Plant growth promoting and antifungal activity in endophytic Bacillus strains from pearl millet (Pennisetum glaucum)

Prity Kushwaha1,2, Prem Lal Kashyap3, Alok Kumar Srivastava2, Rajesh Kumar Tiwari1
1Amity Institute of Biotechnology, Amity University Lucknow Campus, Lucknow, India
2ICAR-National Bureau of Agriculturally Important Microorganisms (NBAIM), Mau, India
3ICAR-Indian Institute of Wheat and Barley Research (IIWBR), Karnal, India

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Yadav OP, Rai KN (2013) Genetic improvement of pearl millet in India. Agric Res 2:275–292

Serba DD, Yadav RS (2016) Genomic tools in pearl millet breeding for drought tolerance: status and prospects. Front Plant Sci 7:1724

Manjunatha BS, Paul S, Aggarwal C, Rathi M (2018) Effect of osmotic stress on growth and plant growth promoting activities of osmotolerant endophytic bacteria from pearl millet. Environ Ecol 34:1223–1228

Abraham A, Philip S, Jacob CK, Jayachandran K (2013) Novel bacterial endophytes from Hevea brasiliensis as biocontrol agent against Phytophthora leaf fall disease. BioControl 58:675–684

Santoyo G, Hagelsieb GM, Orozco-Mosqueda MC, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

Qin S, Feng WW, Wang TT, Ding P, Xing K, Jiang JH (2017) Plant growth promoting effect and genomic analysis of the beneficial endophyte Streptomyces sp. KLBMP 5084 isolated from halophyte Limonium sinense. Plant Soil 416:117–132

Wang T-T, Ding P, Pan C, Xing K, Bai J-L, Wan W, Jiang J-H, Qin S (2017) Complete genome sequence of endophyte Bacillus flexus KLBMP 4941 reveals its plant growth promotion mechanism and genetic basis for salt tolerance. J Biotechnol 260:38–41

Kushwaha P, Kashyap PL, Kuppusamy P, Srivastava AK, Tiwari RK (2019) Functional characterization of endophytic bacilli from pearl millet (Pennisetum glaucum) and their possible role in multiple stress tolerance. Plant Biosyst. https://doi.org/10.1080/11263504.2019.1651773

Gond SK, Bergen MS, Torres MS, White JF Jr (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87

Slama HB, Cherif-Silini H, Bouket AC, Qader M, Silini A, Yahiaoui B, Alenezi FN, Luptakova L, Triki MA, Vallat A, Oszako O, Rateb Mostafa E, Belbahri L (2019) Screening for Fusarium antagonistic bacteria from contrasting niches designated the endophyte Bacillus halotolerans as plant warden against Fusarium. Front Microbiol 9:3236. https://doi.org/10.3389/fmicb.2018.03236

Borah A, Das R, Mazumdar R, Thakur D (2019) Culturable endophytic bacteria of Camellia species endowed with plant growth promoting characteristics. J Appl Microbiol 127(3):825–844

Cheffi M, Bouket AC, Alenezi FN, Luptakova L, Belka M, Vallat A, Rateb ME, Tounsi S, Triki MA, Belbahri L (2019) Olea europaea L. root endophyte Bacillus velezensis OEE1 counteracts oomycete and fungal harmful pathogens and harbours a large repertoire of secreted and volatile metabolites and beneficial functional genes. Microorganisms 7(9)

Ribeiro VP, Marriel IE, deSousa SM, Lana UGP, Mattos BB, deOliveira CA, Gomes EA (2018) Endophytic Bacillus strains enhance pearl millet growth and nutrient uptake under low-P. Braz J Microbiol 49(1):40–46

Kandel SL, Joubert PM, Doty SL (2017) Bacterial endophyte colonization and distribution within plants. Microorganisms 5:77

Qi G, Zhang XF, Zhao X (2013) Endophytic Bacillus subtilis WH2 containing Pinellia ternate agglutinin showed insecticidal activity against white backed plant hopper Sogatella furcifera. BioControl 58:233–246

Lopes R, Tsui S, Gonçalves PJRO, de Queiroz MV (2018) A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World J Microbiol Biotechnol 34(7):94

Hassan SE (2017) Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium L. J Adv Res 8:687–695

Caulier S, Nannan C, Gillis A, Licciardi F, Bragard C, Mahillon J (2019) Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol 10:302. https://doi.org/10.3389/fmicb.2019.00302

Jamali H, Sharma A, Prity Kushwaha P, Kashyap PL, Roohi, Srivastava AK (2018) Exploitation of multifarious abiotic stresses, antagonistic activity and plant growth promoting attributes of Bacillus amyloliquefaciens AH53 for sustainable agriculture production. Int J Curr Microbiol App Sci 7(10):751–763

