Characterisation of Plant Growth-Promoting Endophytic Bacteria from Sugarcane and Their Antagonistic Activity against Fusarium moniliforme

Main Article Content

Nittaya Pitiwittayakul
Duanpen Wongsorn
Somboon Tanasupawat

Abstract


The use of endophytic bacteria in agriculture provides an effective way of improving crop yield and significantly reducing chemical usage, such as fungicides. This research was conducted to explore endophytic bacteria with plant growth promotion (PGP) and antifungal activities against Fusarium moniliforme AIT01. In this study, we obtained 52 isolates of endophytic bacteria associated with the roots and stems of sugarcane from Nakhon Ratchasima province, Thailand. In vitro antagonistic activity test showed that 14 out of 52 isolates had antagonistic activity against the fungal pathogen F. moniliforme AIT01. These antagonistic endophytic bacteria were identified as belonging to six different species as follows: Nguyenibacter vanlangensis, Acidomonas methanolica, Asaia bogorensis, Tanticharoenia aidae, Burkholderia gladioli and Bacillus altitudinis based on phenotypic characteristics, along with phylogenetic analysis of their 16S rRNA gene sequences. Seven isolates effectively inhibited F. moniliforme AIT01 mycelial growth by up to 40%. The volatile compounds of six isolates reduced the growth of F. moniliforme AIT01 by over 23%. Moreover, riceberry rice seedlings previously treated with B. gladioli CP28 were found to strongly reduce infection with phytopathogen by 80% in comparison to the non-treated control. Furthermore, the isolates also showed relevant PGP features, including ammonia production, zinc and phosphate solubilisation, auxin and siderophore biosynthesis. These results demonstrated that the tested endophytic bacteria could be successfully utilised as a source of PGP and biocontrol agent to manage diseases caused by F. moniliforme.


Article Details

How to Cite
Characterisation of Plant Growth-Promoting Endophytic Bacteria from Sugarcane and Their Antagonistic Activity against Fusarium moniliforme. (2021). Tropical Life Sciences Research, 32(3), 97–118. https://doi.org/10.21315/tlsr2021.32.3.6
Section
Original Article

References

Ahmad T, Bashir A, Farooq S and Riyaz-Ul-Hassan S. (2021). Burkholderia gladioli E39CS3, an endophyte of Crocus sativus Linn., induces host resistance against corm-rot caused by Fusarium oxysporum. Journal of Applied Microbiology (Early View). https://doi.org/10.1111/jam.15190

Arya A, Sharma R, Sharma G, Kabdwal B C, Negi A and Mishra B. (2017). Evaluation of fungal and bacterial antagonists for managing phytopathogen Fusarium moniliforme var. subglutinans Sheldon, causing Pokkah Boeng disease of sugarcane. Journal of Biological Control 31(4): 217–222. https://doi.org/10.18311/jbc/2017/15456

Asai T, Iizuka H and Komagata K. (1964). The flagellation and taxonomy of genera Gluconobacter and Acetobacter with reference to the existence of intermediate strains. Journal of General and Applied Microbiology 10: 95–126. https://doi.org/10.2323/jgam.10.95

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, 331.

Cappuccino J C and Sherman N. (2001). Microbiology: a laboratory manual, 6th ed. New York: Benjamin/Cummings.

Cavalcante V A and Döbereiner J. (1988). A new acid-tolerant nitrogen-fixing bacteria associated with sugarcane. Plant Soil 108: 23–31.

Chaturvedi H, Singh V and Gupta G. (2016). Potential of bacterial endophytes as plant growth promoting factors. Journal of Plant Pathology Microbiology 7: 376. https://doi.org/10.4172/2157-7471.1000376

Devereux R and Wills S G. (1995). Amplification of ribosomal RNA sequences. In A D L Akkermans, J D van Elsas and F J De Bruijn (Eds.). Molecular Microbial Ecology Manual. Dordrecht: Academic Publishers, 3.3.1–3.3.2.

