Skip to main content

Advertisement

Log in

Unveiling the putative functional genes present in root-associated endophytic microbiome from maize plant using the shotgun approach

  • Microbial Genetics • Original Paper
  • Published:
Journal of Applied Genetics Aims and scope Submit manuscript

Abstract

To ensure food security for the ever-increasing world’s population, it is important to explore other alternatives for enhancing plant productivity. This study is aimed at identifying the putative plant growth–promoting (PGP) and endophytic gene clusters in root-associated endophytic microbes from maize root and to also verify if their abundance is affected by different farming practices. To achieve this, we characterize endophytic microbiome genes involved in PGP and endophytic lifestyle inside maize root using the shotgun metagenomic approach. Our results revealed the presence of genes involved in PGP activities such as nitrogen fixation, HCN biosynthesis, siderophore, 4-hydroxybenzoate, ACC deaminase, phenazine, phosphate solubilization, butanediol, methanol utilization, acetoin, nitrogen metabolism, and IAA biosynthesis. We also identify genes involved in stress resistance such as glutathione, catalase, and peroxidase. Our results further revealed the presence of putative genes involved in endophytic behaviors such as aerotaxis, regulator proteins, motility mechanisms, flagellum biosynthesis, nitrogen regulation, regulation of carbon storage, formation of biofilm, reduction of nitric oxide, regulation of beta-lactamase resistance, type III secretion, type IV conjugal DNA, type I pilus assembly, phosphotransferase system (PTS), and ATP-binding cassette (ABC). Our study suggests a high possibility in the utilization of endophytic microbial community for plant growth promotion, biocontrol activities, and stress mitigation. Further studies in ascertaining this claim through culturing of the beneficial isolates as well as pot and field experiments are necessary.

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
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nat Rev Mol Cell Biol 7:601–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saudi Univ Sci 26:1–20

    Article  Google Scholar 

  • Alenezi FN, Rekik I, Chenari Bouket A, Luptakova L, Weitz HJ, Rateb ME, Jaspars M, Woodward S, Belbahri L (2017) Increased biological activity of Aneurinibacillus migulanus strains correlates with the production of new gramicidin secondary metabolites. Front Microbiol 8:517

    Article  PubMed  PubMed Central  Google Scholar 

  • Aloo B, Makumba B, Mbega E (2019) The potential of bacilli rhizobacteria for sustainable crop production and environmental sustainability. Microbiol Res 219:26–39

    Article  CAS  PubMed  Google Scholar 

  • Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68:73–78

    Article  CAS  Google Scholar 

  • Babalola OO (2010) Ethylene quantification in three rhizobacterial isolates from Striga hermonthica-infested maize and sorghum. Egypt J Biol 12:1–5

    Google Scholar 

  • Berg G, Eberl L, Hartmann A (2005) The rhizosphere as a reservoir of opportunistic human pathogenic bacteria. Minireview. Environ Microbiol 7:1673–1685

    Article  CAS  PubMed  Google Scholar 

  • Blaser M, Bork P, Fraser C, Knight R, Wang J (2013) The microbiome explored: recent insights and future challenges. Nat Rev Microbiol 11:213–217

    Article  CAS  PubMed  Google Scholar 

  • Böhm M, Hurek T, Reinhold-Hurek B (2007) Twitching motility is essential for endophytic rice colonization by the N2-fixing endophyte Azoarcus sp. strain BH72. Mol Plant-Microbe Interact 20:526–533

    Article  PubMed  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma L-J, Sessitsch A (2017) Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol 55:61–83

    Article  CAS  PubMed  Google Scholar 

  • Carrell AA, Frank C (2015) Bacterial endophyte communities in the foliage of coast redwood and giant sequoia. Front Microbiol 6:1008

    Article  PubMed  PubMed Central  Google Scholar 

  • Carrión VJ, Perez-Jaramillo J, Cordovez V, Tracanna V, De Hollander M, Ruiz-Buck D, Mendes LW, Van Ijcken WF, Gomez-Exposito R, Elsayed SS (2019) Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366:606–612

    Article  PubMed  Google Scholar 

  • Chauhan NM, Gutama AD, Aysa A (2019) Endophytic fungal diversity isolated from different agro-ecosystem of Enset (Ensete ventericosum) in Gedeo zone, SNNPRS, Ethiopia. BMC Microbiol 19:172

    Article  PubMed  PubMed Central  Google Scholar 

  • Correa-Galeote D, Bedmar EJ, Arone GJ (2018) Maize endophytic bacterial diversity as affected by soil cultivation history. Front Microbiol 9:484

