Endophytic bacteria of rice plants (Oryza sativa L.) from eight different cultivars were screened for their ability in inducing disease symptoms, plant growth promotion and antagonistic activity against Xanthomonas oryzae pv. oryzae. Out of the 63 whole isolates, five were plant pathogens. Based on phenotypic characteristics and 16S rDNA sequence analysis, these were identified as Pseudomonas oryzihabitans, P. fulva, Pantoea ananatis, Pantoea sp., Cellulomonas sp. Four out of the 63 isolates behaved as potentially good plant growth-promoting and biocontrol agents. These were identified as Bacillus sp., B. subtilis, Pseudomonas putida and Enterobacter sp. This is the first report of pathogenic and endophytic bacteria from rice grown in field conditions in North of Iran.
If the inline PDF is not rendering correctly, you can download the PDF file here.
Aravind R. Kumar A. Eapen S.J. and Ramana K.V. 2009. Endophytic bacterial flora in root and stem tissues of black pepper (Piper nigrum L.) genotype: isolation identification and evaluation against Phytophthora capsici. Letters in Applied Microbiology 48: 58–64.
Baki A.A.A. and Anderson J.D. 1973. Vigour determination in soybean seed by multiple criteria. Crop Science 31: 630–633.Barka E. A. Gognies S. Nowak J. Audran J. C. and Belarbi A. 2002. Inhibitory effect of endophytic bacteria on Botrytis cinerea and its influence to promote the grape vine growth. Biological Control 24: 135–142.
Berg G. Eberl L. and Hartmann A. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environmental Microbiology 7(11): 1673–1685.
Bouallegue O. Mzoughi R. Weill F. X. Mahdhaoui N. Ben Salem Y. Sboui H. Grimont F. and Grimont P.A. 2004. Outbreak of Pseudomonas putida bacteraemia in a neonatal intensive care unit. The Journal of Hospital Infection 57(1): 88–91.
Brenner D.J. Mcwhorter A.C. Kai A. Steiger Walt A.G. and Farmer J.J. 1986. Enterobacter asburiae sp-nov a new species found in clinical specimens and reassignment of Erwinia dissolvens and Erwinia nimipressuralis to the genus Enterobacter as Enterobacter dissolvens comb-nov and Enterobacter nimipressuralis comb-nov. Journal of Clinical Microbiology 23(6): 1114–1120.
Chithrashree-Udayashankar A.C. Chandra-Nayaka S. Reddy M.S. and Srinivas C. 2011. Plant growth-promoting rhizobacteria mediate induced systemic resistance in rice against bacterial leaf blight caused by Xanthomonas oryzae pv. oryzae. Biological Control 59: 114–122.
Cho H.S. Park S.Y. Ryu C.M. Kim J.F. Kim J.G. and Park S.H. 2007. Interference of quorum sensing and virulence of the rice pathogen Burkholderia glumae by an engineered endophytic bacterium. Microbial Ecology 60: 14–23.
Chung E.J. Hossain M.T. Khan A. Kim K.H. Jeon C.O. and Chung Y.R. 2015. Bacillus oryzicola sp. nov. an endophytic bacterium isolated from the root of rice with anti-microbial plantgrowth promoting and systemic resistance-inducing activities in rice. The Plant Pathology Journal 31: 152–164.
Compant S. Duffy B. Nowak J. Cle´ment CH. and Ait Bark E. 2005. Use of Plant Growth-Promoting Bacteria for Biocontrol of Plant Diseases: Principles Mechanisms of Action and Future Prospects. Applied and Environmental Microbiology 71(9): 4951–4959.
Cother E.J. Noble D.H. van de Ven R.J. Lanoiselet V. Ash G. Vuthy N. Visarto P. and Stodart B. 2010. Bacterial pathogens of rice in the Kingdom of Cambodia and description of a new pathogen causing a serious sheath rot disease. Plant Pathology 59: 944–953.
Cottyn B. Regalado E. Lanoot B. De Cleene M. Mew T.W. and Swings J. 2001. Bacterial Populations Associated with Rice Seed in the Tropical Environment. Phytopathology 91(3): 282–292.
Cottyn B. Debode J. Regalado E. Mew T.W. and Swings J. 2009. Phenotypic and genetic diversity of rice seed-associated bacteria and their role in pathogenicity and biological control. Journal of Applied Microbiology 107:885–897.
D’Alessandro M. Erb M. Ton J. Brandenburg A. Karlen D. Zopfi J. and Turlings T.C.J. 2014. Volatiles produced by soil-borne endophytic bacteria increase plant pathogen resistance and affect tritrophic interactions. Plant Cell and Environment 37(4): 813–826.
