Skip to main content

Advertisement

Log in

The stimulatory effects of plant growth promoting rhizobacteria and plant growth regulators on wheat physiology grown in sandy soil

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The present study was aimed to investigate the effects of plant growth promoting rhizobacteria (PGPR) and plant growth regulators (PGRs) on the physiology and yield of wheat grown in less fertile sandy soil. The isolated PGPR strains were identified by 16S-rRNA gene sequencing as Planomicrobium chinense (P1), Bacillus cereus (P2) and Pseudomonas fluorescens (P3). Wheat varieties (Galaxy-13 and Pak-2013) differing in sensitivity to drought were soaked in fresh cultures of bacterial isolates and the PGRs (salicylic acid and putrescine) were sprayed at 150 mg/L on seedlings at three leaf stage. PGPR and PGRs treated plants showed significant increase in the contents of chlorophyll, sugar and protein even under harsh environmental conditions. Drought stress enhanced the production of proline, antioxidant enzymes and lipid peroxidation but a decrease was noted in the biochemical content (i.e. chlorophyll, protein and sugar) of inoculated plants. PGPR inoculation also significantly enhanced the yield parameters (i.e. plant height, spike length, grain yield and weight) and improved the fertility status of sandy soil. The accumulation of macronutrient, total NO3-N and P concentration and soil moisture content of rhizosphere soil was also enhanced by PGPRs inoculation. It is concluded that the combined effects of PGPR and PGRs have profound effects on the biochemical responses and drought tolerance of wheat grown in sandy soils.

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

Access this article

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

Similar content being viewed by others

References

  • Abbas T, Balal RM, Shahid MA, Pervez MA, Ayyub CM, Aqueel MA, Javaid MM (2015) Silicon-induced alleviation of NaCl toxicity in okra (Abelmoschus esculentus) is associated with enhanced photosynthesis, osmoprotectants and antioxidant metabolism. Acta Physiol Plant 37(2):1–15. https://doi.org/10.1007/s11738-014-1768-5

    Article  CAS  Google Scholar 

  • Abdi G, Mohammadi M, Hedayat M (2011) Effect of salicylic acid on Na+ accumulation in shoot and roots of tomato in different K+ status. J Biol Environ Sci 5(13)

  • Adesemoye AO, Egamberdieva D (2013) Beneficial effects of plant growth-promoting rhizobacteria on improved crop production: prospects for developing economies. Bacteria in agrobiology: Crop productivity. Springer, Berlin, Heidelberg, pp 45–63

    Chapter  Google Scholar 

  • Arfan M, Athar HR, Ashraf M (2007) Does exogenous application of salicylic acid through the rooting medium modulate growth and photosynthetic capacity in two differently adapted spring wheat cultivars under salt stress? J Plant Physiol 164(6):685–694. https://doi.org/10.1016/j.jplph.2006.05.010

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Takahashi M (1987) Production and scavenging of active oxygen in photosynthesis. In: Kyle DJ, Osmond CB, Arntzen CJ (eds) Photoinhibition. Elsevier, Amsterdam, pp 227–287

    Google Scholar 

  • Barka EA, Nowak J, Clément C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72(11):7246–7252. https://doi.org/10.1128/AEM.01047-06

    Article  CAS  Google Scholar 

  • Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000Res. A. https://doi.org/10.12688/f1000research.7678.1

    Article  Google Scholar 

  • Bates LS, Waldern TID (1983) Rapid determination of free proline for water stress studies. Plant Soil 39:205–297. https://doi.org/10.1007/BF00018060

    Article  Google Scholar 

  • Borsani O, Valpuesta V, Botella MA (2001) Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiol 126(3):1024–1030

    Article  CAS  Google Scholar 

  • Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59(1):39–46

    Article  CAS  Google Scholar 

  • Cag S, Cevahir-Oz G, Sarsag M, Goren-Saglam N (2009) Effect of salicylic acid on pigment, protein content and peroxidase activity in excised sunflower cotyledons. Pak J Bot 41(5):2297–2303

