Metagenomic insights into plant growth promoting genes inherent in bacterial endophytes of Emilia sonchifolia (Linn.) DC
DOI:
https://doi.org/10.14719/pst.1357Keywords:
Functional annotation, Gene prediction, Metagenomeanalysis, Nutrient uptake, SiderophoresAbstract
Studies on the genome of endophytes reveal the metabolic potential of endophytic microbiome including both culturable and unculturable fractions. The metagenome analysis through the Illumina HiSeq platform gives access to the genetic data encrypted for the molecular machinery, which takes part in plant growth promotion activity of the endophyte in various aspects including production of plant growth hormones and enhancing nutrient availability for the host plant. The present work was undertaken to identify the genes involved in plant growth promotion activities from the endophytes of Emilia sonchifolia(Linn.) DC. through metagenome analysis. Metagenomic studies include the analysis of functional annotations which aid in the detection of biocatalysts taking part in the metabolic pathway of host plants. The annotations of expressed genes in different databases like NCBI Nr, KEGG, eggnog and CAZy resulted in enlisting the vast array of information on the genetic diversity of the endophytic microbiome. The metagenome analysis of endophytic bacteria from the medicinal plant E.sonchifolia unveiled characteristic functional genes involved in plant growth promotion such as nitrogen metabolism (nif) and siderophore production (enterobactin category), ipdC and tnaA (IAA producing), ACC deaminase coding genes (regulation of elevated ethylene levels in host tissues), Mo-Nitrogenase, nitrous-oxide reductase (nosZ), nitrate reductase (narG, napA), nitrite reductase (nirD) (nutrient assimilation and absorption) enterobactin siderophore synthetase components F and D and acid phosphatase genes. This clearly explains the effective plant-microbe relationship and the role of bacterial endophytic microbes in regulating the growth of host plants.
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Rai N, Keshri PK, Verma A, Kamble SC, Mishra P, Barik S, Singh SK, Gautam V. Plant associated fungal endophytes as a source of natural bioactive compounds. Mycology. 2021. https://doi.org/10.1080/21501203.2020.1870579.
Ek-Ramos MJ, Gomez-Flores R, Orozco-Flores AA, Rodríguez-Padilla C, González-Ochoa G, Tamez-Guerra P. Bioactive Products from Plant-Endophytic Gram-Positive Bacteria. Frontiers in Microbiology. 2019.10:463. https://doi.org/10.3389/fmicb.2019.00463.
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN. Bacterial endophytes: recent developments and applications. FEMS MicrobiolLett. 2008.278(1–9). https://doi.org/10.1111/j.1574-6968.2007.00918. x.
Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. The microbial pan-genome. Curr. Opin. Genet. Dev. 2005. 15: 589-594. https://doi.org/10.1016/j.gde.2005.09.006
Knief C. Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front. Plant Sci. 2014. 5(216):1-23. https://doi.org/ 10.3389/fpls.2014.00216.
Strobel G, Daisy B. Bioprospecting for microbial endophytes and their natural products. Microbiol. Mol. Biol. Rev.2003.67(4):491-502. https://doi.org/10.1128/mmbr. 67.4.491-502.2003.
Das A, Varma A. Symbiosis: the art of living, in symbiotic fungi principles and practice: Varma A, Kharkwal. eds. 1-28. Springer-Verlang, Berlin. 2009. https://doi.org/10.1007/ 978-3-540-95894-9.
Shi YW, Lou K, Li C. Promotion of plant growth by phytohormone-producing endophytic microbes of Sugar beet. Biol. Fertl. Soils. 2009. 45:645-653. https://doi.org/10.1007/s00374-009-0376-9.
Nikolic B, Schwab H, Sessitsch A. Metagenomic analysis of the 1-aminocyclopropane-1- carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanumtuberosum L. Arch. Microbiol. 2011.193(9)665-676. DOI: 10.1007/s00203-011-0703-z.
