Abstract
Purpose
Application of beneficial microbes such as plant growth promoting rhizobacteria (PGPR) and endophytic fungi as bio-fertilizer may act as a substitute to minimize the utilization of chemical fertilizers, which often cause negative impacts on environment. In this regard, bio-fertilizer resurged as an alternate and eco-friendly technique for sustainable agriculture to improve crop growth and yield by the introduction of beneficial microorganisms in soil. Therefore, this experiment was designed to investigate whether the following microbial candidates, i.e., Enterobacter sp., Bacillus sp., and Piriformospora indica have the ability to influence growth of canola through uptake of nutrient and production of growth hormone.
Materials and methods
A pot experiment with three beneficial microorganisms such as Enterobacter sp., Bacillus sp., and a root endophytic fungus, P. indica, was conducted on two cultivars of canola (DGL and Punjab canola). The bacterial strain of Enterobacter sp. MN17 and Bacillus sp. MN54 (108 bacteria per seed) were applied individually as well as along with fungal strain (P. indica), and their impact was assessed against an uninoculated control treatment under normal soil condition.
Results and discussion
Results depicted that application of Enterobacter sp. MN17 and Bacillus sp. MN54 with P. indica significantly increased growth, physiological attributes, nutrient uptake, and soil microbiological attributes of canola. In particular, treatment MN54 + P. indica showed highest improvement in shoot biomass, stem diameter, and root length 100%, 65%, and 50% respectively in var. DGL, while increase in number of pods per plant was also recorded for treatment MN17 + P. indica and MN54 + P. indica for DGL (63%) and Punjab Canola (73%), respectively, as compared to control plants. The combined inoculation also increased root or/and shoot nutrient uptake and enhanced plant auxin pool. Therefore, colonization of P. indica and microbial strain, especially Bacillus sp., improves plant health by enhancing root proliferation because of upregulation of auxin producing genes and release of organic acids, respectively, which leads to better nutrient uptake and eventually enhanced crop growth.
Conclusion
Our results proposed that inoculation of Bacillus sp. MN54 with P. indica could be exploited to increase crop growth and seed yield through enhanced nutrient uptake and production of plant growth hormones.
Similar content being viewed by others
References
Abbas T, Zahir ZA, Naveed M, Abbas S, Alwahibi MS, Elshikh MS, Mustafa A (2020) Large scale screening of rhizospheric allelopathic bacteria and their potential for the biocontrol of wheat-associated weeds. Agronomy 10(10):1469
Ahmad F, Ahmad I, Khan M (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181
Ahmad M, Naseer I, Hussain A, Zahid MM, Mustafa A, Hilger TH, Minggang X (2019) Appraising endophyte–plant symbiosis for improved growth, nodulation, nitrogen fixation and abiotic stress tolerance: an experimental investigation with chickpea (Cicer arietinum L.). Agronomy 9(10):621
Ahmad M, Wang X, Hilger TH, Luqman M, Nazli F, Hussain A, Mustafa A (2020) Evaluating biochar-microbe synergies for improved growth, yield of maize, and post-harvest soil characteristics in a semi-arid climate. Agronomy 10(7):1055
Akinrinlola RJ, Yuen GY, Drijber RA, Adesemoye AO (2018) Evaluation of Bacillus strains for plant growth promotion and predictability of efficacy by in vitro physiological traits. Int J Microbiol 2018:1–11
Ali MA, Naveed M, Mustafa A, Abbas A (2017) The good, the bad, and the ugly of rhizosphere microbiome. Probiotics and plant health. Springer, Singapore, pp 253–290