Elshafie H S and Camele I. (2021). An overview of metabolic activity, beneficial and pathogenic aspects of Burkholderia spp. Metabolites 11: 321. http://doi.org/10.3390/metabo11050321

Felsenstein J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783–791. https://doi.org/10.2307/2408678

Gandhi A and Muralidharan G. (2016). Assessment of zinc solubilizing potentiality of Acinetobacter sp. isolated from rice rhizosphere. European Journal of Soil Biology 76: 1–8. https://doi.org/10.1016/j.ejsobi.2016.06.006

Gillis M, Kersters K, Hoste B, Janssens D, Kroppenstedt R M, Stephan M P, Teixeira K R S, Döbereiner J and De Ley J. (1989). Acetobacter diazotrophicus sp. nov., a nitrogen fixing acetic acid bacterium associated with sugarcane. International Journal of Systematic and Bacteriology 39: 361–364. https://doi.org/10.1099/00207713-39-3-361

Glickmann E and Dessaux Y. (1995). A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Applied and Environment Microbiology 61(2): 793–796. https://doi.org/10.1128/aem.61.2.793-796.1995

Gond S K, Bergen M, Torres M S and White J F. (2015). Effect of bacterial endophyte on expression of defense genes in Indian popcorn against Fusarium moniliforme. Symbiosis 66: 133–140. https://doi.org/10.1007/s13199-015-0348-9

Gordon S A and Weber R P. (1951). Colorimetric estimation of indoleacetic acid. Plant Physiology 26(1): 192–195. https://doi.org/10.1104/pp.26.1.192

Hall T A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.

Hardoim P R, van Overbeek L S, Berg G, Pirttilä C S, Campisano A, Dörin M and Sessitch A. (2015). The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79: 293–320. https://doi.org/10.1128/MMBR.00050-14

Hazarika D J, Goswami G, Gautom T, Parveen A, Das P, Barooah M and Boro R C. (2019). Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiology 19: 71. https://doi.org/10.1186/s12866-019-1440-8

Hossain M T, Khan A, Chung E J, Rashid M H and Chung Y R. (2016). Biological control of rice bakanae by endophytic Bacillus oryzicola YC7007. The Plant Pathology Journal 32(3): 228–241. https://doi.org/10.5423/PPJ.OA.10.2015.0218

Khaskheli M A, Wu L, Chen G, Chen L, Hussain S, Song D, Liu S and Feng G. (2020). Isolation and characterization of root-associated bacterial endophytes and their biocontrol potential against major fungal phytopathogens of rice (Oryza sativa L.). Pathogen 9(3): 172. https://doi.org/10.3390/pathogens9030172

Kim O S, Cho Y J, Lee K, Yoon S H, Kim M, Na H, Park S C, Jeon Y S, Lee J H, Yi H, et al. (2012). Introducing EzTaxon-e: A prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. International Journal of Systematic and Evolutionary Microbiology 62: 716–721. https://doi.org/10.1099/ijs.0.038075-0

Kimura M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120. https://doi.org/10.1007/BF01731581

Kumar S, Stecher G and Tamura K. (2016). MEGA7: Molecular evolution genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054

Leslie J F and Summerell B A. (2006). The Fusarium Laboratory Manual, 1st ed. Blackwell.

Li X, Li Y, Wang R, Wang Q and Lu L. (2019). Toxoflavin produced by Burkholderia gladioli from Lycoris aurea is a new broad-spectrum fungicide. Applied and Environmental Microbiology 85(9): e00106-19. https://doi.org/10.1128/AEM.00106-19

Logeshwarn P, Thangaraju M and Rajasundari K. (2011). Antagonistic potential of Gluconacetobacter diazotrophicus against Fusarium oxysporum in sweet potato (Ipomea batatus). Archives of Phytopathology and Plant Protection 44(3): 216–223. https://doi.org/10.1080/03235400902952707

Luo T, Ou-Yang X Q, Yang L T, Li Y R, Song X P, Zhang G M, Gao Y J, Duan W X and An Q. (2016). Raoultella sp. strain L03 fixes N2 in association with micropropagated sugarcane plants. Journal of Basic Microbiology 56(8): 934–940. https://doi.org/10.1002/jobm.201500738

