Abstract
Finger millet is an important food crop that grows in arid and semi-arid parts of Africa and Asia and serve as a staple food source for millions of people. However, compared to other major crops, finger millet gives lower yield. For major crops high yield has been achieved through the introduction of improved varieties coupled with an intensive use of synthetic agrochemicals, often at the expense of the environment. In recent years endophytes received attention because of their potential to increase crop yield without massive application of synthetic chemicals. In this study seeds collected from three finger millet growing regions of Ethiopia contained a high load of bacterial endophytes. But no fungal endophytes were isolated from any of the samples. Based on their 16S rRNA gene sequence the isolates were identified as members of the genera Pantoea, Pseudomonas, Enterobacter, Sphingobacterium, Microbacterium, and Curtobacterium. A significant number of the isolates produced indole-3-acetic acid (IAA), were able to grow on nitrogen free medium, solubilized phosphate, and produced hydrogen cyanide. The most interesting observation was that the different genera showed restricted occurrence to a specific geographic location. Differences in plant growth promotion capacity based on the geographic location from which the isolates were obtained was also observed. Therefore, location specific differences in the distribution of the different taxonomic groups and their difference in plant growth promotion capacity could have important practical implication for the selection of the best microbial inoculants to improve plant growth and crop yield.
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References
Alstrom S, Burns RG (1989) Cyanide production by rhizobacteria as a possible mechanism of plant growth inhibition. Biol Fertil Soils 7:232–238
Bandyopadhyay T, Muthamilarasan M, Prasad M (2017) Millets for next generation climate-smart agriculture. Front. Plant Sci 8:1266. https://doi.org/10.3389/fpls.2017.01266
Barraquio W, Revilla L, Ladha J (1997) Isolation of endophytic diazotrophic bacteria from wetland rice. Plant Soil 194:15–24. https://doi.org/10.1023/A:1004246904803
Bresson J, Vasseur F, Dauzat M, Labadie M, Varoquax F, Touraine B, Vile D (2014) Interact to survive: Phyllobacterium brassicacearum improves Arabidopsis tolerance to severe water deficit and growth recovery. PLoS One 9:e107607. https://doi.org/10.1371/journal.pone.0107607
Chen B, Luo S, Wu Y, Ye J, Wang Q, Xu X, Pan F, Khan KY, Feng Y, Yang X (2017) The effects of the endophytic bacterium Pseudomonas fluorescens Sasm05 and IAA on the plant growth and cadmium uptake of Sedum alfredii Hance. Front Microbiol 8:2538. https://doi.org/10.3389/fmicb.2017.02538
Contesto C, Milesi S, Mantelin S, Zancarini A, Desbrosses G, Varoquaux F, Bellini C, Kowalczyk M, Touraine B (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455–1470. https://doi.org/10.1007/s00425-010-1264-0
Deletoile A, Decre D, Courant S, Passet V, Audo J, Grimont P, Arlet G, Brisse S (2009) Phylogeny and identification of Pantoea species and typing of Pantoea agglomerans strains by multilocus gene sequencing. J Clin Microbiol 47:300–310. https://doi.org/10.1128/JCM.01916-08
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. https://doi.org/10.1016/j.mex.2015.02.008
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15
Frank AC, Guzmán JPS, Shay JE (2017) Transmission of bacterial endophytes. Microorganisms 5:70. https://doi.org/10.3390/microorganisms5040070
Funke G, Aravena-Roman M, Frodl R (2005) First description of Curtobacterium spp. isolated from human clinical specimens. J Clin Microbiol 43:1032–1036. https://doi.org/10.1128/JCM.43.3.1032-1036.2005
Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39. https://doi.org/10.1016/j.micres.2013.09.009