Cao Y, Pi H, Chandrangsu P, Li Y, Wang Y, Zhou H, Xiong H, Helmann JD, Cai Y (2018) Antagonism of two plant-growth promoting Bacillus velezensis isolates against Ralstonia solanacearum and Fusarium oxysporum. Sci Rep 8:4360

Solanki MK, Singh RK, Srivastava S, Kumar S, Kashyap PL, Srivastava AK (2015) Characterization of antagonistic-potential of two Bacillus strains and their biocontrol activity against Rhizoctonia solani in tomato. J Basic Microbiol 55(1):82–90

Mora I, Cabrefiga J, Montesinos E (2011) Antimicrobial peptide genes in Bacillus strains from plant environments. Int Microbiol 14:213–223

Koumoutsi A, Chen XH, Henne A, Liesegang H, Hitzeroth G, Franke P, Vater J, Borriss R (2004) Structural and functional characterization of gene clusters directing nonribosomal synthesis of bioactive cyclic lipopeptides in Bacillus amyloliquefaciens strain FZB42. J Bacteriol 186:1084–1096

Romero D, de Vicente A, Rakotoal RH, Dufour SE, Veening JW, Arrebola E, Cazorla FM, Kuipers OP, Paquot M, Pérez-García A (2007) The iturin and fengycin families of lipopeptides are key factors in antagonism of Bacillus subtilis toward Podosphaera fusca. Mol Plant-Microbe Interact 20:430–440

Chung S, Kong H, Buyer JS, Lakshman DK, Lydon J, Kim SD, Roberts DP (2008) Isolation and partial characterization of Bacillus subtilis ME488 for suppression of soilborne pathogens of cucumber and pepper. Appl Microbiol Biotechnol 80(1):115–123

Mora I, Cabrefiga J, Montesinos E (2015) Cyclic Lipopeptide biosynthetic genes and products, and inhibitory activity of plant-associated Bacillus against phytopathogenic bacteria. PLoS One 10(5):e0127738

Zhao L, Xu Y, Lai X-H, Shan C, Deng Z, Ji Y (2015) Screening and characterization of endophytic Bacillus and Paenibacillus strains from medicinal plant Lonicera japonica for use as potential plant growth promoters. Braz J Microbiol 46(4):977–989

Zhang X, Yingying Z, Yan L, Xuechi F (2017) Screening and characterization of endophytic Bacillus for biocontrol of grapevine downy mildew. Crop Prot 96:173–179

Haidar B, Ferdous M, Fatema B, Ferdous AS, Islam MR, Khan H (2018) Population diversity of bacterial endophytes from jute (Corchorus olitorius) and evaluation of their potential role as bioinoculants. Microbiol Res 208:43–53

Coombs JT, Franco CM (2003) isolation and identification of Actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69:5603–5608

Sharma A, Singh P, Kumar S, Kashyap PL, Srivastava AK, Chakdar H, Singh RN, Kaushik R, Saxena AK, Sharma AK (2015) Deciphering diversity of salt-tolerant bacilli from saline soils of eastern Indo-gangetic plains of India. Geomicrobiology 32:170–180

Ramnani P, Gupta R (2004) Optimization of medium composition for keratinase production on feather by Bacillus licheniformis RG1 using statistical methods involving response surface methodology. Biotechnol Appl Biochem 40:191–196

Sharma A, Kashyap PL, Srivastava AK, Bansal YK, Kaushik R (2019) Isolation and characterization of halotolerant bacilli from chickpea (Cicer arietinum L.) rhizosphere for plant growth promotion and biocontrol traits. Eur J Plant Pathol 153(3):787–800

Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

Prescott LM, Harley JP, Klein DA (1996) Antimicrobial chemotherapy. In: Microbiology, 3th edn. WCB Publishers, London, pp 657–671

Soutourina OA, Semenova EA, Parfenova VV, Danchin A, Bertin P (2001) Control of bacterial motility by environmental factors in polarly flagellated and peritrichous bacteria isolated from lake Baikal. Appl Environ Microbiol 67(9):3852

Cappuccino JG, Sherman N (1992) Biochemical activities of microorganisms. In: Harvey AR, Champe PC (eds) Microbiology. The Benjamin/Cummings Publishing Co., California, pp 49–197

Bakker AW, Schippers B (1987) Microbial cyanide production in the rhizosphere in relation to potato yield reduction and Pseudomonas spp-mediated plant growth reduction. Soil Biol Biochem 19:452–458

Solanki MK, Singh RK, Srivastava S, Kumar S, Kashyap PL, Srivastava AK, Arora DK (2014) Isolation and characterization of siderophore producing antagonistic rhizobacteria against Rhizoctonia solani. J Basic Microbiol 54(6):585–597

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

Bric JM, Bostock RM, Silverstone SE (1991) Rapid in situ assay for indoleacetic Acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microbiol 7(2):535–538

