Skip to main content

Advertisement

Log in

Deciphering distinct biological control and growth promoting potential of multi-stress tolerant Bacillus subtilis PM32 for potato stem canker

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Plant growth-promoting rhizobacteria (PGPR) represent a set of microorganisms that play significant role in improving plant growth and controlling the phytopathogens. Unpredictable performance after the application of PGPR has been observed when these were shifted from in-vitro to in-vivo conditions due to the prevalence of various abiotic stress conditions. During growing period, the potato crop is subjected to a combination of biotic and abiotic stresses. Rhizoctonia solani, a soil-borne plant pathogen, causes reduced vigor and yield of potato crop worldwide. In the current study, multi-stress-tolerant rhizobacterial strain, Bacillus subtilis PM32, was isolated from field-grown potato with various plant growth promoting (PGP) traits including zinc and potassium solubilization, biological nitrogen fixation, ammonia and siderophore, as well as extracellular enzyme productions (cellulase, catalase, amylase, protease, pectinase, and chitinase). The strain PM32 exhibited a distinct potential to support plant growth by demonstrating production of indole-3-acetic acid (102.6 μM/mL), ACC-deaminase activity (1.63 μM of α-ketobutyrate/h/mg protein), and exopolysaccharides (2.27 mg/mL). By retarding mycelial growth of R. solani the strain PM32 drastically reduced pathogenicity of R. solani. The strain PM32 also suppressed the pathogenic activity significantly by impeding mycelial expansion of R. solani with inhibition co-efficient of 49.87. The B. subtilis PM32 also depicted significant tolerance towards salt, heavy metal (Pb), heat and drought stress. PCR based amplification of ituC and acds genes coding for iturin and ACC-deaminase activity respectively indicated potential of strain PM32 for lipopeptides production and ACC deaminase enzyme activity. Results of both in-vitro and pot experiments under greenhouse conditions depicted the efficiency of B. subtilis PM32 as a promising bio-control agent for R. solani infection together with enhanced growth of potato plants as deciphered from biomass accumulation, chlorophyll a, b, and carotenoid contents. Therefore, it was envisioned that application of indigenous multi-stress tolerant PGPR may serve to induce biotic and abiotic stress tolerance in crops/plants for pathogen control and sustainable global food supply.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Afridi MS, Mahmood T, Salam A, Mukhtar T, Mehmood S, Ali J, Khatoon Z, Bibi M, Javed MT, Sultan T, Chooudhary HJ (2019) Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: Involvement of ACC deaminase and antioxidant enzymes. Plant Physiol Biochem 139:569–577

    Article  CAS  PubMed  Google Scholar 

  • Afridi MS, Van Hamme JD, Bundschuh J, Khan MN, Salam A, Waqar M, Chaudhary HJ (2021) Biotechnological approaches in agriculture and environmental management-bacterium Kocuria rhizophila 14ASP as heavy metal and salt-tolerant plant growth-promoting strain. Biologia 76:3091–3105

    Article  CAS  Google Scholar 

  • Ahmad I, Akhtar MJ, Mehmood S, Akhter K, Tahir M, Saeed MF, Hussain S (2018) Combined application of compost and Bacillus sp. CIK-512 ameliorated the lead toxicity in radish by regulating the homeostasis of antioxidants and lead. Ecotoxicol Environ Saf 148:805–812

    Article  CAS  PubMed  Google Scholar 

  • Ahmed OB, Asghar AH, Elhassan MM (2014) Comparison of three DNA extraction methods for polymerase chain reaction (PCR) analysis of bacterial genomic DNA. Afr J Microbiol Res 8(6):598–602

    Article  CAS  Google Scholar 

  • Ali SZ, Sandhya V, Grover M, Kishore N, Rao LV, Venkateswarlu B (2009) Pseudomonas sp. strain AKM-P6 enhances tolerance of sorghum seedlings to elevated temperatures. Biol Fert Soil 46:45–55

    Article  CAS  Google Scholar 

  • Ali SZ, Sandhya V, Rao LV (2014) Isolation and characterization of drought-tolerant ACC deaminase and exopolysaccharide-producing fluorescent Pseudomonas sp. Ann Microbiol 64(2):493–502