Gneiding K, Frodl R, Funke G (2008) Identities of Microbacterium spp. encountered in human clinical specimens. J Clin Microbiol 46:3646–3652. https://doi.org/10.1128/JCM.01202-08
Gordon AS, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195
Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK (2018) Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res 206:131–140. https://doi.org/10.1016/j.micres.2017.08.016
Hardoim PR, Hardoim CCP, van Overbeek LS, van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7(2):e30438. https://doi.org/10.1371/journal.pone.0030438
Harman GE (2011) Trichoderma—not just for biocontrol anymore. Phytoparasitica 39:103–108. https://doi.org/10.1007/s12600-011-0151-y
Jakob K, Goss EM, Araki H, Van T, Kreitman M, Bergelson J (2002) Pseudomonas viridiflava and P. syringae—natural pathogens of Arabidopsis thaliana. Mol Plant-Microbe Interact 15:1195–1203. https://doi.org/10.1094/MPMI.2002.15.12.1195
Jensen V (1951) Notes on the biology of Azotobacter. Proc Soc Appl Bacteriol 74:93–98
Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian Protein Metabolism. Academic Press, New York, pp 21–132. https://doi.org/10.1016/B978-1-4832-3211-9.50009-7
Le Cocq K, Gurr SJ, Hirsch PR, Mauchline TH (2017) Exploitation of endophytes for sustainable agricultural intensification. Mol Plant Pathol 18:469–473. https://doi.org/10.1111/mpp.12483
Li X-Z, Song M-L, Yao X, Chai Q, Simpson WR, Li C-J, Nan Z-B (2017) The effect of seed-borne fungi and Epichloë endophyte on seed germination and biomass of Elymus sibiricus. Front Microbiol 8:2488. https://doi.org/10.3389/fmicb.2017.02488
Liu H, Zhang L, Meng A, Zhang J, Xie M, Qin Y, Dylan Chase Faulk DC, Zhang B, Yang S, Qiu L (2017) Isolation and molecular identification of endophytic diazotrophs from seeds and stems of three cereal crops. PLoS ONE 12:e0187383. https://doi.org/10.1371/journal.pone.0187383
López-López A, Rogel MA, Ormeño-Orrillo E, Martínez-Romero J, Martínez-Romero E (2010) Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol 33:322–327. https://doi.org/10.1016/j.syapm.2010.07.005
Marathe RJ, Phatake YB, Shaikh AC, Shinde BP, Gajbhiye MH (2017) Effect of IAA produced by Pseudomonas aeruginosa 6a (bc4) on seed germination and plant growth of Glycin max. J Exp Biol Agri Sci 5:351–358. https://doi.org/10.18006/2017.5(3).351.358
Marulanda A, Barea J-M, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124. https://doi.org/10.1007/s00344-009-9079-6
Matos ADM, Gomes ICP, Nietsche S, Xavier AA, Gomes WS, Neto JAD, Pereira MCT (2017) Phosphate solubilization by endophytic bacteria isolated from banana trees. An Acad Bras Cienc 89:2945–2954. https://doi.org/10.1590/0001-3765201720160111
Moore ERB, Arnscheidt A, Krüger A, Strömpl C, Mau M (1999) Simplified protocols for the preparation of genomic DNA from bacterial cultures. In: Akkermans ADL, van Elsas JD, de Bruijn FJ (eds) Molecular Microbial Ecology Manual. Kluwer Academic Publisher, Dordrecht, pp 1–15
Moss B (2008) Water pollution by agriculture. Phil Trans R Soc B 363:659–666. https://doi.org/10.1098/rstb.2007.2176
Naik BS, Shashikala J, Krishnamurthy YL (2009) Study on the diversity of endophytic communities from rice (Oryza sativa L.) and their antagonistic activities in vitro. Microbiol Res 164:290–296. https://doi.org/10.1016/j.micres.2006.12.003
Ngumbi E, Kloepper J (2016) Bacterial-mediated drought tolerance: Current and future prospects. Appl Soil Ecol 105:109–125 doi.org/10.1016/j.apsoil.2016.04.009
Olsen GJ, Matsuda H, Hagstrom R, Overbeek R (1994) FastDNAml: a tool for construction of phylogenetic trees of DNA sequences using maximum likelihood. Comput Appl Biosci 10:41–48
Oteino N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745. https://doi.org/10.3389/fmicb.2015.00745
Pan JJ, Baumgarten AM, May G (2008) Effects of host plant environment and Ustilago maydis infection on the fungal endophyte community of maize (Zea mays). New Phytol 178:147–156. https://doi.org/10.1111/j.1469-8137.2007.02350.x
