Genome Insight and factorial design to elucidate the regulation of the tryptophan-mediated IAA biosynthetic pathway in an endophyte

genome-insight-and-factorial-design-to-elucidate-the-regulation-of-the-tryptophan-mediated-iaa-biosynthetic-pathway-in-an-endophyte
Genome Insight and factorial design to elucidate the regulation of the tryptophan-mediated IAA biosynthetic pathway in an endophyte

References

  1. Abo Elsoud, M. M., Hasan, S. F. & Elhateir, M. M. Optimization of Indole-3-acetic acid production by Bacillus velezensis isolated from Pyrus rhizosphere and its effect on plant growth. Biocatal. Agric. Biotechnol. 50, 102714. https://doi.org/10.1016/j.bcab.2023.102714 (2023).

    Google Scholar 

  2. Adeleke, B., Ayangbenro, A. & Babalola, O. Genomic Analysis of Endophytic Bacillus cereus T4S and Its Plant Growth-Promoting Traits. Plants 10 (9), 1776. https://doi.org/10.3390/plants10091776 (2021).

    Google Scholar 

  3. Almirón, C. et al. Functional and genomic analyses of plant growth promoting traits in Priestia aryabhattai and Paenibacillus sp. isolates from tomato rhizosphere. Sci. Rep. 15 (1), 3498. https://doi.org/10.1038/s41598-025-87390-0 (2025).

    Google Scholar 

  4. Arora, P., Tabssum, R., Gupta, A. P., Kumar, S. & Gupta, S. Optimization of indole acetic acid produced by plant growth promoting fungus, aided by response surface methodology. Heliyon 10 (14), e34356. https://doi.org/10.1016/j.heliyon.2024.e34356 (2024).

    Google Scholar 

  5. Benadjila, A., Zamoum, M., Aouar, L., Zitouni, A. & Goudjal, Y. Optimization of cultural conditions using response surface methodology and modeling of indole-3-acetic acid production by Saccharothrix texasensis MB15. Biocatal. Agric. Biotechnol. 39, 102271. https://doi.org/10.1016/j.bcab.2021.102271 (2022).

    Google Scholar 

  6. Blin, K. et al. antiSMASH 8.0: extended gene cluster detection capabilities and analyses of chemistry, enzymology, and regulation. Nucleic Acids Res. 53 (W1), W32–W38. https://doi.org/10.1093/nar/gkaf334 (2025).

    Google Scholar 

  7. Boondaeng, A. et al. Biological Conversion of Agricultural Wastes into Indole-3-acetic Acid by Streptomyces lavenduligriseus BS50-1 Using a Response Surface Methodology (RSM). ACS Omega. 8 (43), 40433–40441. https://doi.org/10.1021/acsomega.3c05004 (2023).

    Google Scholar 

  8. Bunsangiam, S., Thongpae, N., Limtong, S. & Srisuk, N. Large scale production of indole-3-acetic acid and evaluation of the inhibitory effect of indole-3-acetic acid on weed growth. Sci. Rep. 11 (1), 13094. https://doi.org/10.1038/s41598-021-92305-w (2021).

    Google Scholar 

  9. Cen, X., Li, H., Zhang, Y., Huang, L. & Luo, Y. Isolation and Plant Growth Promotion Effect of Endophytic Siderophore-Producing Bacteria: A Study on Halophyte Sesuvium portulacastrum. Plants 13 (19), 2703. https://doi.org/10.3390/plants13192703 (2024).

    Google Scholar 

  10. Chandra, S., Askari, K. & Kumari, M. Optimization of indole acetic acid production by isolated bacteria from Stevia rebaudiana rhizosphere and its effects on plant growth. J. Genetic Eng. Biotechnol. 16 (2), 581–586. https://doi.org/10.1016/j.jgeb.2018.09.001 (2018).

    Google Scholar 

  11. Chaudhary, T., Yadav, D., Chhabra, D., Gera, R. & Shukla, P. Low-cost media engineering for phosphate and IAA production by Kosakonia pseudosacchari TCPS-4 using Multi-objective Genetic Algorithm (MOGA) statistical tool. 3 Biotech. 11 (4), 158. https://doi.org/10.1007/s13205-021-02690-2 (2021).

    Google Scholar 

  12. Cheynier, V., Comte, G., Davies, K. M., Lattanzio, V. & Martens, S. Plant phenolics: Recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol. Biochem. 72, 1–20. https://doi.org/10.1016/j.plaphy.2013.05.009 (2013).