    Article  CAS  Google Scholar 

  • Ali S, Hameed S, Shahid M, Iqbal M, Lazarovits G, Imran A (2020) Functional characterization of potential PGPR exhibiting broad-spectrum antifungal activity. Microbiol Res 232:126389

    Article  CAS  PubMed  Google Scholar 

  • Ali J, Ali F, Ahmad I, Rafique M, Munis MFH, Hassan SW, Chaudhary HJ (2021) Mechanistic elucidation of germination potential and growth of Sesbania sesban seedlings with Bacillus anthracis PM21 under heavy metals stress: An in vitro study. Ecotoxicol Environ Saf 208:111769

    Article  CAS  PubMed  Google Scholar 

  • Amna XY, Farooq MA, Javed MT, Kamran MA, Mukhtar T, Ali J, Tabassumf T, Rehmang S, Munis MFH, Sultan T, Chaudhary HJ (2020) Multi-stress tolerant PGPR Bacillus xiamenensis PM14 activating sugarcane (Saccharum officinarum L.) red rot disease resistance. Plant Physiol Biochem 151:640–649

    Article  CAS  PubMed  Google Scholar 

  • Amna, Din BU, Sarfraz S, Xia Y, Kamran MA, Javed MT, Sultan T (2019) Mechanistic elucidation of germination potential and growth of wheat inoculated with exopolysaccharide and ACC-deaminase producing Bacillus strains under induced salinity stress. Ecotoxicol Environ Saf, 183:109466

  • Amna, Mahmood T, Khan UN, Amin B, Javed MT, Mehmood S, Farooq MA, Chaudhary HJ (2021) Characterization of bio‐fabricated silver nanoparticles for distinct anti‐fungal activity against sugarcane phytopathogens. Microsc Res Tech, https://doi.org/10.1002/jemt.23708

  • Arora NK, Fatima T, Mishra J, Mishra I, Verma S, Verma R (2020) Halo-tolerant plant growth promoting rhizobacteria for improving productivity and remediation of saline soils. J Adv Res 26:69–82

    Article  CAS  Google Scholar 

  • Batool R, Rehman SU, Rafique M, Amna Ali J, Mukhtar T, Mahmood S, Sultan T, Munis FH, Chaudhary HJ (2019) Biocontrol potential of Bacillus gibsonii and Brevibacterium frigoritolerans in suppression of Fusarium stalk rot of maize: a sustainable approach. Asian J Agric Biol 7:320–333

    Google Scholar 

  • Bhatt P, Sharma A, Rene ER, Kumar AJ, Zhang W, Chen S (2021) Bioremediation of fipronil using Bacillus sp. FA3: Mechanism, kinetics and resource recovery potential from contaminated environments. J Water Process Eng 39:101712

    Article  Google Scholar 

  • Bibi F, Yasir M, Al-Sofyani A, Naseer MI, Azhar EI (2020) Antimicrobial activity of bacteria from marine sponge Suberea mollis and bioactive metabolites of Vibrio sp. EA348. Saudi J Biol Sci 4:1139–1147

    Article  CAS  Google Scholar 

  • Bokhari N, Siddiqui I, Perveen K, Siddique I, Soliman D (2015) Mycocidal ability of Toona ciliata against Rhizoctonia salani. Janimal Plant Sci 25:1477–1481

    CAS  Google Scholar 

  • Bonanomi G, Lorito M, Vinale F, Woo SL (2018) Organic amendments, beneficial microbes, and soil microbiota: toward a unified framework for disease suppression. Ann Rev Phytopathol 56:1–20

    Article  CAS  Google Scholar 

  • Cao Y, Xu Z, Ling N, Yuan Y, Yang X, Chen L, Shen B, Shen Q (2012) Isolation and identification of lipopeptides produced by B. subtilis SQR 9 for suppressing Fusarium wilt of cucumber. Sci Hortic 135:32–39