American Association of Cereal Chemists (2000) Approved methods of the american association of cereal chemists, 10th Edn. St. Paul, MN, USA
Asghar H, Zahir Z, Arshad M (2004) Screening rhizobacteria for improving the growth, yield, and oil content of canola (Brassica napus L.). Aust J Agric Res 55:187–194
Ashraf MN, Jusheng G, Lei W, Mustafa A, Waqas A, Aziz T, Khan WUD, Hussain B, Farooq M, Wenju Z, Minggang X (2021) Soil microbial biomass and extracellular enzyme–mediated mineralization potentials of carbon and nitrogen under long-term fertilization (> 30 years) in a rice–rice cropping system. J Soils Sediments 21(12):3789–3800
Aziz MZ, Yaseen M, Naveed M, Wang X, Fatima K, Saeed Q, Mustafa A (2020) Polymer-Paraburkholderia phytofirmans PsJN coated diammonium phosphate enhanced microbial survival, phosphorous use efficiency, and production of wheat. Agronomy 10(9):1344
Bagde US, Prasad R, Varma A (2011) Influence of culture filtrate of Piriformospora indica on growth and yield of seed oil in Helianthus annus. Symbiosis 53:83–88
Basurto-Cadena MGL, Vázquez-Arista M, García-Jiménez J, Salcedo-Hernández R, Bideshi DK, Barboza-Corona JE (2012) Isolation of a new Mexican strain of Bacillus subtilis with antifungal and antibacterial activities. Sci World J 2012:1–7
Bertramson B (1942) Phosphorus analysis of plant material. Plant Physiol 17:447–454
Bhandari G (2014) An overview of agrochemicals and their effects on environment in nepal. Appl Ecol Environ Sci 2:66–73
Bharathi R, Vivekananthan R, Harish S, Ramanathan A, Samiyappan R (2004) Rhizobacteria-based bio-formulations for the management of fruit rot infection in chillies. Crop Prot 23:835–843
Borriss R (2011) Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents in agriculture. In: Maheshwari DK (ed) Bacteria in agrobiology: Plant growth responses. Springer, New York, pp 41–76
Chen J (2006) The combined use of chemical and organic fertilizers and/or biofertilizer for crop growth and soil fertility. In International workshop on sustained management of the soil-rhizosphere system for efficient crop production and fertilizer use. Land Development Department. Bangkok, Thailand
Dixit VK, Misra S, Mishra SK, Tewari SK, Joshi N, Chauhan PS (2020) Characterization of plant growth-promoting alkalotolerant Alcaligenes and Bacillus strains for mitigating the alkaline stress in Zea mays. Antonie Van Leeuwenhoek 113(7):889–905
Dolatabadi HK, Goltapeh EM, Jaimand K, Rohani N, Varma A (2011) Effects of Piriformospora indica and Sebacina vermifera on growth and yield of essential oil in fennel (Foeniculum vulgare) under greenhouse conditions. J Basic Microbiol 51(1):33–39
Dong SQ, Tian ZH, Chen PJ, Kumar RS, Shen CH, Cai DG, Oelmüller R, Yeh KW (2013) The maturation zone is an important target of Piriformospora indica in Chinese cabbage roots. J Exp Bot 64:4529–4540
El-Nagdy G, Nassar DM, El-Kady EA, El-Yamanee GS (2010) Response of flax plant Linum usitatissimum L. to treatments with mineral and bio-fertilizers from nitrogen and phosphorus. J Am Sci 6:207–217
Ferreira MJ, Silva H, Cunha A (2019) Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: a review. Pedosphere 29:409–420
Godfray HCJ, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327:812–818
Goswami D, Thakker JN, Dhandhukia PC (2016) Portraying mechanics of plant growth promoting rhizobacteria (PGPR): a review. Cogent Food Agric 2(1):1–19
Hazirah HM, Noraini J, Naim MK, Norhanani A (2017) Effect of Bacillus subtilis as plant beneficial bacteria on growth performance of pegaga (Centella asiatica). Biosci Res 14:1074–1079