    Google Scholar 

  13. Cimermancic, P. et al. Insights into Secondary Metabolism from a Global Analysis of Prokaryotic Biosynthetic Gene Clusters. Cell 158 (2), 412–421. https://doi.org/10.1016/j.cell.2014.06.034 (2014).

    Google Scholar 

  14. Duca, D., Lorv, J., Patten, C. L., Rose, D. & Glick, B. R. Indole-3-acetic acid in plant–microbe interactions. Antonie van Leeuwenhoek. 106 (1), 85–125. https://doi.org/10.1007/s10482-013-0095-y (2014).

    Google Scholar 

  15. Egamberdieva, D., Wirth, S. J., Alqarawi, A. A., Abd_Allah, E. F. & Hashem, A. Phytohormones and Beneficial Microbes: Essential Components for Plants to Balance Stress and Fitness. Front. Microbiol., 8. (2017). https://doi.org/10.3389/fmicb.2017.02104

  16. Elsayed, H. H., Abdallah, N. A. & Amer, S. K. Sustainable bioconversion of rice straw into indole-3-acetic acid by Streptomyces coelicoflavus using response surface methodology. Biomass Convers. Biorefinery. https://doi.org/10.1007/s13399-024-06252-3 (2024).

    Google Scholar 

  17. Etesami, H. & Glick, B. R. Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience. Microbiol. Res. 281, 127602. https://doi.org/10.1016/j.micres.2024.127602 (2024a).

    Google Scholar 

  18. Etesami, H. & Glick, B. R. Bacterial indole-3-acetic acid: A key regulator for plant growth, plant-microbe interactions, and agricultural adaptive resilience. Microbiol. Res. 281, 127602. https://doi.org/10.1016/j.micres.2024.127602 (2024b).

    Google Scholar 

  19. Fang, Z., Zhang, J., Liu, B., Du, G. & Chen, J. Enhancement of the catalytic efficiency and thermostability of < scp> S tenotrophomonas sp. Microb. Biotechnol. 9 (1), 35–46. https://doi.org/10.1111/1751-7915.12300 (2016). keratinase < scp>KerSMD by domain exchange with < scp>KerSMF

    Google Scholar 

  20. Felsenstein, J. CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP. Evolution 39 (4), 783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x (1985).

    Google Scholar 

  21. Folkes, L. K. & Wardman, P. Oxidative activation of indole-3-acetic acids to cytotoxic species— a potential new role for plant auxins in cancer therapy. Biochem. Pharmacol. 61 (2), 129–136. https://doi.org/10.1016/S0006-2952(00)00498-6 (2001).

    Google Scholar 

  22. Goris, J. et al. DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. MicroBiol. 57 (1), 81–91. https://doi.org/10.1099/ijs.0.64483-0 (2007).

    Google Scholar 

  23. Guo, D., Kong, S., Chu, X., Li, X. & Pan, H. De Novo Biosynthesis of Indole-3-acetic Acid in Engineered Escherichia coli. J. Agric. Food Chem. 67 (29), 8186–8190. https://doi.org/10.1021/acs.jafc.9b02048 (2019).

    Google Scholar 

  24. Hu, J. et al. Genomic and metabolic features of Bacillus cereus, inhibiting the growth of Sclerotinia sclerotiorum by synthesizing secondary metabolites. Arch. Microbiol. 205 (1), 8. https://doi.org/10.1007/s00203-022-03351-5 (2023).

    Google Scholar 

  25. Imada, E. L., Rolla dos Santos, A. A., de Oliveira, P., de Hungria, A. L. M., Rodrigues, E. P. & M., & Indole-3-acetic acid production via the indole-3-pyruvate pathway by plant growth promoter Rhizobium tropici CIAT 899 is strongly inhibited by ammonium. Res. Microbiol. 168 (3), 283–292. https://doi.org/10.1016/j.resmic.2016.10.010 (2017).

    Google Scholar 

  26. Jiang, L. et al. Genome insights into the plant growth-promoting bacterium Saccharibacillus brassicae ATSA2T. AMB Express. 13 (1), 9. https://doi.org/10.1186/s13568-023-01514-1 (2023).

    Google Scholar 

  27. Kautsar, S. A. et al. MIBiG 2.0: a repository for biosynthetic gene clusters of known function. Nucleic Acids Res. (2019) https://doi.org/10.1093/nar/gkz882.

