Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Changes of enzyme activities related to oxidative stress in rice plants inoculated with random mutants of a Pseudomonas fluorescens strain able to improve plant fitness upon biotic and abiotic conditions

Jose A. Lucas A B , Ana Garcia-Villaraco Velasco A , Beatriz Ramos A and Francisco J. Gutierrez-Mañero A
+ Author Affiliations
- Author Affiliations

A Universidad San Pablo CEU, Dept. Pharmaceutical Science and Health, Facultad Farmacia, Urb. Monteprincipe, Boadilla del Monte, 28668 Madrid, Spain.

B Corresponding author. Email: alucgar@ceu.es

Functional Plant Biology 44(11) 1063-1074 https://doi.org/10.1071/FP17022
Submitted: 5 October 2016  Accepted: 30 June 2017   Published: 31 July 2017

Abstract

The Pseudomonas fluorescens strain used in this work (Aur 6) has demonstrated its ability to improve fitness of different plant species upon biotic and abiotic stress conditions. Random mutants of this strain were constructed with the Tn5 transposon technology, and biological tests to evaluate loss of salt protection were conducted with all the mutants (104 mutants) on rice seedlings. Mutant 33 showed an evident reduction in its ability to protect plants upon salt stress challenge, whereas mutant 19 was more effective than the wild type. Enzymes related with oxidative stress were studied in both mutants and wild type. Enzyme activities were decreased with mutant 33 with regard to wild type, whereas mutant 19 did not produce important changes suggesting involvement of redox balance associated to the observed modifications in these antioxidant enzymes as one of the probable mechanisms used by these strains. Data of malondialdehyde (MDA) were consistent with this fact. Mutants also affected accumulation of proline, the most common osmolyte in plants. A second experiment to evaluate the ability of both mutants and wild type to stimulate growth on tomato plants was conducted, as this feature was previously demonstrated by wild type. Similar results were obtained in growth of both species, suggesting that mutations of both mutants are related with the capacities of the wild type to stimulate growth. To reveal mutated genes, both mutants were mapped. Three mutated genes were found in mutant 33. A gene related with a general secretion pathway protein D, a gene related with a putative two-component system sensor kinase (ColS), and a gene related with flagellar motor switch protein (FliG). In mutant 19, two mutated genes were found. One gene related with heavy metal efflux pump Czca family, and other gene of 16s rRNA.

Additional keywords: antioxidant enzymes, PGPR, reactive oxygen species, rice, ROS, salt stress.


References

AbdElgawad H, Zinta G, Hegab MM, Pandey R, Asard H, Abuelsoud W (2016) High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs. Frontiers in Plant Science 7, 145–156.
High salinity induces different oxidative stress and antioxidant responses in maize seedlings organs.CrossRef |

Alvarez MI, Sueldo RJ, Barassi CA (1996) Effect of Azospirillum on coleoptile growth in wheat seedlings under water stress. Cereal Research Communications 24, 101–107.

Barriuso J, Solano B, Gutiérrez Mañero F (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp. on Arabidopsis thaliana. Phytopathology 98, 666–672.
Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp. on Arabidopsis thaliana.CrossRef | 1:STN:280:DC%2BD1cjlslKmtA%3D%3D&md5=88e35b12065148bc23edf2a8ed2dd8a4CAS |

Bitter W, Koster M, Latijnhouwers M, Cock H, Tommassen J (1998) Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa. Molecular Microbiology 27, 209–219.
Formation of oligomeric rings by XcpQ and PilQ, which are involved in protein transport across the outer membrane of Pseudomonas aeruginosa.CrossRef | 1:CAS:528:DyaK1cXjtlymtQ%3D%3D&md5=d519dcf21e344dc41622e9fad8289fd5CAS |

Bojórquez-Quintal E, Velarde-Buendía A, Ku-González A, Carillo-Pech M, Ortega-Camacho D, Echevarría-Machado I (2014) Mechanisms of salt tolerance in habanero pepper plants (Capsicum chinense Jacq.): proline accumulation, ions dynamics and sodium root-shoot partition and compartmentation. Frontiers in Plant Science 5, 605–618.

Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A (2008) Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Functional Plant Biology 35, 412–426.
Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine.CrossRef | 1:CAS:528:DC%2BD1cXotlCksLk%3D&md5=f3d4efa14705c2a8f7d1a5f7df57267fCAS |

Cattelan AJ, Hartel PG, Fuhrmann JJ (1999) Screening for plant growth-promoting rhizobacteria to promote early soybean growth. Soil Science Society of America Journal 63, 1670–1680.
Screening for plant growth-promoting rhizobacteria to promote early soybean growth.CrossRef | 1:CAS:528:DC%2BD3cXhsFyku7s%3D&md5=e4a8c6ce4ae3cd6379c4bb7ecc6c78dfCAS |

Cezón R, Mañero FG, Probanza A, Ramos B, Lucas García JA (2003) Effects of two plant growth-promoting rhizobacteria on the germination and growth of pepper seedlings (Capsicum Annum) cv. Roxy. Archives of Agronomy and Soil Science 49, 593–603.
Effects of two plant growth-promoting rhizobacteria on the germination and growth of pepper seedlings (Capsicum Annum) cv. Roxy.CrossRef |

Conrath U (2011) Molecular aspects of defence priming. Trends in Plant Science 16, 524–531.
Molecular aspects of defence priming.CrossRef | 1:CAS:528:DC%2BC3MXht1GgsLfF&md5=fbe13531c605c61e922cec11b03a3ac0CAS |

Conrath U, Beckers GJM, Flors V, García-Agustín P, Jakab G, Mauch F, Newman MA (2006) Priming: getting ready for battle. Molecular Plant-Microbe Interactions 19, 1062–1071.
Priming: getting ready for battle.CrossRef | 1:CAS:528:DC%2BD28Xht12ht77F&md5=1aff3b0cc347a7186ca2a72c40f1b704CAS |

de Freitas JR, Banerjee MR, Germida JJ (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biology and Fertility of Soils 24, 358–364.
Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.).CrossRef | 1:CAS:528:DyaK2sXjsFSrsb0%3D&md5=2b7fa42cfd8416dd8a4142510d7528c5CAS |

De Vleesschauwer D, Höfte M (2009) Rhizobacteria-induced systemic resistance. Advances in Botanical Research 51, 223–281.
Rhizobacteria-induced systemic resistance.CrossRef | 1:CAS:528:DC%2BD1MXhs1Slsr%2FE&md5=6839e3077d3b6f32697e719bfd6489acCAS |

De Weert S, Dekkers LC, Bitter W, Tuinman S, Wijfjes AHM, Van Boxtel R, Lugtenberg BJJ (2006) The two-component colR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane. FEMS Microbiology Ecology 58, 205–213.
The two-component colR/S system of Pseudomonas fluorescens WCS365 plays a role in rhizosphere competence through maintaining the structure and function of the outer membrane.CrossRef | 1:CAS:528:DC%2BD28XhtF2rtrvL&md5=e7f33f15ebe668628ef5cdd133e1adb5CAS |

de Zelicourt A, Al-Yousif M, Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Molecular Plant Pathology 6, 242–245.

Dekkers LC, Bloemendaal CJ, de Weger LA, Wijffelman CA, Spaink HP, Lugtenberg BJ (1998) A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365. Molecular Plant-Microbe Interactions 11, 45–56.
A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365.CrossRef | 1:CAS:528:DyaK1cXivFChtg%3D%3D&md5=fbadb29ff5a3b4104ba642de4c1b4963CAS |

del Río LA (2015) ROS and RNS in plant physiology: an overview. Journal of Experimental Botany 66, 2827–2837.
ROS and RNS in plant physiology: an overview.CrossRef |

Djavaheri M, Mercado-Blanco J, Versluis C, Meyer JM, van Loon LC, Bakker PAHM (2012) Iron-regulated metabolites produced by Pseudomonas fluorescens WCS374r are not required for eliciting induced systemic resistance against Pseudomonas syringae pv. tomato in Arabidopsis. MicrobiologyOpen 1, 311–325.
Iron-regulated metabolites produced by Pseudomonas fluorescens WCS374r are not required for eliciting induced systemic resistance against Pseudomonas syringae pv. tomato in Arabidopsis.CrossRef | 1:CAS:528:DC%2BC38XhsVeitL%2FP&md5=faec6792d7ee3999678e5728bc88b9bdCAS |

