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In vitro production of IAA by endophytic fungus Aspergillus awamori and its growth promoting activities in Zea mays

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Abstract

Indole-3-acetic acid (IAA) plays an important role in plant microbe interactions. Current study explored the role of indole-3-acetic acid (IAA) as a signalling molecule for chemical dialogue between endophytic fungus and host plant roots. The endophytic fungus was isolated from the leaves of drought stressed Withenia somnifera and was identified as Aspergillus awamori Wl1 through ITS region of 18 S rDNA sequence. The isolated Wl1 strain was capable of producing important secondary metabolites, including IAA, phenols and sugars. Culture filtrate of the strain contained 24.2, 275.4 and 127.4 μg/mL of IAA, phenols and sugars, respectively. The strain has efficiently colonized the maize roots and enhanced the growth of host plant. In order to determine the role of IAA in root colonization by endophyte, we inhibited the biosynthesis of IAA. Inhibition of IAA production by foliar application of yucasin effectively reduced the colonization of endophyte in maize roots by 52%, whereas root application of yucasin has decreased the colonization frequency by 66%. However, the application of IAA restored the ability of Aspergillus awamori to colonize maize roots and significantly improved various growth parameters. From these observations, it is concluded that IAA plays a vital role in initiating a crosstalk between the two partners.

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References

  • Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turkish J Biol 29:29–34

    CAS  Google Scholar 

  • Arenal F, Platas G, Pelaez F (2007) A new endophytic species of Preussia (Sporormiaceae) inferred from morphological observations and molecular phylogenetic analysis. Fungal Divers 25:1–17

    Google Scholar 

  • Badri DV, Quintana N, El Kassis EG, Kim HK, Choi YH, Sugiyama A, Verpoorte R, Martinoia E, Manter DK, Vivanco JM (2009) An ABC transporter mutation alters root exudation of phytochemicals that provoke an overhaul of natural soil microbiota. Plant Physiol 151:2006–2017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, Van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nature biotechnol 22:583–588

    Article  CAS  Google Scholar 

  • Bashan Y, Holguin GAND, De-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997-2003). Can J Microbiol 50:521–577

    Article  CAS  PubMed  Google Scholar 

  • Chadha N, Prasad R, Varma A (2015) Plant promoting activities of fungal endophytes associated with tomato roots from central Himalaya, India and their interaction with Piriformospora indica. Int J Pharm Bio Sci 6:333–343

    Google Scholar 

  • Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18

    Article  PubMed  Google Scholar 

  • Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). Biochem Mol biol plants 24:1250–1319

    Google Scholar 

  • Dardanelli MS, Manyani H, Gonzalez-Barroso S, Rodriguez-Carvajal MA, Gil-Serrano AM, Espuny MR, Lopez-Baena FJ, Bellogín RA, Megías M, Ollero FJ (2010) Effect of the presence of the plant growth promoting rhizobacterium (PGPR) Chryseobacterium balustinum Aur9 and salt stress in the pattern of flavonoids exuded by soybean roots. Plant Soil 328:483–493

    Article  CAS  Google Scholar 

  • Dastogeer KM, LI H, Sivasithamparam K, Jones MG, DU X, Ren Y, Wylie SJ (2017) Metabolic responses of endophytic Nicotiana benthamiana plants experiencing water stress. Environ Exp Bot 143:59–71

    Article  CAS  Google Scholar 

  • El-Tarabily KA (2004) Suppression of Rhizoctonia solani diseases of sugar beet by antagonistic and plant growth-promoting yeasts. J Appl Microbiol 96:69–75

    Article  CAS  PubMed  Google Scholar 

  • Fahad S, Bano A (2012) Effect of salicylic acid on physiological and biochemical characterization of maize grown in saline area. Pak J Bot 44:1433–1438

    Google Scholar 

  • Fouda AH, Hassan SE-D, Eid AM, Ewais EE-D (2015) Biotechnological applications of fungal endophytes associated with medicinal plant Asclepias sinaica (Bioss.). Ann Agric Sci 60:95–104

    Article  Google Scholar 

  • Frankenberger WT, Poth M (1987) Biosynthesis of indole-3-acetic acid by the pine ectomycorrhizal fungus Pisolithus tinctorius. Appl Environ Microbiol 53:2908–2913

    CAS  PubMed  PubMed Central  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 10:1048052

    Article  CAS  Google Scholar 

  • Gouda S, Das G, Sen SK, Shin HS, Patra JK (2016) Endophytes: a treasure house of bioactive compounds of medicinal importance. Front Microbiol 7:1538

