Skip to main content

Advertisement

SpringerLink
Log in

Improved Phosphorus Uptake by Wheat Plant (Triticum aestivum L.) with Rhizosphere Fluorescent Pseudomonads Strains Under Water-Deficit Stress

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The aim of this study was to characterize fluorescent pseudomonads isolates of dryland wheat for salinity and drought tolerance and plant growth-promoting (PGP) traits in the presence or absence of salinity (4% NaCl) and evaluate the effect of two effective strains, Pseudomonas helmanticensis B30 and P. baetica B21, on phosphorus (P) uptake by wheat plant grown in a saline calcareous soil fertilized with rock phosphate (RP) and triple superphosphate (TSP) under water-deficit stress (55% of field capacity (FC) and 88% FC). All fluorescent pseudomonads isolates had the ability to grow at different drought stress levels and at salinity level of 4% NaCl. In addition, a significant percentage of these isolates retained their ability to produce PGP traits (especially P solubilization and indole-3-acetic acid production) in the presence of salinity. The results showed that 80% FC moisture level compared to 55% FC moisture level significantly increased plant growth indices and P uptake by wheat plant. In most of the measured parameters, RP treatment (8 mg P kg−1 soil) alone did not show any significant difference compared to negative control (without RP and TSP), but combination treatments with RP and TSP at all levels (3, 6, and 9 mg P kg−1 soil) increased these parameters compared to negative control. In non-stress and water-deficit stress conditions, bacterial strains significantly increased soil available P, growth indices (a 41.6% increase in root dry weight and an 11% increase in shoot dry weight), grain yield (a 17% increase), shoot P uptake of wheat plant as compared to control (without bacterial strains). Overall, the results of this study showed that dryland wheat rhizosphere harbors drought- and salinity-tolerant phosphate-solubilizing fluorescent pseudomonads isolates with potential of producing PGP traits in the presence or absence of salinity and improving P uptake by the plant under water-deficit stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abbas G, Saqib M, Akhtar J, Haq MAu (2015) Interactive effects of salinity and iron deficiency on different rice genotypes. J Plant Nutr Soil Sci 178(2):306–311

    CAS  Google Scholar 

  • Abbasi S, Zahedi H, Sadeghipour O, Akbari R (2013) Effect of plant growth promoting rhizobacteria (PGPR) on physiological parameters and nitrogen content of soybean grown under different irrigation regimes. Res Crops 14:798–803

    Google Scholar 

  • Abdelwahab RAI, Cherif A, Cristina C, Nabti E (2018) Extracts from Marine macroalgae and Opuntia ficus-indica cladodes enhance halotolerance and enzymatic potential of diazotrophic rhizobacteria and their impact on wheat germination under salt stress. Pedosphere 28(2):241–254

    Google Scholar 

  • Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85(1):1–12

    CAS  PubMed  Google Scholar 

  • Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Biol 29(1):29–34

    CAS  Google Scholar 

  • Argandoña M, Nieto JJ, Iglesias-Guerra F, Calderón MI, García-Estepa R, Vargas C (2010) Interplay between iron homeostasis and the osmotic stress response in the halophilic bacterium Chromohalobacter salexigens. Appl Environ Microbiol 76(11):3575–3589

    PubMed  PubMed Central  Google Scholar 

  • Arif MS, Muhammad R, Shahzad SM, Yasmeen T, Shafaqat ALI, Akhtar MJ (2017) Phosphorus-mobilizing rhizobacterial strain Bacillus cereus GS6 improves symbiotic efficiency of soybean on an Aridisol amended with phosphorus-enriched compost. Pedosphere 27(6):1049–1061

    CAS  Google Scholar 

  • Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp-mediated plant growth-stimulation. Soil Biol Biochem 19(4):451–457

    CAS  Google Scholar 

  • Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soil 45(4):405–413

    Google Scholar 

  • Bano Q, Ilyas N, Bano A, Zafar N, Akram A, Hassan F (2013) Effect of Azospirillum inoculation on maize (Zea mays L.) under drought stress. Pak J Bot 45(S1):13–20

    CAS  Google Scholar 

  • Bashan Y, Kamnev AA, de-Bashan LE (2013) A proposal for isolating and testing phosphate-solubilizing bacteria that enhance plant growth. Biol Fertil Soil 49:1–2

    Google Scholar 

  • Bates LS, Waldren RP, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    CAS  Google Scholar 

  • Belnap J (2011) Biological phosphorus cycling in dryland regions. In: Oberson A (ed) Phosphorus in action. Springer, Berlin, pp 371–406

