid biosynthesis in the mutant maize orange pericarp, a tryptophan auxotroph. Science 254:998–1000

    CAS  PubMed  Google Scholar 

  • Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida CR12-2 that overproduce indoleacetic acid. Curr Microbiol 32:67–71

    CAS  Google Scholar 

  • Yu P, Hegeman AD, Cohen JD (2014) A facile means for the identification of indolic compounds from plant tissues. Plant J 79:1065–1075

    CAS  PubMed  Google Scholar 

  • Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ 101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64:991–997

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Zboralski A, Biessy A, Savoie M-C, Novinscak A, Filion M (2020) Metabolic and genomic traits of phytobeneficial phenazine producing Pseudomonas spp. are linked to rhizosphere colonization in Arabidopsis thaliana and Solanum tuberosum. Appl Environ Microbiol 86:e02443–e02419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang P, Jin T, Sahu SK, Xu J, Shi Q, Liu H, Wang Y (2019) The distribution of tryptophan-dependent indole-3-acetic acid synthesis pathways in bacteria unraveled by large-scale genomic analysis. Molecules 2019:1411

    Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmer W, Hundeshagen B, Niederau E (1994) Demonstration of the indole pyruvate decarboxylase gene homologue in different auxin-producing species of the Enterobacteriaceae. Can J Microbiol 40:1072–1076

    CAS  PubMed  Google Scholar 

Download references

Contributors

All the authors have contributed equally, have read and approved the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Estibaliz Sansinenea.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Keswani, C., Singh, S.P., Cueto, L. et al. Auxins of microbial origin and their use in agriculture. Appl Microbiol Biotechnol 104, 8549–8565 (2020). https://doi.org/10.1007/s00253-020-10890-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10890-8

Keywords

Navigation