347
Views
6
CrossRef citations to date
0
Altmetric
Review Articles

Biocontrol of plant pathogens in omics era—with special focus on endophytic bacilli

, , , , , ORCID Icon & show all
Pages 562-580 | Received 24 Aug 2022, Accepted 06 Feb 2023, Published online: 13 Apr 2023

References

  • Ab Rahman SFS, Singh E, Pieterse CM, et al. Emerging microbial biocontrol strategies for plant pathogens. Plant Sci. 2018;267:102–111.
  • Waghunde RR, Khunt MD, Shelake RM, et al. Culturable plant-associated endophytic microbial communities from leguminous and nonleguminous crops. In: Advances in plant microbiome and sustainable agriculture. Singapore: Springer; 2020. p. 83–103.
  • Dean R, Van Kan JA, Pretorius ZA, et al. The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol. 2012;13(4):414–430.
  • Mansfield J, Genin S, Magori S, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol. 2012;13(6):614–629.
  • Schwelm A, Badstöber J, Bulman S, et al. Not in your usual Top 10: protists that infect plants and algae. Mol Plant Pathol. 2018;19(4):1029–1044.
  • Pais M, Yoshida K, Giannakopoulou A, et al. Gene expression polymorphism underpins evasion of host immunity in an asexual lineage of the Irish potato famine pathogen. BMC Evol Biol. 2018;18(1):93.
  • Donnelly JS. Great Irish potato famine. UK: Oxford University Press; 2002.
  • Singh BK, Trivedi P. Microbiome and the future for food and nutrient security. Microb Biotechnol. 2017;10(1):50–53.
  • Dhananjayan V, Jayanthi P, Jayakumar S, et al. Agrochemicals impact on ecosystem and bio-monitoring. In: Resources use efficiency in agriculture. Singapore: Springer; 2020. p. 349–388.
  • Mandal A, Sarkar B, Mandal S, et al. Impact of agrochemicals on soil health. In: Agrochemicals detection, treatment and remediation. UK: Butterworth-Heinemann; 2020. p. 161–187.
  • Meena RS, Kumar S, Datta R, et al. Impact of agrochemicals on soil microbiota and management: a review. Land. 2020;9(2):34.
  • Haney CH, Samuel BS, Bush J, et al. Associations with rhizosphere bacteria can confer an adaptive advantage to plants. Nature plants. 2015;1(6):1–9.
  • Trivedi P, Leach JE, Tringe SG, et al. Plant–microbiome interactions: from community assembly to plant health. Nature Rev Microbiol. 2020;18(11):607–621.
  • Singh BK, Trivedi P, Egidi E, et al. Crop microbiome and sustainable agriculture. Nature Rev Microbiol. 2020;18(11):601–602.
  • Toju H, Peay KG, Yamamichi M, et al. Core microbiomes for sustainable agroecosystems. Nature Plants. 2018;4(5):247–257.
  • Nataraja KN, Suryanarayanan T, Shaanker RU, et al. Plant–microbe interaction: prospects for crop improvement and management. Plant Physiol Rep. 2019;24(4):461–462.
  • Zicca S, De Bellis P, Masiello M, et al. Antagonistic activity of olive endophytic bacteria and of Bacillus spp. strains against Xylella fastidiosa. Microbiol Res. 2020;236:126467.
  • Munir S, Ahmed A, Li Y, et al. The hidden treasures of citrus: finding Huanglongbing cure where it was lost. Crit Rev Biotechnol. 2021;42(4):1–16.
  • Fan B, Wang C, Song X, et al. Bacillus velezensis FZB42 in 2018: the Gram-positive model strain for plant growth promotion and biocontrol. Front Microbiol. 2018;9:2491.
  • Barkodia M, Joshi U, Rami N, et al. Endophytes: a hidden treasure inside plant. IJCS. 2018;6(5):1660–1665.
  • Brader G, Compant S, Vescio K, et al. Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol. 2017;55:61–83.
  • Babalola OO, Fadiji AE, Enagbonma BJ, et al. The nexus between plant and plant microbiome: revelation of the networking strategies. Front Microbiol. 2020;11:2128.
  • Fadiji AE, Babalola OO. Metagenomics methods for the study of plant-associated microbial communities: a review. J Microbiol Methods. 2020;170:105860.