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamayun M, Khan SA, Iqbal I, Ahmad B, Lee I-J (2010) Isolation of a gibberellin-producing fungus (Penicillium sp. MH7) and growth promotion of crown daisy (Chrysanthemum coronarium). J Microbiol Biotechnol 20:202–207

    CAS  PubMed  Google Scholar 

  • Hassan SE, Hijri M, St-Arnaud M (2013) Effect of arbuscular mycorrhizal fungi on trace metal uptake by sunflower plants grown on cadmium contaminated soil. New Biotechnol 30:780–787

    Article  CAS  Google Scholar 

  • Hilbert, M., (2012). Biochemical and molecular analyses of the biosynthesis pathway of the indole derivatives in Piriformospora indica

    Google Scholar 

  • Huang X-F, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92:267–275

    Article  Google Scholar 

  • Hussain A, Shah ST, Rahman H, Irshad M, Iqbal A (2015) Effect of IAA on in vitro growth and colonization of Nostoc in plant roots. Front Plant Sci 6:46

    Article  PubMed  PubMed Central  Google Scholar 

  • Hutsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407

    Article  CAS  Google Scholar 

  • Kaya C, Ashraf M, Dikilitas M, Tuna AL (2013) Alleviation of salt stress-induced adverse effects on maize plants by exogenous application of indoleacetic acid (IAA) and inorganic nutrients-a field trial. Aust J Crop Sci 7:249

    CAS  Google Scholar 

  • Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480

    Article  CAS  PubMed  Google Scholar 

  • Khan SA, Hamayun M, Yoon H, Kim H-Y, Suh S-J, Hwang S-K, Kim J-M, Lee I-J, Choo Y-S, Yoon U-H (2008) Plant growth promotion and Penicillium citrinum. BMC Microbiol 8:231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan R, Shahzad S, Choudhary MI, Khan SA, Ahmad A (2010) Communities of endophytic fungi in medicinal plant Withania somnifera. Pak J Bot 42:1281–1287

    Google Scholar 

  • Khan N, Bano A, Babar MA (2016) The root growth of wheat plants, the water conservation and fertility status of sandy soils influenced by plant growth promoting rhizobacteria. Symbiosis, 72:(3), 195–205

  • Khan N, Bano A, Babar MA (2017) The root growth of wheat plants, the water conservation and fertility status of sandy soils influenced by plant growth promoting rhizobacteria. Symbiosis 72:195–205

    Article  CAS  Google Scholar 

  • Khan N, Bano A, Zandi P (2018) Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. J Plant Interact 13:239–247

    Article  CAS  Google Scholar 

  • Khatoon S, Hanif NQ, Tahira I, Sultana N, Sultana K, Ayub N (2012) Natural occurrence of aflatoxins, zearalenone and trichothecenes in maize grown in Pakistan. Pak J Bot 44:231–236

    CAS  Google Scholar 

  • Klamer M, Bååth E (2004) Estimation of conversion factors for fungal biomass determination in compost using ergosterol and PLFA 18: 2ω6, 9. Soil Biology and Biochemistry, 36:(1), 57–65

  • Lubna AS, Hamayun M, Gul H, Lee IJ, Hussain A (2018) Aspergillus niger CSR3 regulates plant endogenous hormones and secondary metabolites by producing gibberellins and indoleacetic acid. J Plant Interact 13:100–111

    Article  CAS  Google Scholar 

  • Ludwig-Muller J (2015) Bacteria and fungi controlling plant growth by manipulating auxin: balance between development and defense. J Plant Physiol 172:4–12

    Article  CAS  PubMed  Google Scholar 

  • Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martens DA (2002) Relationship between plant phenolic acids released during soil mineralization and aggregate stabilization. Soil Sci Soc Am J 66:1857–1867

    Article  CAS  Google Scholar 

  • Meletiadis J, Meis JF, Mouton JW, Verweij PE (2001) Analysis of growth characteristics of filamentous fungi in different nutrient media. J Clin Microbiol 39:478–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura T, Hayashi KI, Suzuki H, Gyohda A, Takaoka C, Sakaguchi Y, Matsumoto S, Kasahara H, Sakai T, Kato JI (2014) Yucasin is a potent inhibitor of YUCCA, a key enzyme in auxin biosynthesis. Plant J 77:352–366

    Article  CAS  PubMed  Google Scholar 

  • Pandey SS, Singh S, Pandey H, Srivastava M, Ray T, Soni S, Pandey A, Shanker K, Babu CV, Banerjee S, Gupta MM (2018) Endophytes of Withania somnifera modulate in planta content and the site of withanolide biosynthesis. Sci Rep 8:5450

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Photita W, Lumyong S, Lumyong P, Hyde KD (2001) Endophytic fungi of wild banana (Musa acuminata) at doi Suthep Pui National Park. Thailand Mycol Res 105:1508–1513