Makarewicz O, Dubrac S, Msadek T, Borriss R. Dual role of the PhoP?P response regulator: Bacillus amyloliquefaciensFZB45 phytase gene transcription is directed by positive and negative interactions with the phyC promoter. J Bacteriol. 2006. 188(19): 6953–6965. https://doi.org/ 10.1128/JB.00681-06.
Wei CY, Lin L, Luo L-J, Xing Y-X, Hu C-J, Yang L-T, Li Y-R, An Q. Endophytic nitrogen- fixing Klebsiellavariicola strain DX120E promotes sugarcane growth. Biol. Fertil. Soils. 2014. 50: 657-666. https://doi.org/10.1007/s00374-013-0878-3.
Jahanian A, Chaichi MR, Rezaei K, Rezayazdi K, Khavazi K. The effect of plant growth promoting rhizobacteria (PGPR) on germination and primary growth of artichoke (Cynarascolymus). Int. J. Agric. Crop. Sci. 2012. 4:923-929.
Meziane H, Van der SI, Van Loon LC, Höfte M, Bakker PA. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 2005. 6(2):177-185. https://doi.org/10.1111/j.1364-3703.2005. 00276.x.
Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R. Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiol. 2002. 148(7):2097-109. https://doi.org/10.1099/00221287-148-7-2097.
Tank N, Saraf M. Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on Tomato plants. J. Plant Interact. 2010. 5:51-58. https://doi.org/10.1080/17429140903125848
Guazzaroni ME, Morgante V, Mirete S, Gonzalez-Pastor JE. Novel acid resistance genes from the metagenome of the Tinto River, an extremely acidic environment. Environ. Microbiol. 2013.15:1088-1102. https://doi.org/10.1111/1462-2920.12021
Berendsen RL, Pieterse CMJ, Bakker PAHM. The rhizospheremicrobiome and the plant health. Tren .Pl. Sci. 2012.17:8. http://dx.doi.org/10.1016/j. tplants.2012.04.001
Janssen PH, Yates PS, Grinton BE, Taylor PM, Sait M. Improved culturability of soil bacteria and isolation in pure culture of novel members of the divisions Acidobacteria, Actinobacteria, Proteobacteria, and Verrucomicrobia. App. Environ. Microbiol. 2002. 68 (5) 2391-2396. https://doi.org/10.1128/AEM.68.5.2391-2396.2002.
SpainAM, Krumholz LR,Elshahed MS. Abundance, composition, diversity and novelty of soil Proteobacteria. Microbial ecology and functional diversity of natural habitats. The ISME J. 2009.992–1000. https://doi.org/10.1038/ismej.2009.43.
Smith DR, Quinlan AR, Peckham HE, Makowsky K, Tao W, Woolf B, Shen L, Donahue WF, Tusneem N, Stromberg MP, Stewart DA, Zhang L, Ranade SS, Warner JB, Lee CC, Coleman BE, Zhang Z, McLaughlin SF, Malek JA, Sorenson JM, Blanchard AP, Chapman J, Hillman D, Chen F, Rokhsar DS, McKernan KJ, Jeffries TW, Marth GT, Richardson PM. Rapid whole-genome mutational profiling using next generation sequencing technologies. Genome Res. 2008.18:1638-1642. https://doi.org/10.1101/gr.077776.108
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc. Natl. Acad. Sci. USA.108 (Suppl 1): 2011. 4516-4522. https://doi.org/10.1073/pnas.1000080107
Ram JL, Karim AS, Sendler ED, Kato I. Strategy for microbiome analysis using 16s rRNA gene sequence analysis on the Illumina sequencing platform. Systems Biol. Reprod. Med. 2011. 57:162-170. https://doi.org/10.3109/19396368.2011.555598
Kumar DG,Syafiq AM, Ruhaiyem Y. Traditional uses, phytochemical and pharmacological aspects of Emilia sonchifolia(L.) DC. Int. J. Res. Ayurveda Pharm. 2015. 6(4):551-556. https://doi.org/10.7897/2277-4343.064103
Sophia D, Ragavendran P, Arulraj C, Gopalakrishnan VK. In vitro antioxidant activity and HPTLC determination of n-hexane extract of Emilia sonchifolia (L.) DC. J. Basic Clin. Pharm. 2011. 2(4):179-18:179e183.