  • Khalaf EM, Raizada MN. Bacterial seed endophytes of domesticated cucurbits antagonize fungal and oomycete pathogens including powdery mildew. Front Microbiol. 2018;9:42.
  • Pandit MA, Kumar J, Gulati S, et al. Major biological control strategies for plant pathogens. Pathogens. 2022;11(2):273.
  • Shen F-T, Yen J-H, Liao C-S, et al. Screening of rice endophytic biofertilizers with fungicide tolerance and plant growth-promoting characteristics. Sustainability. 2019;11(4):1133.
  • Rangjaroen C, Lumyong S, Sloan WT, et al. Herbicide-tolerant endophytic bacteria of rice plants as the biopriming agents for fertility recovery and disease suppression of unhealthy rice seeds. BMC Plant Biol. 2019;19(1):1–16.
  • Gamalero E, Glick BR. Bacterial modulation of plant ethylene levels. Plant Physiol. 2015;169(1):13–22.
  • Singh R, Dubey AK. Diversity and applications of endophytic actinobacteria of plants in special and other ecological niches. Front Microbiol. 2018;9:1767.
  • Bodhankar S, Grover M, Hemanth S, et al. Maize seed endophytic bacteria: dominance of antagonistic, lytic enzyme-producing Bacillus spp. 3 Biotech. 2017;7(4):232.
  • Ranjith S, Kalaiselvi T, Muthusami M, et al. Maize apoplastic fluid bacteria alter feeding characteristics of herbivore (Spodoptera frugiperda) in maize. Microorganisms. 2022;10(9):1850.
  • Thomas P, Reddy KM. Microscopic elucidation of abundant endophytic bacteria colonizing the cell wall–plasma membrane peri-space in the shoot-tip tissue of banana. AoB Plants. 2013;5:1–12.
  • de Almeida CV, Andreote FD, Yara R, et al. Bacteriosomes in axenic plants: endophytes as stable endosymbionts. World J Microbiol Biotechnol. 2009;25(10):1757–1764.
  • White JF, Torres MS, Johnson H, et al. A functional view of plant microbiomes: endosymbiotic systems that enhance plant growth and survival. In: Advances in endophytic research. New Delhi: Springer; 2014. p. 425–439.
  • Yadav AN, Verma P, Kour D, et al. Plant microbiomes and its beneficial multifunctional plant growth promoting attributes. Int J Environ Sci Nat Resour. 2017;3(1):1–8.
  • Compant S, Mitter B, Colli-Mull JG, et al. Endophytes of grapevine flowers, berries, and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microbial Ecol. 2011;62(1):188–197.
  • Sessitsch A, Hardoim P, Döring J, et al. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Mol Plant Microbe Interact. 2012;25(1):28–36.
  • Edwards J, Johnson C, Santos-Medellín C, et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc Natl Acad Sci U S A. 2015;112(8):E911–E920.
  • Santoyo G, Moreno-Hagelsieb G, del Carmen Orozco-Mosqueda M, et al. Plant growth-promoting bacterial endophytes. Microbiol Res. 2016;183:92–99.
  • Afzal I, Shinwari ZK, Sikandar S, et al. Plant beneficial endophytic bacteria: mechanisms, diversity, host range and genetic determinants. Microbiol Res. 2019;221:36–49.
  • Ghiasian M. Endophytic microbiomes: biodiversity, current status, and potential agricultural applications. In: Advances in plant microbiome and sustainable agriculture. Singapore: Springer; 2020. p. 61–82.
  • Jackson CR, Randolph KC, Osborn SL, et al. Culture dependent and independent analysis of bacterial communities associated with commercial salad leaf vegetables. BMC Microbiol. 2013;13(1):274.
  • Hardoim PR, Hardoim CC, Van Overbeek LS, et al. Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS One. 2012;7(2):e30438.
  • Shehzadi M, Afzal M, Khan MU, et al. Enhanced degradation of textile effluent in constructed wetland system using Typha domingensis and textile effluent-degrading endophytic bacteria. Water Res. 2014;58:152–159.
  • Mora-Ruiz MDR, Font-Verdera F, Orfila A, et al. Endophytic microbial diversity of the halophyte Arthrocnemum macrostachyum across plant compartments. FEMS Microbiol Ecol. 2016;92(9):fiw145.