Ma L, Ji Z, Bao J, Zhu X, Li X, Zhuang J, Yang C and Xia Y. (2008). Responses of rice genotypes carrying different dwarf genes to Fusarium moniliforme and Gibberellic acid. Plant Production Science 11(1): 134–138. https://doi.org/10.1626/pps.11.134

Madhaiyan M, Saravanan V S, Bhakiya Silba Sandal Jovi D, Lee H, Thenmozhi R, Hari K and Sa T M. (2004). Occurrence of Gluconacetobacter diazotrophicus in tropical and subtropical plants of Western Ghats, India. Microbiological Research 159: 233–243. https://doi.org/10.1016/j.micres.2004.04.001

Muangthong A, Youpensuk S and Rerkasem B. (2015). Isolation and characterization of nitrogen fixing bacteria in sugarcane. Tropical Life Sciences Research 26(1): 41–51.

Olanrewaju O, Glick B R and Babalola O O. (2017). Mechanisms of action of plant growth bacteria. World Journal of Microbiology and Biotechnology 33: 197. https://doi.org/10.1007/s11274-017-2364-9

Oliveira M M, Ramos E T A, Drechsel M M, Vidal M S, Schwab S and Baldani J I. (2018). Gluconacin from Gluconacetobacter diazotrophicus PAL5 is an active bacteriocin against phytopathogenic and beneficial sugarcane bacteria. Journal of Applied Microbiology 125: 1812–1826. https://doi.org/10.1111/jam.14074

Pande A, Pandey P, Mehra S, Mehra S, Singh M and Kaushik S. (2017). Phenotypic and genotypic characterization of phosphate solubilizing bacteria and their efficiency on the growth of maize. Journal of Genetic Engineering and Biotechnology 15: 379–391. https://doi.org/10.1016/j.jgeb.2017.06.005

Potshangbam M, Sahoo D, Verma P, Verma S, Chandra Kalita M and Indira Devi S. (2018). Draft genome sequence of Bacillus altitudinis Lc5, a biocontrol and plant growthpromoting endophyte strain isolated from indigenous black rice of Manipur. Genome Announcements 6(26): e00601-18. https://doi.org/10.1128/genomeA.00601-18

Reis V M and Teixeira K R. (2015). Nitrogen fixing bacteria in the family Acetobacteraceae and their role in agriculture. Journal of Basic Microbiology 55(8): 931–949. https://doi.org/10.1002/jobm.201400898

Rezamahalleh H M, Khodakaramian G and Hassanzadeh N. (2019). Diversity of endophytic bacteria from sugarcane in Khuzestan, Iran. Brazilian Archives of Biology and Technology 62: e19180407. https://doi.org/10.1590/1678-4324-2019180407

Rocha F Y O, Negrisoli Júnior A S, de Matos G F, Gitahy P M, Rossi C N, Vidal M S and Baldani J I. (2021). Endophytic Bacillus bacteria living in sugarcane plant tissues Telchin licus licus larvae (Drury) (Lepidoptera: Castniidae): the symbiosis that may open new paths in the biological control. Frontiers in Microbiology 12: 659965. https://doi.org/10.3389/fmicb.2021.659965

Saechow S, Thammasittirong A, Kittakoop P, Prachya S and Thammasittirong S N. (2018). Antagonistic activity against dirty panicle rice fungal pathogens and plant growthpromoting activity of Bacillus amyloliquefaciens BAS23. Journal of Microbiology and Biotechnology 28(9): 1527–1535. https://doi.org/10.4014/jmb.1804.04025

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

Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda Mdel C and Glick B R. (2016). Plant growth-promoting bacterial endophytes. Microbiological Research 183: 92–99. https://doi.org/10.1016/j.micres.2015.11.008

Schwyn B and Neilands J B. (1987). Universal assay for the detection and determination of siderophores. Analytical Biochemistry 160: 47–56. https://doi.org/10.1016/0003-2697(87)90612-9

Seearunruangchai A, Tanasupawat S, Keeratipibut S, Thawai C, Itoh T and Yamada Y. (2004). Identification of acetic acid bacteria isolated from fruits and related materials collected in Thailand. Journal of General and Applied Microbiology 50: 47–53. https://doi.org/10.2323/jgam.50.47

Sunder S, Singh R and Dodan D S. (2014). Management of bakanae disease of rice caused by Fusarium moniliforme. Indian Journal of Agricultural Sciences 84(1): 48-52.