    CAS  Google Scholar 

  • Cappuccino JG, Sherman N (1992) Serial dilution agar plating procedure to quantitate viable cells. Microbiology: a laboratory manual, 3rd edn. The Benjamin Cummings Publishing Co., Inc, Bedwood, pp 77–82

    Google Scholar 

  • Chandlee JM, Scandalios JG (1984) Analysis of variants affecting the catalase developmental program in maize scutellum. Theor Appl Genet 69:71–77. https://doi.org/10.1007/BF00262543

    Article  CAS  PubMed  Google Scholar 

  • Chen WP, Kuo TT (1993) A simple and rapid method for the preparation of Gram –ve bacterial genomic DNA. Nucleic acid Res 21:2260

    Article  CAS  Google Scholar 

  • Chen Q, Zhang M, Shen S (2011) Effect of salt on malondialdehyde and antioxidant enzymes in seedling roots of Jerusalem artichoke (Helianthus tuberosus L.). Acta Physiol Plant 33:273–278. https://doi.org/10.1007/s11738-010-0543-5

    Article  CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379

    Article  CAS  Google Scholar 

  • Dube DH, Bertozzi CR (1956) Glycans in cancer and inflammation—potential for therapeutics and diagnostics. Nat Rev Drug Discov 4:477–488. https://doi.org/10.1038/nrd1751

    Article  CAS  Google Scholar 

  • Fariduddin Q, Hayat S, Ahmad A (2003) Salicylic acid influences net photosynthetic rate, carboxylation efficiency, nitrate reductase activity, and seed yield in Brassica juncea. Photosynthesis 41(2):281–284. https://doi.org/10.1023/B:PHOT.0000011962.05991.6c

    Article  CAS  Google Scholar 

  • Farooq M, Aziz T, Hussain M, Rehman H, Jabran K, Khan MB (2008) Glycinebetaine improves chilling tolerance in hybrid maize. J Agron Crop Sci 194:152–160. https://doi.org/10.1111/j.1439-037X.2008.00295.x

    Article  CAS  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. In: Sustainable agriculture. Springer Netherlands, pp 153–188. https://link.springer.com/chapter/10.1007%2F978-90-481-2666-8_12

  • Gorin N, Heidema FT (1976) Peroxidase activity in Golden Delicious apples as a possible parameter of ripening and senescence. J Agric Food Chem 24:200–201. https://doi.org/10.1080/07352680701572966

    Article  CAS  PubMed  Google Scholar 

  • Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113(1–4):17–35

    Article  Google Scholar 

  • Government of Pakistan. Agricultural statistics of Pakistan (2011)

  • Grover M, Ali SZ, Sandhya V, Rasul A, Venkateswarlu B (2010) Role of microorganisms in adaptation of agriculture crops to abiotic stress. World J Microbiol Biotechnol 27:1231–1240. https://doi.org/10.1007/s11274-010-0572-7

    Article  Google Scholar 

  • Idowu KM, Adote Aduayi E (2007) Sodium-potassium interaction on growth, yield and quality of tomato in ultisol. J Plant Interact 2(4):263–271

    Article  CAS  Google Scholar 

  • Jafar MS, Slam MH, Amir AS, Ghorban N, Ghasem Z (2007) The effects of water deficitduring growth stages of canola (Brassiccanapus L). American-Eurasian J Agric Environ Sci 2(4):417–422

    Google Scholar 

  • Jaleel CA, Manivannan P, Sankar B, Kishorekumar A, Gopi R, Somasundaram R, Panneerselvam R (2007) Pseudomonas fluorescens enhances biomass yield and ajmalicine production in Catharanthus roseus under water deficit stress. Colloids Surf B Biointerfaces 60(1):7–11. https://doi.org/10.1016/j.colsurfb.2007.05.012

    Article  CAS  PubMed  Google Scholar 

  • Jaleel CA, Manivannan P, Wahid A, Farooq M, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105