  • Kampapongsa D, Kaewkla O. Biodiversity of endophytic actinobacteria from jasmine rice (Oryza sativa L. KDML 105) grown in Roi-Et Province, Thailand and their antimicrobial activity against rice pathogens. Ann Microbiol. 2016;66(2):587–595.
  • Jog R, Pandya M, Nareshkumar G, et al. Mechanism of phosphate solubilization and antifungal activity of Streptomyces spp. isolated from wheat roots and rhizosphere and their application in improving plant growth. Microbiology. 2014;160(4):778–788.
  • Bulgarelli D, Rott M, Schlaeppi K, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 2012;488(7409):91–95.
  • Liu H, Carvalhais LC, Schenk PM, et al. Effects of jasmonic acid signalling on the wheat microbiome differ between body sites. Sci Rep. 2017;7(1):1–8.
  • Haruna E, Zin NM, Kerfahi D, et al. Extensive overlap of tropical rainforest bacterial endophytes between soil, plant parts, and plant species. Microbial Ecol. 2018;75(1):88–103.
  • Hameed A, Yeh M-W, Hsieh Y-T, et al. Diversity and functional characterization of bacterial endophytes dwelling in various rice (Oryza sativa L.) tissues, and their seed-borne dissemination into rhizosphere under gnotobiotic P-stress. Plant Soil. 2015;394(1-2):177–197.
  • Hamonts K, Trivedi P, Garg A, et al. Field study reveals core plant microbiota and relative importance of their drivers. Environ Microbiol. 2018;20(1):124–140.
  • Philippot L, Raaijmakers JM, Lemanceau P, et al. Going back to the roots: the microbial ecology of the rhizosphere. Nature Rev Microbiol. 2013;11(11):789–799.
  • Tosi M, Gaiero J, Linton N, et al. Bacterial endophytes: diversity, functional importance, and potential for manipulation. In: Rhizosphere biology: interactions between microbes and plants. Singapore: Springer; 2020. p. 1–49.
  • Turner TR, James EK, Poole PS. The plant microbiome. Genome Biol. 2013;14(6):1–10.
  • Knief C, Ramette A, Frances L, et al. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME J. 2010;4(6):719–728.
  • Li L, Sinkko H, Montonen L, et al. Biogeography of symbiotic and other endophytic bacteria isolated from medicinal G lycyrrhiza species in China. FEMS Microbiol Ecol. 2012;79(1):46–68.
  • Kandel SL, Joubert PM, Doty SL. Bacterial endophyte colonization and distribution within plants. Microorganisms. 2017;5(4):77.
  • van Dam NM, Bouwmeester HJ. Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci. 2016;21(3):256–265.
  • Bulgarelli D, Schlaeppi K, Spaepen S, et al. Structure and functions of the bacterial microbiota of plants. Ann Rev Plant Biol. 2013;64:807–838.
  • Chagas FO, de Cassia Pessotti R, Caraballo-Rodriguez AM, et al. Chemical signaling involved in plant–microbe interactions. Chem Soc Rev. 2018;47(5):1652–1704.
  • Liu H, Carvalhais LC, Crawford M, et al. Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol. 2017;8:2552.
  • Pathak P, Rai VK, Can H, et al. Plant-endophyte interaction during biotic stress management. Plants. 2022;11(17):2203.
  • Yu K, Liu Y, Tichelaar R, et al. Rhizosphere-associated Pseudomonas suppress local root immune responses by gluconic acid-mediated lowering of environmental pH. Curr Biol. 2019;29(22):3913.e4–3920.e4.
  • Liu Z, Beskrovnaya P, Melnyk RA, et al. A genome-wide screen identifies genes in rhizosphere-associated Pseudomonas required to evade plant defenses. MBio. 2018;9(6):e00433–e00518.
  • Zhou F, Emonet A, Tendon VD, et al. Co-incidence of damage and microbial patterns controls localized immune responses in roots. Cell. 2020;180(3):440.e18–453.e18.
  • Lundberg DS, Lebeis SL, Paredes SH, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012;488(7409):86–90.
  • Jones P, Garcia B, Furches A, et al. Plant host-associated mechanisms for microbial selection. Front Plant Sci. 2019;10:862.
  • Russo A, Pollastri S, Ruocco M, et al. Volatile organic compounds in the interaction between plants and beneficial microorganisms. J Plant Interact. 2022;17(1):840–852.
  • Zhang YZ, Wang ET, Li M, et al. Effects of rhizobial inoculation, cropping systems and growth stages on endophytic bacterial community of soybean roots. Plant Soil. 2011;347(1):147–161.
