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.
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
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
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J. King Saud Univ Sci 26:1–20
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
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
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
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
Babalola OO (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570
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
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
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
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
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
Borriss H (1955) Über einen Krümmungstest zum spezifischen Nachweis kleinster Wuchsstoffmengen. Ber Deut Bot Ges 68:24–25
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
Brown ME, Burlingham LSK (1968) Production of plant growth substances by Azotobacter chroococcum. J Gen Microbial 53:135–144
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
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
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
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
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
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
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
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
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
Enders TA, Strader LC (2015) Auxin activity: past, present, and future. Am J Bot 102:180–196
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
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
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
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
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
Fritze D (2004) Taxonomy of the genus Bacillus and related genera: the aerobic endospore forming bacteria. Phytopathology 94:1245–1248
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
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
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
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
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
Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2:1127500
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
Gruen HE (1959) Auxins and fungi. Annu Rev Plant Physiol 10:405–440
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
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
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
Haas H (2014) Fungal siderophore metabolism with a focus on Aspergillus fumigatus. Nat Prod Rep 31:1266–1276
Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42
Hermosa R, Viterbo A, Chet I, Monte E (2012) Plant-beneficial effects of Trichoderma and of its genes. Microbiology 158:17–25
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
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
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
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
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
Jameson P (2000) Cytokinins and auxins in plant-pathogen interactions-an overview. Plant Growth Regul 32:369–380
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
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
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
Kamoun S (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 10:358–365
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
Kende H (1993) Ethylene biosynthesis. Annu Rev Plant Physiol Plant Mol Biol 44:283–307
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
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
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
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
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
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
Korasick DA, Enders TA, Strader LC (2013) Auxin biosynthesis and storage forms. J Exp Bot 64:2541–2555
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
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
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
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
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
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
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
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
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
Limtong S, Koowadjanakul N (2012) Yeasts from phylloplane and their capability to produce indole-3-acetic acid. World J Microbiol Biotechnol 28:3323–3335
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
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
Mano Y, Nemoto K (2012) The pathway of auxin biosynthesis in plants. J Exp Bot 63:2853–2872
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
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
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
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
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
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
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
Mole BM, Baltrus DA, Dangl JL, Grant SR (2007) Global virulence regulation networks in phytopathogenic bacteria. Trends Microbiol 15:363–371
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
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
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
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197
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
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
Parsek M, Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13:27–33
Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220
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
Persello-Cartieaux F, Nussaume L, Robaglia C (2003) Tales from the underground: molecular plant–rhizobacteria interactions. Plant Cell Environ 26:189–199
Petrášek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688
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
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
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
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
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
Pokorny R (1941) New compounds. Some chlorophenoxyacetic acids. J Am Chem Soc 63:1768
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
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
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
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
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
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
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
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
Robinson M, Riov J, Sharon A (1998) Indole-3-acetic acid biosynthesis in Colletotrichum gloeosporioides f. sp. aeschynomene. Appl Environ Microbiol 64:5030–5032
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
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
Ruzzi M, Aroca R (2015) Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Sci Hortic 196:124–134
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
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
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
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
Singh HB, Sarma BK, Keswani C (2016) Agriculturally important microorganisms: commercialization and regulatory requirements in Asia. Springer, Singapore, 336 pages
Singh HB, Sarma BK, Keswani C (2017) Advances in PGPR Research. CABI, UK, 408 pages
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
Spaepen S, Vanderleyden J (2011) Auxin and plant – microbe interactions. Cold Spring Harb Perspect Biol 3:a001438
Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448
Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9:737–748
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
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
Tanimoto E (2005) Regulation of root growth by plant hormones—roles for auxin and gibberellin. CRC Crit Rev Plant Sci 24:249–265
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
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
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
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
Timmusk S, Nicander B, Granhall U, Tillberg E (1999) Cytokinin production by Paenibacillus polymyxa. Soil Biol Biochem 31:1847–1852
Tivendale ND, Ross JJ, Cohen JD (2014) The shifting paradigms of auxin biosynthesis. Trends Plant Sci 19:44–51
Tzeng D (2004) Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustilago esculenta. J Biol Sci 4:744–750
Ulrich J (2006) Auxin production by mycorrhizal fungi. Physiol Plant 13:429–443
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
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
Vediyappan G, Dumontet V, Pelissier F, d'Enfert C (2013) Gymnemic acids inhibit hyphal growth and virulence in Candida albicans. PLoS One 8:e74189
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
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
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
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
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346
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
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
Yu P, Hegeman AD, Cohen JD (2014) A facile means for the identification of indolic compounds from plant tissues. Plant J 79:1065–1075
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
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
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
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
Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64
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
Contributors
All the authors have contributed equally, have read and approved the manuscript.
Author information
Authors and Affiliations
Corresponding author
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-020-10890-8