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Investigating the diversity of bacterial endophytes in maize and their plant growth-promoting attributes

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Abstract

Maize is a widely known crop in cereals for its importance as staple food, and the endophytic bacteria which dwell within the maize tissues may have impact on the yield and quality of crop. In this study, endophytic bacteria associated with maize were characterized based on their plant growth promoting traits and identified at molecular level to provide valuable information for developing a microbial consortium to enhance the productivity of crop. The bacterial strains having multi-trait plant growth promoting attributes were studied quantitatively, and highest phosphate solubilization was shown by the isolate KL3E1 (573 µg/mL), while K solubilization has reported maximum of 39 mg/L by the isolate PdS3E1, IAA production was found maximum by the isolate LL3E1 (165 μg/mL), and maximum siderophore production (93%) was shown by the isolate VaR3E1 and exopolysaccharide production was found highest by LS3E3 (65 mg/L). The efficient isolates identified by 16S rRNA gene sequencing were found as Gordonia hongkongensis, Microbacterium hydrothermale, Kosakonia radicincitans, Kosakonia cowanii, Priestia megaterium, Priestia aryabhattai, Klebsiella pneumoniae, Cellulosimicrobium funkei, Bacillus licheniformis, Pantoea dispersa, Pseudomonas aeruginosa, and Methylorubrum populi. The results showed that these multi-trait plant growth promoting endophytic bacterial isolates could be used as bio inoculants for sustainable improvement of maize crop productivity.

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References

  • Akhtar SS, Andersen MN, Naveed M, Zahir ZA, Liu F (2015) Interactive effect of biochar and plant growth-promoting bacterial endophytes on ameliorating salinity stress in maize. Functional Plant Biol 42:770. https://doi.org/10.1071/fp15054

    Article  CAS  Google Scholar 

  • Ali S, Isaacson J, Kroner Y, Saldias S, Kandasamy S, Lazarovits G (2018) Corn sap bacterial endophytes and their potential in plant growth-promotion. Environ Sustain 1:341–355. https://doi.org/10.1007/s42398-018-00030-4

    Article  Google Scholar 

  • Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C, Mengoni A (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microbial Ecol 53:306–316

    Article  CAS  Google Scholar 

  • Beneduzi A, Moreira F, Costa PB, Vargas LK, Lisboa BB, Favreto R, Passaglia LMP (2013) Diversity and plant growth promoting evaluation abilities of bacteria isolated from sugarcane cultivated in the south of Brazil. Appl Soil Ecol 63:94–104. https://doi.org/10.1016/j.apsoil.2012.08.010

    Article  Google Scholar 

  • Bodhankar S, Grover M, Hemanth S, Reddy G, Rasul S, Yadav SK., Srinivasarao C (2017) Maize seed endophytic bacteria: dominance of antagonistic, lytic enzyme-producing Bacillus spp. 3 Biotech 7:1–13. https://doi.org/10.1007/s13205-017-0860-0

  • Chaiharn M, Lumyong S (2009) Phosphate solubilization potential and stress tolerance of rhizobacteria from rice soil in Northern Thailand. World J Microbiol Biotechnol 25:305–314

    Article  CAS  Google Scholar 

  • Chelius MK, Triplett EW (2000a) Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl Environ Microbiol 66:783–787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chelius MK, Triplett EW (2000b) Diazotrophic endophytes associated with maize. In: Triplett EW (ed) Prokaryotic nitrogen fixation: a model system for the analysis of a biological process. Horizon Scientific Press, Norfolk, pp 779–792

    Google Scholar 

  • De Abreu CS, Figueiredo JEF, Oliveira-Paiva CA, Dos Santos VL, Gomes EA, Ribeiro VP, Barros BDA, Lana UDP, Marriel IE (2017) Maize endophytic bacteria as mineral phosphate solubilizers. Gen Mol Res 16:1–13. https://www.alice.cnptia.embrapa.br/alice/handle/doc/1065208

