Nitric oxide synthase expression in Pseudomonas koreensis MME3 improves plant growth promotion traits.
Brachypodium
Nitric oxide synthase
Nitrogen
Plant growth–promoting rhizobacteria
Pseudomonas
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
15 Feb 2024
15 Feb 2024
Historique:
received:
29
06
2023
accepted:
25
01
2024
revised:
03
01
2024
medline:
15
2
2024
pubmed:
15
2
2024
entrez:
15
2
2024
Statut:
epublish
Résumé
The development of novel biotechnologies that promote a better use of N to optimize crop yield is a central goal for sustainable agriculture. Phytostimulation, biofertilization, and bioprotection through the use of bio-inputs are promising technologies for this purpose. In this study, the plant growth-promoting rhizobacteria Pseudomonas koreensis MME3 was genetically modified to express a nitric oxide synthase of Synechococcus SyNOS, an atypical enzyme with a globin domain that converts nitric oxide to nitrate. A cassette for constitutive expression of synos was introduced as a single insertion into the genome of P. koreensis MME3 using a miniTn7 system. The resulting recombinant strain MME3:SyNOS showed improved growth, motility, and biofilm formation. The impact of MME3:SyNOS inoculation on Brachypodium distachyon growth and N uptake and use efficiencies under different N availability situations was analyzed, in comparison to the control strain MME3:c. After 35 days of inoculation, plants treated with MME3:SyNOS had a higher root dry weight, both under semi-hydroponic and greenhouse conditions. At harvest, both MME3:SyNOS and MME3:c increased N uptake and use efficiency of plants grown under low N soil. Our results indicate that synos expression is a valid strategy to boost the phytostimulatory capacity of plant-associated bacteria and improve the adaptability of plants to N deficiency. KEY POINTS: • synos expression improves P. koreensis MME3 traits important for rhizospheric colonization • B. distachyon inoculated with MME3:SyNOS shows improved root growth • MME3 inoculation improves plant N uptake and use efficiencies in N-deficient soil.
Identifiants
pubmed: 38358431
doi: 10.1007/s00253-024-13029-1
pii: 10.1007/s00253-024-13029-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
212Subventions
Organisme : Fondo para la Investigación Científica y Tecnológica
ID : PICT2019-2186
Informations de copyright
© 2024. The Author(s).
Références
Altaf MM, Ahmad I (2019) In vitro biofilm development and enhanced rhizosphere colonization of Triticum aestivum by fluorescent Pseudomonas sp. J Pure Appl Microbiol 13:1441–1449. https://doi.org/10.22207/JPAM.13.3.14
doi: 10.22207/JPAM.13.3.14
Arruebarrena Di Palma A, Pereyra MC, Moreno Ramirez L, Xiqui Vázquez ML, Baca BE, Pereyra MA, Lamattina L, Creus CM (2013) Denitrification-derived nitric oxide modulates biofilm formation in Azospirillum brasilense. FEMS Microbiol Lett 338:77–85. https://doi.org/10.1111/1574-6968.12030
doi: 10.1111/1574-6968.12030
pubmed: 23082946
Banaei-Asl F, Farajzadeh D, Bandehagh A, Komatsu S (2016) Comprehensive proteomic analysis of canola leaf inoculated with a plant growth-promoting bacterium, Pseudomonas fluorescens, under salt stress. Biochim Biophys Acta Proteins Proteom 1864:1222–1236. https://doi.org/10.1016/j.bbapap.2016.04.013
doi: 10.1016/j.bbapap.2016.04.013
