Identification and Optimization of Indole-3-Acetic Acid Production of Endophytic Bacteria and Their Effects on Plant Growth

Main Article Content

Saowapar Khianngam
Pimjai Meetum
Pantipa Na Chiangmai
Somboon Tanasupawat

Abstract

Indole-3-acetic acid (IAA) is one of the most physiologically active auxins produced by rhizobacteria and is potentially applied for agriculture. Two endophytic bacteria, VR2 and MG9, isolated from the root of Chrysopogon zizanioides (L.) collected at Cha-Am, and the leaf of Bruguiera cylindrica (L.) Blume collected from a mangrove forest at Ban Laem, Phetchaburi Province, Thailand, were taxonomic characterised based on their phenotypic characteristics and 16S rRNA gene analysis. Strain VR2 was closely related to Enterobacter hormaechei CIP 103441T (99.6% similarity), while strain MG9 was closely related to Bacillus aryabhattai B8W22T (99.9% similarity). Consequently, they were identified as Enterobacter hormaechei and Bacillus aryabhattai, respectively. The IAA production of VR2 and MG9 strains are determined and applied to rice seeds for their root and shoot germination. Strains VR2 and MG9 greatly produced a yield of IAA, 246.00 and 195.55 µg/mL in 1,000 µg/mL of L-tryptophan at pH 6 for 48 h. They showed no significant differences in IAA to root and shoot development. However, the bacterial IAA exhibited potential nearby synthetic IAA, which had a significant effect compared to the control. IAA produced from these two strains might preferably trim down the use of synthetic IAA and could contribute to sustainable agriculture.

Article Details

How to Cite
Identification and Optimization of Indole-3-Acetic Acid Production of Endophytic Bacteria and Their Effects on Plant Growth. (2023). Tropical Life Sciences Research, 34(1), 219–239. https://doi.org/10.21315/tlsr2023.34.1.12
Section
Original Article

References

Abari A K, Nasr M H, Hojjati M and Bayat D. (2011). Salt effects on seed germination and seedling emergence of two Acacia species. African Journal of Plant Science 5(1): 52–56.

Abraham J and Silambarasan S. (2015). Plant growth promoting bacteria Enterobacter asburiae JAS5 and Enterobacter cloacae JAS7 in mineralization of endosulfan. Applied Biochemistry and Biotechnology 175: 3336–3348. https://doi.org/10.1007/s12010-015-1504-7

Ait Bessai S, Bensidhoum L and Nabti E -h. (2022). Optimization of IAA production by telluric bacteria isolated from northern Algeria. Biocatalysis and Agricultural Biotechnology 41: 102319. https://doi.org/10.1016/j.bcab.2022.102319

Akinrinlola R J, Yuen G Y, Drijber R A and Adesemoye A O. (2018). Evaluation of Bacillus strains for plant growth promotion and predictability of efficacy by in vitro physiological traits. International Journal of Microbiology 2018: 1–11. https://doi.org/10.1155/2018/5686874

Alizadeh M A, Arab H A, Tabaie R and Nasiri M. (2013). Evaluation of seed and seedling emergence enhancement of some population of Sahandy savory (Satureja sahendica) by gibberlic acid, potassium nitrate, pre-cooling physical and chemical scarification treatment. Pakistan Journal of Biological Sciences 16(20): 1208–1211. https://doi.org/10.3923/pjbs.2013.1208.1211

Anugrah F A, Fanany R, Putra S A, Masita R and Safitri D Y. (2021). Indole acetic acid (IAA) hormone production by endophytic bacteria isolate from Cinchona plant (Cinchona ledgerina Moens.) root. AIP Conference Proceedings 2353: 030082. https://doi.org/10.1063/5.0052923

Barrow G I and Feltham R K A. (1993). Cowan and Steel’s manual for the identification of medical bacteria, 3rd ed. Cambridge: Cambridge University press.

Belwal T, Bisht A, Bhatt I D and Rawal R S. (2015). Influence of seed priming and storage time on germination and enzymatic activity of selected Berberis species. Plant Growth Regulation 77(2): 189–199. https://doi.org/10.1007/s10725-015-0051-0

Bharucha U, Patel K and Trivedi U B. (2013).Optimization of indole acetic acid production by Pseudomonas putida UB1 and its effect as plant growth-promoting rhizobacteria on mustard (Brassica nigra). Agricultural Research 2(3): 215–221. https://doi.org/10.1007/s40003-013-0065-7

Bhutani N, Maheshwar R, Negi M and Suneja P. (2018). Optimization of IAA production by endophytic Bacillus spp. From Vigna radiata for their potential use as plant growth promoters. Israel Journal of Plant Sciences 65: 1–2. https://doi.org/10.1163/22238980-00001025