Elbeltagy A. Nishioka K. Suzuki H. Sato T. Sato Y.I. Morisaki H. Mitsui H. and Minamisawa K. 2000. Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice Varieties. Soil Science and Plant Nutrition 46(3): 617–629.
Elboutahiri N. Thami-Alami I. Zaïd E. and M.Udupa S. 2009. Genotypic characterization of indigenous Sinorhizobium meliloti and Rhizobium sullae by rep-PCR RAPD and ARDRA analyses. African Journal of Biotechnology 8 (6): 979–985.
Fang Z.D. Xu Z.G. Guo C.J. Yin S.Z. Wu S.Z. Xu X.M. and Zhang Q. 1990. Studies on pathotypes of Xanthomonas campestris pv. oryzae in China. Acta Phytopathologica Sinica 20: 81–88.
Flores-Tena F.J. Guerrero-Barrera A.L. Avelar-González F.J. Ramírez-López E.M. and Martínez-Saldaña M.C. 2007. Pathogenic and opportunistic gram-negative bacteria in soil leachate and air in San Nicolás landfill at Aguascalientes México. Revista Latinoamericana de Microbiología 49: 25-30.
Gupta A. Saxena A. K. Gopal M. and Tilak K. V. B. R. 1998. Effect of plant growth promoting rhizobacteria on competitive ability of introduced Bradyrhizobium sp. (Vigna) for nodulation. Microbiol Res 153:113–117.
Hallmann J. Quadt-Hallmann A. Mahaffee W.F. and Kleopper W. 1997. Bacterial endophytes in agricultural crops. Canadian Journal of Microbiology 43: 895–914.
Hossain M.T. Khan A. Chung E.J. Harun-Or Rashid Md. and Chung Y.R. 2016. Biological Control of Rice Bakanae by an Endophytic Bacillus oryzicola YC7007. The Plant Pathology Journal 32(3): 228–241.
ISTA. 1993. Proceedings of the international Seed Testing Association International Rules for Seed Testing. Seed Science and Technology 21: 25–30.
Jabeen R. Iftikhar T. Ashraf M. and Ahmad I. 2011. Virulence/aggressiveness testing of Xanthomonas oryzae pv. oryza isolates causes BLB disease in rice cultivars of Pakistan. Pakistan Journal of Botany 43(3): 1725-1728.
Ji S.H. Gururani M.A. and Chun S.Ch. 2014. Isolation and characterization of plant growth promoting endophytic diazotrophic bacteria from Korean rice cultivars. Microbiological Research 169: 83–98.
Kaga H. Mano H. Tanaka F. Watanabe A. Kaneko S. and Morisaki H. 2009. Rice Seeds as Sources of Endophytic Bacteria. Microbes and Environments 24(2): 154–162.
Kang S.H. Cho H.S. Cheong H. Ryu C.M. Kim J.F. and Park S.H. 2007. Two bacterial endophytes eliciting both plant growth promotion and plant defense on Pepper (Capsicum annuum L.). Journal of Microbiology and Biotechnology 17(1): 96-103.
Kauffman H.E. Reddy A.P.K. Hsieh S.P.Y. and Merca S.D. 1973. An improved technique for evaluating resistance of rice varieties to Xanthomonas oryzae. Plant Disease Reporter 57: 537–541.
Khalifa A.Y.Z. Alsyeeh A.M. Almalki M.A. and Saleh F.A. 2016. Characterization of the plant growth promoting bacterium Enterobacter cloacae MSR1 isolated from roots of non-nodulating Medicago sativa. Saudi Journal of Biological Sciences 23: 79–86.
Kumar S. Stecher G. and Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.
Lund B.M. and Wyatt G.M. 1972. The effect of oxygen and carbon dioxide concentrations on bacterial soft rot of potatoes. I. King Edward potatoes inoculated with Erwinia carotovora var. atroseptica. Potato Research 15: 174–179.
Mano H. Tanaka F. Watanabe A. Kaga H. Okunishi S. and Morisaki H. 2006. Culturable surface and endophytic bacterial flora of the maturing seeds of rice plants (Oryza sativa) cultivated in a paddy field. Microbes and Environments 21: 86–100.
Mano H. Tanaka F. Nakamura C.H. Kaga H. and Morisaki H. 2007. Culturable endophytic bacterial flora of the maturing leaves and roots of rice plants (Oryza sativa) cultivated in a paddy field. Microbes and Environments 22 (2): 175–185.
Mano H. and Morisaki H. 2008. Endophytic Bacteria in the Rice Plant. Microbes and Environments 23(2): 109–117.
McInroy J.A. and Kloepper J.W. 1995. Population dynamics of endophytic bacteria in field-grown sweet corn and cotton. Canadian Journal of Microbiology 41: 895–901.