  • Esikova TZ, Anokhina TO, Abashina TN, Suzina NE, Solyanikova IP (2021) Characterization of soil bacteria with potential to degrade benzoate and antagonistic to fungal and bacterial phytopathogens. Microorganisms 9:755. https://doi.org/10.3390/microorganisms9040755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon SA, Weber RP (1951) Colorimetric estimation of indole acetic acid. Plant Physiol 26:192–195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green PN, Ardley JK (2018) Review of the genus Methylobacterium and closely related organisms: a proposal that some Methylobacterium species be reclassified into a new genus, Methylorubrum gen. nov. Int J Syst Evol Microbiol 68:2727–2748. https://doi.org/10.1099/ijsem.0.002856

    Article  CAS  PubMed  Google Scholar 

  • Grządziel J, Gałązka A (2018) Microplot long-term experiment reveals strong soil type influence on bacteria composition and its functional diversity. Appl Soil Ecol 124:117–123

    Article  Google Scholar 

  • Gupta RS, Patel S, Saini N, Chen S (2020) Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the subtilis and cereus clades of species. Microbiol Soc 70(11). https://doi.org/10.1099/ijsem.0.004475

  • Hu QP, Xu JG (2011) A simple double-layered chrome azurol S agar (SDCASA) plate assay to optimize the production of siderophores by a potential biocontrol agent Bacillus. Afr J Microbiol Res 5:4321–4327

    CAS  Google Scholar 

  • Ikeda AC, Bassani LL, Adamoski D, Stringari D, Cordeiro VK, Glienke C, Galli Terasawa LV (2012) Morphological and genetic characterization of endophytic bacteria isolated from roots of different maize genotypes. Microbiol Ecol 65:154–160

    Article  Google Scholar 

  • Ikeda AC, Savi DC, Hungria M, Kava V, Glienke C, Galli-Terasawa LV (2020) Bioprospecting of elite plant growth-promoting bacteria for the maize crop. Acta Sci Agron 42:e44364. https://doi.org/10.4025/actasciagron.v42i1.4

    Article  Google Scholar 

  • Ivanova EG, Doronina NV, Trotsenko IA (2001) Aerobic methylobacteria are capable of synthesizing auxins. Microbiol 70:452–458

    CAS  Google Scholar 

  • Jasim B, Jimtha JC, Jyothis M, Radhakrishnan EK (2013) Plant growth promoting potential of endophytic bacteria isolated from Piper nigrum. Plant Growth Regul 71:1–11. https://doi.org/10.1007/s10725-013-9802-y

    Article  CAS  Google Scholar 

  • Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, New York, USA, pp 199–233

    Google Scholar 

  • Kour D, Rana KL, Kaur T, Devi R, Yadav N, Halder SK (2020) Potassium solubilizing and mobilizing microbes: biodiversity, mechanisms of solubilization and biotechnological implication for alleviations of abiotic stress. In: Rastegari AA, Yadav AN, Yadav N (eds) Trends of microbial biotechnology for sustainable agriculture and biomedicine systems: diversity and functional perspective. Elsevier, Amsterdam, Netherlands, pp 177–202

    Google Scholar 

  • Krishnamoorthy A, Agarwal T, Kotamreddy JNR, Bhattacharya R, Mitra A, Maiti TK, Maiti MK (2020) Impact of seed-transmitted endophytic bacteria on intra- and inter-cultivar plant growth promotion modulated by certain sets of metabolites in rice crop. Microbiol Res 214:126582. https://doi.org/10.1016/j.micres.2020.126582

    Article  CAS  Google Scholar 

  • Kumar MA, Anandapandian KTK, Parthiban K (2011) Production and characterization of exopolysaccharides (EPS) from biofilm forming marine bacterium. Brazilian Archives of Bio and Tech 54:259–265. https://doi.org/10.1590/s1516-89132011000200006