    Article  CAS  Google Scholar 

  • Chávez-Ramírez B, Kerber-Díaz JC, Acoltzi-Conde MC, Ibarra JA, Vásquez-Murrieta MS, Estrada-de Los Santos P (2020) Inhibition of Rhizoctonia solani RhCh-14 and Pythium ultimum PyFr-14 by Paenibacillus polymyxa NMA1017 and Burkholderia cenocepacia CACua-24: a proposal for biocontrol of phytopathogenic fungi. Microbiol Re 230:126347

    Article  Google Scholar 

  • Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo JH (2013) Biocontrol of tomato wilt disease by B acillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15(3):848–864

    Article  PubMed  Google Scholar 

  • Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y, Zhang L (2017) Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 7:41564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Compant S, Brade G, Muzammil S, Sessitsch A, Mathieu LA, F, (2013) Use of beneficial bacteria and their secondary metabolites to control grapevine pathogen diseases. Biocontrol 58:435–455

    Article  Google Scholar 

  • Costa PBD, Granada CE, Ambrosini A, Moreira F, de Souza R, dos Passos JFM, Arruda L, Passaglia LMP (2014) A model to explain plant growth promotion traits: a multivariate analysis of 2211 bacterial isolates. PLoS ONE 9:116020

    Article  CAS  Google Scholar 

  • Cray JA, Houghton JD, Cooke LR, Hallsworth JE (2015) A simple inhibition coefficient for quantifying potency of biocontrol agents against plant-pathogenic fungi. Biocontrol 81:93–100

    Google Scholar 

  • Daami-Remadi M, Zammouri S, El-Mahjoub M (2008a) Effect of the level of seed tuber infection by Rhizoctonia solaniat planting on potato growth and disease severity. Afr J Plant Sci Biotechnol 2:34–38

    Google Scholar 

  • Daami-Remadi M, Zammouri S, El-Mahjoub M (2008b) Relative susceptibility of nine potato (Solanum tuberosum L.) cultivars to artificial and natural infection by Rhizoctonia solanias measured by stem canker severity, black scurf and plant growth. Afr J Plant Sci Biotechnol 2:57–66

    Google Scholar 

  • Dahala B, NandaKaflea G, Perkins L, Brözel VS (2017) Diversity of free-Living 519 nitrogen fixing Streptomyces in soils of the bad lands of South Dakota. Microbiol Res 195:31–39

    Article  CAS  Google Scholar 

  • Din BU, Rafique M, Javed MT, Kamran MA, Mehmood S, Khan M, Chaudhary HJ (2020) Assisted phytoremediation of chromium spiked soils by Sesbania Sesban in association with Bacillus xiamenensis PM14: a biochemical analysis. Plant Physiol Biochem 146:249–258

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Fang L, Ye Z, Zhu G, Lai Q, Liu S (2021) Screening of biocontrol bacteria against soft rot disease of Colocasia esculenta (L.) schott and its field application. PLoS ONE 16(7):e0254070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esfahani MN (2020) Genetic variability and virulence of some Iranian Rhizoctonia solani isolates associated with stem canker and black scurf of potato (Solanum tuberosum L.). J Plant Prot Res 60:21–30

    CAS  Google Scholar 

  • Ferreira CM, Soares HM, Soares EV (2019) Promising bacterial genera for agricultural practices: an insight on plant growth-promoting properties and microbial safety aspects. Sci Total Environ 682:779–799

    Article  CAS  PubMed  Google Scholar 

  • Ghosh S, Ghosh P, Maiti TK (2011) Production and metabolism of indole acetic acid (IAA) by root nodule bacteria (Rhizobium): a review. J Pure Appl Microbiol 5:523–540

    CAS  Google Scholar 

  • Glick BR (2020) Introduction to plant growth-promoting bacteria. In Beneficial plant-bacterial interactions. Springer, Cham

    Book  Google Scholar 

  • Gontia-Mishra I, Sapre S, Tiwari S (2017) Zinc solubilizing bacteria from the rhizosphere of rice as prospective modulator of zinc biofortification in rice. Rhizosphere 3:185–190

    Article  Google Scholar 

  • Gupta PK (2018) Toxicity of fungicides. In Veterinary toxicology. Academic Press, Cambridge