Urumbil SK, Kumar AM. Diversity analysis of endophytic bacterial microflora in Emilia sonchifolia(Linn.) DC on IlluminaMiSeq platforms. J. Pure and Appl. Microbiol. 2020.14(1):679-687.https://doi.Org/10.22207/jpam.14.1.70
Yasuda M, Isawa T, Shinozaki S, Minamisawa K, Nakashita H. Effects of colonization of a bacterial endophyte, Azospirillum sp. B510, on disease resistance in rice. Biosci. Biotechnol. Biochem. 2009. 73(12):2595-9. https://doi.org/10.1271/bbb.90402.
Isawa T, Yasuda M, Awazaki H, Minamisawa K, Shinozaki S, Nakashita H. Azospirillum sp. strain B510 enhances rice growth and yield. Microbes Environ. 2010. 25(1):58-61. https://doi.org/10.1264/jsme2.me09174.
Glick BR. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol. Res. 2014. 169(1):30-39. https://doi.org/10.1016/j.micres.2013.09.009.
Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev. 2007.31(4):425-448. https://doi.org/10.1111/j.1574-6976.2007.00072. x.
Khan AL, Waqas M, Kang SM, Al-Harrasi A, Hussain J, Al-Rawahi A, Al-Khiziri S, Ullah I, Ali L, Jung HY, Lee I J.Bacterial endophyte Sphingomonas sp. LK11 produces gibberellins and IAA and promotes tomato plant growth. J. Microbiol. 2014. 52(8):689-95. https://doi.org/10.1007/s12275-014-4002-7.
Ji SH, Gururani MA, Chun SC. Isolation and characterization of plant growth promoting endophyticdiazotrophic bacteria from Korean rice cultivars. Microbiol. Res. 2014. 169(1):83-98. https://doi.org/10.1016/j.micres.2013.06.003.
Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth and development of poplar trees. Appl. Environ. Microbiol. 2009.75(3):748-757. https://doi.org/10.1128/AEM.02239-08.
Bhattacharyya C, Bakshi U, Mallick I, Mukherji S, Bera B, Ghosh A. Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile Bacillus aryabhattai Strain AB211. Front. Microbiol. 2017.8:411. https://doi.org/10.3389/fmicb. 2017.00411.
Duca D, Lorv J, Patten CL, Rose D, Glick BR.Indole-3-acetic acid in plant-microbe interactions. Antonie Van Leeuwenhoek. 2014.106(1):85-125. https://doi.org/10.1007/s10482-013-0095-y.
Ryu CM, Farag MA, HuCH, Reddy MS, Wei HX, Paré PW, Kloepper JW. Bacterial volatiles promote growth in Arabidopsis. Proc. Natl. Acad. Sci.USA. 2003. 100(8):4927-32. https://doi.org/10.1073/pnas.0730845100.
Bertagnolli BL, Hager LP. Role of flavin in acetoin production by two bacterial pyruvateoxidases. Arch. Biochem. Biophys. 1993. 300(1):364-71. https://doi.org/10.1006/abbi.1993.1049.
Hidayati U, Chaniago IA, Munif A, Santosa DA. Potency of plant growth promoting endophytic bacteria from rubber plants (Heveabrasiliensis Mull. Arg.). J. Agronomy. 2014. 13(3):147-152. https://doi.org/10.3923/ja.2014.147.152.
Zhang Y, He L, Chen Z, Wang Q, Qian M, Sheng X. Characterisation of ACC deaminase producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere. 2011. 83(1): 57-62. http://doi.org/10.1016/j.chemosphere.2011.01.041.