Domenech J, Reddy MS, Kloepper JW, Ramos B, Gutierrez-Mañero J (2006) Combined application of the biological product LS213 with Bacillus, Pseudomonas or Chryseobacterium for growth promotion and biological control of soil-borne diseases in pepper and tomato. BioControl 51, 245–258.
Combined application of the biological product LS213 with Bacillus, Pseudomonas or Chryseobacterium for growth promotion and biological control of soil-borne diseases in pepper and tomato.CrossRef | 1:CAS:528:DC%2BD28XktVeju7k%3D&md5=7513b04af4d69fea72c59722a3ec4ca9CAS |

Dutta S, Podile AR (2010) Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone. Critical Reviews in Microbiology 36, 232–244.
Plant growth promoting rhizobacteria (PGPR): the bugs to debug the root zone.CrossRef |

Erbs G, Newman MA (2012) The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity. Molecular Plant Pathology 13, 95–104.
The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity.CrossRef | 1:CAS:528:DC%2BC38XhtFCgu7g%3D&md5=9dbcef92a89b53125c49dee5623f03abCAS |

Francis NR, Irikura VM, Yamaguchi S, DeRosier DJ, Macnab RM (1992) Localization of the Salmonella typhimurium flagellar switch protein FliG to the cytoplasmic M-ring face of the basal body. Proceedings of the National Academy of Sciences of the United States of America 89, 6304–6308.
Localization of the Salmonella typhimurium flagellar switch protein FliG to the cytoplasmic M-ring face of the basal body.CrossRef | 1:CAS:528:DyaK38Xlt1Oqs78%3D&md5=e05ea7b6926f167b5a0fa02eeefdf3f1CAS |

Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martinez-Romero E (2011) Microbially mediated plant functional traits. Annual Review of Ecology Evolution and Systematics 42, 23–46.
Microbially mediated plant functional traits.CrossRef |

García-Limones C, Hervás A, Navas-Cortés JA, Jiménez-Díaz RM, Tena M (2002) Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceris. Physiological and Molecular Plant Pathology 61, 325–337.
Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceris.CrossRef |

Genin S, Boucher CA (1994) A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain. Molecular & General Genetics 243, 112–118.
A superfamily of proteins involved in different secretion pathways in gram-negative bacteria: modular structure and specificity of the N-terminal domain.CrossRef | 1:CAS:528:DyaK2cXkt12msrk%3D&md5=83ec99614bbb0232d5d317ffc96d7f2fCAS |

Goldberg M, Pribyl T, Juhnke S, Nies DH (1999) Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family. The Journal of Biological Chemistry 274, 26065–26070.
Energetics and topology of CzcA, a cation/proton antiporter of the resistance-nodulation-cell division protein family.CrossRef | 1:CAS:528:DyaK1MXmtVKmt7Y%3D&md5=549fa0aebfa4ba2668f147340bddb63fCAS |

Gupta G, Parihar SS, Ahirwar NK, Snehi SK, Singh V (2015) Plant growth promoting rhizobacteria (PGPR): current and future prospects for development of sustainable agriculture. Journal of Microbial & Biochemical Technology 7, 96–102.

Gutiérrez Mañero FJ, Ramos-Solano B, Probanza A, Mehouachi J, Tadeo FR, Talon M (2001) The plant‐growth‐promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiologia Plantarum 111, 206–211.
The plant‐growth‐promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins.CrossRef |

Gutiérrez Mañero F, Probanza A, Ramos B, Colon Flores J, Lucas Garcia JA (2003) Effects of culture filtrates of rhizobacteria isolated from wild lupine on germination, growth, and biological nitrogen fixation of lupine seedlings. Journal of Plant Nutrition 26, 1101–1115.
Effects of culture filtrates of rhizobacteria isolated from wild lupine on germination, growth, and biological nitrogen fixation of lupine seedlings.CrossRef |

Han HS, Lee KD (2005) Plant growth-promoting rhizobacteria: effect on antioxidant status, photo- synthesis, mineral uptake and growth of lettuce under soil salinity. Research Journal of Agriculture and Biological Sciences 1, 210–215.

Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology 60, 579–598.
Soil beneficial bacteria and their role in plant growth promotion: a review.CrossRef |

Hirt H (2009) ‘Plant stress biology: from genomics to systems biology.’ (Wiley-Blackwell: Hoboken, NJ, USA)

Hoben HJ, Somasegran P (1982) Comparison of the pour spread and drop plate methods for enumeration of Rhizobium ssp. in inoculants made from pre-sterilized peat. Applied and Environmental Microbiology 44, 1246–1247.

Hong CY, Chao YY, Yang MY, Cheng SY, Cho SC (2009) NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid. Plant and Soil 320, 103–115.
NaCl-induced expression of glutathione reductase in roots of rice (Oryza sativa L.) seedlings is mediated through hydrogen peroxide but not abscisic acid.CrossRef | 1:CAS:528:DC%2BD1MXmvFGjtrc%3D&md5=57bc9b47a702dbe39ea01b11992be57fCAS |

Hu Z, Fan J, Chen K, Amombo E, Chen L, Fu J (2016) Effects of ethylene on photosystem II and antioxidant enzyme activity in Bermuda grass under low temperature. Photosynthesis Research 128, 59–72.
Effects of ethylene on photosystem II and antioxidant enzyme activity in Bermuda grass under low temperature.CrossRef | 1:CAS:528:DC%2BC2MXhslWhsbzE&md5=fc1067ac80ea267f242a6434b2de2bbeCAS |

Irikura VM, Kihara M, Yamaguchi S, Sockett H, Macnab RM (1993) Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor. Journal of Bacteriology 175, 802–810.
Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor.CrossRef | 1:CAS:528:DyaK3sXht1Smu74%3D&md5=3da285d937657449725a8c3a28fcba4aCAS |

Ito M, Kim YG, Tsuji H, Kiwaki M, Nomoto K, Tanaka R, Okada N, Danbara H (2010) A practical random mutagenesis system for probiotic Lactobacillus casei using Tn5 transposition complexes. Journal of Applied Microbiology 109, 657–666.

Kazmierczak BI, Mielke DL, Russel M, Model P (1994) pIV, a filamentous phage protein that mediates phage export across the bacterial cell envelope, forms a multimer. Journal of Molecular Biology 238, 187–198.
pIV, a filamentous phage protein that mediates phage export across the bacterial cell envelope, forms a multimer.CrossRef | 1:CAS:528:DyaK2cXktVCltbc%3D&md5=aacb002b97fe97e819c8c51746ba2ad4CAS |

Kihara M, Miller GU, Macnab RM (2000) Deletion analysis of the flagellar switch protein FliG of Salmonella. Journal of Bacteriology 182, 3022–3028.
Deletion analysis of the flagellar switch protein FliG of Salmonella.CrossRef | 1:CAS:528:DC%2BD3cXjsVylsbY%3D&md5=3e4f0fe8acbfd7abab4f2f9b3542303bCAS |

Kim SY, Lim JH, Park MR, Kim YJ, Park T, Seo YW, Choi KG, Yun SJ (2005) Enhanced antioxidant enzymes are associated with reduced hydrogen peroxide in barley roots under saline stress. Journal of Biochemistry and Molecular Biology 38, 218–224.

Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environmental and Experimental Botany 65, 245–252.
Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress.CrossRef | 1:CAS:528:DC%2BD1MXhtlKqtro%3D&md5=7069ddbd77a80221e533c55dcadf34aeCAS |

Korotkov KV, Sandkvist M, Hol WGJ (2012) The type II secretion system: biogenesis, molecular architecture and mechanism. Nature Reviews. Microbiology 10, 336–351.