    Article  PubMed  PubMed Central  Google Scholar 

  • Da Costa PB, Beneduzi A, De Souza R, Schoenfeld R, Vargas LK, Passaglia LM (2013) The effects of different fertilization conditions on bacterial plant growth promoting traits: guidelines for directed bacterial prospection and testing. Plant Soil 368:267–280

    Article  Google Scholar 

  • De Tender C (2017) "Microbial community analysis in soil (rhizosphere) and the marine (plastisphere) environment in function of plant health and biofilm formation". Doctor (PhD) in Biotechnology Thesis, Ghent University. pp1-274

  • Dimkpa C, Merten D, Svatoš A, Büchel G, Kothe E (2009) Siderophores mediate reduced and increased uptake of cadmium by Streptomyces tendae F4 and sunflower (Helianthus annuus), respectively. J Appl Microbiol 107:1687–1696

    Article  CAS  PubMed  Google Scholar 

  • Downie JA (2010) The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol Rev 34:150–170

    Article  CAS  PubMed  Google Scholar 

  • Eid AM, Salim SS, Hassan SE-D, Ismail MA, Fouda A (2019) Role of endophytes in plant health and abiotic stress management. In: Microbiome in Plant Health and Disease. Springer, pp 119–144

  • Enagbonma BJ, Babalola OO (2020) Unveiling plant-beneficial function as seen in bacteria genes from termite mound soil. J Soil Sci Plant Nutr 20:431–430

    Article  Google Scholar 

  • Fadiji AE, Babalola OO (2020a) Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front Bioeng Biotechnol 8:467

    Article  PubMed  PubMed Central  Google Scholar 

  • Fadiji AE, Babalola OO (2020b) Metagenomics methods for the study of plant-associated microbial communities: a review. J Microbiol Methods 170:105860

    Article  CAS  PubMed  Google Scholar 

  • Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartmann A, Schmid M, Van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257

    Article  CAS  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Hong CE, Kim JU, Lee JW, Bang KH, Jo IH (2019) Metagenomic analysis of bacterial endophyte community structure and functions in Panax ginseng at different ages. 3 Biotech 9:300

    Article  PubMed  PubMed Central  Google Scholar 

  • Iniguez AL, Dong Y, Carter HD, Ahmer BM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant-Microbe Interact 18:169–178

    Article  CAS  PubMed  Google Scholar 

  • Jayakodi M, Choi BS, Lee SC, Kim NH, Park JY, Jang W, Lakshmanan M, Mohan SVG, Lee DY, Yang TJ (2018) Ginseng genome database: an open-access platform for genomics of Panax ginseng. BMC Plant Biol 18:62

    Article  PubMed  PubMed Central  Google Scholar 

  • Jog R, Pandya M, Nareshkumar G, Rajkumar S (2014) Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology 160:778–788

    Article  CAS  PubMed  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khare E, Mishra J, Arora NK (2018) Multifaceted interactions between endophytes and plant: developments and prospects. Front Microbiol 9:2732

    Article  PubMed  PubMed Central  Google Scholar 

  • Latz MA, Jensen B, Collinge DB, Jørgensen HJ (2018) Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression. Plant Ecol Divers 11:555–567

    Article  Google Scholar 

  • Liu Y, Wang R, Li Y, Cao Y, Chen C, Qiu C, Bai F, Xu T, Zhang X, Dai W (2017) High-throughput sequencing-based analysis of the composition and diversity of endophytic bacterial community in seeds of “Beijing” hybrid maize planted in China. Plant Growth Regul 81:317–324

    Article  CAS  Google Scholar 

  • Lumactud R, Fulthorpe RR (2018) Endophytic bacterial community structure and function of herbaceous plants from petroleum hydrocarbon contaminated and non-contaminated sites. Front Microbiol 9:1926

    Article  PubMed  PubMed Central  Google Scholar 

  • Mashiane AR, Adeleke RA, Bezuidenhout CC, Chirima GJ (2018) Community composition and functions of endophytic bacteria of Bt maize. S Afr J Sci 114:88–97

    Google Scholar 

  • Mefteh BF, Chenari Bouket A, Daoud A, Luptakova L, Alenezi FN, Gharsallah N, Belbahri L (2019) Metagenomic insights and genomic analysis of phosphogypsum and its associated plant endophytic microbiomes reveals valuable actors for waste bioremediation. Microorganisms 7:382

    Article  PubMed Central  Google Scholar 

  • Meng Y, Li Y, Galvani CD, Hao G, Turner JN, Burr TJ, Hoch H (2005) Upstream migration of Xylella fastidiosa via pilus-driven twitching motility. J Bacteriol 187:5560–5567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Mitter B, Petric A, Shin MW, Chain PS, Hauberg-Lotte L, Reinhold-Hurek B, Nowak J, Sessitsch A (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4:120

