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

Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress

Josiane Fukami A B , Clara de la Osa C , Francisco Javier Ollero D , Manuel Megías D and Mariangela Hungria A B E
+ Author Affiliations
- Author Affiliations

A Embrapa Soja, CP 231, 86001-970, Londrina, Paraná, Brazil.

B Universidade Estadual de Londrina, Dept. Biochemistry and Biotechnology, CP 60001, 86051-990, Londrina, Paraná, Brazil.

C Universidad de Sevilla, Facultad de Biología, Dept. de Fisiología Vegetal, CP 41012 Sevilla, Spain.

D Universidad de Sevilla, Facultad de Biología, Dept. de Microbiología, CP 41012 Sevilla, Spain.

E Corresponding author. Emails: mariangela.hungria@embrapa.br; biotecnologia.solo@hotmail.com; hungria@pq.cnpq.br

Functional Plant Biology - https://doi.org/10.1071/FP17167
Submitted: 11 June 2017  Accepted: 9 September 2017   Published online: 10 October 2017

Abstract

Plants are highly affected by salinity, but some plant growth-promoting bacteria (PGPB) may trigger induced systemic tolerance (IST), conferring protection against abiotic stresses. We investigated plant mechanisms under saline stress (170 mM NaCl) when maize was singly or co-inoculated with Azospirillum brasilense strains Ab-V5 and Ab-V6 and Rhizobium tropici strain CIAT 899. Under greenhouse conditions, plants responded positively to inoculation and co-inoculation, but with differences between strains. Inoculation affected antioxidant enzymes that detoxify reactive oxygen species (ROS) – ascorbate peroxidase (APX), catalase (CAT) and superoxide dismutase (SOD) – mainly in leaves. Proline contents in leaves and roots and malondialdehyde (MDA) in leaves – plant-stress-marker molecules – were significantly reduced due to the inoculation, indicating reduced need for the synthesis of these molecules. Significant differences were attributed to inoculation in the expression of genes related to antioxidant activity, in general with upregulation of APX1, CAT1, SOD2 and SOD4 in leaves, and APX2 in roots. Pathogenesis-related genes PR1, prp2, prp4 and heat-shock protein hsp70 were downregulated in leaves and roots, indicating that inoculation with PGPB might reduce the need for this protection. Together the results indicate that inoculation with PGPB might provide protection from the negative effects of saline stress. However, differences were observed between strains, as A. brasilense Ab-V5 did not show salt tolerance, while the best inoculation treatments to mitigate saline stress were with Ab-V6 and co-inoculation with Ab-V6+CIAT 899. Inoculation with these strains may represent an effective strategy to mitigate salinity stress.

Additional keywords: abiotic stress, Azospirillum spp., oxidative stress, PGPB, Rhizobium spp., salinity stress, Zea mays.


References

Ahmed N (2010) Physiological and molecular basis of AzospirillumArabidopsis interaction. PhD thesis, Universität Würzburg, Würzburg, Germany.

Ardakani MR, Mazaheri D, Mafakheri S, Moghaddam A (2011) Absorption efficiency of N, P, K through triple inoculation of wheat (Triticum aestivum L.) by Azospirillum brasilense, Streptomyces sp., Glomus intraradices and manure application. Physiology and Molecular Biology of Plants 17, 181–192.
Absorption efficiency of N, P, K through triple inoculation of wheat (Triticum aestivum L.) by Azospirillum brasilense, Streptomyces sp., Glomus intraradices and manure application.CrossRef |

Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601–639.
The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons.CrossRef | 1:CAS:528:DyaK1MXkt1yktr0%3D&md5=0a882839acf99e081c96a6c5c55c9ef4CAS |

Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Reviews in Plant Science 24, 23–58.
Drought and salt tolerance in plants.CrossRef | 1:CAS:528:DC%2BD2MXis12ns7c%3D&md5=130d8916f5b86c6c0ea306578cbbb7b8CAS |

Bashan Y, de-Bashan LE (2010) How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment. Advances in Agronomy 108, 77–136.
How the plant growth-promoting bacterium Azospirillum promotes plant growth – a critical assessment.CrossRef | 1:CAS:528:DC%2BC3cXhsFKgurrI&md5=1e06c4d8d7b2bd7778e47bd462701ceaCAS |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205–207.
Rapid determination of free proline for water-stress studies.CrossRef | 1:CAS:528:DyaE3sXlsVGitLk%3D&md5=7defff6fc79bf274d695d8ed5adb8abcCAS |

Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276–287.
Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.CrossRef | 1:CAS:528:DyaE38XjtFKhsg%3D%3D&md5=41a81f7134ea2a9b8a235b3333eaa8b0CAS |

Beers RF, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. The Journal of Biological Chemistry 195, 133–140.