Glick BR. Bacterial ACC deaminase and the alleviation of plant stress. Adv. Appl. Microbiol. 2004. 56:291-312. DOI: 10.1016/S0065-2164(04)56009-4.
Glick BR, Li J, Shah S, Penrose DM, Moffatt BA. ACC Deaminase is Central to the Functioning of Plant Growth Promoting Rhizobacteria. In: Kanellis AK, Chang C, Klee H, Bleecker AB, Pech J C, Grierson D. (Eds) Biology and Biotechnology of the Plant Hormone Ethylene II. Springer, Dordrecht. 1999. 293-298. https://doi.org/10.1007/978-94-011-4453-7_54.
Sun Y, Cheng Z, Glick BR. The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderiaphytofirmans PsJN. FEMS Microbiol. Lett. 2009. 296(1):131-136. https://doi.org/10.1111/j.1574-6968.2009.01625. x.
Xie SS, Wu HJ, Zang HY, Wu LM, Zhu QQ, Gao XW. Plant growth promotion by spermidine- producing Bacillus subtilis OKB105. Mol. Plant. Microbe Interac. 2014. 27:655-663. https://doi.org/10.1094/MPMI-01-14-0010-R.
Tholl D. Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Curr. Opin. Plant. Biol. 2006. 9:297-304. https://doi.org/10.1016/j.pbi.2006. 03.014.
Mazid M, Khan T, Mohammad F. Role of secondary metabolites in defense mechanisms of plants. Biol. Med. 3(2 special issue): 2011. 232-249.
Wang C, Liwei M, Park JB, Jeong S-H, Wei G, Wang Y, Kin S-W. Microbial platform for terpenoid production: Eschericia coli and Yeast. Front. Microbiol. 2018. 9:2460. https://doi.org/ 10.3389/fmicb.2018. 02460.
Khalid A, Takagi H, Panthee S, Muroi M, Chappell J, Osada H, Takahashi S. Development of terpenoid-production platform in Streptomyces reveromyceticus SN-593. ACS Synth. Biol. 2017.6:2339-2349. https://doi.org/10.1021/acssynbio. 7600249.
Sundstrom E, Yaegashi J, Yan J, Masson F, Papa G, Rodriguez A, Mirsiaghi O, Liang L, He Q, Tanjore D, Pray T R, Singh S, Simmons B, Sun N, Magnuson J, Gladden J. Demonstrating a separation-free process coupling ionic liquid pre-treatment, sccharification and fermentation with Rhodosporidium toruloidesto produce advanced biofuels. Green Chem. 2018. 20:2870-2879. https://doi.org/10.1039/C8GC00518D.
Miller SH, Browne P, Prigent-Cambaret C, Combes-Meynet E, Morrissey JP, O’Gara F. Biochemical and genomic comparison of inorganic phosphate solubilisation in Pseudomonas species. Environ. Microbiol. Rep. 2010. 2: 403-411. https://doi.org/10.1111/j.1758-2229.2009.00105.x.
Bergkemper F, Schöler A, Engel M, Lang F, Krüger J, Schloter M, Schulz S. Phosphorus depletion in forest soils shapes bacterial communities towards phosphorus recycling systems. Environ. Microbiol. 2016. 18(6):1988-2000. https://doi.org/10.1111/1462-2920.13188.
Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine JK, Dowling DN. Plant growth promotion induced by phosphate solubilising endophyticPseudomonas isolates. Front. Microbiol. 2015. 6(745):1-9. https://doi.org/10.3389/fmic.2015.00745.
Gupta M, Kiran S, Singh B, Gulati A, Tewari R. Enhanced biomass and steviol glycosides in Stevia rebaudiana treated with phosphate-solubilizing bacteria and rock phosphate. Plant Gro.Regul. 2011. 65. 449-457. https://doi.org/10.1007/s10725-011-9615-9.