Hong Y, Devaiah SP, Bahn SC, Thamasandra BN, Li M, Welti R, Wang X (2009) Phospholipase Dε and phosphatidic acid enhance arabidopsis nitrogen signaling and growth. Plant J 58(3):76–387
Idris A, Labuschagne N, Korsten L (2009) Efficacy of rhizobacteria for growth promotion in sorghum under greenhouse conditions and selected modes of action studies. J Agric Sci 147:17–30
Iqbal M, Habib-ur-Rehman A, Muhammad I, Javed M, Zafar ZU, Ashraf M (2019) Leaf proteome analysis signified that photosynthesis and antioxidants are key indicators of salinity tolerance in canola (Brassica napus L.). Pak J Bot 51(6):1955–1968
Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the kEC value. Soil Biol Biochem 28(1):25–31
Júnior RFG, Pedrinho EAN, Castellane TCL, Lemos EGDM (2011) Auxin-producing bacteria isolated from the roots of Cattleya walkeriana, an endangered Brazilian orchid, and their role in acclimatization. Rev Bras Ciên Solo 35(3):729–737
Justice AH, Faust JE, Kerrigan JL (2018) Evaluating a novel method to introduce a mycorrhizal-like fungus, Piriformospora indica, via an inoculated rooting substrate to improve adventitious root formation. HortTechnology 28(2):149–153
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
Khan AAH, Naseem RL, Prathibha B (2011) Screening and potency evaluation of antifungal from soil isolates of Bacillus subtilis on selected fungi. Adv Biotechol 10(7):35–37
Khan N (2020) Plant-microbial interactions and their role in sustainable agriculture and sustainability of agriculture soils. Recent Pat Food Nutr Agric 11(2):94–95
Khan N, Bano A (2019) Exopolysaccharide producing rhizobacteria and their impact on growth and drought tolerance of wheat grown under rainfed conditions. PLoS ONE 14(9):e0222302
Khan N, Bano A, Babar MA (2019) The stimulatory effects of plant growth promoting rhizobacteria and plant growth regulators on wheat physiology grown in sandy soil. Arch Microbiol 201(6):769–785
Khan N, Bano A, Curá JA (2020) Role of beneficial microorganisms and salicylic acid in improving rainfed agriculture and future food safety. Microorganisms 8(7):1018
Kjeldahl C (1883) A new method for the determination of nitrogen in organic matter. Z Anal Chem 22:366–382
Kumar M, Mishra S, Dixit V, Kumar M, Agarwal L, Chauhan PS, Nautiyal CS (2016) Synergistic effect of Pseudomonas putida and Bacillus amyloliquefaciens ameliorates drought stress in chickpea (Cicer arietinum L.). Plant Signal Behav 11(1):e1071004
Kumar M, Yadav V, Tuteja N, Johri AK (2009) Antioxidant enzyme activities in maize plants colonized with Piriformospora indica. Microbiology 155:780–790
Kumar S, Sindhu SS, Kumar R (2021) Biofertilizers: an ecofriendly technology for nutrient recycling and environmental sustainability. Curr Res Microbiol 3:100094
Li B, Chen Y, Liang WZ, Mu L, Bridges WC, Jacobson AR, Darnault CJ (2017) Influence of cerium oxide nanoparticles on the soil enzyme activities in a soil-grass microcosm system. Geoderma 299:54–62
Li J, Yang Q, Zhao L, Zhang S, Wang Y, Zhao X (2009) Purification and characterization of a novel antifungal protein from Bacillus subtilis strain B29. J Zhejiang Univ Sci B 10(4):264–272
Mazoyer M, Roudart L (2006) A history of world agriculture: from the neolithic age to the current crisis. Monthly review press, New York
Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microbiol Ecol 51:326–335
Merino C, Godoy R, Matus F (2016) Soil enzymes and biological activity at different levels of organic matter stability. J Soil Sci Plant Nutr 16:14–30
Mustafa A, Naveed M, Abbas T, Saeed Q, Hussain A, Ashraf MN, Minggang X (2019a) Growth response of wheat and associated weeds to plant antagonistic rhizobacteria and fungi. Italian J Agron 14(4):191–198