Beringer JE (1974) R factor transfer in Rhizobium leguminosarum. Journal of General Microbiology 84, 188–198.

Bian S, Jiang Y (2009) Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery. Scientia Horticulturae 120, 264–270.
Reactive oxygen species, antioxidant enzyme activities and gene expression patterns in leaves and roots of Kentucky bluegrass in response to drought stress and recovery.CrossRef | 1:CAS:528:DC%2BD1MXisFKjtrs%3D&md5=876c3886e8bc6adb57889d5d01786db4CAS |

Bor M, Ozdermir F, Turkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Science 164, 77–84.
The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L.CrossRef | 1:CAS:528:DC%2BD38XovFertrw%3D&md5=eca15f72a98f3a8595629d8a647f7403CAS |

Bottini R, Fulchieri M, Pearce D, Pharis RP (1989) Identification of gibberellins A1, A3, and iso-A3 in cultures of Azospirillum lipoferum. Plant Physiology 90, 45–47.
Identification of gibberellins A1, A3, and iso-A3 in cultures of Azospirillum lipoferum.CrossRef | 1:CAS:528:DyaL1MXltlSgtL4%3D&md5=a42f21632d621f1c16e8599b7134f952CAS |

Bowler C, Van Montagu M, Inzé D (1992) Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43, 83–116.
Superoxide dismutase and stress tolerance.CrossRef | 1:CAS:528:DyaK38XltVyjsb0%3D&md5=1919387dd4e37383ba9a9f76bbf6c308CAS |

Bradford M (1976) A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation microgram quantities of protein utilizing the principle of protein-dye binding.CrossRef | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2821bcfbf01a16b0f1b14eb3a73c5812CAS |

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 |

Cassán F, Vanderleyden J, Spaepen S (2014) Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum. Journal of Plant Growth Regulation 33, 440–459.
Physiological and agronomical aspects of phytohormone production by model plant-growth-promoting rhizobacteria (PGPR) belonging to the genus Azospirillum.CrossRef |

Cerezini P, Kuwano B, Santos M, Terassi F, Hungria M, Nogueira MA (2016) Strategies to promote early nodulation in soybean under drought. Field Crops Research 196, 160–167.
Strategies to promote early nodulation in soybean under drought.CrossRef |

Chen CT, Chen LM, Lin CC, Kao CH (2001) Regulation of proline accumulation in detached rice leaves exposed to excess copper. Plant Science 160, 283–290.
Regulation of proline accumulation in detached rice leaves exposed to excess copper.CrossRef | 1:CAS:528:DC%2BD3MXnsVektQ%3D%3D&md5=a50d5d03d8e1d63ade92052e75fe0d3dCAS |

Cordovilla M del P, Berrido SI, Ligero F, Lluch C (1999) Rhizobium strain effects on the growth and nitrogen assimilation in Pisum sativum and Vicia faba plant growth under salt stress. Journal of Plant Physiology 154, 127–131.
Rhizobium strain effects on the growth and nitrogen assimilation in Pisum sativum and Vicia faba plant growth under salt stress.CrossRef |

Dardanelli MS, Fernández de Córdoba FJ, Espuny MR, Carvajal MAR, Díaz MES, Serrano AMG, Okon Y, Megías M (2008) Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress. Soil Biology & Biochemistry 40, 2713–2721.
Effect of Azospirillum brasilense coinoculated with Rhizobium on Phaseolus vulgaris flavonoids and Nod factor production under salt stress.CrossRef | 1:CAS:528:DC%2BD1cXht1KnsrjL&md5=d37b1276f6a43d2aec1480d935d1cac4CAS |

de Souza JEB, Ferreira EPB (2017) Improving sustainability of common bean production systems by co-inoculating rhizobia and azospirilla. Agriculture, Ecosystems & Environment 237, 250–257.
Improving sustainability of common bean production systems by co-inoculating rhizobia and azospirilla.CrossRef |

Dwivedi SL, Sahrawat KL, Upadhyaya HD, Mengoni A, Galardini M, Bazzicalupo M, Biondi EG, Hungria M, Kaschuk G, Blair MW, Ortiz R (2015) Advances in host plant and Rhizobium genomics to enhance symbiotic nitrogen fixation in grain legumes. In ‘Advances in agronomy’. (Ed. DL Sparks) pp. 1–116. (Academic Press: Cambridge, MA, USA)

Fahraeus G (1957) The infection of clover root hairs by nodule bacteria studied by a simple glass slide technique. Journal of General Microbiology 16, 374–381.

Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiologia Plantarum 119, 355–364.
Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria.CrossRef | 1:CAS:528:DC%2BD3sXoslekt74%3D&md5=73fe336574e0f414e295e500a7a40306CAS |

García-Fraile P, Carro L, Robledo M, Ramírez-Bahena M-H, Flores-Félix J-D, Fernández MT, Mateos PF, Rivas R, Igual JM, Martínez-Molina E, Álvaro Peix A, Velázquez E (2012) Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One 7, e38122
Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans.CrossRef |

Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry 48, 909–930.
Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.CrossRef | 1:CAS:528:DC%2BC3cXhtlKnu7fF&md5=7ab4ec21ad4002e48078e2efd99cff90CAS |

Gomes DF, Ormeno-Orrillo E, Hungria M (2015) Biodiversity, symbiotic efficiency and genomics of Rhizobium tropici and related species. In ‘Biological nitrogen fixation’. (Ed. FJ de Bruijn) pp. 747–756. (John Wiley & Sons Inc., Hoboken, NJ, USA)

Goswami D, Thakker JN, Dhandhukia PC, Tejada Moral M (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food & Agriculture 2, 1127500
Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review.CrossRef |

Hamdia MAES, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regulation 44, 165–174.
Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions.CrossRef | 1:CAS:528:DC%2BD2cXhtFWqsb%2FP&md5=840e9230d577ff26ac194c51d425226fCAS |

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

Hodges DM, De Long JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604–611.
Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds.CrossRef | 1:CAS:528:DyaK1MXhslKisLw%3D&md5=19c2c9677886e16fb031144ada6dc4d9CAS |

Hossain MA, Asada K (1984) Inactivation of ascorbate peroxidase in spinach chloroplasts on dark addition of hydrogen peroxide: its protection by ascorbate. Plant & Cell Physiology 25, 1285–1295.

Hungria M (2011) Inoculação com Azospirillum brasilense: inovação em rendimento a baixo custo. Circular Técnica 325, Embrapa Soja.

Hungria M, Campo RJ, Souza EM, Pedrosa FO (2010) Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil. Plant and Soil 331, 413–425.
Inoculation with selected strains of Azospirillum brasilense and A. lipoferum improves yields of maize and wheat in Brazil.CrossRef | 1:CAS:528:DC%2BC3cXlvVOhs78%3D&md5=ca483a2a68f4e023f53f70d513a0afd2CAS |

Hungria M, Nogueira MA, Araujo RS (2013) Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability. Biology and Fertility of Soils 49, 791–801.
Co-inoculation of soybeans and common beans with rhizobia and azospirilla: strategies to improve sustainability.CrossRef |

Hungria M, Nogueira MA, Araujo RS (2015) Soybean seed co-inoculation with Bradyrhizobium spp. and Azospirillum brasilense: a new biotechnological tool to improve yield and sustainability. American Journal of Plant Sciences 6, 811–817.
Soybean seed co-inoculation with Bradyrhizobium spp. and Azospirillum brasilense: a new biotechnological tool to improve yield and sustainability.CrossRef | 1:CAS:528:DC%2BC2MXntlKhtb0%3D&md5=04b0c2957d51fa024c82aec1ef63cd7eCAS |

Jiang L, Chen Z, Gao Q, Ci L, Cao S, Han Y, Wang W (2016) Loss-of-function mutations in the APX1 gene result in enhanced selenium tolerance in Arabidopsis thaliana. Plant, Cell & Environment 39, 2133–2144.
Loss-of-function mutations in the APX1 gene result in enhanced selenium tolerance in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BC28XhsVCqtrjF&md5=c04597b9e38a58979184504edeabd5c0CAS |