  • White JF, Kingsley KL, Zhang Q, et al. Endophytic microbes and their potential applications in crop management. Pest Manag Sci. 2019;75(10):2558–2565.
  • Beltran-Garcia MJ, White JF Jr, Prado FM, et al. Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Rep. 2014;4:6938.
  • Verma SK, Kingsley K, Irizarry I, et al. Seed‐vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol. 2017;122(6):1680–1691.
  • Verma SK, Kingsley KL, Bergen M, et al. Fungal disease protection in rice (Oryza sativa) seedlings by growth promoting seed-associated endophytic bacteria from invasive Phragmites australis. Microorganisms. 2018;6:21.
  • Irizarry I, White J. Application of bacteria from non‐cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. J Appl Microbiol. 2017;122(4):1110–1120.
  • Soares MA, Li H-Y, Bergen M, et al. Functional role of an endophytic Bacillus amyloliquefaciens in enhancing growth and disease protection of invasive English ivy (Hedera helix L.). Plant Soil. 2016;405(1-2):107–123.
  • Pitzschke A. Developmental peculiarities and seed-borne endophytes in quinoa: omnipresent, robust bacilli contribute to plant fitness. Front Microbiol. 2016;7(2):1–15.
  • Cope‐Selby N, Cookson A, Squance M, et al. Endophytic bacteria in miscanthus seed: implications for germination, vertical inheritance of endophytes, plant evolution and breeding. GCB Bioenergy. 2017;9(1):57–77.
  • Verma SK, Kharwar RN, White JF. The role of seed-vectored endophytes in seedling development and establishment. Symbiosis. 2019;78(2):107–113.
  • Verma SK, Kingsley K, Bergen M, et al. Bacterial endophytes from rice cut grass (Leersia oryzoides L.) increase growth, promote root gravitropic response, stimulate root hair formation, and protect rice seedlings from disease. Plant Soil. 2018;422(1-2):223–238.
  • Glick BR. Plant growth-promoting bacteria: mechanisms and applications. Scientifica. 2012;2012:1–15.
  • Mitter B, Petric A, SG Chain P, et al. Genome analysis, ecology, and plant growth promotion of the endophyte Burkholderia phytofirmans strain PsJN. Mol Microbial Ecol Rhizosphere. 2013;1:865–874.
  • Coutinho BG, Licastro D, Mendonça-Previato L, et al. Plant-influenced gene expression in the rice endophyte Burkholderia kururiensis M130. Mol Plant Microbe Interact. 2015;28(1):10–21.
  • Puri A, Padda KP, Chanway CP. Nitrogen-fixation by endophytic bacteria in agricultural crops: recent advances. In: Amanullah, Fahad S, editors. Nitrogen in agriculture – updates. London: IntechOpen; 2018. p. 73–94.
  • Hassan SE-D. Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium L. J Adv Res. 2017;8(6):687–695.
  • Lebeis SL, Paredes SH, Lundberg DS, et al. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science. 2015;349(6250):860–864.
  • Faria PSA, de Oliveira Marques V, Selari PJRG, et al. Multifunctional potential of endophytic bacteria from Anacardium othonianum Rizzini in promoting in vitro and ex vitro plant growth. Microbiol Res. 2020;242:126600.
  • ALKahtani MD, Fouda A, Attia KA, et al. Isolation and characterization of plant growth promoting endophytic bacteria from desert plants and their application as bioinoculants for sustainable agriculture. Agronomy. 2020;10(9):1325.
  • Naveed M, Mitter B, Reichenauer TG, et al. Increased drought stress resilience of maize through endophytic colonization by Burkholderia phytofirmans PsJN and Enterobacter sp. FD17. Environ Exp Bot. 2014;97:30–39.
  • Vaishnav A, Shukla AK, Sharma A, et al. Endophytic bacteria in plant salt stress tolerance: current and future prospects. J Plant Growth Regulat. 2019;38(2):650–668.
  • Etesami H, Noori F, Ebadi A, et al. Alleviation of stress-induced ethylene-mediated negative impact on crop plants by bacterial ACC deaminase: perspectives and applications in stressed agriculture management. Plant Microbiomes Sustain Agric. 2020;25:287–315.