Mustafa A, Naveed M, Saeed Q, Ashraf MN, Hussain A, Abbas T, Minggang X (2019b) Application potentials of plant growth promoting rhizobacteria and fungi as an alternative to conventional weed control methods. In: Sustainable Crop Production. IntechOpen
Nakkeeran S, Fernando WD, Siddiqui ZA (2005) Plant growth promoting rhizobacteria formulations and its scope in commercialization for the management of pests and diseases. Pgpr. Biocontrol and biofertilization.Springer, Dordrecht, pp 257–296
Nautiyal CS, Chauhan PS, DasGupta SM, Seem K, Varma A, Staddon WJ (2010) Tripartite interactions among Paenibacillus lentimorbus NRRL B-30488, Piriformospora indica DSM 11827, and Cicer arietinum L. World J Microbiol Biot 26:1393–1399
Nazli F, Mustafa A, Ahmad M, Hussain A, Jamil M, Wang X, El-Esawi MA (2020) A review on practical application and potentials of phytohormone-producing plant growth-promoting rhizobacteria for inducing heavy metal tolerance in crops. Sustainability 12(21):9056
Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33:197
Peskan-Berghofer T, Shahollari B, Giong PH et al (2004) Association of Piriformospora indica with Arabidopsis thaliana roots represents a novel system to study beneficial plant–microbe interactions and involves early plant protein modifications in the endoplasmic reticulum and at the plasma membrane. Physiol Plant 122:465–477
Pirttilä AM, Mohammad Parast Tabas H, Baruah N, Koskimäki JJ (2021) Biofertilizers and biocontrol agents for agriculture: How to identify and develop new potent microbial strains and traits. Microorganisms 9(4):817
Rafique M, Naveed M, Mustafa A et al (2021) The combined effects of gibberellic acid and rhizobium on growth, yield and nutritional status in chickpea (Cicer arietinum L.). Agronomy 11(1):105
Rai M, Acharya D, Singh A, Varma A (2001) Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. Mycorrhiza 11:123–128
Saeed Q, Xiukang W, Haider FU, Kučerik J, Mumtaz MZ, Holatko J, Naseem M, Kintl A, Ejaz M, Naveed M, Brtnicky M (2021) Rhizosphere bacteria in plant growth promotion, biocontrol, and bioremediation of contaminated sites: a comprehensive review of effects and mechanisms. Int J Mol Sci 22(19):10529
Saeed Z, Naveed M, Imran M, Bashir MA, Sattar A, Mustafa A, Xu M (2019) Combined use of Enterobacter sp. MN17 and zeolite reverts the adverse effects of cadmium on growth, physiology and antioxidant activity of Brassica napus. PLoS ONE 14(3):e0213016
Sanaullah M, Blagodatskaya E, Chabbi A, Rumpel C, Kuzyakov Y (2011) Drought effects on microbial biomass and enzyme activities in the rhizosphere of grasses depend on plant community composition. Appl Soil Ecol 48:38–44
Sandhya VSKZ, Ali SZ, Grover M, Reddy G, Venkateswarlu B (2010) Effect of plant growth promoting Pseudomonas spp. on compatible solutes, antioxidant status and plant growth of maize under drought stress. Plant Growth Regul 62(1):21–30
Sarwar M, Arshad M, Martens DA, Frankenberger W (1992) Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147:207–215
Shameer S, Prasad TNVKV (2018) Plant growth promoting rhizobacteria for sustainable agricultural practices with special reference to biotic and abiotic stresses. Plant Growth Regul 84(3):603–615
Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmuller R (2005a) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem 280:26241–26247
Sherameti I, Shahollari B, Venus Y, Altschmied L, Varma A, Oelmüller R (2005b) The endophytic fungus Piriformospora indica stimulates the expression of nitrate reductase and the starch-degrading enzyme glucan-water dikinase in tobacco and Arabidopsis roots through a homeodomain transcription factor that binds to a conserved motif in their promoters. J Biol Chem 280(28):26241–26247