Linderoth NA, Model P, Russel M (1996) Essential role of a sodium dodecyl sulfate-resistant protein IV multimer in assembly-export of filamentous phage. Journal of Bacteriology 178, 1962–1970.
Essential role of a sodium dodecyl sulfate-resistant protein IV multimer in assembly-export of filamentous phage.CrossRef | 1:CAS:528:DyaK28XhvFOksbY%3D&md5=6f6ad9f606a27a011b695e952ba5558fCAS |

Llamas I, Argandoña M, Quesada E, del Moral A (2000) Transposon mutagenesis in Halomonas eurihalina. Research in Microbiology 151, 13–18.
Transposon mutagenesis in Halomonas eurihalina.CrossRef | 1:CAS:528:DC%2BD3cXivVOnt70%3D&md5=f3aefc07e9fec73af2df21fb4bb7cc2cCAS |

Lloyd SA, Tang H, Wang X, Billings S, Blair DF (1996) Torque generation in the flagellar motor of Escherichia coli: evidence of a direct role for FliG but not FliM or FliN. Journal of Bacteriology 178, 223–231.
Torque generation in the flagellar motor of Escherichia coli: evidence of a direct role for FliG but not FliM or FliN.CrossRef | 1:CAS:528:DyaK28XhvFOktQ%3D%3D&md5=7e646cbd126b9bcd95c77388f1612c73CAS |

Lucas JA, Ramos Solano B, Montes F, Ojeda J, Megias M, Gutierrez Maņero FJ (2009) Use of two PGPR strains in the integrated management of blast disease in rice (Oryza sativa) in Southern Spain. Field Crops Research 114, 404–410.
Use of two PGPR strains in the integrated management of blast disease in rice (Oryza sativa) in Southern Spain.CrossRef |

Lucas García JA, Schloter M, Durkaya T, Hartmann A, Gutiérrez Mañero FJ (2003) Colonization of pepper roots by a plant growth promoting Pseudomonas fluorescens strain. Biology and Fertility of Soils 37, 381–385.

Lucas García JA, Domenech J, Santamaría C, Camacho M, Daza A, Gutierrez-Mañero FJ (2004) Growth of forest plants (pine and holm oak) inoculated with rhizobacteria: relationship with microbial community structure and biological activity of its rhizosphere. Environmental and Experimental Botany 52, 239–251.
Growth of forest plants (pine and holm oak) inoculated with rhizobacteria: relationship with microbial community structure and biological activity of its rhizosphere.CrossRef |

Lucas García JA, Probanza A, Ramos B, Colón Flores J, Gutiérrez Mañero FJ (2004b) Effects of plant growth promoting rhizobacteria (PGPRs) on the biological nitrogen fixation, nodulation, and growth of Lupinus albus l. cv. Multolupa. Engineering in Life Sciences 4, 71–77.
Effects of plant growth promoting rhizobacteria (PGPRs) on the biological nitrogen fixation, nodulation, and growth of Lupinus albus l. cv. Multolupa.CrossRef |

Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annual Review of Microbiology 63, 541–556.
Plant-growth-promoting rhizobacteria.CrossRef | 1:CAS:528:DC%2BD1MXhtlSitLnN&md5=291e46c31375c0285813c84fcdd35d91CAS |

Maldonado-González MM, Bakker PAHM, Prieto P, Mercado-Blanco J (2015) Arabidopsis thaliana as a tool to identify traits involved in Verticillium dahliae biocontrol by the olive root endophyte Pseudomonas fluorescens PICF7. Frontiers in Microbiology 6, 266
Arabidopsis thaliana as a tool to identify traits involved in Verticillium dahliae biocontrol by the olive root endophyte Pseudomonas fluorescens PICF7.CrossRef |

Moraleda-Muñoz A, Pérez J, Extremera AL, Muñoz-Dorado J (2010) Differential regulation of six heavy metal efflux systems in the response of Myxococcus xanthus to copper. Applied and Environmental Microbiology 76, 6069–6076.
Differential regulation of six heavy metal efflux systems in the response of Myxococcus xanthus to copper.CrossRef |

Pal KK, Tilak KV, Saxena AK, Dey R, Singh CS (2001) Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria. Microbiological Research 156, 209–223.
Suppression of maize root diseases caused by Macrophomina phaseolina, Fusarium moniliforme and Fusarium graminearum by plant growth promoting rhizobacteria.CrossRef | 1:STN:280:DC%2BD3MnmvFelsA%3D%3D&md5=17edd62151d90aea4cbf62d41861512aCAS |