    Google Scholar 

  • Haidar R, Fermaud M, Calvo-Garrido C, Roudet J, Deschamps A (2016) Modes of action for biological control of Botrytis cinerea by antagonistic bacteria. Phytopathol Mediterr 55:301–322

    CAS  Google Scholar 

  • Huang Y, Zhang W, Pang S, Chen J, Bhatt P, Mishra S, Chen S (2020) Insights into the microbial degradation and catalytic mechanisms of chlorpyrifos. Environ Res 194:110660

    Article  PubMed  CAS  Google Scholar 

  • Hussain T, Khan AA (2020) Bacillus subtilis HussainT-AMU and its Antifungal activity against Potato Black scurf caused by Rhizoctonia solani on seed tubers. Biocatal Agric Biotechnol 23:101443

    Article  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  CAS  Google Scholar 

  • Kang Y, Carlson R, Tharpe W, Schell MA (1998) Characterization of genes involved in biosynthesis of a novel antibiotic from Burkholderia cepacia BC11 and their role in biological control of Rhizoctonia solani. Appl Environ Microbiol 64:3939–3947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keswani C, Singh HB, García-Estrada C, Caradus J, He YW, Mezaache-Aichour S (2020) Antimicrobial secondary metabolites from agriculturally important bacteria as next-generation pesticides. Appl Microbiol Biotechnol 104:1013–1034

    Article  CAS  PubMed  Google Scholar 

  • Khan AL, Halo BA, Elyassi A, Ali S, Al-Hosni K, Hussain J, Lee IJ (2016) Indole acetic acid and ACC deaminase from endophytic bacteria improves the growth of Solanum lycopersicum. Elec J Biotechnol 21:58–64

    Article  Google Scholar 

  • Khan N, Bano A, Ali S, Babar MA (2020) Crosstalk amongst phytohormones from planta and PGPR under biotic and abiotic stresses. Plant Growth and Reg 90:189–203

    Article  CAS  Google Scholar 

  • Lamichhane JR, You MP, Laudinot V, Barbetti MJ, Aubertot JN (2020) Revisiting Sustainability of Fungicide Seed Treatments for Field Crops. Plant Disease 104(3):610–623. https://doi.org/10.1094/PDIS-06-19-1157-FE

    Article  CAS  PubMed  Google Scholar 

  • Lucas JA (2020) Plant pathology and plant pathogens. Wiley, USA

    Google Scholar 

  • Lugtenberg BJ, Chin-A-Woeng TF, Bloemberg GV (2002) Microbe–plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383

    Article  CAS  PubMed  Google Scholar 

  • Mahmoud OMB, Hidri R, Talbi-Zribi O, Taamalli W, Abdelly C, Djébali N (2020) Auxin and proline producing rhizobacteria mitigate salt-induced growth inhibition of barley plants by enhancing water and nutrient status. S Afr J Bot 128:209–217

    Article  CAS  Google Scholar 

  • Maqbool S, Amna A, Mehmood S, Suhaib M, Sultan T, Munis MFH (2021) Interaction of Acc deaminase and antioxidant enzymes to induce drought tolerance in enterobacter Cloacae 2wc2 inoculated maize genotypes. Pak J Bot 53:3

    Article  Google Scholar 

  • Marulanda A, Porcel R, Barea JM, Azcón R (2007) Drought tolerance and antioxidant activities in lavender plants colonized by native drought-tolerant or drought-sensitive Glomus species. Microb Ecol 54(3):543

    Article  CAS  PubMed  Google Scholar 

  • Mehmood S, Khan AA, Shi F, Tahir M, Sultan T, Munis MFH, Chaudhary HJ (2021) Alleviation of salt stress in wheat seedlings via Multifunctional Bacillus aryabhattai PM34: an In-Vitro Study. Sustainability 13(14):8030

    Article  Google Scholar 

  • Mejdoub-Trabelsi B, Jabnoun-Khiareddine H, Daami-Remadi M (2012) Effect of Fusarium species and temperature of storage on the susceptibility ranking of potato cultivars to tuber dry rot. Pest Technol 6:41–46