    Article  PubMed  PubMed Central  Google Scholar 

  • Müller H, Berg C, Landa BB, Auerbach A, Moissl-Eichinger C, Berg G (2015) Plant genotype-specific archaeal and bacterial endophytes but similar Bacillus antagonists colonize Mediterranean olive trees. Front Microbiol 6:138

    Article  PubMed  PubMed Central  Google Scholar 

  • Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol 33(197):191–116

    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 

  • Omomowo OI, Babalola OO (2019) Bacterial and fungal endophytes: tiny giants with immense beneficial potential for plant growth and sustainable agricultural productivity. Microorganisms 7:481

    Article  PubMed Central  Google Scholar 

  • Otieno N, Lally RD, Kiwanuka S, Lloyd A, Ryan D, Germaine KJ, Dowling DN (2015) Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol 6:745

    Google Scholar 

  • Porter SL, Wadhams GH, Armitage JP (2011) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9:153–165

    Article  CAS  PubMed  Google Scholar 

  • Purbajanti ED, Slamet W, and Fuskhah E (2019) "Effects of organic and inorganic fertilizers on growth, activity of nitrate reductase and chlorophyll contents of peanuts (Arachis hypogaea L.)", in: IOP conference series: earth and environmental science: IOP Publishing), 250: 012048

  • Rajkumar M, Ae N, Freitas H (2009) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160

    Article  CAS  PubMed  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14:435–443

    Article  PubMed  Google Scholar 

  • Rijavec T, Lapanje A (2016) Hydrogen cyanide in the rhizosphere: not suppressing plant pathogens, but rather regulating availability of phosphate. Front Microbiol 7:1785

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodríguez-Blanco A, Sicardi M, Frioni L (2015) Plant genotype and nitrogen fertilization effects on abundance and diversity of diazotrophic bacteria associated with maize (Zea mays L.). Biol Fertil Soils 51:391–402

    Article  Google Scholar 

  • Ruppel S, Franken P, Witzel K (2013) Properties of the halophyte microbiome and their implications for plant salt tolerance. Funct Plant Biol 40:940–951

    Article  CAS  PubMed  Google Scholar 

  • Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA, Grishin NV, Mirzaei H, Orth K (2014) Marker for type VI secretion system effectors. Proc Natl Acad Sci 111:9271–9276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santoyo G, Moreno-Hagelsieb G, Del Carmen Orozco-Mosqueda M, Glick BR (2016) Plant growth-promoting bacterial endophytes. Microbiol Res 183:92–99

    Article  CAS  PubMed  Google Scholar 

  • Sessitsch A, Hardoim P, Döring J, Weilharter A, Krause A, Woyke T, Mitter B, Hauberg-Lotte L, Friedrich F, Rahalkar M (2012) Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant-Microbe Interact 25:28–36

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Dubey AK (2018) Diversity and applications of endophytic actinobacteria of plants in special and other ecological niches. Front Microbiol 9:1767

    Article  PubMed  PubMed Central  Google Scholar 

  • Slama HB, Cherif-Silini H, Chenari Bouket A, Qader M, Silini A, Yahiaoui B, Alenezi FN, Luptakova L, Triki MA, Vallat A (2019) Screening for Fusarium antagonistic bacteria from contrasting niches designated the endophyte Bacillus halotolerans as plant warden against Fusarium. Front Microbiol 9:3236

    Article  PubMed  PubMed Central  Google Scholar 

  • Sugawara S, Mashiguchi K, Tanaka K, Hishiyama S, Sakai T, Hanada K, Kinoshita-Tsujimura K, Yu H, Dai X, Takebayashi Y (2015) Distinct characteristics of indole-3-acetic acid and phenylacetic acid, two common auxins in plants. Plant Cell Physiol 56:1641–1654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun W, Xiong Z, Chu L, Li W, Soares MA, White JF Jr, Li H (2019) Bacterial communities of three plant species from Pb-Zn contaminated sites and plant-growth promotional benefits of endophytic Microbacterium sp.(strain BXGe71). J Hazard Mater 370:225–231

    Article  CAS  PubMed  Google Scholar 

  • Syranidou E, Christofilopoulos S, Politi M, Weyens N, Venieri D, Vangronsveld J, Kalogerakis N (2017) Bisphenol-A removal by the halophyte Juncus acutus in a phytoremediation pilot: characterization and potential role of the endophytic community. J Hazard Mater 323:350–358