Puente ME, Li CY, Bashan Y (2009) Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot 66:402–408. https://doi.org/10.1016/j.envexpbot.2009.04.007
Puri A, Padda KP, Chanway CP (2016) Seedling growth promotion and nitrogen fixation by a bacterial endophyte Paenibacillus polymyxa P2b-2R and its GFP derivative in corn in a long-term trial. Symbiosis 69:123–129. https://doi.org/10.1007/s13199-016-0385-z
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 4:1–11. https://doi.org/10.1186/s40538-016-0083-3
Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9. https://doi.org/10.1111/j.1574-6968.2007.00918.x
Santoyo G, Moreno-Hagelsieb G, Orozco-Mosquedac MDC, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99. https://doi.org/10.1016/j.micres.2015.11.008
Shade A, Jacques M-A, Barret M (2017) Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol 37:15–22. https://doi.org/10.1016/j.mib.2017.03.010
Shearin ZRC, Filipek M, Desai R, Bickford WA, Kowalski KP, Clay K (2018) Fungal endophytes from seeds of invasive, non-native Phragmites australis and their potential role in germination and seedling growth. Plant Soil 422:183–194. https://doi.org/10.1007/s11104-017-3241-x
Suman A, Yadav AN, Verma P (2016) Endophytic microbes in crops: diversity and beneficial impact for sustainable agriculture. In: Singh DP, Abhilash PC, Ratna P (eds) Microbial inoculants in sustainable agricultural productivity. Springer, Dordrecht, pp 117–143. https://doi.org/10.1007/978-81-322-2647-5_7
Sun L, Qiu F, Zhang X, Dai X, Dong X, Song W (2008) Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microb Ecol 55:415. https://doi.org/10.1007/s00248-007-9287-1
Tadele Z (2016) Drought adaptation in millets. In: Shanker AK, Shanker C (eds) Abiotic and biotic stress in plants—recent advances and future perspectives. ISBN 978-953-51-2250-0. https://doi.org/10.5772/61929
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Thompson JD, Higgins DG, Gibson TG (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Env Microbiol Rep 7:40–50. https://doi.org/10.1111/1758-2229.12181
Vejan P, Abdullah R, Khadiran T, Ismail S, Boyce AN (2016) Role of plant growth promoting rhizobacteria in agricultural sustainability—a review. Molecules 21:573. https://doi.org/10.3390/molecules21050573
Ventorino V, Aliberti A, Faraco V, Robertiello A, Giacobbe S, Ercolini D, Amore A, Fagnano M, Pepe O (2015) Exploring the microbiota dynamics related to vegetable biomasses degradation and study of lignocellulose-degrading bacteria for industrial biotechnological application. Sci Rep 5:8161–8174. https://doi.org/10.1038/srep08161
Verma SK, Kingsley K, Irizarry I, Bergen M, Kharwar RN, White JF (2017) Seed-vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol 122:1680–1691. https://doi.org/10.1111/jam.13463
Vinodhini J, Kannan R, Uma Sankareswari R, Akila R, Arumugam Pillai M (2017) Characterization of new bacterial leaf blight of rice caused by Pantoea stewartii subsp. indologenes in southern districts of Tamil Nadu. Int J Environ Agric Biotech 2:3279–3284
Vujanovic V, Germida JJ (2017) Seed endosymbiosis: a vital relationship in providing prenatal care to plants. Can J Plant Sci 97:972–981. https://doi.org/10.1139/cjps-2016-0261
Yadav A, Yadav K (2017) Exploring the potential of endophytes in agriculture: a minireview. Adv Plants Agric Res 6:102–106. https://doi.org/10.15406/apar.2017.06.00221
Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci 14:1–4. https://doi.org/10.1016/j.tplants.2008.10.004
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Misganaw, G., Simachew, A. & Gessesse, A. Endophytes of finger millet (Eleusine coracana) seeds. Symbiosis 78, 203–213 (2019). https://doi.org/10.1007/s13199-019-00607-5
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DOI: https://doi.org/10.1007/s13199-019-00607-5