Jung S, Kernodle SP, Scandalios JG (2001) Differential antioxidant responses to norflurazon-induced oxidative stress in maize. Redox Report 6, 311–317.
Differential antioxidant responses to norflurazon-induced oxidative stress in maize.CrossRef | 1:CAS:528:DC%2BD38XlvFyruw%3D%3D&md5=a2bf5e28fa7489922189f3b3b7faccd0CAS |

Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284, 654–657.
Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis.CrossRef | 1:CAS:528:DyaK1MXislyrtbc%3D&md5=9cc4f0c3ebb710ba0a3cb068a0afafbfCAS |

Kaschuk G, Hungria M, Leffelaar PA, Giller KE, Kuyper TW (2010) Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max (L.) Merrill) dependent on N2 fixation or nitrate supply. Plant Biology 12, 60–69.
Differences in photosynthetic behaviour and leaf senescence of soybean (Glycine max (L.) Merrill) dependent on N2 fixation or nitrate supply.CrossRef | 1:CAS:528:DC%2BC3cXlslWqtrY%3D&md5=ceae429df90d992db869c23bb683d562CAS |

Kauffmann S, Legrand M, Geoffroy P, Fritig B (1987) Biological function of “pathogenesis-related” proteins: four PR proteins of tobacco have 1,3-β-glucanase activity. EMBO Journal 6, 3209–3212.

Kaushal M, Wani SP (2016) Rhizobacterial–plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agriculture, Ecosystems & Environment 231, 68–78.
Rhizobacterial–plant interactions: strategies ensuring plant growth promotion under drought and salinity stress.CrossRef | 1:CAS:528:DC%2BC28XhtFWhtrnJ&md5=ff2168af11be15d18506430d5f859af7CAS |

Khalid M, Bilal M, Hassani D, Iqbal HMN, Wang H, Huang D (2017) Mitigation of salt stress in white clover (Trifolium repens) by Azospirillum brasilense and its inoculation effect. Botanical Studies (Taipei, Taiwan) 58, 5
Mitigation of salt stress in white clover (Trifolium repens) by Azospirillum brasilense and its inoculation effect.CrossRef |

Kim K, Jang YJ, Lee SM, Oh BT, Chae JC, Lee KJ (2014) Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by up-regulation of conserved salinity responsive factors in plants. Molecules and Cells 37, 109–117.
Alleviation of salt stress by Enterobacter sp. EJ01 in tomato and Arabidopsis is accompanied by up-regulation of conserved salinity responsive factors in plants.CrossRef |

Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275.
The oxidative burst in plant disease resistance.CrossRef | 1:CAS:528:DyaK2sXjs1entr8%3D&md5=25b67f82b8c4a3f7f3c94e2223505bf4CAS |

Lim JH, Kim SD (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. The Plant Pathology Journal 29, 201–208.
Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper.CrossRef |

Maheshwari DK (Ed.) (2012) ‘Bacteria in agrobiology: stress management.’ (Springer: Berlin, Heidelberg)

Manoli A, Sturaro A, Trevisan S, Quaggiotti S, Nonis A (2012) Evaluation of candidate reference genes for qPCR in maize. Journal of Plant Physiology 169, 807–815.
Evaluation of candidate reference genes for qPCR in maize.CrossRef | 1:CAS:528:DC%2BC38XkslaqtLs%3D&md5=80f4f9571da7be2599f772222f6d1ff3CAS |

Marques ACR, de Oliveira LB, Nicoloso FT, Jacques JS, Giacomini SJ, Quadros FLF (2017) Biological nitrogen fixation in C4 grasses of different growth strategies of South America natural grasslands. Applied Soil Ecology 113, 54–62.
Biological nitrogen fixation in C4 grasses of different growth strategies of South America natural grasslands.CrossRef |

Matsumura EE, Secco VA, Moreira RS, Santos OJP, Hungria M, Oliveira ALM (2015) Composition and activity of endophytic bacterial communities in field-grown maize plants inoculated with Azospirillum brasilense. Annals of Microbiology 65, 2187–2200.
Composition and activity of endophytic bacterial communities in field-grown maize plants inoculated with Azospirillum brasilense.CrossRef | 1:CAS:528:DC%2BC2MXhvVKmsLbL&md5=d974c3308d2e639eb8b53808053c8977CAS |