Paul K, Brunstetter D, Titen S, Blair DF (2011) A molecular mechanism of direction switching in the flagellar motor of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 108, 17171–17176.
A molecular mechanism of direction switching in the flagellar motor of Escherichia coli.CrossRef | 1:CAS:528:DC%2BC3MXhtlCrurrJ&md5=ebd40ddecce9d54d29e6141012fddc00CAS |

Penrose D, Glick B (2003) Methods for isolating and characterizing ACC deaminase‐containing plant growth‐promoting rhizobacteria. Physiologia Plantarum 118, 10–15.
Methods for isolating and characterizing ACC deaminase‐containing plant growth‐promoting rhizobacteria.CrossRef | 1:CAS:528:DC%2BD3sXjs1egsr8%3D&md5=14490284f7ab085a587cf967ceea21f1CAS |

Ramos Solano B, Barriuso Maicas J, Pereyra De La Iglesia M, Domenech J, Gutiérrez Mañero FJ (2008) Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection, and biotic elicitors. Phytopathology 98, 451–457.
Systemic disease protection elicited by plant growth promoting rhizobacteria strains: relationship between metabolic responses, systemic disease protection, and biotic elicitors.CrossRef | 1:STN:280:DC%2BD1cjlslKntQ%3D%3D&md5=d7632a00ad7432d876eb3e30a5f950f1CAS |

Ramos-Solano B, Lucas García JA, Garcia-Villaraco A, Algar E, Garcia-Cristobal J, Gutierrez Mañero FJ (2010b) Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum lycopersicum L. Plant and Soil 334, 189–197.
Siderophore and chitinase producing isolates from the rhizosphere of Nicotiana glauca Graham enhance growth and induce systemic resistance in Solanum lycopersicum L.CrossRef | 1:CAS:528:DC%2BC3cXhtVaqtbfO&md5=261ffd583560666d5616cfa55f2e5516CAS |

Richardson AE, Barea JM, Mcneill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by micro-organisms. Plant and Soil 321, 305–339.
Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by micro-organisms.CrossRef | 1:CAS:528:DC%2BD1MXos1enu7w%3D&md5=d8ee18a8235e10e157ad41d89156770eCAS |

Saleem M, Arshad M, Hussain S, Bhatti AS (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. Journal of Industrial Microbiology & Biotechnology 34, 635–648.
Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture.CrossRef | 1:CAS:528:DC%2BD2sXhtVajsL%2FJ&md5=4c0f809f1506fdcbe3746a90ffb0b4e1CAS |

Sambrook J, Russel DW (2001) ‘Molecular Cloning: A Laboratory Manual. 3rd Edition.’ (Cold Spring Harbor Laboratory Press: New York)

Sandkvist M (2001) Type II secretion and pathogenesis. Infection and Immunity 69, 3523–3535.
Type II secretion and pathogenesis.CrossRef | 1:STN:280:DC%2BD3MzntFejtg%3D%3D&md5=6c0c8a854d0b43bbe661e28b98729c2fCAS |

Sandkvist MM, Hough LPL, Bagdasarian MMM, Bagdasarian MM (1999) Direct interaction of the EpsL and EpsM proteins of the general secretion apparatus in Vibrio cholerae. Journal of Bacteriology 181, 3129–3135.

Silver S, Phung LT (2005) A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. Journal of Industrial Microbiology & Biotechnology 32, 587–605.
A bacterial view of the periodic table: genes and proteins for toxic inorganic ions.CrossRef | 1:CAS:528:DC%2BD2MXht1Oks7vO&md5=5926aada5b89a5e9bc91644ad4ff6327CAS |

Singh JS, Pandey VC, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustain- able agriculture and environmental development. Agriculture, Ecosystems & Environment 140, 339–353.
Efficient soil microorganisms: a new dimension for sustain- able agriculture and environmental development.CrossRef |

Sokal RR, Rohlf FJ (1980) ‘Introducción a la bioestadística.’ (SA Reverté: Barcelona, Spain)

Štajner D, Gasaić O, Matković B, Varga SZI (1995) Metolachlor effect on antioxidants enzyme activities and pigments content in seeds and young leaves of wheat (Triticum aestivum L.). Agricoltura Mediterranea 125, 267–273.