  28. Khalifa, A. & Alsowayeh, N. Whole-Genome Sequence Insight into the Plant-Growth-Promoting Bacterium Priestia filamentosa Strain AZC66 Obtained from Zygophyllum coccineum Rhizosphere. Plants, 12(10), 1944. (2023). https://doi.org/10.3390/plants12101944

  29. Khan, S. & Mathur, A. LC–MS and GC-MS-based bioactive metabolites profiling of endophytic bacterium from Humulus lupulus and production of Indole-3-acetic acid. Curr. Trends Biotechnol. Pharm. 19 (3), 2422–2432. https://doi.org/10.5530/ctbp.2025.3.27 (2025).

    Google Scholar 

  30. Khan, S., Mathur, A. & Khan, F. Endophytic fungi-bioinspired nanoparticles potential to control infectious disease. Crit. Rev. Microbiol. 1–23. https://doi.org/10.1080/1040841X.2025.2497795 (2025).

  31. Koskiniemi, S., Sun, S., Berg, O. G. & Andersson, D. I. Selection-Driven Gene Loss in Bacteria. PLoS Genet. 8 (6), e1002787. https://doi.org/10.1371/journal.pgen.1002787 (2012).

    Google Scholar 

  32. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 35 (6), 1547–1549. https://doi.org/10.1093/molbev/msy096 (2018).

    Google Scholar 

  33. Law, D. M. Gibberellin-enhanced indole‐3‐acetic acid biosynthesis: D‐Tryptophan as the precursor of indole‐3‐acetic acid. Physiol. Plant. 70 (4), 626–632. https://doi.org/10.1111/j.1399-3054.1987.tb04316.x (1987).

    Google Scholar 

  34. Leontidou, K. et al. Plant growth promoting rhizobacteria isolated from halophytes and drought-tolerant plants: genomic characterisation and exploration of phyto-beneficial traits. Sci. Rep. 10 (1), 14857. https://doi.org/10.1038/s41598-020-71652-0 (2020).

    Google Scholar 

  35. Lin, L. & Xu, X. Indole-3-Acetic Acid Production by Endophytic Streptomyces sp. En-1 Isolated from Medicinal Plants. Curr. Microbiol. 67 (2), 209–217. https://doi.org/10.1007/s00284-013-0348-z (2013).

    Google Scholar 

  36. Mano, Y. & Nemoto, K. The pathway of auxin biosynthesis in plants. J. Exp. Bot. 63 (8), 2853–2872. https://doi.org/10.1093/jxb/ers091 (2012).

    Google Scholar 

  37. MartÃnez-Cano, D. J. et al. Evolution of small prokaryotic genomes. Front. Microbiol. 5 https://doi.org/10.3389/fmicb.2014.00742 (2015).

  38. Melini, F. et al. Optimization of the growth conditions through response surface methodology and metabolomics for maximizing the auxin production by Pantoea agglomerans C1. Front. Microbiol. 14 https://doi.org/10.3389/fmicb.2023.1022248 (2023).

  39. Myo, E. M. et al. Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiol. 19 (1), 155. https://doi.org/10.1186/s12866-019-1528-1 (2019).

    Google Scholar 

  40. Numponsak, T., Kumla, J., Suwannarach, N., Matsui, K. & Lumyong, S. Biosynthetic pathway and optimal conditions for the production of indole-3-acetic acid by an endophytic fungus, Colletotrichum fructicola CMU-A109. PLOS ONE. 13 (10), e0205070. https://doi.org/10.1371/journal.pone.0205070 (2018).

    Google Scholar 

  41. Nutaratat, P., Monprasit, A. & Srisuk, N. High-yield production of indole-3-acetic acid by Enterobacter sp. DMKU-RP206, a rice phyllosphere bacterium that possesses plant growth-promoting traits. 3 Biotech. 7 (5), 305. https://doi.org/10.1007/s13205-017-0937-9 (2017).

    Google Scholar 

  42. Nutaratat, P., Srisuk, N., Arunrattiyakorn, P. & Limtong, S. Plant growth-promoting traits of epiphytic and endophytic yeasts isolated from rice and sugar cane leaves in Thailand. Fungal Biology. 118 (8), 683–694. https://doi.org/10.1016/j.funbio.2014.04.010 (2014).

    Google Scholar 

  43. Özdal, M., Gür Özdal, Ö., Sezen, A. & Algur, Ö. F. Biosynthesis Of Indole-3-Acetic Acid By Bacillus cereus Immobilized Cells. Cumhuriyet Sci. J. 37(3), 212. https://doi.org/10.17776/csj.34085 (2016).