Medici LO, Azevedo RA, Smith RJ, Lea PJ (2004) The influence of nitrogen supply on antioxidant enzymes in plant roots. Functional Plant Biology 31, 1–9.
The influence of nitrogen supply on antioxidant enzymes in plant roots.CrossRef | 1:CAS:528:DC%2BD2cXmvVGgtQ%3D%3D&md5=de83adce72226f7928661bc3d0e351c7CAS |

Molazem D, Bashirzadeh A (2015) Impact of salinity stress on proline reaction, peroxide activity, and antioxidant enzymes in maize (Zea mays L.). Polish Journal of Environmental Studies 24, 597–603.
Impact of salinity stress on proline reaction, peroxide activity, and antioxidant enzymes in maize (Zea mays L.).CrossRef | 1:CAS:528:DC%2BC2MXhtVKiur%2FI&md5=b7ebd82e3ac87959b0799361ed40805dCAS |

Morris SW, Vernooij B, Titatarn S, Starrett M, Thomas S, Wiltse CC, Frederiksen RA, Bhandhufalck A, Hulbert S, Uknes S (1998) Induced resistance responses in maize. Molecular Plant-Microbe Interactions 11, 643–658.
Induced resistance responses in maize.CrossRef | 1:CAS:528:DyaK1cXktFCjurs%3D&md5=18ba44c0060f5849572477e6518ab2cbCAS |

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Biology 59, 651–681.
Mechanisms of salinity tolerance.CrossRef | 1:CAS:528:DC%2BD1cXntFaqtrw%3D&md5=b30f07d810b3303a6dcacfac2b459d6cCAS |

Nasser W, de Tapia M, Kauffmann S, Montasser-Kouhsari S, Burkard G (1988) Identification and characterization of maize pathogenesis-related proteins. Four maize PR proteins are chitinases. Plant Molecular Biology 11, 529–538.
Identification and characterization of maize pathogenesis-related proteins. Four maize PR proteins are chitinases.CrossRef | 1:CAS:528:DyaL1MXkvVCk&md5=0013b24da067352bea0b99740894f818CAS |

Ormeño-Orrillo E, Menna P, Almeida LGP, Ollero FJ, Nicolás MF, Rodrigues EP, Nakatami AS, Batista JSS, Chueire LMO, Souza RC, Vasconcelos ATR, Megías M, Hungria M, Martínez-Romero E (2012) Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 which are used in inoculants for common bean (Phaseolus vulgaris L.). BMC Genomics 13, 735
Genomic basis of broad host range and environmental adaptability of Rhizobium tropici CIAT 899 and Rhizobium sp. PRF 81 which are used in inoculants for common bean (Phaseolus vulgaris L.).CrossRef |

Pereg L, de-Bashan LE, Bashan Y (2016) Assessment of affinity and specificity of Azospirillum for plants. Plant and Soil 399, 389–414.
Assessment of affinity and specificity of Azospirillum for plants.CrossRef | 1:CAS:528:DC%2BC28Xps12l&md5=d1cca825cd09cf1f3af8042fcac21ab6CAS |

Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Research 30, e36
Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR.CrossRef |

Rodrigues Neto J, Malavolta Jr VA, Victor O (1986) Meio simples para o isolamento e cultivo de Xanthomonas campestris pv. citri tipo B. Summa Phytopathologica 12, 32

Rodriguez H, Gonzalez T, Goire I, Bashan Y (2004) Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp. Naturwissenschaften 91, 552–555.
Gluconic acid production and phosphate solubilization by the plant growth-promoting bacterium Azospirillum spp.CrossRef | 1:CAS:528:DC%2BD2cXpsFaht7w%3D&md5=116318b51ab61341cd86aa4456bd1621CAS |

Sahoo RK, Ansari MW, Pradhan M, Dangar TK, Mohanty S, Tuteja N (2014) Phenotypic and molecular characterization of native Azospirillum strains from rice fields to improve crop productivity. Protoplasma 251, 943–953.
Phenotypic and molecular characterization of native Azospirillum strains from rice fields to improve crop productivity.CrossRef | 1:CAS:528:DC%2BC2cXhtVagsbjO&md5=584d4627c07ba909bab5345775eac466CAS |

Sarma RK, Saikia R (2014) Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant and Soil 377, 111–126.
Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21.CrossRef | 1:CAS:528:DC%2BC3sXhvFeksrzM&md5=d3f88ee885054d0fe4fd49e044aa74e9CAS |