    Google Scholar 

  • Karlidag H, Yildirim E, Turan M, Pehluvan M, Donmez F (2013) Plant growth-promoting rhizobacteria mitigate deleterious effects of salt stress on strawberry plants (Fragaria ×ananassa). Hortscience 48(5):563–567

    Article  CAS  Google Scholar 

  • Khalid A, Arshad M, Zahir ZA (2004) Screening plant growth promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96(3):473–480. https://doi.org/10.1046/j.1365-2672.2003.02161.x

    Article  CAS  PubMed  Google Scholar 

  • Khan N, Bano A (2016a) Role of plant growth promoting rhizobacteria and Ag-nano particle in the bioremediation of heavy metals and maize growth under municipal wastewater irrigation. Int J Phytoremediation 18:211–221. https://doi.org/10.1080/15226514.2015.1064352

    Article  CAS  PubMed  Google Scholar 

  • Khan N, Bano A (2016b) Modulation of phytoremediation and plant growth by the treatment of PGPR, Ag nanoaprticle and untreated municipal wastewater. Int J Phytoremediation 18:1258–1269. https://doi.org/10.1080/15226514.2016.1203287

    Article  CAS  PubMed  Google Scholar 

  • Khan N, Bano A, Babar MA (2017) The root growth of wheat plants, the water conservation and fertility status of sandy soils influenced by plant growth promoting rhizobacteria. Symbiosis 72(3):195–205

    Article  CAS  Google Scholar 

  • Khan N, Bano A, Zandi P (2018) Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. J Plant Interact 13(1):239–247

    Article  CAS  Google Scholar 

  • Khan N, Bano A, Rahman MA, Rathinasabapathi B, Babar MA (2019a) UPLC-HRMS-based untargeted metabolic profiling reveals changes in chickpea (Cicer arietinum) metabolome following long-term drought stress. Plant Cell Environ 42(1):115–132

    Article  CAS  Google Scholar 

  • Khan N, Bano A, Rahman MA, Guo J, Kang Z, Babar MA (2019b) Comparative physiological and metabolic analysis reveals a complex mechanism involved in drought tolerance in chickpea (Cicer arietinum L.) induced by PGPR and PGRs. Sci Rep 9(1):2097

    Article  Google Scholar 

  • Kim YC, Leveau J, McSpadden Gardener BB, Pierson EA, Pierson LS, Ryu CM III (2011) The multifactorial basis for plant health promotion by plant associated bacteria. Appl Environ Microbiol 77:1548–1555. https://doi.org/10.1128/AEM.01867-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kohler J, Caravaca F, Roldán A (2009) Effect of drought on the stability of rhizosphere soil aggregates of Lactuca sativa grown in a degraded soil inoculated with PGPR and AM fungi. Appl Soil Ecol 42(2):160–165

    Article  Google Scholar 

  • Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703. https://doi.org/10.1038/178703a0

    Article  CAS  PubMed  Google Scholar 

  • Li QT, Yeo MH, Tan BK (2000) Lipid peroxidation in small and large phospholipid unilamellar vesicles induced by water-soluble free radical sources. Biochem Biophy Res Commun 273:72–76. https://doi.org/10.1006/bbrc.2000.2908

    Article  CAS  Google Scholar 

  • Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1(2):142–146

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265–275. http://devbio.wustl.edu/InfoSource/ISPDFs/Lowry%201951.pdf

  • MacFaddin (1980) Biochemical tests for identification of medical bacteria. Williams and Wilkins, Baltimore, pp 51–54

    Google Scholar 

  • Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42(6):565–572. https://doi.org/10.1016/j.plaphy.2004.05.009

    Article  CAS  PubMed  Google Scholar 

  • Mehboob I, Naveed M, Zahir Z (2009) Rhizobial association with non-legumes: mechanisms and applications. Crit Rev Plant Sci 28:432–456. https://doi.org/10.1080/07352680903187753