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol Biol and Evol 35:1547–1549

    Article  CAS  Google Scholar 

  • Loaces I, Ferrando L, Scavino AF (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microbial Ecol 61:606–618

    Article  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Ryu J, Sa T (2006) Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense. Planta 224:268–278

    Article  CAS  PubMed  Google Scholar 

  • Maheshwari R, Bhutani N, Suneja P (2019) Screening and characterization of siderophore producing endophytic bacteria from Cicer arietinum and Pisum sativum plants. J Appl Biol Biotech 7:7–14

    Article  CAS  Google Scholar 

  • Marag PS, Yadav AN, Suman A (2018) Growth stage and tissue specific colonization of endophytic bacteria having plant growth promoting traits in hybrid and composite maize (Zea mays L.). Microbiol Res 214:101–113. https://doi.org/10.1016/j.micres.2018.05.016

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

    Article  CAS  PubMed  Google Scholar 

  • Ngamau CN, Matiru VN, Tani A, Muthuri CW (2012) Isolation and identification of endophytic bacteria of bananas (Musa sp.) in Kenya and their potential as biofertilizers for sustainable banana production. Afr J Microbiol Res 6(34):6414–6422

  • Noori F, Etesami H, Zarini HN, Khoshkholgh-Sima NA, Salekdeh GH, Alishahi F (2018) Mining alfalfa (Medicago sativa L.) nodules for salinity tolerant non-rhizobial bacteria to improve growth of alfalfa under salinity stress. Ecotoxicol Environ Safety 162:129–138. https://doi.org/10.1016/j.ecoenv.2018.06.092

  • Panigrahi S, Rath CC (2019) Condition Optimization for phosphate solubilization by Kosakonia cowanii MK834804, an endophytic bacterium isolated from Aegle marmelos. Int J Curr Microbiol App Sci 8:2823–2835

    Article  CAS  Google Scholar 

  • Payne SM (1993) Iron acquisition in microbial pathogenesis. Trends Microbiol 1:66–69

    Article  CAS  PubMed  Google Scholar 

  • Rai R, Dash PK, Prasanna BM, Singh A (2007) Endophytic bacterial flora in the stem tissue of a tropical maize (Zea mays L.) genotype: isolation, identification and enumeration. World J Microbiol Biotechnol 23:853–858

    Article  Google Scholar 

  • Rajawat MV, Singh R, Singh D, Yadav AN, Singh S, Kumar M, Saxena AK (2020) Spatial distribution and identification of bacteria in stressed environments capable to weather potassium aluminosilicate mineral. Brazilian J Microbiol 51:751–764

    Article  CAS  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837. https://doi.org/10.1094/MPMI-19-0827

    Article  CAS  PubMed  Google Scholar 

  • Sandhya V, 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 62:21–30. https://doi.org/10.1007/s10725-010-9479-4

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating 1093 inhibitors. PNAS 74:5463–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santoyo G, Moreno HG, del Carmen OMM, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Silambarasan S, Logeswari P, Cornejo P, Kannan VR (2019) Evaluation of the production of exopolysaccharide by plant growth promoting yeast Rhodotorula sp. strain CAH2 under abiotic stress conditions. Int J Biol Macromol 121:55–62

    Article  CAS  PubMed  Google Scholar 

  • Singh TB, Sahai V, Goyal D, Prasad M, Yadav A, Shrivastav P, Ali A, Dantu PK (2020) Identification, characterization and evaluation of multifaceted traits of plant growth promoting rhizobacteria from soil for sustainable approach to agriculture. Curr Microbiol 77:3633–3642

    Article  CAS  PubMed  Google Scholar 

  • Subba Rao NS (1982) Phosphate solubilization by soil microorganisms. Adv Agric Microbiol Oxford & IBH Publishing Co, pp. 1–149