  • Lata R, Chowdhury S, Gond SK, et al. Induction of abiotic stress tolerance in plants by endophytic microbes. Lett Appl Microbiol. 2018;66(4):268–276.
  • Afridi MS, Mahmood T, Salam A, et al. Induction of tolerance to salinity in wheat genotypes by plant growth promoting endophytes: involvement of ACC deaminase and antioxidant enzymes. Plant Physiol Biochem. 2019;139:569–577.
  • Nascimento FX, Rossi MJ, Glick BR. Ethylene and 1-aminocyclopropane-1-carboxylate (ACC) in plant–bacterial interactions. Front Plant Sci. 2018;9:114.
  • Su F, Jacquard C, Villaume S, et al. Burkholderia phytofirmans PsJN reduces impact of freezing temperatures on photosynthesis in Arabidopsis thaliana. Front Plant Sci. 2015;6:810.
  • Vargas L, Santa Brigida AB, Mota Filho JP, et al. Drought tolerance conferred to sugarcane by association with Gluconacetobacter diazotrophicus: a transcriptomic view of hormone pathways. PLoS One. 2014;9(12):e114744.
  • Jha Y, Subramanian R, Patel S. Combination of endophytic and rhizospheric plant growth promoting rhizobacteria in Oryza sativa shows higher accumulation of osmoprotectant against saline stress. Acta Physiol Plant. 2011;33(3):797–802.
  • Fernandez O, Theocharis A, Bordiec S, et al. Burkholderia phytofirmans PsJN acclimates grapevine to cold by modulating carbohydrate metabolism. Mol Plant Microbe Interact. 2012;25(4):496–504.
  • Babu AG, Shea PJ, Sudhakar D, et al. Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal (loid)-contaminated mining site soil. J Environ Manag. 2015;151:160–166.
  • Mukherjee G, Saha C, Naskar N, et al. An endophytic bacterial consortium modulates multiple strategies to improve arsenic phytoremediation efficacy in Solanum nigrum. Sci Rep. 2018;8(1):1–16.
  • Asaf S, Numan M, Khan AL, et al. Sphingomonas: from diversity and genomics to functional role in environmental remediation and plant growth. Crit Rev Biotechnol. 2020;40(2):138–152.
  • Raymaekers K, Ponet L, Holtappels D, et al. Screening for novel biocontrol agents applicable in plant disease management–a review. Biol Control. 2020;114:104240.
  • Omomowo OI, Babalola OO. Bacterial and fungal endophytes: tiny giants with immense beneficial potential for plant growth and sustainable agricultural productivity. Microorganisms. 2019;7(11):481.
  • Ahmed A, Munir S, He P, et al. Biocontrol arsenals of bacterial endophyte: an imminent triumph against clubroot disease. Microbiol Res. 2020;241:126565.
  • Constantin ME, de Lamo FJ, Vlieger BV, et al. Endophyte-mediated resistance in tomato to Fusarium oxysporum is independent of ET, JA, and SA. Front Plant Sci. 2019;10:979.
  • Griffin MR. Biocontrol and bioremediation: two areas of endophytic research which hold great promise. In: Advances in endophytic research. New Delhi: Springer; 2014. p. 257–282.
  • Latz MA, Jensen B, Collinge DB, et al. Endophytic fungi as biocontrol agents: elucidating mechanisms in disease suppression. Plant Ecol Divers. 2018;11(5-6):555–567.
  • Pohjanen J, Koskimäki JJ, Pirttilä AM. Interactions of meristem-associated endophytic bacteria. In: Advances in endophytic research. New Delhi: Springer; 2014. p. 103–113.
  • Kramer J, Özkaya Ö, Kümmerli R. Bacterial siderophores in community and host interactions. Nature Rev Microbiol. 2019;18:1–12.
  • Martinuz A, Schouten A, Sikora R. Systemically induced resistance and microbial competitive exclusion: implications on biological control. Phytopathology. 2012;102(3):260–266.
  • Fadiji AE, Babalola OO. Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front Bioeng Biotechnol. 2020;8:467.
  • Palmieri D, Vitale S, Lima G, et al. A bacterial endophyte exploits chemotropism of a fungal pathogen for plant colonization. Nature Commun. 2020;11(1):1–11.
  • Law JW-F, Ser H-L, Khan TM, et al. The potential of Streptomyces as biocontrol agents against the rice blast fungus, Magnaporthe oryzae (Pyricularia oryzae). Front Microbiol. 2017;8:3.