    Article  CAS  Google Scholar 

  • Meloni DA, Oliva MA, Ruiz HA, Martinez CA (2001) Contribution of proline and inorganic solutes to osmotic adjustment in cotton under salt stress. J Plant Nutr 24:599–612. https://doi.org/10.1081/PLN-100104983

    Article  CAS  Google Scholar 

  • Meloni DA, Oliva MA, Martinez CA, Cambraia J (2003) Photosynthesis and activity of superoxide dismutase, peroxidase and glutathione reductase in cotton under salt stress. Environ Exp Bot 28(1):69–76. https://doi.org/10.1016/S0098-8472(02)00058-8

    Article  Google Scholar 

  • Moghadam HRT, Zahedi H, Ghooshchi F (2011) Oil quality of canola cultivars in response to water stress and super absorbent polymer application. Pesq Agropec Trop Goiânia 41:579–586. https://doi.org/10.5216/pat.v41i4.13366

    Article  Google Scholar 

  • Muthukumar T, Udaiyan K, Rajeshkannan V (2013) Response of neem (Azdirachta indica A. juss) to indigenous arbuscular mycorrhizal fungi, phosphate solubilizing and symbiotic nitrogen fixing bacteria under tropical nursery conditions. Biol Fertil Soils 34:417–420. https://doi.org/10.1007/s00374-001-0425-5

    Article  CAS  Google Scholar 

  • Mylavarapu RS, Zinati GM (2009) Improvement of soil properties using compost for optimum parsley production in sandy soils. Sci Hortic 120(3):426–430

    Article  Google Scholar 

  • Naseem H, Ahsan M, Shahid MA, Khan N (2018) Exopolysaccharides producing rhizobacteria and their role in plant growth and drought tolerance. J Basic Microbiol 58(12):1009–1022

    Article  CAS  Google Scholar 

  • Navarro V, Villarreal M, Rojas G, Lozoya X (1996) Antimicrobial evaluation of some plants used in Mexican traditional medicine for the treatment of infectious diseases. J Ethnopharmacol 53(3):143–147. https://doi.org/10.1016/0378-8741(96)01429-8

    Article  CAS  PubMed  Google Scholar 

  • Nezamia A, Boroumand Rezazadehb Z, Hosseini A (2007) Effects of drought stress and defoliation on sunflower (Helianthus annuus) in controlled conditions. Desert 12(2):99–104

    Google Scholar 

  • Parfitt RL, Salt GJ, Hill LF (2002) Clear-cutting reduces nitrate leaching in a pine plantation of high natural N status. For Ecol Manage 170(1–3):43–53

    Article  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorous in soil in the connection with vital activity of some microbial species. Mikorobiology 17:362–370

    CAS  Google Scholar 

  • Rajasekaran LR, Blake TJ (1999) New plant growth regulators protect photosynthesis and enhance growth under drought of jack pine seedlings. J Plant Growth Regul 18(4):175–81

    Article  CAS  Google Scholar 

  • Rubio V, Bustos R, Irigoyen ML, Cardona-López X, Rojas-Triana M, Paz-Ares J (2009) Plant hormones and nutrient signaling. Plant Mol Biol 69(4):361–373. https://doi.org/10.1007/s11103-008-9380-y

    Article  CAS  PubMed  Google Scholar 

  • Sadasivam S, Manickam A (1992) Biochemical methods for agricultural sciences. Wiley eastern limited

  • Sairam RK, Rao KV, Srivastava GC (2002) Differential response of wheat genotypes to long term salinitystress in relation to oxidative stress, antioxidant activity and osmolyte concentration. Plant Sci 163(5):1037–1046

    Article  CAS  Google Scholar 

  • Saravanakumar A, Rajkumar M, Serebiah JS, Thivakaran GA (2008) Seasonal variations in physicochemical characteristics of water, sediment and soil texture in arid zone mangroves of Kachchh-Gujarat. J Environ Biol 29(5):725–732