Melnick R.L. Zidack N.K. Bailey B.A. Maximova S.N. Guiltinan M. Backman P.A. 2008. Bacterial endophytes: Bacillus spp. from annual crops as potential biological control agents of black pod rot of cacao. Biological Control 46: 46–56. doi:10.1016/j.biocontrol.2008.01.022.
Mishra R.P. Singh R.K. Jaiswal H.K. Kumar V. and Maurya S. 2006. Rhizobium-mediated induction of phenolics and plant growth promotion in rice (Oryza sativa L.). Current Microbiology 52 (5): 383-9.
Molina L. Duque E. Gómez M.J. Krell T. Lacal J. García-Puente A. García V. Matilla M.A. Ramos J.L. and Segura A. 2011. The pGRT1 plasmid of Pseudomonas putida DOT-T1E encodes functions relevant for survival under harsh conditions in the environment. Environmental Microbiology 13(8): 2315-27.
Molina L. Udaondo Z. Duque E. Fernández M. Molina-Santiago C. Roca A. Porcel M. de la Torre J. Segura A. Plesiat P. Jeannot K. and Ramos J.L. 2014. Antibiotic resistance determinants in a Pseudomonas putida strain isolated from a hospital. PLoS ONE 9(1): e81604. doi: 10.1371/journal.pone.0081604.
Moronta-Barrios F. Gionechetti F. Pallavicini A. Marys E. and Venturi V. 2017. Isolation and studies on bacterial endophytes from two venezuelan rice cultivars. Preprints (www.preprints.org). doi:10.20944/preprints201709.0031.v1
Nhu V.T.P. and Diep C.N. 2014. Isolation characterization and phylogenetic analysis of endophytic bacteria in rice plant cultivated on soil of Phu Yen province Vietnam. American Journal of Life Sciences 2(3): 117–127.
Okunishi S. Sako K. Mano H. Imamura A. and Morisaki H. 2005. Bacterial Flora of Endophytes in the Maturing Seed of Cultivated Rice (Oryza sativa). Microbes and Environments 20(3): 168–177.
Oliveira A.L.M. Canuto E.L. Reis V.M. and Baldani J.I. 2003. Response of micropropagated sugarcane varieties to inoculation with endophytic diazotrophic bacteria. Brazilian Journal of Microbiology 34: 59–61.
Ou S.H. 1985. Rice Diseases. 2nd ed. Kew-Surrey-England: Common Wealth Mycological Institute 380 p.
Palacio-Bielsa A. Cambra M.A. and López M.M. 2009. PCR detection and identification of plantpathogenic bacteria: updated review of protocols (1989-2007). Journal of Plant Pathology 91 (2): 249–297.
Peng H. Chen Z. H. Fang Z. H. Zhou J. Xi Z. H. Gao L. Chen L. Li L. Li T. Zhai W. and Zhang W. 2015. Rice Xa21 primed genes and pathways that are critical for combating bacterial blight infection. Scientific Reports 5: 12165. doi: 10.1038/srep12165.
Roberts D. P. Short N. M. Maloney A. P. Nelson E. B. and Schaff D. A. 1994. Role of colonization in biocontrol: studies with Enterobacter cloacae. Plant Science 101: 83–89.
Qiang SH. Ming L. Jingjing G. Xianglin Zh. and Chunzhu Zh. 2017. Characterization of Pseudomonas fulva as a new pathogen of pepper leaf spot isolated from Xinjiang in China. Journal of Plant Protection 2.
Reinhold-Hurek B. and Hurek T. 2011. Living inside plants: bacterial endophytes. Curren Opinion in Plant Biology 14: 435–443.
Reiter B. Pfeifer U. Schwab H. and Sessitsch A. 2002. Response of endophytic bacterial communities in potato plants to infection with Erwinia carotovora sub sp. atroseptica. Applied and Environmental Microbiology 68: 2261–2268.
Rodriguez R.J. Henson J. Van Volkenburgh E. Hoy M. Wright L. Beckwith F. Kim Y.O. and Redman R.S. 2008. Stress tolerance in plants via habitat-adapted symbiosis. The ISME Journal 2(4): 404–16.
Rodriguez R.J. White J.F.Jr. Arnold A.E. Redman R.S. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182 (2): 314-30.
Rosenblueth M. and Martínez-Romero E. 2006. Bacterial Endophytes and Their Interactions with Hosts. Molecular Plant-Microbe Interactions 19 (8): 827–837.
Ryan R.P. Germaine K. Franks A. Ryan D.J. and Dowling D.N. 2008. Bacterial endophytes: recent developments and applications. FEMS Microbiology Letters 278 (1): 1-9.
