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.
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
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
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
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
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
Basu S, Ramegowda V, Kumar A, Pereira A (2016) Plant adaptation to drought stress. F1000Res. A. https://doi.org/10.12688/f1000research.7678.1
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
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
Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59(1):39–46
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
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
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
Chen WP, Kuo TT (1993) A simple and rapid method for the preparation of Gram –ve bacterial genomic DNA. Nucleic acid Res 21:2260
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
Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379
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
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
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
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
Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113(1–4):17–35
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Kovacs N (1956) Identification of Pseudomonas pyocyanea by the oxidase reaction. Nature 178:703. https://doi.org/10.1038/178703a0
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
Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1(2):142–146
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
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
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
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
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
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
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
Mylavarapu RS, Zinati GM (2009) Improvement of soil properties using compost for optimum parsley production in sandy soils. Sci Hortic 120(3):426–430
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
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
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
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
Pikovskaya RI (1948) Mobilization of phosphorous in soil in the connection with vital activity of some microbial species. Mikorobiology 17:362–370
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
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
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
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
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
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
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
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
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
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
Steel KJ (1956) The oxidase reaction as a toxic tool. J Gen Microbiol 25:297–306
Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signaling Behav 2(2):79–85
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
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
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
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
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
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
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53(1):247–273
Author information
Authors and Affiliations
Corresponding author
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
About this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-019-01644-w