    Google Scholar 

  • Borymski S, Cycoń M, Beckmann M, Mur LA, Piotrowska-Seget Z (2018) Plant species and heavy metals affect biodiversity of microbial communities associated with metal-tolerant plants in metalliferous soils. Front Microbiol 9:1425

    PubMed  PubMed Central  Google Scholar 

  • Bremner J (1996) Nitrogen-total. In: Sparks DL (ed) Methods of soil analyses, part 3, chemical methods. Soil Science Society of America and American Society of Agronomy, Madison, pp 1085–1122

    Google Scholar 

  • Bremner J, Mulvaney C, Page A, Miller R, Keeney D (1982) Methods of soil analysis: chemical and microbiological properties Part 2. American Society of Agronomy, Inc Soil Science Society of America, Inc Publisher, Madison

    Google Scholar 

  • Bultreys A, Gheysen I, Wathelet B, Maraite H, De Hoffmann E (2003) High-performance liquid chromatography analyses of pyoverdin siderophores differentiate among phytopathogenic fluorescent Pseudomonas species. Appl Environ Microbiol 69(2):1143–1153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cassel D, Nielsen D (1986) Field capacity and available water capacity. Methods Soil Anal 5:901–926

    Google Scholar 

  • Chandra D, Srivastava R, Glick BR, Sharma AK (2018) Drought-tolerant Pseudomonas spp improve the growth performance of finger millet (Eleusine coracana (L.) Gaertn.) under non-stressed and drought-stressed conditions. Pedosphere 28(2):227–240

    Google Scholar 

  • Chen L, Figueredo A, Villani H, Michajluk J, Hungria M (2002) Diversity and symbiotic effectiveness of rhizobia isolated from field-grown soybean nodules in Paraguay. Biol Fertil Soil 35(6):448–457

    CAS  Google Scholar 

  • Edwards U, Rogall T, Blöcker H, Emde M, Böttger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17(19):7843–7853

    CAS  PubMed  PubMed Central  Google Scholar 

  • Etesami H, Beattie GA (2017) Plant-microbe interactions in adaptation of agricultural crops to abiotic stress conditions. In: Probiotics and plant health. Springer, Singapore, pp 163–200

  • Etesami H, Beattie GA (2018) Mining halophytes for plant growth-promoting halotolerant bacteria to enhance the salinity tolerance of non-halophytic crops. Front Microbiol 9:148

    PubMed  PubMed Central  Google Scholar 

  • Etesami H, Maheshwari DK (2018) Use of plant growth promoting rhizobacteria (PGPRs) with multiple plant growth promoting traits in stress agriculture: action mechanisms and future prospects. Ecot Environ Saf 156:225–246. https://doi.org/10.1016/j.ecoenv.2018.03.013

    Article  CAS  Google Scholar 

  • Gasparatos D, Haidouti C (2001) A comparison of wet oxidation methods for determination of total phosphorus in soils. J Plant Nutr Soil Sci 164(4):435–439

    CAS  Google Scholar 

  • Gee G, Bauder J (1986) Particle-size analysis. In: Klute A (ed) Methods of soil analysis, part 1. American society of Agronomy Inc, Madison

    Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41(2):109–117

    CAS  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica. https://doi.org/10.6064/2012/963401

    Article  PubMed  PubMed Central  Google Scholar 

  • Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169(1):30–39. https://doi.org/10.1016/j.micres.2013.09.009

    Article  CAS  PubMed  Google Scholar 

  • Gordon B, Tindall T (2006) Fluid P performance improved with polymers. Fluid J 14:12–13

    Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26(1):192

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grant CA, Flaten DN, Tomasiewicz DJ, Sheppard SC (2001) The importance of early season phosphorus nutrition. Can J Plant Sci 81(2):211–224

    CAS  Google Scholar 

  • Hasanuzzaman M, Nahar K, Hossain MA (2019) Wheat production in changing environments. Springer, New York

    Google Scholar 

  • Iqbal Hussain M, Naeem Asghar H, Javed Akhtar M, Arshad M (2013) Impact of phosphate solubilizing bacteria on growth and yield of maize. Soil Environ 32(1):71–78

    Google Scholar 

  • Jackson ML (2005) Soil chemical analysis: advanced course. UW-Madison Libraries Parallel Press, Madison

    Google Scholar 

  • Jeshni MG, Mousavinik M, Khammari I, Rahimi M (2017) The changes of yield and essential oil components of German Chamomile (Matricaria recutita L.) under application of phosphorus and zinc fertilizers and drought stress conditions. J Saudi Soc Agric Sci 16(1):60–65

    Google Scholar 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163(3):459–480