    Google Scholar 

  44. Patten, C. L., Blakney, A. J. C. & Coulson, T. J. D. Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria. Crit. Rev. Microbiol. 39 (4), 395–415. https://doi.org/10.3109/1040841X.2012.716819 (2013).

    Google Scholar 

  45. Patten, C. L. & Glick, B. R. Role of Pseudomonas putida Indoleacetic Acid in Development of the Host Plant Root System. Appl. Environ. Microbiol. 68 (8), 3795–3801. https://doi.org/10.1128/AEM.68.8.3795-3801.2002 (2002).

    Google Scholar 

  46. Peng, Y., He, Y., Wu, Z., Lu, J. & Li, C. Screening and optimization of low-cost medium for Pseudomonas putida Rs-198 culture using RSM. Brazilian J. Microbiol. 45 (4), 1229–1237. https://doi.org/10.1590/S1517-83822014000400013 (2014).

    Google Scholar 

  47. Put, H. et al. Bacillus subtilis as a host for natural product discovery and engineering of biosynthetic gene clusters. Nat. Prod. Rep. 41 (7), 1113–1151. https://doi.org/10.1039/D3NP00065F (2024).

    Google Scholar 

  48. Ranea, J. A. G., Buchan, D. W. A., Thornton, J. M. & Orengo, C. A. Evolution of Protein Superfamilies and Bacterial Genome Size. J. Mol. Biol. 336 (4), 871–887. https://doi.org/10.1016/j.jmb.2003.12.044 (2004).

    Google Scholar 

  49. Rey, M. W. et al. Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related Bacillusspecies. Genome Biol., 5(10), r77. (2004). https://doi.org/10.1186/gb-2004-5-10-r77.

  50. Richter, M., Rosselló-Móra, R., Glöckner, O., Peplies, J. & F., & JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32 (6), 929–931. https://doi.org/10.1093/bioinformatics/btv681 (2016).

    Google Scholar 

  51. Sam-on, M. F. S. et al. Mining the genome of Bacillus velezensis FS26 for probiotic markers and secondary metabolites with antimicrobial properties against aquaculture pathogens. Microb. Pathog. 181, 106161. https://doi.org/10.1016/j.micpath.2023.106161 (2023).

    Google Scholar 

  52. Sarmiento-López, L. G. et al. Production of indole-3-acetic acid by Bacillus circulans E9 in a low-cost medium in a bioreactor. J. Biosci. Bioeng. 134 (1), 21–28. https://doi.org/10.1016/j.jbiosc.2022.03.007 (2022).

    Google Scholar 

  53. Sasirekha, B. (ed, S.) Statistical optimization for improved indole-3-acetic acid (iaa) production by Pseudomonas aeruginosa and demonstration of enhanced plant growth promotion. J. Soil. Sci. Plant. Nutr. ahead 0-0 https://doi.org/10.4067/S0718-95162012005000038 (2012).

  54. Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30 (14), 2068–2069. https://doi.org/10.1093/bioinformatics/btu153 (2014).

    Google Scholar 

  55. Seo, Y. D. & Wargo, J. A. From bugs to drugs: Bacterial 3-IAA enhances efficacy of chemotherapy in pancreatic cancer. Cell. Rep. Med. 4 (5), 101039. https://doi.org/10.1016/j.xcrm.2023.101039 (2023).

    Google Scholar 

  56. Shahzad, R. et al. Indoleacetic acid production and plant growth promoting potential of bacterial endophytes isolated from rice (Oryza sativa L.) seeds. Acta Biol. Hung. 68 (2), 175–186. https://doi.org/10.1556/018.68.2017.2.5 (2017).

    Google Scholar 

  57. Shani, E. et al. Plant Stress Tolerance Requires Auxin-Sensitive Aux/IAA Transcriptional Repressors. Curr. Biol. 27 (3), 437–444. https://doi.org/10.1016/j.cub.2016.12.016 (2017).

    Google Scholar 

  58. Shen, J. et al. Indole-3-Acetic Acid Alters Intestinal Microbiota and Alleviates Ankylosing Spondylitis in Mice. Front. Immunol. 13 https://doi.org/10.3389/fimmu.2022.762580 (2022).

  59. Shokri, D. & Emtiazi, G. Indole-3-Acetic Acid (IAA) Production in Symbiotic and Non-Symbiotic Nitrogen-Fixing Bacteria and its Optimization by Taguchi Design. Curr. Microbiol. 61 (3), 217–225. https://doi.org/10.1007/s00284-010-9600-y (2010).