Santoyo G. Moreno-Hagelsieb G. Orozco-Mosqueda M.C. and Glick B.R. 2016. Plant growth-promoting bacterial endophytes. Microbiological Research 183: 92–99.
Schaad N.W. Jones J. B. and Chun W. 2001. Laboratory guide for identification of plant pathogenic bacteria. 3rd ed. St Paul Minnesota-USA: APS 245 p.
Schulz B. and Boyle C. 2005. The endophytic continuum. Mycological Research 109: 661-686.
Schulz B. Boyle C. 2006. What are endophytes? In: Schulz B.J.E. Boyle C.J.C. Sieber T.N. (eds). Microbial Root Endophytes. Berlin Germany Springer pp 1–13.
Sessitsch A. Reiter B. and Berg G. 2004. Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Canadian Journal of Microbiology 53: 239–249.
Sheoran N. Nadakkakathb A V. Munjal V. Kundu A. Subaharand K. Venugopal V. Rajamma S. Eapen. S. J. and Kumara A. 2015. Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiological Research 173: 66–78.
Shrestha B.K. Karki H.S. Groth D.E. Jungkhun N. and Ham J.H. 2016. Biological control activities of rice-associated Bacillus sp. strains against sheath blight and bacterial panicle blight of rice. PLoS ONE 11(1): e0146764. doi:10.1371/journal.pone.0146764.
Sturz A.V. Christie B.R. Matheson B.G. and Nowak J. 1997. Biodiversity of endophytic bacteria which colonize red clover nodules roots stems and foliage and their influence on host growth. Biology and Fertility of Soils 25: 13-19.
Sturz A.V. Christie B.R. and Nowak J. 2000. Bacterial endophytes: potential role in developing sustainable system of crop production. Critical Reviews in Plant Sciences 19: 1–30.
Szilagyi-Zecchin V.J. Ikeda A.C. Hungria M. Adamoski D. Kava-Cordeiro V. Glienke C.H. and Galli-Terasawa L.V. 2014. Identification and characterization of endophytic bacteria from corn (Zea mays L.) roots with biotechnological potential in agriculture. AMB Express 4: 26.
Taghavi S. Van der Lelie D. Hoffman A. Zhang Y-B. Walla M.D. Vangronsveld J. Newman L. and Monchy S. 2010. Genome Sequence of the Plant Growth Promoting Endophytic Bacterium Enterobacter sp. 638. PLoS Genetics 6(5): e1000943. doi:10.1371/journal.pgen.1000943.
Tamura K. Stecher G. Peterson D. Filipski A. and Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30: 2725-2729.
Thomas B.S. Okamoto K. Bankowski M.J. and Seto T.B. 2013. A lethal case of Pseudomonas putida bacteremia due to soft tissue infection. Infectious Diseases in Clinical Practice 21(3): 147-213.
Tsuda K. Kosaka Y. Tsuge S. Kubo Y. and Horino O. 2001. Evaluation of the endophyte Enterobacter cloacae SM10 isolated from spinach roots for biological control against Fusarium wilt of spinach. Journal of General Plant Pathology 67: 78-84.
van Peer R. Punte H.L.M. de Weger L.A. and Schippers B. 1990. Characterization of root surface and endorhizosphere pseudomonads in relation to their colonization of roots. Applied and Environmental Microbiology 56: 2462-2470.
Verma S.C. Ladha J.K. and Tripathi A.K. 2001. Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. Journal of Biotechnology 91: 127–141.
Witzel K. Gwinn-Giglio M. Nadendla S. Shefchek K. and Ruppel S. 2012. Genome sequence of enterobacter radicincitans DSM16656T a plant growth-promoting endophyte. Journal of Bacteriology 194 (19): p. 5469.
Zhu B. Chen M. Lin L. Yang L. Li Y. and An Q. 2012. Genome sequence of Enterobacter sp. strain SP1 an endophytic nitrogen-fixing bacterium isolated from sugarcane. Journal of Bacteriology 194 (24): p. 6963–6964.
Zou L.F. Wang X.P. Xiang Y. Zhang B. Li Y.R. Xiao Y.L. Wang J.Sh. R. Walmsley A. and Chen G. You. 2006. Elucidation of the hrp clusters of Xanthomonas oryzae pv. oryzicola that control the hypersensitive response in nonhost tobacco and pathogenicity in susceptible host rice. Applied and Environmental Microbiology 72: 6212–6224.
Yang J.H. Liu H.X. Zhu G.M. Pan Y.L. Xu L.P. and Guo J.H. 2008. Diversity analysis of antagonists from rice-associated bacteria and their application in biocontrol of rice diseases. Journal of Applied Microbiology 104: 91–104.