    Article  CAS  PubMed  Google Scholar 

  • Sziderics A, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53:1195–1202

    Article  CAS  PubMed  Google Scholar 

  • Toju H, Peay KG, Yamamichi M, Narisawa K, Hiruma K, Naito K, Fukuda S, Ushio M, Nakaoka S, Onoda Y (2018) Core microbiomes for sustainable agroecosystems. Nat Plants 4:247–257

    Article  PubMed  Google Scholar 

  • Tsurumaru H, Okubo T, Okazaki K, Hashimoto M, Kakizaki K, Hanzawa E, Takahashi H, Asanome N, Tanaka F, Sekiyama Y (2015) Metagenomic analysis of the bacterial community associated with the taproot of sugar beet. Microbes Environ 30:63–69

    Article  PubMed  PubMed Central  Google Scholar 

  • U. S. Department of Agriculture [USDA] (2014) Organic Regulations. Title 7, Subtitle B, Chapter I, Subchapter M, Section 205. Available at: http://www.ams. usda.gov/AMSv1.0/NOPOrganicStandards

  • Van Der Heijden MG, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    Article  PubMed  Google Scholar 

  • Van Overbeek L, Van Doorn J, Wichers J, Van Amerongen A, Van Roermund H, Willemsen P (2014) The arable ecosystem as battleground for emergence of new human pathogens. Front Microbiol 5:104

    PubMed  PubMed Central  Google Scholar 

  • Vardharajula S, Skz A, Shiva Krishna Prasad Vurukonda S, Shrivastava M (2017) Plant growth promoting endophytes and their interaction with plants to alleviate abiotic stress. Curr Biotechnol 6:252–263

    Article  Google Scholar 

  • Vincent JM (1970) A manual for the practical study of the root-nodule bacteria. Wiley-Blackwell, Hoboken, p 440

    Google Scholar 

  • Wilke A, Harrison T, Wilkening J, Field D, Glass EM, Kyrpides N, Mavrommatis K, Meyer F (2012) The M5nr: a novel non-redundant database containing protein sequences and annotations from multiple sources and associated tools. BMC Bioinform 13:141

    Article  CAS  Google Scholar 

  • Xia Y, DeBolt S, Dreyer J, Scott D, Williams MA (2015) Characterization of culturable bacterial endophytes and their capacity to promote plant growth from plants grown using organic or conventional practices. Frontiers in Plant Science 6:490

  • Xia Y, Sahib MR, Amna A, Opiyo SO, Zhao Z, Gao YG (2019) Culturable endophytic fungal communities associated with plants in organic and conventional farming systems and their effects on plant growth. Sci Rep 9:1669

    Article  PubMed  PubMed Central  Google Scholar 

  • Xing K, Bian G-K, Qin S, Klenk H-P, Yuan B, Zhang Y-J, Li W-J, Jiang J-H (2012) Kibdelosporangium phytohabitans sp. nov., a novel endophytic actinomycete isolated from oil-seed plant Jatropha curcas L. containing 1-aminocyclopropane-1-carboxylic acid deaminase. Antonie Van Leeuwenhoek 101:433–441

    Article  CAS  PubMed  Google Scholar 

  • Yurgel SN, Douglas GM, Langille MG (2019) Metagenomic functional shifts to plant induced environmental changes. Front Microbiol 10:1682

    Article  PubMed  PubMed Central  Google Scholar 

  • Zolti A, Green SJ, Sela N, Hadar Y, Minz D (2020) The microbiome as a biosensor: functional profiles elucidate hidden stress in hosts. Microbiome 8:1–18

    Google Scholar 

Download references

Acknowledgments

AEF appreciates NRF/TWAS African Renaissance scholarship (UID116107) which was of great encouragement for his Ph.D. studies. OOB acknowledged the National Research Foundation, South Africa, for the research grant (UID123634) that supported research in her laboratory.

Funding

The funding for this project was provided by the National Research Foundation, South Africa (UID123634).

Author information

Authors and Affiliations

Authors

Contributions

AEF handled the literature findings, carried out the planting and laboratory work, performed the analyses, interpreted the results, and wrote the manuscript. ASA provided technical input, result interpretation, and proofread the manuscript. OOB initiated the metagenomic research, provided academic and technical inputs to the co-authors, critiqued and helped shape the research, verified the analytical methods, and secured funding for the research.

Corresponding author

Correspondence to Olubukola Oluranti Babalola.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Communicated by: Agnieszka Szalewska-Palasz

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fadiji, A.E., Ayangbenro, A.S. & Babalola, O.O. Unveiling the putative functional genes present in root-associated endophytic microbiome from maize plant using the shotgun approach. J Appl Genetics 62, 339–351 (2021). https://doi.org/10.1007/s13353-021-00611-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-021-00611-w

Keywords

Navigation