Cao L, Qiu Z, Dai X, Tan H, Lin Y and Zhou S. (2004). Isolation of endophytic actinomycetes from roots and leaves of banana (Musa acuminate) plants and their activities against Fusarium oxysporum f. sp. cubense. World Journal of Microbiology and Biotechnology 20(5): 501–504. http://doi.org/10.1023/B:WIBI.0000040406.30495.48

Chiwocha S D S, Cutler A J, Abrams S R, Ambrose S J, Yang J, Ross A R S and Kermode A R. (2005). The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. The Plant Journal 42(1): 35–48. https://doi.org/10.1111/j.1365-313X.2005.02359.x

Eklöf S, Astot C, Sitbon F, Moritz T, Olsson O and Sandberg G. (2000). Transgenic tobacco plants co-expressing Agrobacterium iaa and ipt genes have wild-type hormone levels but display both auxin- and cytokinin-overproducing phenotypes. The Plant Journal 23(2): 279–284. https://doi.org/10.1046/j.1365-313x.2000.00762.x

Felsenstein J. (1985). 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

Hanh H T T and Mongkolthanaruk W. (2017). Correlation of growth and IAA production ofLysinbacillus fusiformisud UD 270. Journal of Applied and Physical Sciences 3(3): 98–106. https://doi.org/10.20474/japs-3.3.3

Hentrich M, Böttcher C, Düchting P, Cheng Y, Zhao Y, Berkowitz O, Masle J, Medina J and Pollmann S. (2013). The jasmonic acid signaling pathway is linked to auxin homeostasis through the modulation of YUCCA8 and YUCCA9 gene expression. The Plant Journal 74(4): 626–637. https://doi.org/10.1111/tpj.12152

Jeyanthi V and Ganesh P. (2013). Production, optimization and characterization of phytohormone indole acetic acid by Pseudomonas fluorescence. International Journal of Pharmaceutical and Biological Archives 4(3): 514–520.

Koga J, Syono K, Ichikawa T and Adachi T. (1994). Involvement of L-tryptophan aminotransferase in indole-3-acetic acid biosynthesis in Enterobacter cloacae. Biochimica et Biophysica Acta (BBA) – Protein Structure and Molecular Enzymology 1209(2): 241–247. https://doi.org/10.1016/0167-4838(94)90191-0

Kumari S, Prabha C, Singh A, Kumari S and Kiran S. (2018). Optimization of indole-3- acetic acid production by diazotrophic B. subtilis DR2 (KP455653), isolated from rhizosphere of Eragrostis cynosuroides. International Journal of Pharma Medicine and Biological Sciences 7(2): 20–27. https://doi.org/10.18178/ijpmbs.7.2.20-27

Kushwaha P, Kashyap L P, Srivastava K A and Tiwari R K. (2020). Plant growth promoting and antifungal activity in endophytic Bacillus strains from pearl millet (Pennisetum glaucum). Brazilian Journal of Microbiology 51(1): 229–241. https://doi.org/10.1007/s42770-019-00172-5

Lavenus J, Goh T, Roberts I, Guyomar?h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M and Laplaze L. (2013). Lateral root development in Arabidopsis: Fifty shades of auxin. Trends in Plant Science 18(8): 450–458. https://doi.org/10.1016/j.tplants.2013.04.006

Liu P -P, Montgomery T A, Fahlgren N, Kasschau K D, Nonogaki H and Carrington J C. (2007). Repression of AUXIN REPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. The Plant Journal 52(1): 133–146. https://doi.org/10.1111/j.1365-313X.2007.03218.x

Lu G, Coneva V, Casaretto J A, Ying S, Mahmood K, Liu F, Nambara E, Bi Y and Rothstein S J. (2015). OsPIN5b modulates rice (Oryza sativa) plant architecture and yield by changing auxin homeostasis, transport and distribution. The Plant Journal 83(5): 913–925. https://doi.org/10.1111/tpj.12939

Lwin K M, Myint M M, Tar T and Aung W Z M. (2012). Isolation of plant hormone (indole-3-acetic acid-IAA) producing rhizobacteria and study on their effects on maize seedling. Engineering Journal 16(5): 137–144. https://doi.org/10.4186/ej.2012.16.5.137

Lynch J M. (1985). Origin, nature and biological activity of aliphatic substances and growth hormones found in soil. In Vaughan D and R E Malcom R E (eds.), Soil organic matter and biological activity. Dordrecht, Boston: Lancaster: Martinus Nijhoff/Dr. W. Junk Publishers, 151–174. https://doi.org/10.1007/978-94-009-5105-1_5

Maraghni M, Gorai M and Neffati M. (2010). Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Ziziphus lotus. South African Journal of Botany 76(3): 453–459. https://doi.org/10.1016/j.sajb.2010.02.092

Mavi K, Demir I and Matthews S. (2010). Mean germination time estimates relative emergence of seed lots of three cucurbit crops under stressful conditions. Seed Science and Technology 38(1): 14–25. https://doi.org/10.15258/sst.2010.38.1.02