Bao Y, Lies DP, Fu H, Roberts GP (1991) An improved Tn7-based system for the single-copy insertion of cloned genes into chromosomes of Gram-negative bacteria. Gene 109:177–178. https://doi.org/10.1016/0378-1119(91)90604-A
doi: 10.1016/0378-1119(91)90604-A
Basu A, Prasad P, Das SN, Kalam S, Sayyed RZ, Reddy MS, El EH (2021) Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability (switzerland) 13:1140
doi: 10.3390/su13031140
Bertani G (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62:293–300
doi: 10.1128/jb.62.3.293-300.1951
pubmed: 14888646
pmcid: 386127
Bloemberg GV, Wijfjes AHM, Lamers GEM, Stuurman N, Lugtenberg BJJ (2000) Simultaneous imaging of Pseudomonas fluorescens WCS365 populations expressing three different autofluorescent proteins in the rhizosphere: new perspectives for studying microbial communities. Mol Plant Microbe Interact 13:1170–1176. https://doi.org/10.1094/MPMI.2000.13.11.1170
doi: 10.1094/MPMI.2000.13.11.1170
pubmed: 11059483
Bogard M, Allard V, Brancourt-Hulmel M, Heumez E, MacHet JM, Jeuffroy MH, Gate P, Martre P, Le Gouis J (2010) Deviation from the grain protein concentration-grain yield negative relationship is highly correlated to post-anthesis N uptake in winter wheat. J Exp Bot 61:4303–1312. https://doi.org/10.1093/jxb/erq238
doi: 10.1093/jxb/erq238
pubmed: 20679251
Bradford M (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Brkljacic J, Grotewold E, Scholl R, Mockler T, Garvin DF, Vain P, Brutnell T, Sibout R, Bevan M, Budak H, Caicedo AL, Gao C, Gu Y, Hazen SP, Holt BF, Hong SY, Jordan M, Manzaneda AJ, Mitchell-Olds T, Mochida K, Mur LAJ, Park CM, Sedbrook J, Watt M, Zheng SJ, Vogel JP (2011) Brachypodium as a model for the grasses: today and the future. Plant Physiol 157:3–13. https://doi.org/10.1104/pp.111.179531
doi: 10.1104/pp.111.179531
pubmed: 21771916
pmcid: 3165879
Capdevila S, Martínez-Granero FM, Sánchez-Contreras M, Rivilla R, Martín M (2004) Analysis of Pseudomonas fluorescens F113 genes implicated in flagellar filament synthesis and their role in competitive root colonization. Microbiol 150:3889–3897. https://doi.org/10.1099/mic.0.27362-0
doi: 10.1099/mic.0.27362-0
Chaudhari SS, Kim M, Lei S, Razvi F, Alqarzaee AA, Hutfless EH, Powers R, Zimmerman MC, Fey PD, Thomas VC (2017) Nitrite derived from endogenous bacterial nitric oxide synthase activity promotes aerobic respiration. MBio 8:887–917. https://doi.org/10.1128/mBio.00887-17
doi: 10.1128/mBio.00887-17
Correa-Aragunde N, Foresi N, Del Castello F, Lamattina L (2018) A singular nitric oxide synthase with a globin domain found in Synechococcus PCC 7335 mobilizes N from arginine to nitrate. Sci Rep 8:12505. https://doi.org/10.1038/s41598-018-30889-6
doi: 10.1038/s41598-018-30889-6
pubmed: 30131503
pmcid: 6104048
Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi CA, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303. https://doi.org/10.1007/s00425-005-1523-7
doi: 10.1007/s00425-005-1523-7
pubmed: 15824907
Cutruzzolà F, Frankenberg-Dinkel N (2016) Origin and impact of nitric oxide in Pseudomonas aeruginosa biofilms. J Bacteriol 198:55–65
doi: 10.1128/JB.00371-15
pubmed: 26260455
David LC, Girin T, Fleurisson E, Phommabouth E, Mahfoudhi A, Citerne S, Berquin P, Daniel-Vedele F, Krapp A, Ferrario-Méry S (2019) Developmental and physiological responses of Brachypodium distachyon to fluctuating nitrogen availability. Sci Rep 9:3824. https://doi.org/10.1038/s41598-019-40569-8
doi: 10.1038/s41598-019-40569-8