Tam H M and Diep C N. (2014). Isolation, characterization and identification of endophytic bacteria in sugarcane (Saccharum spp. L.) cultivate on soils of the Dong Nai Province, Southeast of Vietnam. American Journal of Life Sciences 2(6): 361–368. https://doi.org/10.11648/j.ajls.20140206.16

Tanasupawat S, Okada S and Komagata K. (1998). Lactic acid bacteria found in fermented fish in Thailand. Journal of General and Applied Microbiology 44: 193–200. https://doi.org/10.2323/jgam.44.193

Tenorio-Salgado S, Tinoco R, Vazquez-Duhalt R, Caballero-Mellado J and Perez-Rueda E. (2013). Identification of volatile compounds produced by the bacterium Burkholderia tropica that inhibit the growth of fungal pathogens. Bioengineered 4(4): 236–243. https://doi.org/10.4161/bioe.23808

Thompson J D, Higgins D G and Gibson T J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positionspecific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680. https://doi.org/10.1093/nar/22.22.4673

Verma S K, Kingsley K, Bergen M S, Kowalski K P and White J F. (2018). Fungal disease prevention in seedling of rice (Oryza sativa) and other grasses by growthpromoting seed-associated endophytic bacteria from invasive Phragmites australis. Microorganisms 6: 21. https://doi.org/10.3390/microorganisms6010021

Vishwakarma S K, Kumar P, Nigam A, Singh A and Kumar A. (2013). Pokkah Boeng: An emerging disease of sugarcane. Journal of Plant Pathology and Microbiology 4: 3. https://doi.org/10.4172/2157-7471.1000170

Vu H T L, Bui V T T, Bui U T T, Yukphan P, Malimas T, Kieu N P, Muramatsu Y, Tanasupawat S, Le B T, Yamada Y et al. (2019a). The traits of the plant growth promoting acetic acid bacterium, Nguyenibacter vanlangensis. Vietnam Journal of Science and Technology 57(4): 439–448. https://doi.org/10.15625/2525-2518/57/4/13523

Vu H TL, Malimas T, Chaipitakchonlatarn W, Bui V T T, Yukphan P, Bui U T T, Muramatsu Y, Sitdhipol J, Tanasupawat S, Duong K C, et al. (2016). Tanticharoenia aidae sp. nov., for acetic acid bacteria isolated in Vietnam. Annals of Microbiology 66: 417–423. https://doi.org/10.1007/s13213-015-1124-z

Vu H T L, Yukphan P, Bui V T T, Charoenyingcharoen P, Malimas S, Nguyen L K, Muramatsu Y, Tanaka N, Tanasupawat S, Le B T et al. (2019b). Acetobacter sacchari sp. nov., for a plant growth-promoting acetic acid bacterium isolated in Vietnam. Annals of Microbiology 69: 1155–1163. https://doi.org/10.1007/s13213-019-01497-0

Vu H T L, Yukphan P, Chaipitakchonlatarn W, Malimas T, Muramatsu Y, Bui U T T, Tanasupawat S, Duong K C, Nakagawa Y, Pham H T et al. (2013). Nguyenibacter vanlangensis gen. nov., sp. nov., an unusual acetic acid bacterium in the ?-Proteobacteria. Journal of General and Applied Microbiology 59(2): 153–166. https://doi.org/10.2323/jgam.59.2_153

Zain M, Yasmin S and Hafeez F Y. (2019). Isolation and characterization of plant growth promoting antagonistic bacteria from cotton and sugarcane plants for suppression of phytopathogenic Fusarium species. Iranian Journal of Biotechnology 17(2): e1974. https://doi.org/10.21859/ijb.1974

Zeng Q, Shi G Y, Nong Z, Ye X L and Hu C J. (2020). Complete genome sequence of Pantoea ananatis strain NN08200, an endophytic bacterium isolated from sugarcane. Current Microbiology 77: 1864–1870. https://doi.org/10.1007/s00284-020-01972-x