Cavalcante VA, Dobereiner (1988) A new acid-tolerant nitrogen-fixing bacterium associated with sugarcane. J Plant Soil 108:23–31

Hu XF, Chen J, Guo JF (2006) Two phosphate and potassium solubilizing bacterial isolated from Tiannu Mountain, Zhijiang, China. World J Microbiol Biotechnol 22:983–990

Pikovskaya RL (1948) Mobilzation of phosphorus in soil. In: Connection with vital activity of some microbial species. Microbiologiya 17:362–370

Claus H, Filip Z (1988) Behaviour of phenoloxidases in the presence of clays and other soil-related adsorbents. Appl Microbiol Biotechnol 28(4):506–511

Teather RM, Wood PJ (1982) Use of Congo red-polysaccharide interactions in enumeration and characterization of cellulolytic bacteria from the bovine rumen. Appl Environ Microbiol 43:777–780

Vermelho AB, Meirelles MNL, Lopes A, Petinate SDG, Chaia AA, Branquinha MH (1996) Detection of extracellular proteases from microorganisms on agar plates. Mem Inst Oswaldo Cruz 91(6):755–760

Lusty CJ, Doudoroff M (1966) Poly-β-Hydroxybutyrate depolymerases of Pseudomonas Lemoignei. Proc Natl Acad Sci U S A 56:960–965

Amira MB, Lopez D, Mohamed AT, Khouaja A, Chaar H, Fumanal B, Gousset-Dupont A, Bonhomme L, Label P, Goupil P, Ribeiro S, Pujade-Renaud V, Julien JL, Auguin D, Venisse JS (2017) Beneficial effect of Trichoderma harzianum strain Ths97 in biocontrolling Fusarium solani causal agent of root rot disease in olive trees. Biol Control 110:70–78

Chandrashekhara, Niranjanraj S, Deepak SA, Amruthesh KN, Shetty NP, Shetty HS (2007) Endophytic bacteria from different plant origin enhance growth and induce downy mildew resistance in pearl millet. Asian J Plant Pathol 1:1–11

Romero FM, Marina M, Pieckenstain FL (2014) The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S-ribosomal RNA gene pyrosequencing. FEMS Microbiol Lett 351:187–194

Bai Y, Zhou X, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781

Lin L, Qiao YS, Ju ZY, Ma CW, Liu YH, Zhou YJ, Dong HS (2009) Isolation and characterization of endophytic Bacillus subtilis Jaas ed1 antagonist of eggplant Verticillium wilt. Biosci Biotechnol Biochem 73(7):1489–1493

Okunishi S, Sako K, Mano H, Imamura, Morisaki H (2005) Bacterial flora of endophytes in the maturing seeds of cultivated rice (Oryza sativa). Microbes Environ 20:168–177

Panchal H, Ingle S (2011) Isolation and characterization of endophytes from the root of the medicinal plant Chlorophytum borivilianum (Safed musli). J Adv Dev Res 2:205–209

Goswami SK, Singh V, Kashyap PL (2017) Population genetic structure of Rhizoctonia solani AG1IA from rice field in North India. Phytoparasitica 45(3):299–316

Elisabeth ZP, Paco S, Vibeke L, Philippe S, Irenee S, Adama N (2008) Importance of seed-borne fungi of sorghum and pearl millet in burkina faso and their control using plant extracts. Pak J Biol Sci 11:321–331

Pleban S, Ingel F, Chet I (1995) Control of Rhizoctonia solani and Sclerotium rolfsii in the greenhouse using endophytic Bacillus spp. Eur J Plant Pathol 101(6):665–672

Prasad G, Kumar V, Dwivedi SK (2018) Antifungal activity of some selected medicinal plants against Fusarium solani causing wilt and rot in Pearl millet. Asian J Bio Sci 13(1):21–27

Vinayarani G, Prakash HS (2018) Growth promoting rhizospheric and endophytic bacteria from Curcuma longa L. as biocontrol agents against rhizome rot and leaf blight diseases. Plant Pathol J 34(3):218–235

Gao T, Foulston L, Chai Y, Wang Q, Losick R (2015) Alternative modes of biofilm formation by plant-associated Bacillus cereus. Microbiologyopen 4(3):452–464

Hu HJ, Chen YL, Wang YF, Tang YY, Chen SL, Yan SZ (2017) Endophytic Bacillus cereus effectively controls Meloidogyne incognita on tomato plants through rapid rhizosphere occupation and repellent action. Plant Dis 101(3):448–455

Ahmad Z, Wu J, Chen L, Dong W (2017) Isolated Bacillus subtilis strain 330-2 and its antagonistic genes identified by the removing PCR. Sci Rep 7:1777