pubmed: 30846873
pmcid: 6405861
Dawson JC, Huggins DR, Jones SS (2008) Characterizing nitrogen use efficiency in natural and agricultural ecosystems to improve the performance of cereal crops in low-input and organic agricultural systems. Field Crops Res 107:89–101
doi: 10.1016/j.fcr.2008.01.001
Del Castello F, Nejamkin A, Foresi N, Lamattina L, Correa-Aragunde N (2020) Chimera of globin/nitric oxide synthase: toward improving nitric oxide homeostasis and nitrogen recycling and availability. Front Plant Sci 11:575651. https://doi.org/10.3389/fpls.2020.575651
doi: 10.3389/fpls.2020.575651
pubmed: 33101345
pmcid: 7554344
Del Castello F, Foresi N, Nejamkin A, Lindermayr C, Buegger F, Lamattina L, Correa-Aragunde N (2021) Cyanobacterial NOS expression improves nitrogen use efficiency, nitrogen-deficiency tolerance and yield in Arabidopsis. Plant Sci 307:10860. https://doi.org/10.1016/j.plantsci.2021.110860
doi: 10.1016/j.plantsci.2021.110860
Di Benedetto NA, Corbo MR, Campaniello D, Cataldi MP, Bevilacqua A, Sinigaglia M, Flagella Z (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiol 3:413–434
doi: 10.3934/microbiol.2017.3.413
pubmed: 31294169
pmcid: 6604983
Dobermann A (2007) Nutrient use efficiency – measurement and management. In: Kraus A, Isherwood K, Heffer P (eds) Fertil Best management practices: general principles, strategy for their adoption and voluntary initiatives vs regulations, 1st edn. Proceeding of International Fertilizer Industry Association, Paris, France pp 1–22. https://digitalcommons.unl.edu/cgi/viewcontent.cgi?article=2431&context=agronomyfacpub
Dupont FM, Altenbach SB (2003) Molecular and biochemical impacts of environmental factors on wheat grain development and protein synthesis. J Cereal Sci 38:133–146
doi: 10.1016/S0733-5210(03)00030-4
Finan TM, Kunkel B, De Vos GF, Signer ER (1986) Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 167:66–72. https://doi.org/10.1128/jb.167.1.66-72.1986
doi: 10.1128/jb.167.1.66-72.1986
pubmed: 3013840
pmcid: 212841
Ganeshan G, Kumar AM (2005) Pseudomonas fluorescens, a potential bacterial antagonist to control plant diseases. J Plant Interact 1:123–134
doi: 10.1080/17429140600907043
Garnett T, Conn V, Kaiser BN (2009) Root based approaches to improving nitrogen use efficiency in plants. Plant Cell Environ 32:1272–1283. https://doi.org/10.1111/j.1365-3040.2009.02011.x
doi: 10.1111/j.1365-3040.2009.02011.x
pubmed: 19558408
Ghazy N, El-Nahrawy S (2021) Siderophore production by Bacillus subtilis MF497446 and Pseudomonas koreensis MG209738 and their efficacy in controlling Cephalosporium maydis in maize plant. Arch Microbiol 203:1195–1209. https://doi.org/10.1007/s00203-020-02113-5
doi: 10.1007/s00203-020-02113-5
pubmed: 33231747
Ghiglione JF, Gourbiere F, Potier P, Philippot L, Lensi R (2000) Role of respiratory nitrate reductase in ability of Pseudomonas fluorescens YT101 to colonize the rhizosphere of maize. Appl Environ Microbiol 66:4012–4016. https://doi.org/10.1128/AEM.66.9.4012-4016.2000
doi: 10.1128/AEM.66.9.4012-4016.2000
pubmed: 10966422
pmcid: 92252
Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796
doi: 10.1128/aem.61.2.793-796.1995
pubmed: 16534942
pmcid: 1388360
Guo Q, Shi M, Chen L, Zhou J, Zhang L, Li Y, Xue Q, Lai H (2020) The biocontrol agent Streptomyces pactum increases Pseudomonas koreensis populations in the rhizosphere by enhancing chemotaxis and biofilm formation. Soil Biol Biochem 144:107755. https://doi.org/10.1016/j.soilbio.2020.107755