Štajner D, Kevrešan S, Gašić O, Mimica-Dukić N, Zongli H (1997) Nitrogen and Azotobacter chroococcum engance oxidative stress tolerance in sugar beet. Biologia Plantarum 39, 441–445.
Nitrogen and Azotobacter chroococcum engance oxidative stress tolerance in sugar beet.CrossRef |

TerBraak CFJ, Šmilauer P (1998) ‘CANOCO reference manual and user’s guide to Canoco for Windows. Software for canonical community ordination (ver. 4)’. (Centre for Biometry: Wageningen, Germany)

Tsai YC, Hong CY, Liu LF, Kao CH (2004) Relative importance of Na+ and Cl in NaCl-induced antioxidant systems in roots of rice seedlings. Physiologia Plantarum 122, 86–94.
Relative importance of Na+ and Cl in NaCl-induced antioxidant systems in roots of rice seedlings.CrossRef | 1:CAS:528:DC%2BD2cXnvFeht7k%3D&md5=058d6f04fee84bbd789d34854a44dad4CAS |

van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J (2006) Costs and benefits of priming for defense in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 5602–5607.
Costs and benefits of priming for defense in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD28XjslejsLY%3D&md5=94b73e657feabca25710b488d6fbfbe3CAS |

van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annual Review of Phytopathology 36, 453–483.
Systemic resistance induced by rhizosphere bacteria.CrossRef | 1:CAS:528:DyaK1cXmtlaltLo%3D&md5=8684a7825a72b83001ff3fd227473520CAS |

Větrovský T, Baldrian P (2013) The variability of the 16S rRNA gene in bacterial genomes and Its consequences for bacterial community analyses. PLoS One 8, e57923
The variability of the 16S rRNA gene in bacterial genomes and Its consequences for bacterial community analyses.CrossRef |

Washio K, Lim SP, Roongsawang N, Morikawa M (2010) Identification and characterization of the genes responsible for the production of the cyclic lipopeptide arthrofactin by Pseudomonas sp. MIS38. Bioscience, Biotechnology, and Biochemistry 74, 992–999.
Identification and characterization of the genes responsible for the production of the cyclic lipopeptide arthrofactin by Pseudomonas sp. MIS38.CrossRef | 1:CAS:528:DC%2BC3cXnt1GmsL4%3D&md5=204c837205bfb9c37cee2715b32064cfCAS |

Wiesel L, Newton AC, Elliott I, Booty D, Gilroy EM, Birch PRJ, Hein I (2014) Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Frontiers in Plant Science 5, 655
Molecular effects of resistance elicitors from biological origin and their potential for crop protection.CrossRef |

Xu C, Natarajan S, Sullivan JH (2008) Impact of solar ultraviolet-B radiation on the antioxidant defense system in soybean lines differing in flavonoid contents. Environmental and Experimental Botany 63, 39–48.
Impact of solar ultraviolet-B radiation on the antioxidant defense system in soybean lines differing in flavonoid contents.CrossRef | 1:CAS:528:DC%2BD1cXivVeju74%3D&md5=45c75104b11a3359041bcd4f25f332ccCAS |

Yan Q, Wang N (2011) The ColR/ColS two-component system plays multiple roles in the pathogenicity of the citrus canker pathogen Xanthomonas citri subsp. citri. Journal of Bacteriology 193, 1590–1599.
The ColR/ColS two-component system plays multiple roles in the pathogenicity of the citrus canker pathogen Xanthomonas citri subsp. citri.CrossRef | 1:CAS:528:DC%2BC3MXotVyrtLw%3D&md5=444bcb81d6c04a8cfda01cd668e7fb1dCAS |

Zhang S, Reddy M, Kloepper J (2004) Tobacco growth enhancement and blue mold disease protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166. Plant and Soil 262, 277–288.
Tobacco growth enhancement and blue mold disease protection by rhizobacteria: relationship between plant growth promotion and systemic disease protection by PGPR strain 90-166.CrossRef | 1:CAS:528:DC%2BD2cXmtlGgu7Y%3D&md5=fdd56422fecf493cc9df02efa3352b5cCAS |



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