    Google Scholar 

  • Moncada A, Miceli A, Vetrano F (2020) Use of plant growth-promoting rhizobacteria (PGPR) and organic fertilization for soilless cultivation of basil. Sci Hortic 275:109733

    Article  CAS  Google Scholar 

  • Muneer MA, Wang P, Zhang J, Li Y, Munir MZ, Ji B (2020a) Formation of common mycorrhizal networks significantly affect plant biomass and soil properties of the neighboring plants under various nitrogen levels. Microorganisms 8:230

    Article  CAS  PubMed Central  Google Scholar 

  • Muneer MA, Wang P, Lin C, Ji B (2020b) Potential role of common mycorrhizal networks in improving plant growth and soil physicochemical properties under varying nitrogen levels in a grassland ecosystem. Glob Ecol Conserv 24:e01352

    Article  Google Scholar 

  • Nalini S, Parthasarathi R (2018) Optimization of rhamnolipid biosurfactant production from Serratia rubidaea SNAU02 under solid-state fermentation and its biocontrol efficacy against Fusarium wilt of eggplant. Ann Agric Sci 16:108–115

    Google Scholar 

  • Natasha SM, Niazi NK, Khalid S, Murtaza B, Bibi I, Rashid MI (2018) A criticalreview of selenium biogeochemical behavior in soil-plant system with an inference to human health. Environ Pollu 234:915–934

    Article  CAS  Google Scholar 

  • Olanrewaju OS, Ayangbenro AS, Glick BR, Babalola OO (2019) Plant health: feedback effect of root exudates-rhizobiome interactions. Appl Microbiol Biotechnol 103:1155–1166

    Article  CAS  PubMed  Google Scholar 

  • Parmar P, Sindhu SS (2013) Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J Microbiol Res 3:25–31

    Google Scholar 

  • Rahman SFS, Singh E, Pieterse CM, Schenk PM (2018) Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267:102–111

    Article  CAS  Google Scholar 

  • Rfaki A, Zennouhi O, Aliyat FZ, Nassiri L, Ibijbijen J (2020) Isolation, selection and characterization of root-associated rock phosphate solubilizing bacteria in moroccan wheat (Triticum aestivum L.). Geomicrobiol J 37(3):230–241

    Article  CAS  Google Scholar 

  • Santoyo GG, Moreno-Hagelsieb MC, Orozco-Mosqueda GBR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Sasirekha B, Srividya S (2016) Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agric Nat Resour 50:250–256

    CAS  Google Scholar 

  • Van Schoonhoven A (1987) Standard system for the evaluation of bean germplasm. CIAT

  • Sethi S, Datta A, Gupta BL, Gupta S (2013) Optimization of cellulase production from bacteria isolated from soil. International Scholarly Research Notices

  • Shahid M, Farooq ABU, Rabbani F, Khalid S, Dumat C (2020) Risk assessment and biophysiochemical responses of spinach to foliar application of lead oxide nanoparticles: a multivariate analysis. Chemosphere 245:125605

    Article  PubMed  CAS  Google Scholar 

  • Shahzad SM, Arif MS, Riaz M, Iqbal Z, Ashraf M (2013) PGPR with varied ACCdeaminase activity induced different growth and yield response in maize (Zea mays L.) under fertilized conditions. Eur J Soil Biol 57:27–34

    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  PubMed  PubMed Central  Google Scholar 

  • Singh RK, Singh P, Li H, Song QQ, Guo DJ, Solanki MK (2020b) Diversity of nitrogen-fixing rhizobacteria associated with sugarcane: a comprehensive study of plant-microbe interactions for growth enhancement in Saccharum spp. BMC Plant Biol 20:1–21

    Article  CAS  Google Scholar 

  • Singh A, Kumari R, Yadav AN, Mishra S, Sachan A, Sachan SG (2020a) Tiny microbes, big yields: Microorganisms for enhancing food crop production for sustainable development. In New and Future Developments in Microbial Biotechnology and Bioengineering (pp. 1–15). Elsevier, USA