doi: 10.1016/j.soilbio.2020.107755
Guo Q, Sun Y, Shi M, Han X, Jing Y, Li Y, Li H, Lai H (2021) Pseudomonas koreensis promotes tomato growth and shows potential to induce stress tolerance via auxin and polyphenol-related pathways. Plant Soil 462:141–158. https://doi.org/10.1007/s11104-021-04837-9
doi: 10.1007/s11104-021-04837-9
Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319
doi: 10.1038/nrmicro1129
pubmed: 15759041
Hakeem KR, Sabir M, Ozturk M, Akhtar MS, Ibrahim FH, Ashraf M, Ahmad MSA (2017) Nitrate and nitrogen oxides: sources, health effects and their remediation. Rev Environ Contam Toxicol 242:183–217. https://doi.org/10.1007/398_2016_11
doi: 10.1007/398_2016_11
pubmed: 27734212
Havlin JL, Tisdale SL, Nelson WL, Beaton JD (2016) Soil fertility and fertilizers: an introduction to nutrient management, 8th edn. Pearson India Education Services, Noida, Uttar Pradesh, pp 1–529. https://www.pearson.com/en-us/subject-catalog/p/soil-fertility-and-fertilizers-an-introduction-to-nutrient-management/P200000001208/9780137593392
Kang A, Zhang N, Xun W, Dong X, Xiao M, Liu Z, Xu Z, Feng H, Zou J, Shen Q, Zhang R (2022) Nitrogen fertilization modulates beneficial rhizosphere interactions through signaling effect of nitric oxide. Plant Physiol 188:1129–1140. https://doi.org/10.1093/plphys/kiab555
doi: 10.1093/plphys/kiab555
pubmed: 34865137
King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44:301–307
Knights HE, Jorrin B, Haskett TL, Poole PS (2021) Deciphering bacterial mechanisms of root colonization. Environ Microbiol Rep 13:428–444
doi: 10.1111/1758-2229.12934
pubmed: 33538402
Koch B, Jensen LE, Nybroe O (2001) A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J Microbiol Methods 45:187–195. https://doi.org/10.1016/S0167-7012(01)00246-9
doi: 10.1016/S0167-7012(01)00246-9
pubmed: 11348676
Kuang W, Sanow S, Kelm JM, Linow MM, Andeer P, Kohlheyer D, Northen T, Vogel JP, Watt M, Arsova B (2022) N-dependent dynamics of root growth and nitrate and ammonium uptake are altered by the bacterium Herbaspirillum seropedicae in the cereal model Brachypodium distachyon. J Exp Bot 73:5306–5321. https://doi.org/10.1093/jxb/erac184
doi: 10.1093/jxb/erac184
pubmed: 35512445
pmcid: 9440436
Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
doi: 10.1146/annurev.arplant.54.031902.134752
pubmed: 14502987
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Liu Q, Wu K, Song W, Zhong N, Wu Y, Fu X (2022) Improving crop nitrogen use efficiency toward sustainable green revolution. Annu Rev Plant Biol 73:523–551
doi: 10.1146/annurev-arplant-070121-015752
pubmed: 35595292
Maheshwari DK, Dheeman S, Agarwal M (2015) Phytohormone-producing PGPR for sustainable agriculture. In: Bacterial metabolites in sustainable agroecosystem. Sustainable development and biodiversity. Springer, Cham, Uttarakhand, 12:159–182. https://doi.org/10.1007/978-3-319-24654-3_7
Man M, Deen B, Dunfield KE, Wagner-Riddle C, Simpson MJ (2021) Altered soil organic matter composition and degradation after a decade of nitrogen fertilization in a temperate agroecosystem. Agric Ecosyst Environ 310:107305. https://doi.org/10.1016/j.agee.2021.107305
doi: 10.1016/j.agee.2021.107305