    CAS  PubMed  Google Scholar 

  • Senthilraja G, Anand T, Kennedy JS, Raguchander T, Samiyappan R (2013) Plant growth promoting rhizobacteria (PGPR) and entomopathogenic fungus bioformulation enhance the expression of defense enzymes and pathogenesis-related proteins in groundnut plants against leafminer insect and collar rot pathogen. Physiol Mol Plant Pathol 82:10–19

    Article  CAS  Google Scholar 

  • Shah F, Huang J, Cui K, Nie L, Shah T, Chen C, Wang K (2011) Impact of high-temperature stress on rice plant and its traits related to tolerance. J Agric Sci 149(5):545–556

    Article  CAS  Google Scholar 

  • Shi Q, Bao Z, Zhu Z, Ying Q, Qian Q (2006) Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescens, and antioxidant enzyme activity in seedlings of Cucumis sativa L. Plant Growth Regul 48(2):127–135. https://doi.org/10.1007/s10725-005-5482-6

    Article  CAS  Google Scholar 

  • Singh RP, Jha PN (2017) The PGPR Stenotrophomonas maltophilia SBP-9 augments resistance against biotic and abiotic stress in wheat plants. Front Microbiol 8:1945

    Article  Google Scholar 

  • Singh B, Usha K (2003) Salicylic acid induced physiological and biochemical changes in wheat seedlings under water stress. Plant Growth Regul 39(2):137–141. https://doi.org/10.1023/A:1022556103536

    Article  CAS  Google Scholar 

  • Soltanpour PA, Schwab AP (1977) A new soil test for simultaneous extraction of macro- and micro-nutrients in alkaline soils. Commun Soil Sci Plant Anal 8(3):195–207

    Article  CAS  Google Scholar 

  • Steel KJ (1956) The oxidase reaction as a toxic tool. J Gen Microbiol 25:297–306

    Article  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signaling Behav 2(2):79–85

    Article  Google Scholar 

  • Ullah F, Bano A, Nosheen A (2012) Effects of plant growth regulators on growth and oil quality of canola (Brassica napus L.) under drought stress. J Bot 44:1873–1880. http://www.pakbs.org/pjbot/PDFs/44(6)/08.pdf

  • Upreti KK, Sharma M (2016) Role of plant growth regulators in abiotic stress tolerance. Abiotic stressphysiology of horticultural crops. Springer, New Delhi, pp 19–46

    Chapter  Google Scholar 

  • Walia H, Wilson C, Zeng L, Ismail AM, Condamine P, Close TJ (2007) Genome-wide transcriptional analysis of salinity stressed japonica and indica rice genotypes during panicle initiation stage. Plant Mol Biol 63(5):609–623

    Article  CAS  Google Scholar 

  • Washington JA, Sutter VL (1980) Dilution susceptibility test agar and micro broth dilution procedure. Annals of Clinical Microbiology, 3rd edn. American Society of Microbiology, Washington, DC, p 453

    Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) I6S-ribosomal DNA amplification for phylogenetic study. J Biotechnol 173:16–22. https://doi.org/10.1128/jb.173.2.697-703.1991

    Article  Google Scholar 

  • Wingler A, Roitsch T (2008) Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biol 10(S1):50–62. https://doi.org/10.1111/j.1438-8677.2008.00086.x

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Wang RG, Mao G, Koczan JM (2006) Identification of drought tolerance determinants by genetic analysis of root response to drought stress and abscisic acid. Plant Physiol 142(3):1065–1074

    Article  CAS  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53(1):247–273

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Naeem Khan.

Additional information

Communicated by Shuang-Jiang Liu.

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, N., Bano, A. & Babar, M.A. The stimulatory effects of plant growth promoting rhizobacteria and plant growth regulators on wheat physiology grown in sandy soil. Arch Microbiol 201, 769–785 (2019). https://doi.org/10.1007/s00203-019-01644-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-019-01644-w

Keywords

Navigation