Scandalios JG, Guan L, Polidoros AN (1997) Catalases in plants: gene structure, properties, regulation, and expression. In ‘Oxidative stress and the molecular biology of antioxidant defenses’. (Ed. JG Scandalios) pp. 343–406. (Cold Spring Harbor Laboratory: Cold Spring Harbor, NY, USA)

Shafi A, Chauhan R, Gill T, Swarnkar MK, Sreenivasulu Y, Kumar S, Kumar N, Shankar R, Ahuja PS, Singh AK (2015) Expression of SOD and APX genes positively regulates secondary cell wall biosynthesis and promotes plant growth and yield in Arabidopsis under salt stress. Plant Molecular Biology 87, 615–631.
Expression of SOD and APX genes positively regulates secondary cell wall biosynthesis and promotes plant growth and yield in Arabidopsis under salt stress.CrossRef | 1:CAS:528:DC%2BC2MXktVKltL4%3D&md5=f0c321b69644ec06e276d8fc5eb81647CAS |

Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Le Journal de Botanique 2012, 1–26.

Shigeoka S, Maruta T (2014) Cellular redox regulation, signaling, and stress response in plants. Bioscience, Biotechnology, and Biochemistry 78, 1457–1470.
Cellular redox regulation, signaling, and stress response in plants.CrossRef | 1:CAS:528:DC%2BC2cXhs1Ors7%2FK&md5=e403dbaa00c11ca8784f8671e66d1da8CAS |

Spaepen S, Vanderleyden J (2015) Auxin signaling in Azospirillum brasilense: a proteome analysis. In ‘Biological nitrogen fixation’. (Ed. FJ de Brujin) pp. 937–940. (John Wiley & Sons Inc.: Hoboken, NJ, USA)

Sunkar R, Bartels D, Kirch HH (2003) Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance. The Plant Journal 35, 452–464.
Overexpression of a stress-inducible aldehyde dehydrogenase gene from Arabidopsis thaliana in transgenic plants improves stress tolerance.CrossRef | 1:CAS:528:DC%2BD3sXnsFyitLo%3D&md5=515cbe6534aac6e376de53526df3aff6CAS |

Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of Pearl Millet (Pennisetum americanum L.). Applied and Environmental Microbiology 37, 1016–1024.

Trani PE, Hiroce R, Bataglia OC (1983) ‘Análise foliar: amostragem e interpretação.’ (Fundação Cargill: Campinas, Brazil)

Upadhyay SK, Singh JS, Saxena AK, Singh DP (2012) Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions. Plant Biology 14, 605–611.
Impact of PGPR inoculation on growth and antioxidant status of wheat under saline conditions.CrossRef | 1:CAS:528:DC%2BC38XhsVKjsLbP&md5=ba0c3217cdb1e1760d4b093947901417CAS |

van Loon LC, Bakker P (2005) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In ‘PGPR: biocontrol and biofertilization’. (Ed. ZA Siddiqui) pp. 39–66. (Springer: Dordrecht, The Netherlands)

Vincent JM (1970) ‘A manual for the practical study of root-nodule bacteria.’ (Blackwell Scientific Publications: Oxford, UK)

Vriezen JAC, De Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Applied and Environmental Microbiology 73, 3451–3459.
Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature.CrossRef | 1:CAS:528:DC%2BD2sXmtlKktrc%3D&md5=a6dd58422213321848eb5b835d427afaCAS |

Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Wang YP, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS One 7, e52565
Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains.CrossRef | 1:CAS:528:DC%2BC3sXnsVylsw%3D%3D&md5=918283964819c609080672f7a3683781CAS |

Yang J, Kloepper JW, Ryu CM (2009) Rhizosphere bacteria help plants tolerate abiotic stress. Trends in Plant Science 14, 1–4.
Rhizosphere bacteria help plants tolerate abiotic stress.CrossRef | 1:CAS:528:DC%2BD1MXntVyhtw%3D%3D&md5=c96f90d9a94f7eab6afea492d1a35596CAS |

Yanni YG, Dazzo FB (2015) Occurrence and ecophysiology of the natural endophytic Rhizobium–rice association and translational assessment of its biofertilzer performance within the Egypt Nile delta. In ‘Biological nitrogen fixation’. (Ed. FJ de Bruijn) pp. 747–756. (John Wiley & Sons Inc.: Hoboken, NJ, USA)



Export Citation