Maroniche GA, Rubio EJ, Consiglio A, Perticari A (2016) Plant-associated fluorescent Pseudomonas from red lateritic soil: beneficial characteristics and their impact on lettuce growth. J Gen Appl Microbiol 62:248–257. https://doi.org/10.2323/jgam.2016.04.006
doi: 10.2323/jgam.2016.04.006
pubmed: 27725403
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5:62–71. https://doi.org/10.1006/niox.2000.0319
doi: 10.1006/niox.2000.0319
pubmed: 11178938
Molina-Favero C, Creus CM, Simontacchi M, Puntarulo S, Lamattina L (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant Microbe Interact 21:62–71. https://doi.org/10.1094/MPMI-21-7-1001
doi: 10.1094/MPMI-21-7-1001
Moll RH, Kamprath EJ, Jackson WA (1982) Analysis and interpretation of factors which contribute to efficiency of nitrogen utilization. Agron J 74:562–564
doi: 10.2134/agronj1982.00021962007400030037x
Mulet M, Bennasar A, Lalucat J, García-Valdés E (2009) An rpoD-based PCR procedure for the identification of Pseudomonas species and for their detection in environmental samples. Mol Cell Probes 23:140–147. https://doi.org/10.1016/j.mcp.2009.02.001
doi: 10.1016/j.mcp.2009.02.001
pubmed: 19268522
Muriel C, Jalvo B, Redondo-Nieto M, Rivilla R, Martín M (2015) Chemotactic motility of Pseudomonas fluorescens F113 under aerobic and denitrification conditions. PLoS ONE 10:132242. https://doi.org/10.1371/journal.pone.0132242
doi: 10.1371/journal.pone.0132242
Nadarajan S, Sukumaran S (2021) Chemistry and toxicology behind chemical fertilizers. Controlled release fertilizers for sustainable agriculture. Firth Edición. Academic Press, London, UK
doi: 10.1016/B978-0-12-819555-0.00012-1
Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agron J 65:109–112. https://doi.org/10.2134/agronj1973.00021962006500010033x
doi: 10.2134/agronj1973.00021962006500010033x
Oku S, Komatsu A, Tajima T, Nakashimada Y, Kato J (2012) Identification of chemotaxis sensory proteins for amino acids in Pseudomonas fluorescens Pf0-1 and their involvement in chemotaxis to tomato root exudate and root colonization. Microbes Environ 27:462–469. https://doi.org/10.1264/jsme2.ME12005
doi: 10.1264/jsme2.ME12005
pubmed: 22972385
pmcid: 4103555
O’Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461. https://doi.org/10.1046/j.1365-2958.1998.00797.x
Padhan BK, Sathee L, Kumar S, Chinnusamy V, Kumar A (2023) Variation in nitrogen partitioning and reproductive stage nitrogen remobilization determines nitrogen grain production efficiency (NUEg) in diverse rice genotypes under varying nitrogen supply. Front Plant Sci 14:1093581. https://doi.org/10.3389/fpls.2023.1093581
doi: 10.3389/fpls.2023.1093581
pubmed: 36938028
pmcid: 10020356
Park KH, Lee CY, Son HJ (2009) Mechanism of insoluble phosphate solubilization by Pseudomonas fluorescens RAF15 isolated from ginseng rhizosphere and its plant growth-promoting activities. Lett in Appl Microbiol 49:222–228. https://doi.org/10.1111/j.1472-765X.2009.02642.x
Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ (2007) O-CAS, a fast and universal method for siderophore detection. J Microbiol Methods 70:127–131. https://doi.org/10.1016/j.mimet.2007.03.023
Picciano AL, Crane BR (2020) Erratum: a nitric oxide synthase-like protein from Synechococcus produces NO/NO3 from L-arginine and NADPH in a tetrahydrobiopterin- and Ca - dependent manner (J Biol Chem (2019) 294:10708–10719. https://doi.org/10.1074/jbc.RA119.08399 ). J Biol Chem 295:897. https://doi.org/10.1016/S0021-9258(17)49944-3