Singh A, Sharma J, Rexer KH, Varma A (2000) Plant productivity determinants beyond minerals, water and light. Piriformospora indica: a revolutionary plant growth promoting fungus. Curr Sci 79:101–106
Singh G, Biswas D, Marwaha T (2010) Mobilization of potassium from waste mica by plant growth promoting rhizobacteria and its assimilation by maize (Zea mays) and wheat (Triticum aestivum L.): A hydroponics study under phytotron growth chamber. J Plant Nutr 33:1236–1251
Steel RG, Torrie JH, Dicky DA (1997) Principles and procedures of statistics: a biometrical approach, 2nd edn. McGraw-Hill Book Co, New York
Su ZZ, Wang T, Shrivastava N, Chen YY, Liu X, Sun C, Lou BG (2017) Piriformospora indica promotes growth, seed yield and quality of Brassica napus L. Microbiol Res 199:29–39
Umar W, Ayub MA, Rehman MZ, Ahmad HR, Farooqi ZUR, Shahzad A, Nadeem M (2020) Nitrogen and phosphorus use efficiency in agroecosystems. Resources Use Efficiency in Agriculture. Springer, Singapore, pp 213–257
Unnikumar K, Sree KS, Varma A (2013) Piriformospora indica: a versatile root endophytic symbiont. Symbiosis 60:107–113
Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and Piriformospora indica Mol Plant. Microbe 21:1371–1383
Van Aarle IM, Plassard C (2010) Spatial distribution of phosphatase activity associated with ectomycorrhizal plants is related to soil type. Soil Biol Biochem 4:324–330
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707
Varma A, Rai M, Sudha N, Sahay N (2000) Microbial biotechnology: new paradigms and role in sustainable agriculture. Microbial biotechnology for sustainable development and productivity. Scientific Publishers, India, pp 22–37
Varma A, Verma S, Sudha Sahay NS, Bütehorn B, Franken P (1999) Piriformospora indica, a cultivable plant growth promoting root endophyte. Appl Environ Microbiol 65:2741–2744
Wagi S, Ahmed A (2019) Bacillus spp.: potent microfactories of bacterial IAA. PeerJ 7:e7258
Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hukelhoven R, Neumann C, von Wettstein V, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proc Natl Acad Sci USA 102:13386–13391
Wolf B (1982) A comprehensive system of leaf analyses and its use for diagnosing crop nutrient status. Commun Soil Sci Plant Anal 13:1035–1059
Yadav AK, Chandra K (2014) Mass production and quality control of microbial inoculants. Proc Indian Natn Sci Acad 80(2):483–489
Yadav V, Kumar M, Deep DK, Kumar H, Sharma R, Tripathi T, Tuteja N, Saxena AK, Johri AK (2010) A phosphate transporter from the root endophytic fungus Piriformospora indica plays a role in phosphate transport to the host plant. J Biol Chem 285:26532–26544
Yang A, Akhtar SS, Iqbal S, Amjad M, Naveed M, Zahir ZA, Jacobsen SE (2016) Enhancing salt tolerance in quinoa by halotolerant bacterial inoculation. Func Plant Biol 43:632–664
Funding
The work was supported by the project of Ministry of Education, Youth and Sports of the Czech Republic, grant number FCH-S-22–8001. The financial assistance was provided by Environment Science Lab., Soil Environmental Bio-Geochemistry Lab., Institute of Soil & Environmental Sciences, and University of Agriculture Faisalabad, Pakistan, to conduct this study.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible editor: Dulce Flores-Rentería
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Iqbal, M., Naveed, M., Sanaullah, M. et al. Plant microbe mediated enhancement in growth and yield of canola (Brassica napus L.) plant through auxin production and increased nutrient acquisition. J Soils Sediments 23, 1233–1249 (2023). https://doi.org/10.1007/s11368-022-03386-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-022-03386-7