  • Suárez-Moreno ZR, Vinchira-Villarraga DM, Vergara-Morales DI, Castellanos L, Ramos FA, Guarnaccia C (2019) Plant-growth promotion and biocontrol properties of three Streptomyces spp. isolates to control bacterial rice pathogens. Front Microbiol 10:290

    Article  PubMed  PubMed Central  Google Scholar 

  • Tahir M, Ahmad I, Shahid M, Shah GM, Farooq ABU, Akram M, Zakir A (2019a) Regulation of antioxidant production, ion uptake and productivity in potato (Solanum tuberosum L.) plant inoculated with growth promoting salt tolerant Bacillus strains. Ecotoxicol Environ Saf 178:33–42

    Article  CAS  PubMed  Google Scholar 

  • Tahir M, Khalid U, Khan MB, Shahid M, Ahmad I, Akram M, Ahmad N (2019b) Auxin and 1-Aminocyclopropane-1-carboxylate deaminase activity exhibiting rhizobacteria improved maize quality and productivity under drought conditions. Int J Agric Biol 21:943–954

    CAS  Google Scholar 

  • Tahir M, Naeem MA, Shahid M, Khalid U, Farooq ABU, Ahmad N, Waqar A (2020) Inoculation of pqqE gene inhabiting Pantoea and Pseudomonas strains improves the growth and grain yield of wheat with a reduced amount of chemical fertilizer. J Appl Microbiol 129(3):575–589

    Article  CAS  PubMed  Google Scholar 

  • Tarhouni B (2007) Chemical control of Rhizoctonia salani. Annual Report of the Technical Center of Potato, Essaida, Tunisia, pp. 81e86 (in Arabic)

  • Thakur N, Kaur S, Tomar P, Thakur S, Yadav AN (2020) Microbial biopesticides: Current status and advancement for sustainable agriculture and environment. In New and Future Developments in Microbial Biotechnology and Bioengineering 243–282.

  • Tilocca B, Cao MQ (2020) Scent of a Killer: microbial volatile and its role in the biological control of plant pathogens. Front Microbiol 11:41

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang M, Riffel M (2011) Making the right conclusions based on wrong results and small sample sizes: interpretation of statistical tests in ecotoxicology. Ecotoxicol Environm Saf 74:684–692

    Article  CAS  Google Scholar 

  • Wang W, Xu B, Xue Y, Chen Z, Liang X (2014) Identification and antifungal activity of the antagonistic bacteria of Cytospora spp. Zhongguo Shengtai Nongye Xuebao/chinese J Eco-Agriculture 22(10):1214–1221

    Google Scholar 

  • Warnakumari NS, Ramanan D, Kanniappan M (2011) Host – pathogen interaction between the soil borne fungi, Fusarium moniliforme and maize plants (Zea mays L.). J Ecobiotechnol 3:01–05

    Google Scholar 

  • Xiao J, Guo X, Qiao X, Zhang X, Chen X, Zhang D (2021) Activity of fengycin and iturin A isolated from Bacillus subtilis Z-14 on Gaeumannomyces graminis var tritici and soil microbial diversity. Front Microbiol. https://doi.org/10.3389/fmicb.2021.682437

    Article  PubMed  PubMed Central  Google Scholar 

  • Zainab N, Din BU, Javed MT, Afridi MS, Mukhtar T, Kamran MA, Chaudhary HJ (2020) Deciphering metal toxicity responses of flax (Linum usitatissimum L.) with exopolysaccharide and ACC-deaminase producing bacteria in industrially contaminated soils. Plant Physiol Biochem 152:90–99

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We are thankful towards National Agricultural Research Center (NARC), Islamabad, Pakistan to provide space for cultivation of potato plants to carry out the experimental work. We are grateful to Quaid-i-Azam University Islamabad for providing funds (URF-2019).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hassan Javed Chaudhary.

Additional information

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.

Supplementary file1 (DOCX 290 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mehmood, S., Muneer, M.A., Tahir, M. et al. Deciphering distinct biological control and growth promoting potential of multi-stress tolerant Bacillus subtilis PM32 for potato stem canker. Physiol Mol Biol Plants 27, 2101–2114 (2021). https://doi.org/10.1007/s12298-021-01067-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01067-2

Keywords

Navigation