Pravisya P, Jayaram KM, Yusuf A (2019) Biotic priming with Pseudomonas fluorescens induce drought stress tolerance in Abelmoschus esculentus (L.) Moench (Okra). Physiol Mol Biol Plants 25:101–112. https://doi.org/10.1007/s12298-018-0621-5
doi: 10.1007/s12298-018-0621-5
pubmed: 30804633
Raissig MT, Woods DP (2022) The wild grass Brachypodium distachyon as a developmental model system. Curr Top Dev Biol 147:33–71
doi: 10.1016/bs.ctdb.2021.12.012
pubmed: 35337454
Redondo-Nieto M, Barret M, Morrissey J, Germaine K, Martínez-Granero F, Barahona E, Navazo A, Sánchez-Contreras M, Moynihan JA, Muriel C, Dowling D, O’Gara F, Martín M, Rivilla R (2013) Genome sequence reveals that Pseudomonas fluorescens F113 possesses a large and diverse array of systems for rhizosphere function and host interaction. BMC Genomics 14:54. https://doi.org/10.1186/1471-2164-14-54
doi: 10.1186/1471-2164-14-54
pubmed: 23350846
pmcid: 3570484
Sainju UM, Ghimire R, Pradhan GP (2020) Nitrogen fertilization I: impact on crop, soil, and environment. In: Rigobelo EC, Serra A (eds) Nitrogen fixation, 1st edn. IntechOpen, London, pp 1–202. https://doi.org/10.5772/intechopen.86028
Saleh D, Sharma M, Seguin P, Jabaji S (2020) Organic acids and root exudates of Brachypodium distachyon: effects on chemotaxis and biofilm formation of endophytic bacteria. Can J Microbiol 66:562–575. https://doi.org/10.1139/cjm-2020-0041
doi: 10.1139/cjm-2020-0041
pubmed: 32348684
Santos MS, Nogueira MA, Hungria M (2019) Microbial inoculants: reviewing the past, discussing the present and previewing an outstanding future for the use of beneficial bacteria in agriculture. AMB Express 9:205
doi: 10.1186/s13568-019-0932-0
pubmed: 31865554
pmcid: 6925611
Santoyo G, Urtis-Flores CA, Loeza-Lara PD, Orozco-Mosqueda MDC, Glick BR (2021) Rhizosphere colonization determinants by plant growth-promoting rhizobacteria (PGPR). Biology (basel) 10:475. https://doi.org/10.3390/biology10060475
doi: 10.3390/biology10060475
pubmed: 34072072
Tang M, Jiang J, Lv Q, Yang B, Zheng M, Gao X, Han J, Zhang Y, Yang Y (2020) Denitrification performance of Pseudomonas fluorescens Z03 immobilized by graphene oxide-modified polyvinyl-alcohol and sodium alginate gel beads at low temperature. R Soc Open Sci 7:205. https://doi.org/10.1098/rsos.191542
doi: 10.1098/rsos.191542
Upadhyay A, Srivastava S (2014) Mechanism of zinc resistance in a plant growth promoting Pseudomonas fluorescens strain. World J Microbiol Biotechnol 30:2273–2282. https://doi.org/10.1007/s11274-014-1648-6
doi: 10.1007/s11274-014-1648-6
pubmed: 24691847
Vaishnav A, Kumari S, Jain S, Varma A, Tuteja N, Choudhary DK (2016) PGPR-mediated expression of salt tolerance gene in soybean through volatiles under sodium nitroprusside. J Basic Microbiol 56:1274–1288. https://doi.org/10.1002/jobm.201600188
doi: 10.1002/jobm.201600188
pubmed: 27439917
Zboralski A, Filion M (2020) Genetic factors involved in rhizosphere colonization by phytobeneficial Pseudomonas spp. Comput Struct Biotechnol J 18:3539–3554
doi: 10.1016/j.csbj.2020.11.025
pubmed: 33304453
pmcid: 7711191
Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528:51–59
doi: 10.1038/nature15743
pubmed: 26595273
Zuber S, Carruthers F, Keel C, Mattart A, Blumer C, Pessi G, Gigot-Bonnefoy C, Schnider-Keel U, Heeb S, Reimmann C, Haas D (2003) GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 16:634–644. https://doi.org/10.1094/MPMI.2003.16.7.634