    Google Scholar 

  60. Singh, R. et al. Comparison of freeze-thaw and sonication cycle-based methods for extracting AMR-associated metabolites from Staphylococcus aureus. Front. Microbiol. 14 https://doi.org/10.3389/fmicb.2023.1152162 (2023).

  61. Šmarda, P. et al. Ecological and evolutionary significance of genomic GC content diversity in monocots. Proc. Natl. Acad. Sci., 111(39), (2014). https://doi.org/10.1073/pnas.1321152111

  62. Spaepen, S., Vanderleyden, J. & Remans, R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31 (4), 425–448. https://doi.org/10.1111/j.1574-6976.2007.00072.x (2007).

    Google Scholar 

  63. Stofan, M. & Guo, G. L. Bile Acids and FXR: Novel Targets for Liver Diseases. Front. Med., 7. (2020). https://doi.org/10.3389/fmed.2020.00544

  64. Stothard, P. & Wishart, D. S. Circular genome visualization and exploration using CGView. Bioinformatics 21 (4), 537–539. https://doi.org/10.1093/bioinformatics/bti054 (2005).

    Google Scholar 

  65. Szkop, M. & Bielawski, W. A simple method for simultaneous RP-HPLC determination of indolic compounds related to bacterial biosynthesis of indole-3-acetic acid. Antonie van Leeuwenhoek. 103 (3), 683–691. https://doi.org/10.1007/s10482-012-9838-4 (2013).

    Google Scholar 

  66. Tang, J. et al. Biosynthetic Pathways and Functions of Indole-3-Acetic Acid in Microorganisms. Microorganisms 11 (8), 2077. https://doi.org/10.3390/microorganisms11082077 (2023).

    Google Scholar 

  67. Teale, W. D., Paponov, I. A. & Palme, K. Auxin in action: signalling, transport and the control of plant growth and development. Nat. Rev. Mol. Cell Biol. 7 (11), 847–859. https://doi.org/10.1038/nrm2020 (2006).

    Google Scholar 

  68. Viet Cuong, P., Hoa, N. P., Optimization of culture condition for IAA roduction by Bacillus sp. isolated from cassava field of Vietnam. Vietnam J. Sci. Technol. 59(3), 312. https://doi.org/10.15625/2525-2518/59/3/15600 (2021).

    Google Scholar 

  69. Wagi, S. & Ahmed, A. Bacillus spp.: potent microfactories of bacterial IAA. PeerJ 7, e7258. https://doi.org/10.7717/peerj.7258 (2019).

    Google Scholar 

  70. Wang, Y. et al. Whole-genome analysis revealed the growth-promoting mechanism of endophytic bacterial strain Q2H1 in potato plants. Front. Microbiol. 13 https://doi.org/10.3389/fmicb.2022.1035901 (2022).

  71. Wu, C. F. J. & Hamada, M. Experiments (Wiley, 2021). https://doi.org/10.1002/9781119470007

  72. Yoon, S. H., Ha, S., Lim, J., Kwon, S. & Chun, J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek. 110 (10), 1281–1286. https://doi.org/10.1007/s10482-017-0844-4 (2017).

    Google Scholar 

  73. Zakharova, E. A. et al. Biosynthesis of indole-3‐acetic acid in Azospirillum brasilense. Eur. J. Biochem. 259 (3), 572–576. https://doi.org/10.1046/j.1432-1327.1999.00033.x (1999).

    Google Scholar 

  74. Zeng, Q. et al. Comparative genomic and functional analyses of four sequenced Bacillus cereus genomes reveal conservation of genes relevant to plant-growth-promoting traits. Sci. Rep. 8 (1), 17009. https://doi.org/10.1038/s41598-018-35300-y (2018a).

    Google Scholar 

  75. Zeng, Q. et al. Comparative genomic and functional analyses of four sequenced Bacillus cereus genomes reveal conservation of genes relevant to plant-growth-promoting traits. Sci. Rep. 8 (1), 17009. https://doi.org/10.1038/s41598-018-35300-y (2018b).

    Google Scholar 

  76. Zeng, Q. et al. Comparative genomic and functional analyses of four sequenced Bacillus cereus genomes reveal conservation of genes relevant to plant-growth-promoting traits. Sci. Rep. 8 (1), 17009. https://doi.org/10.1038/s41598-018-35300-y (2018c).

    Google Scholar 

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