Rodriguez H, Fraga R, Gonzales T, Bashan Y. Genetics of phosphate solubilisation and its potential applications for improving plant growth promoting bacteria. Plant and Soil. 2006. 287:15-21. https://doi.org/10.1007/s11104-006-9056-9.
Idris A, Al-tahir I, Idris E. Antibacterial activity of endophytic fungi extract from the medicinal plant Kigelia Africana. Egypt. Acad. J. Biol. Sci. 2013. 5(1):1-9. https://doi.org/10.21608/eajbsg.2013.16639.
Golovan S, Wang G, Zhang J, Forsberg CW. Characterization and over production of the E.coliappA encoded bifunctional enzyme that exhibit both phytase and acid phosphatase activities. Can J. Microbiol. 2000. 46:59-71. https://doi.org/10.1139/cjm-46-1-59.
Goldstein AH. Involvement of the quinoprotein glucose dehydrogenase in the solubilisation of exogenous phosphates by gram negative bacteria. In: Phosphate in microorganism. Cellular and Molecular Biology.Eds. Torriani-Gorini A, YagilE, SilverS. ASM Press. Washington. DC. 1996. 197-203.
Gyaneshwar P, Parekh LJ, Archana G, Poole PS, Collins MD, Hutson RA, Kumar GN. Involvement of a phosphate starvation inducible glucose dehydrogenase in soil phosphate solubilisation by Enterobacter asburiae. FEMS Microbiol. Lett. 1999. 171:223-229. https://doi.org/10.1111/j.1574-6968.1999. tb13436. x.
Lin L, Li Z, Hu C, Zhang X, Chang S, Yang L, Li Y, An Q. Plant growth promoting nitrogen fixing Enterobacteria are in association with Sugarcane plants growing in Guangxi, China. Microbes Environ. 2012. 27(4): 391-398. https://doi.org/10.1264/ jsme2.me11275.
Poza-Carrion C, Jimenez-Vincente E, Navarro-Rodriguez M, Echavarri- Erasun C, Rubio LM. Kinetics of nif gene expression in a nitrogen fixing bacterium. J. Bacteriol. 2014. 196(3): 595-603. https://doi.org/10.1128/JB.00942-13.
Bhowmik, A, Clotier M, Ball E, Bruns MA. Unexplored microbial metabolisms for enhanced nutrient recycling in agricultural soils. AIMS Microbiology. 2017. 3(4): 826-845. https://doi.org/10.3934/microbial.2017.4.826.
Andres-Barrao C, Lafi FF, Alam I, de Zelicourt A, Eida AA, Bokhari A, Alzubaidy H, Bajic VB, Hirt H, Saad MM. Complete genome sequence analysis of Enterobacter sp. SA187, a plant multi stress tolerance promoting endophytic bacterium. Front. Microbiol. 2017. 8(2023): 1-21. https://doi.org/10.3389/fmicb. 2017.02023.
Forchhammer K. Glutamine signalling in bacteria. Front Biosci. 2007. 12:358-370. https://doi.org/10.2741/2069.
Taghavi S, vanderLelie D, Hoffman A, Zhang Y-B, Walla MD, Vangronsveld J, Newman L, Monchy S. Genome sequence of the plant growth promoting endophytic bacterium Enterobacter Sp.638. PLoS Genetics. 2010.6(5):e1000943. 1-26. https://doi.org/10.1371/journal.pgen.1000943.
Butler A, Theisen RM. Iron (III)-Siderophore coordination chemistry: reactivity of marine siderophores. Co-ord. Chem. Rev. 2010.254:288-296. DOI: 10.1016/j.ccr.2009. 09. 010.
Arya N, Rana A, Rajwar A, Sahgal M, Sharma A. Biocontrol efficacy of Siderophore producing indigenous Pseudomonas strains against Fusarium Wilt in Tomato. Nat. Acad. Sci. Lett. 2018.41. https://doi.org/10.1007/s40009-018-0630-5.
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