Miransari M and Smith D L. (2014). Plant hormones and seed germination. Environmental and Experimental Botany 99: 110–121. https://doi.org/10.1016/j.envexpbot.2013.11.005

Mockaitis K and Estelle M. (2008). Auxin receptors and plant development: A new signaling paradigm. Annual Review of Cell and Developmental Biology 24: 55–80. http://doi.org/10.1146/annurev.cellbio.23.090506.123214

Mohite B. (2013). Isolation and characterization of indole acetic acid (IAA) producing bacteria from rhizospheric soil and its effect on plant growth. Journal of Soil Science and Plant Nutrition 13(3): 638–649. https://doi.org/10.4067/S0718-95162013005000051

Nakamura A, Umemura I, Gomi K, Hasegawa Y, Kitano H, Sazuka T and Matsuoka M. (2006). Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. The Plant Journal 46(2): 297–306. https://doi.org/10.1111/j.1365-313X.2006.02693.x

Nordström A -C and Eliasson L. (1991). Level of endogenous indole-3-acetic and indole-3- acetylaspartic acid during adventitious root formation in pea cuttings. Physiologia Plantarum 82(4): 599–605. https://doi.org/10.1111/j.1399-3054.1991.tb02953.x

Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Astot C, Dolezal K and Sandberg G. (2004). Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: A factor of potential importance for auxin-cytokinin-regulated development. Proceedings of the National Academy of Science of the USA, University of Bristol, Bristol, United Kingdom, 8 April, 8039–8044. https://doi.org/10.1073/pnas.0402504101

Nutaratat P, Monprasit A and Srisuk N. (2017). 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

Panigrahi S, Mohanty S and Rath C C. (2020). Characterization of endophytic bacteria Enterobacter cloacae MG00145 isolated from Ocimum sanctum with indole acetic acid (IAA) production and plant growth promoting capabilities against selected crops. South African Journal of Botany. 134:17–26. https://doi.org/10.1016/j.sajb.2019.09.017

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

Phetcharat P and Duangpaeng A. (2012). Screening of endophytic bacteria from organic rice tissue for indole acetic acid production. Procedia Engineering 32(2012): 177–183. https://doi.org/10.1016/j.proeng.2012.01.1254

Popko J, Hänsch R, Mendel R -R, Polle A and Teichmann T. (2010). The role of abscisic acid and auxin in the response of poplar to abiotic stress. Plant Biology 12(2): 242–258. https://doi.org/10.1111/j.1438-8677.2009.00305.x

Saitou N and Nei M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4(4): 406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454

Shahid I, Han J, Hanooq S, Malik K A, Borchers C H and Mehnaz S. (2021). Profiling of metabolites of Bacillus spp. and their application in sustainable plant growth promotion and biocontrol. Frontiers in Sustainable Food Systems 5: 605195. https://doi.org/10.3389/fsufs.2021.605195

Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J and van der Lelie D. (2009). Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Applied and Environmental Microbiology 75(3): 748–757. https://doi.org/10.1128/AEM.02239-08

Tamura K, Dudley J, Nei M and Kumar S. (2007). MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24(8): 1596–1599. https://doi.org/10.1093/molbev/msm092

Thompson J D, Gibson T J, Plewniak F, Jeanmougin F and Higgins D G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic. Acids Research 25(24): 4876–4882. https://doi.org/10.1093/nar/25.24.4876

Vasanthakumar A and McManus P S. (2004).Indole-3-acetic acid producing bacteria are associated with cranberry stem gall. Phytopathology 94(11): 1164–1171. https://doi.org/10.1094/PHYTO.2004.94.11.1164

Wagi S and Ahmed A. (2019). Bacillus spp.: Potent microfactories of bacterial IAA. PeerJ 7: e7258. http://doi.org/10.7717/peerj.7258

Woodward A W and Bartel B. (2005). Auxin: Regulation, action, and interaction. Annals of Botany 95(5): 707–735. https://doi.org/10.1093/aob/mci083

Yan X, Wang Z, Mei Y, Wang L, Wang X, Xu Q, Peng S, Zhou Y and Wei C. (2018). Isolation, diversity, and growth-promoting activities of endophytic bacteria from tea cultivars of Zijuan and Yunkang-10. Frontiers in Microbiology 9: 1848. https://doi.org/10.3389/fmicb.2018.01848

Yousof F I and El-Saidy A E A. (2014). Application of salicylic acid to improve seed vigor and yield of some bread wheat cultivars (Triticum aestivum L.) under salinity stress. Research Journal of Seed Science 7(2): 52–62. https://doi.org/10.3923/rjss.2014.52.62

Zhang Q, Li J, Zhang W, Yan S, Wang R, Zhao, J, Li Y, Qi Z, Sun Z and Zhu Z. (2012). The putative auxin efflux carrier OsPIN3t is involved in the drought stress response and drought tolerance. The Plant Journal 72(5): 805–816. https://doi.org/10.1111/j.1365-313X.2012.05121.x