    Article  Google Scholar 

  • Rafiq, C. M., Rafique, M., Hussain, A. & Altaf, M. (2010). Studies on heritability, correlation and path analysis in maize (Zea mays L.). J Agric Res 48:35–38

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reversat G, Boyer J, Sannier C, Pando-Bahuon A (1999) Use of a mixture of sand and water-absorbent synthetic polymer as substrate for the xenic culturing of plant-parasitic nematodes in the laboratory. Nematology 1:209–212

    Article  Google Scholar 

  • Rimmer DL, Abbott G (2011) Phenolic compounds in NaOH extracts of UK soils and their contribution to antioxidant capacity. Eur J Soil Sci 62:285–294

    Article  CAS  Google Scholar 

  • Rodriguez, R., White JR, J., Arnold, A. & Redman, A. R. A. 2009. Fungal endophytes: diversity and functional roles. New Phytol 182, 314–330

  • Schubert S, Neubert A, Schierholt A, Sümer A, Zörb C (2009) Development of salt-resistant maize hybrids: the combination of physiological strategies using conventional breeding methods. Plant Sci 177:196–202

    Article  CAS  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109(6):661–686

    Article  PubMed  Google Scholar 

  • Shahab S, Ahmed N, Khan NS (2009) Indole acetic acid production and enhanced plant growth promotion by indigenous PSBs. Afr J Agri Res 4:1312–1316

    Google Scholar 

  • Sieber TN, Waisel Y, EsheL A, Kafkafi U (2002) Fungal root endophytes. Plant roots: the hidden half:887–917

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

    Article  CAS  PubMed  Google Scholar 

  • Strobel G A (2003) Endophytes as sources of bioactive products. Microbes and infection 5:(6), 535–544.

  • Suryanarayanan TS, Venkatesan G, Murali TS (2003) Endophytic fungal communities in leaves of tropical forest trees: diversity and distribution patterns. Curr Sci:489–493

  • Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal biology reviews 23:(1–2), 9–19

  • Taiz, L. and Zeiger, E., (1998). Auxins. Plant Physiology. Sunderland, MA: Sinayer Associates 543–589

  • Vandeleur RK, Sullivan W, Athman A, Jordans C, Gilliham M, Kaiser BN, Tyerman SD (2014) Rapid shoot-to-root signalling regulates root hydraulic conductance via aquaporins. Plant Cell Environ 37:520–538

    Article  CAS  PubMed  Google Scholar 

  • Vila-aiub MM, Martinez-Ghersa MA, Ghersa CM (2003) Evolution of herbicide resistance in weeds: vertically transmitted fungal endophytes as genetic entities. Evol Ecol 17:441–456

    Article  Google Scholar 

  • Waqas M, Khan AL, Kamran M, Hamayun M, Kang S-M, Kim Y-H, Lee I-J (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waqas M, Khan AL, Kang SM, Kim YH, Lee IJ (2014) Phytohormone-producing fungal endophytes and hardwood-derived biochar interact to ameliorate heavy metal stress in soybeans. Biol Fert Soils 50:1155–1167

    Article  CAS  Google Scholar 

  • Weert S, Vermeiren H, Mulders IH, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. MPMI 15:1173–1180

    Article  PubMed  Google Scholar 

  • Yuan ZC, Haudecoeur E, Faure D, Kerr KF, Nester EW (2008) Comparative transcriptome analysis of agrobacterium tumefaciens in response to plant signal salicylic acid, indole-3-acetic acid and γ-amino butyric acid reveals signalling cross-talk and agrobacterium–plant co-evolution. Cell Microbiol 10:2339–2354

    Article  CAS  PubMed  Google Scholar 

  • Yue Q, Miller CJ, White JF, Richardson MD (2000) Isolation and characterization of fungal inhibitors from Epichlo ë festucae. J Agric Food Chem 48:4687–4692

    Article  CAS  PubMed  Google Scholar 

  • Zahoor M, Irshad M, Rahman H, Qasim M, Afridi SG, Qadir M, Hussain A (2017) Alleviation of heavy metal toxicity and phytostimulation of Brassica campestris L. by endophytic Mucor sp. MHR-7. Ecotoxicol Environ Safety 142:139–149

    Article  CAS  PubMed  Google Scholar 

  • Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annual review of plant biology 61:49–64

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Correspondence to Anwar Hussain.

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Mehmood, A., Hussain, A., Irshad, M. et al. In vitro production of IAA by endophytic fungus Aspergillus awamori and its growth promoting activities in Zea mays. Symbiosis 77, 225–235 (2019). https://doi.org/10.1007/s13199-018-0583-y

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