  • Suganya A, Saravanan A, Manivannan N (2020) Role of zinc nutrition for increasing zinc availability, uptake, yield, and quality of maize (Zea mays L.) grains: an overview. Communications in Soil Sci and Plant Anal 51:2001–2021. https://doi.org/10.1080/00103624.2020.1820030

    Article  CAS  Google Scholar 

  • Suman A, Shasany AK, Singh M, Shahi HN, Gaur A, Khanuja SPS (2001) Molecular assessment of diversity among endophytic diazotrophs isolated from subtropical Indian sugarcane World. J Microbiol Biotechnol 17:39–45

    Article  CAS  Google Scholar 

  • Trivedi G, Shah R, Patel P, Saraf M (2017) Role of endophytes in agricultural crops under drought stress: current and future prospects. JAM 3:174–188

    Google Scholar 

  • Verma P, Yadav AN, Khannam KS, Panjiar N, Kumar S, Saxena AK, Suman A (2015) Assessment of genetic diversity and plant growth promoting attributes of psychrotolerant bacteria allied with wheat (Triticum aestivum) from the northern hills zone of India. Ann Microbiol 65:1885–1899

    Article  CAS  Google Scholar 

  • Versalovic J, Schneider M, de Bruijn F, Lupski JR (1994) Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Method Mol Cell Biol 5:25–40

    CAS  Google Scholar 

  • Yaish MW, Antony I, Glick BR (2015) Isolation and characterization of endophytic plant growth-promoting bacteria from date palm tree (Phoenix dactylifera L.) and their potential role in salinity tolerance Antonie Van Leeuw 107:1519–1532

  • Zhang C, Wang MY, Khan N, Tan LL, Yang S (2021) Potentials, utilization, and bioengineering of plant growth-promoting Methylobacterium for sustainable agriculture. Sustainability 13:3941. https://doi.org/10.3390/su13073941

    Article  CAS  Google Scholar 

  • Zhu Y, She X (2018) Evaluation of the plant-growth-promoting abilities of endophytic bacteria from the psammophyte Ammodendron bifolium. Can J Microbiol 64:1–12. https://doi.org/10.1139/cjm-2017-0529

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Authors and Affiliations

  1. Department of Agricultural Microbiology, Acharya N G, Ranga Agricultural University, Lam, Guntur, India

    Uma Sowjanya Moturu

  2. Department of Agricultural Microbiology, Acharya N G, Ranga Agricultural University, Lam, Guntur, 522034, India

    Trimurtulu Nunna

  3. Department of Agricultural Microbiology, Agricultural College, ANGRAU, Bapatla, 522101, India

    Vijaya Gopal Avula

  4. Department of Genetics and Plant Breeding, Agricultural College, ANGRAU, Bapatla, 522101, India

    Venkata Ramana Jagarlamudi

  5. Department of Crop Physiology, Acharya N G, Ranga Agricultural University, Lam, Guntur, 522034, India

    Rama Rao Gutha

  6. Regional Agricultural Research Station, ANGRAU, Amadalavalasa, 532185, India

    Sreelatha Tamminana

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  1. Uma Sowjanya Moturu
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  2. Trimurtulu Nunna
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  3. Vijaya Gopal Avula
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  4. Venkata Ramana Jagarlamudi
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  5. Rama Rao Gutha
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  6. Sreelatha Tamminana
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Contributions

Uma Sowjanya Moturu: conceptualization, methodology, investigation, writing-original draft preparation. Trimurtulu N: conceptualization, data curation, writing-review and editing. Vijaya Gopal A: literature search, review and editing. Ramana J.V.: review and editing. Rama rao G: review and editing. Sreelatha T: supervision.

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Correspondence to Uma Sowjanya Moturu.

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Moturu, U.S., Nunna, T., Avula, V.G. et al. Investigating the diversity of bacterial endophytes in maize and their plant growth-promoting attributes. Folia Microbiol 68, 369–379 (2023). https://doi.org/10.1007/s12223-022-01015-x

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