Ek-Ramos MJ, Gomez-Flores R, Orozco-Flores AA, Rodríguez-Padilla C, González-Ochoa GP (2019) Bioactive products from plant-endophytic gram-positive bacteria. Front Microbiol 10:463

Shafi J, Tian H, Ji M (2017) Bacillus species as versatile weapons for plant pathogens: a review. Biotechnol Biotechnol Equip 31:446–459

Singh RK, Kumar DP, Singh P, Solanki MK, Srivastava S, Kashyap PL, Kumar S, Srivastava AK, Singhal PK, Arora DK (2014) Multifarious plant growth promoting characteristics of chickpea rhizosphere associated Bacilli help to suppress soil-borne pathogens. J Plant Growth Regul 73(1):91–101

Hazarika DJ, Goswami G, Gautom T, Parveen A, Das P, Barooah M, Boro RC (2019) Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiol 19:71

Kim PI, Ryu J, Kim YH, Chi YT (2010) Production of biosurfactant lipopeptides iturin A, fengycin and surfactin A from Bacillus subtilis CMB32 for control of Colletotrichum gloeosporioides. J Microbiol Biotechnol 20:138–145

Toral L, Rodríguez M, Béjar V, Sampedro I (2018) Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Front Microbiol 9:1315

Raaijmakers JM, de Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062

Arguelles-Arias A, Ongena M, Halimi B, Lara Y (2009) Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microb Cell Factories 8:63–74

Vinodkumar S, Nakkeeran S, Renukadevi P, Malathi VG (2017) Biocontrol potentials of antimicrobial peptide producing Bacillus species: multifaceted antagonists for the management of stem rot of carnation caused by Sclerotinia sclerotiorum. Front Microbiol 8:446

Jasim B, Sreelakshmi S, Mathew J, Radhakrishnan EK (2016) Identification of endophytic Bacillus mojavensis with highly specialized broad spectrum antibacterial activity. 3 Biotech 6:187

Jasrotia P, Kashyap PL, Bhardwaj AK, Kumar S, Singh GP (2018) Scope and applications of nanotechnology for wheat production: a review of recent advances. Wheat Barley Res 10(1):1–14

Vaid SK, Kumar B, Sharma A, Shukla AK, Srivastava PC (2014) Effect of zinc solubilizing bacteria on growth promotion and zinc nutrition of rice. J Soil Sci Plant Nutr 14(4):889–910

Shree N, Kashyap PL, Chakdar H, Srivastava AK, Sharma AK (2015) Isolation and characterization of potassium solubilizing bacteria from forest soils of Meghalaya. Indian J Environ Sci 19:43–48

Dinesh R, Srinivasan V, Hamza S, Sarathambal C, Anke Gowda SJ, Ganeshamurthy AN, Gupta SB, Aparna Nair V, Subila KP, Lijina A, Divya VC (2018) Isolation and characterization of potential Zn solubilizing bacteria from soil and its effects on soil Zn release rates, soil available Zn and plant Zn content. Geoderma 321:173–186

Dias ACF, Costa FEC, Andreote FD, Lacava PT, Teixeira MA, Assumpção LC, Araújo WL, Azevedo JL, Melo IS (2009) Isolation of micropropagated strawberry endophytic bacteria and assessment of their potential for plant growth promotion. World J Microbiol Biotechnol 25:189–195

Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization and biofortification of zinc in soybean and wheat cultivated in vertisols of central India. Appl Soil Ecol 73:87–96

Yuan ZS, Liu F, Zhang GF (2015) Characteristics and biodiversity of endophytic phosphorus- and potassium-solubilizing bacteria in Moso Bamboo (Phyllostachys edulis). Acta Biol Hung 66(4):449–459

Nair D, Padmavathy S (2014) Impact of endophytic microorganisms on plants environment and humans. Sci World J:250693

Algam SA, Guan-lin X, Coosemans J (2005) Delivery Methods for introducing endophytic Bacillus into tomato and their effect on growth promotion and suppression of tomato wilt. Plant Pathol J 4:69–74

Ginting RCB, Sukarno N, Widyastuti U, Darusman LK, Kanaya S (2013) Diversity of endophytic fungi from red ginger (Zingiber officinale Rosc.) plant and their inhibitory effect to Fusarium oxysporum plant pathogenic fungi. Hayati J Biosci 20:127–137

Prabhukarthikeyan R, Saravanakumar D, Raguchander T (2013) Combination of endophytic Bacillus and Beauveria for the management of Fusarium wilt and fruit borer in tomato. Pest Manag Sci 70(11):1742–1750

Nejad P, Johnson PA (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18:208–215

Gutiérrez-Zamora ML, Martínez-Romero E (2001) Natural endophytic association between Rhizobium etli and maize (Zea mays L.). J Biotechnol 91:117–126

Raupach GS, Kloepper JW (1998) Mixtures of plant growth promoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88:1158–1164