    CAS  PubMed  Google Scholar 

  • Kadmiri IM, Chaouqui L, Azaroual SE, Sijilmassi B, Yaakoubi K, Wahby I (2018) Phosphate-solubilizing and auxin-producing rhizobacteria promote plant growth under saline conditions. Arab J Sci Eng 43(7):3403–3415

    CAS  Google Scholar 

  • Karlidag H, Esitken A, Turan M, Sahin F (2007) Effects of root inoculation of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient element contents of leaves of apple. Sci Hortic 114(1):16–20

    CAS  Google Scholar 

  • Kasim WA, Osman ME, Omar MN, El-Daim IAA, Bejai S, Meijer J (2013) Control of drought stress in wheat using plant-growth-promoting bacteria. J Plant Growth Regul 32(1):122–130

    CAS  Google Scholar 

  • Kaushal M, Wani SP (2016) Rhizobacterial-plant interactions: strategies ensuring plant growth promotion under drought and salinity stress. Agri Ecosyst Environ 231:68–78

    CAS  Google Scholar 

  • King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44(2):301–307

    CAS  PubMed  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286(5776):885

    CAS  Google Scholar 

  • Kremer RJ, Souissi T (2001) Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr Microbiol 43(3):182–186

    CAS  PubMed  Google Scholar 

  • Li H, Lei P, Pang X, Li S, Xu H, Xu Z, Feng X (2017) Enhanced tolerance to salt stress in canola (Brassica napus L.) seedlings inoculated with the halotolerant Enterobacter cloacae HSNJ4. Appl Soil Ecol 119:26–34

    CAS  Google Scholar 

  • Liu M, Liu X, Cheng B-S, Ma X-L, Lyu X-T, Zhao X-F, Ju Y-L, Min Z, Zhang ZW, Fang YL (2016) Selection and evaluation of phosphate-solubilizing bacteria from grapevine rhizospheres for use as biofertilizers. Span J Agric Res 14(4):26

    Google Scholar 

  • Loeppert R, Suarez L (1996) Carbonate and gypsum. In: Sparks DL (ed) Methods of soil analysis. Part 3. Chemical methods. Soil science Society of America, Madison, pp 437–474

    Google Scholar 

  • Lopez JR, Dieguez AL, Doce A, De la Roca E, De la Herran R, Navas JI, Toranzo AE, Romalde JL (2012) Pseudomonas baetica sp. nov., a fish pathogen isolated from wedge sole, Dicologlossa cuneata (Moreau). Int J Syst Evol Microbiol 62(4):874–882

    CAS  PubMed  Google Scholar 

  • Lugtenberg BJ, Dekkers L, Bloemberg GV (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Ann Rev Phytopathol 39(1):461–490

    CAS  Google Scholar 

  • Mahmoudi TR, Yu JM, Liu S, Pierson LS III, Pierson EA (2019) Drought-stress tolerance in wheat seedlings conferred by phenazine-producing rhizobacteria. Front Microbiol. https://doi.org/10.3389/fmicb.2019.01590

    Article  PubMed  PubMed Central  Google Scholar 

  • McBeath T, McLaughlin M, Kirby J, Armstrong R (2012) The effect of soil water status on fertiliser, topsoil and subsoil phosphorus utilisation by wheat. Plant Soil 358(1–2):337–348

    CAS  Google Scholar 

  • McLean E (1982) Soil pH and lime requirement. Methods Soil Anal 9:199–224

    Google Scholar 

  • Mezaache-Aichour S, Guechi A, Nicklin J, Drider D, Prevost H, Strange R (2012) Isolation, identification and antimicrobial activity of pseudomonads isolated from the rhizosphere of potatoes growing in Algeria. J Plant Pathol 94(1):89–98

    Google Scholar 

  • Misra A (2003) Influence of water conditions on growth and mineral nutrient uptake of native plants on clacareous soil. Lund University, Lund

    Google Scholar 

  • Nadira UA, Ahmed IM, Wu F, Zhang G (2016) The regulation of root growth in response to phosphorus deficiency mediated by phytohormones in a Tibetan wild barley accession. Acta Physiol Plant 38(4):105

    Google Scholar 

  • Nakbanpote W, Panitlurtumpai N, Sangdee A, Sakulpone N, Sirisom P, Pimthong A (2014) Salt-tolerant and plant growth-promoting bacteria isolated from Zn/Cd contaminated soil: identification and effect on rice under saline conditions. J Plant Interact 9(1):379–387

    CAS  Google Scholar 

  • Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organic matter. Methods Soil Anal 5:961–1010