  • Swarnalakshmi K, Senthilkumar M, Ramakrishnan B. Endophytic actinobacteria: nitrogen fixation, phytohormone production, and antibiosis. In: Plant growth promoting actinobacteria. Singapore: Springer; 2016. p. 123–145.
  • González V, Armijos E, Garcés-Claver A. Fungal endophytes as biocontrol agents against the main soil-borne diseases of melon and watermelon in Spain. Agronomy. 2020;10(6):820.
  • Rajani P, Rajasekaran C, Vasanthakumari M, et al. Inhibition of plant pathogenic fungi by endophytic Trichoderma spp. through mycoparasitism and volatile organic compounds. Microbiol Res. 2020;242:126595.
  • Inayati A, Sulistyowati L, Aini LQ, et al. Mycoparasitic activity of indigenous Trichoderma virens strains against mungbean soil borne pathogen Rhizoctonia solani: hyperparasite and hydrolytic enzyme production. AGRIVITA J Agric Sci. 2020;42(2):229–242.
  • Rai S, Solanki MK. Beneficial endophytic Trichoderma functions in plant health management. In: Microbial endophytes and plant growth. USA: Academic Press; 2023. p. 233–244.
  • Sheoran N, Nadakkakath AV, Munjal V, et al. Genetic analysis of plant endophytic Pseudomonas putida BP25 and chemo-profiling of its antimicrobial volatile organic compounds. Microbiol Res. 2015;173:66–78.
  • Raaijmakers JM, De Bruijn I, Nybroe O, et al. Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev. 2010;34(6):1037–1062.
  • Brader G, Compant S, Mitter B, et al. Metabolic potential of endophytic bacteria. Curr Opin Biotechnol. 2014;27:30–37.
  • Li X-Y, Mao Z-C, Wang Y-H, et al. Diversity and active mechanism of fengycin-type cyclopeptides from Bacillus subtilis XF-1 against Plasmodiophora brassicae. J Microbiol Biotechnol. 2013;23(3):313–321.
  • He P, Cui W, Munir S, et al. Plasmodiophora brassicae root hair interaction and control by Bacillus subtilis XF-1 in Chinese cabbage. Biol Control. 2019;128:56–63.
  • Santoyo G, Sánchez-Yáñez JM, de los Santos-Villalobos S. Methods for detecting biocontrol and plant growth-promoting traits in rhizobacteria. In: Methods in rhizosphere biology research. Singapore: Springer; 2019. p. 133–149.
  • Villarreal-Delgado MF, Villa-Rodríguez ED, Cira-Chávez LA, et al. The genus Bacillus as a biological control agent and its implications in the agricultural biosecurity. Mex J Phytopathol. 2018;36:95–130.
  • Mehnaz S. Rhizotrophs: plant growth promotion to bioremediation. Vol. 2. Singapore: Springer; 2017.
  • Khan AR, Mustafa A, Hyder S, et al. Bacillus spp. as bioagents: uses and application for sustainable agriculture. Biology. 2022;11(12):1763.
  • Ngo VA, Wang S-L, Nguyen VB, et al. Phytophthora antagonism of endophytic bacteria isolated from roots of black pepper (Piper nigrum L.). Agronomy. 2020;10(2):286.
  • Netzker T, Shepherdson EM, Zambri MP, et al. Bacterial volatile compounds: functions in communication, cooperation, and competition. Annu Rev Microbiol. 2020;74:409–430.
  • Agisha VN, Kumar A, Eapen SJ, et al. Broad-spectrum antimicrobial activity of volatile organic compounds from endophytic Pseudomonas putida BP25 against diverse plant pathogens. Biocontrol Sci Technol. 2019;29(11):1069–1089.
  • Etminani F, Harighi B, Mozafari AA. Effect of volatile compounds produced by endophytic bacteria on virulence traits of grapevine crown gall pathogen, Agrobacterium tumefaciens. Sci Rep. 2022;12(1):1–13.
  • Pieterse CM, Zamioudis C, Berendsen RL, et al. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol. 2014;52:347–375.
  • Abdul Malik NA, Kumar IS, Nadarajah K. Elicitor and receptor molecules: orchestrators of plant defense and immunity. Int J Mol Sci. 2020;21(3):963.