    Google Scholar 

  • Noori F, Etesami H, Najafi Zarini H, Khoshkholgh-Sima NA, Hosseini Salekdeh G, Alishahi F (2018) Mining alfalfa (Medicago sativa L.) nodules for salinity tolerant non-rhizobial bacteria to improve growth of alfalfa under salinity stress. Ecot Environ Saf 162:129–138. https://doi.org/10.1016/j.ecoenv.2018.06.092

    Article  CAS  Google Scholar 

  • Noori MSS, Saud HM (2012) Potential plant growth-promoting activity of Pseudomonas sp. isolated from paddy soil in Malaysia as biocontrol agent. J Plant Pathol Microb 3(2):1–4

    Google Scholar 

  • Olsen SR (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Dep Agric Circ 939:1–19

    Google Scholar 

  • Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part II. Chemical and microbiological properties. ASA SSSA Publisher, Madison, pp 403–427

    Google Scholar 

  • Orhan F (2016) Alleviation of salt stress by halotolerant and halophilic plant growth-promoting bacteria in wheat (Triticum aestivum). Braz J Microbiol 47(3):621–627

    CAS  PubMed  PubMed Central  Google Scholar 

  • Payne WA, Hossner LR, Onken AB, Wendt CW (1995) Nitrogen and phosphorus uptake in pearl millet and its relation to nutrient and transpiration efficiency. Agronom J 87(3):425–431

    Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118(1):10–15

    CAS  PubMed  Google Scholar 

  • Pereira SI, Castro PM (2014) Phosphate-solubilizing rhizobacteria enhance Zea mays growth in agricultural P-deficient soils. Ecol Eng 73:526–535

    Google Scholar 

  • Praveen Kumar G, Mir Hassan Ahmed S, Desai S, Leo Daniel Amalraj E, Rasul A (2014) In vitro screening for abiotic stress tolerance in potent biocontrol and plant growth promoting strains of Pseudomonas and Bacillus spp. Int J Bacteriol. https://doi.org/10.1155/2014/195946

    Article  PubMed  PubMed Central  Google Scholar 

  • Ramírez-Bahena M-H, Cuesta MJ, Flores-Félix JD, Mulas R, Rivas R, Castro-Pinto J, Brañas J, Mulas D, González-Andrés F, Velázquez E (2014) Pseudomonas helmanticensis sp. nov, isolated from forest soil. Int J Syst Evol Microbiol 64(7):2338–2345

    PubMed  Google Scholar 

  • Rashid M, Khalil S, Ayub N, Alam S, Latif F (2004) Organic acids production and phosphate solubilization by phosphate solubilizing microorganisms (PSM) under in vitro conditions. Pak J Biol Sci 7(2):187–196

    Google Scholar 

  • Razzaghi Komaresofla B, Alikhani HA, Etesami H, Khoshkholgh-Sima NA (2019) Improved growth and salinity tolerance of the halophyte Salicornia sp. by co–inoculation with endophytic and rhizosphere bacteria. Appl Soil Ecol 138:160–170. https://doi.org/10.1016/j.apsoil.2019.02.022

    Article  Google Scholar 

  • Rezakhani L, Motesharezadeh B, Tehrani MM, Etesami H, Hosseini HM (2019) Phosphate–solubilizing bacteria and silicon synergistically augment phosphorus (P) uptake by wheat (Triticum aestivum L.) plant fertilized with soluble or insoluble P source. Ecot Environ Safe 173:504–513

    CAS  Google Scholar 

  • Rockström J, Lannerstad M, Falkenmark M (2007) Assessing the water challenge of a new green revolution in developing countries. Proc Natl Acad Sci USA 104(15):6253–6260

    PubMed  PubMed Central  Google Scholar 

  • Ruppel S, Franken P, Witzel K (2013) Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct Plant Biol 40(9):940–951

    CAS  PubMed  Google Scholar 

  • Saber FM, Abdelhafez AA, Hassan EA, Ramadan EM (2015) Characterization of fluorescent pseudomonads isolates and their efficiency on the growth promotion of tomato plant. Ann Agric Sci 60(1):131–140

    Google Scholar 

  • Sapre S, Gontia-Mishra I, Tiwari S (2018) Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol Res 206:25–32

    CAS  PubMed  Google Scholar 

  • Scarpellini M, Franzetti L, Galli A (2004) Development of PCR assay to identify Pseudomonas fluorescens and its biotype. FEMS Microbiol Lett 236(2):257–260

    CAS  PubMed  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant physiol 116(2):447–453

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160(1):47–56

    CAS  PubMed  Google Scholar 

  • Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Crit Rev Plant Sci 32(4):237–249

    Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. https://doi.org/10.1155/2012/217037

    Article  Google Scholar 

  • Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2(1):587

    PubMed  PubMed Central  Google Scholar 

  • Sönmez O, Turan V, Kaya C (2016) The effects of sulfur, cattle, and poultry manure addition on soil phosphorus. Turk J Agri Forest 40(4):536–541

    Google Scholar 

  • Sperber JI (1958) The incidence of apatite-solubilizing organisms in the rhizosphere and soil. Aus J Agric Res 9(6):778–781

    CAS  Google Scholar 

  • Sumner ME, Miller WP (1996) Cation exchange capacity and exchange coefficients. Methods Soil Anal 5:1201–1229

    Google Scholar 

  • Tank N, Saraf M (2010) Salinity-resistant plant growth promoting rhizobacteria ameliorates sodium chloride stress on tomato plants. J Plant Interact 5(1):51–58

    CAS  Google Scholar 

  • Timmusk S, El-Daim IAA, Copolovici L, Tanilas T, Kännaste A, Behers L, Nevo E, Seisenbaeva G, Stenström E, Niinemets Ü (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PloS ONE 9(5):e96086

    PubMed  PubMed Central  Google Scholar 

  • Tsavkelova EA, Klimova SY, Cherdyntseva TA, Netrusov AI (2006) Microbial producers of plant growth stimulators and their practical use: a review. Appl Biochem Microbiol 42(2):117–126

    CAS  Google Scholar 

  • Upadhyay S, Singh D (2015) Effect of salt-tolerant plant growth-promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biol 17(1):288–293

    CAS  PubMed  Google Scholar 

  • Vimal SR, Gupta J, Singh JS (2018) Effect of salt tolerant Bacillus sp. and Pseudomonas sp on wheat (Triticum aestivum L.) growth under soil salinity: a comparative study. Microbiol Res. https://doi.org/10.4081/mr.2018.7462

    Article  Google Scholar 

  • Viscardi S, Ventorino V, Duran P, Maggio A, De Pascale S, Mora M, Pepe O (2016) Assessment of plant growth promoting activities and abiotic stress tolerance of Azotobacter chroococcum strains for a potential use in sustainable agriculture. J Soil Sci Plant Nutr 16(3):848–863

    CAS  Google Scholar 

  • Vurukonda SSKP, Vardharajula S, Shrivastava M, SkZ A (2016) Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiol Res 184:13–24

    PubMed  Google Scholar 

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathol 97(2):250–256

    Google Scholar 

  • Westerman RL (1990) Soil testing and plant analysis. In: Westerman RL (ed) Soil science Society of America book series, 3rd edn. Inc Madison, Wisconsin

    Google Scholar 

  • Wollum A (1982) Cultural methods for soil microorganisms 1. Methods Soil Anal 9:781–802

    Google Scholar 

  • Woomer P, Bennett J, Yost R (1990) Overcoming the inflexibility of most-probable-number procedures. Agron J 82(2):349–353

    Google Scholar 

  • Xie H, Pasternak JJ, Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 that overproduce indoleacetic acid. Curr Microbiol 32(2):67–71

    CAS  Google Scholar 

  • Zhang X, Ervin EH, Evanylo GK, Haering KC (2009) Impact of biosolids on hormone metabolism in drought-stressed tall fescue. Crop Sci 49(5):1893–1901

    CAS  Google Scholar 

Download references

Acknowledgements

We are grateful for the support of the Tehran University and the financial support of Iran National Science Foundation.

Author information

Authors and Affiliations

  1. Department of Soil Science, University College of Agriculture and Natural Resources, University of Tehran, 31587-77871, Tehran, Iran

    Jamal Karimzadeh, Hossein Ali Alikhani, Hassan Etesami & Ahmad Ali Pourbabaei

Authors
  1. Jamal Karimzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hossein Ali Alikhani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hassan Etesami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ahmad Ali Pourbabaei
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors have contributed equally to this study.

Corresponding authors

Correspondence to Hossein Ali Alikhani or Hassan Etesami.

Ethics declarations

Conflict of interest

The authors have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 46 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Karimzadeh, J., Alikhani, H.A., Etesami, H. et al. Improved Phosphorus Uptake by Wheat Plant (Triticum aestivum L.) with Rhizosphere Fluorescent Pseudomonads Strains Under Water-Deficit Stress. J Plant Growth Regul 40, 162–178 (2021). https://doi.org/10.1007/s00344-020-10087-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-020-10087-3

Keywords

Search

Navigation