  • Fouda A, Hassan SED, Eid AM, et al. The interaction between plants and bacterial endophytes under salinity stress. In: Endophytes and Secondary Metabolites. Cham: Springer; 2019. p. 591–607.
  • Tyagi S, Mulla SI, Lee K-J, et al. VOCs-mediated hormonal signaling and crosstalk with plant growth promoting microbes. Crit Rev Biotechnol. 2018;38(8):1277–1296.
  • Asghari S, Harighi B, Ashengroph M, et al. Induction of systemic resistance to Agrobacterium tumefaciens by endophytic bacteria in grapevine. Plant Pathol. 2020;69(5):827–837.
  • Dhanya S, Varghese S, Divya K, et al. Pseudomonas taiwanensis (MTCC11631) mediated induction of systemic resistance in Anthurium andreanum L against blight disease and visualisation of defence related secondary metabolites using confocal laser scanning microscopy. Biocatal Agric Biotechnol. 2020;24:101561.
  • Jiao R, Munir S, He P, et al. Biocontrol potential of the endophytic Bacillus amyloliquefaciens YN201732 against tobacco powdery mildew and its growth promotion. Biological Control. 2019;143:104160.
  • Liu H, Li J, Carvalhais LC, et al. Evidence for the plant recruitment of beneficial microbes to suppress soil‐borne pathogens. New Phytologist. 2021;229(5):2873–2885.
  • Safara S, Harighi B, Bahramnejad B, et al. Antibacterial activity of endophytic bacteria against sugar beet root rot agent by volatile organic compound production and induction of systemic resistance. Front Microbiol. 2022;13:1–14.
  • Nambirajan G, Ashok G, Baskaran K, et al. Bacillus and endomicrobiome: biodiversity and potential applications in agriculture. In: Advances in plant microbiome and sustainable agriculture. Singapore: Springer; 2020. p. 189–205.
  • Kumar RV, Singh RP, Mishra P. Endophytes as emphatic communication barriers of quorum sensing in Gram-positive and Gram-negative bacteria—a review. Environ Sustain. 2019;2:455–468.
  • Helman Y, Chernin L. Silencing the mob: disrupting quorum sensing as a means to fight plant disease. Mol Plant Pathol. 2015;16(3):316–329.
  • Akbari Kiarood SL, Rahnama K, Golmohammadi M, et al. Quorum‐quenching endophytic bacteria inhibit disease caused by Pseudomonas syringae pv. syringae in citrus cultivars. J Basic Microbiol. 2020;60(9):746–757.
  • Berde CV, Salvi SP, Rawool PP, et al. Role of medicinal plants and endophytic bacteria of medicinal plants in inhibition of biofilm formation: interference in quorum sensing. In: Implication of quorum sensing and biofilm formation in medicine, agriculture and food industry. Singapore: Springer; 2019. p. 177–188.
  • Miljaković D, Marinković J, Balešević-Tubić S. The significance of Bacillus spp. in disease suppression and growth promotion of field and vegeTable crops. Microorganisms. 2020;8(7):1037.
  • De Silva NI, Brooks S, Lumyong S, et al. Use of endophytes as biocontrol agents. Fungal Biol Rev. 2019;33(2):133–148.
  • Bhattacharyya P, Goswami M, Bhattacharyya L. Perspective of beneficial microbes in agriculture under changing climatic scenario: a review. J Phytol. 2016;8:26–41.
  • Prashar P, Kapoor N, Sachdeva S. Rhizosphere: its structure, bacterial diversity and significance. Rev Environ Sci Bio/Technol. 2014;13(1):63–77.
  • Wu L, Wu H-J, Qiao J, et al. Novel routes for improving biocontrol activity of Bacillus based bioinoculants. Front Microbiol. 2015;6:1395.
  • Lastochkina O, Seifikalhor M, Aliniaeifard S, et al. Bacillus spp.: efficient biotic strategy to control postharvest diseases of fruits and vegetables. Plants. 2019;8(4):97.
  • Pandey PK, Singh MC, Singh S, et al. Inside the plants: endophytic bacteria and their functional attributes for plant growth promotion. Int J Curr Microbiol Appl Sci. 2017;6:11–21.
  • Souza Rd, Ambrosini A, Passaglia LM. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet Mol Biol. 2015;38(4):401–419.
  • Frank AC, Saldierna Guzmán JP, Shay JE. Transmission of bacterial endophytes. Microorganisms. 2017;5(4):70.
  • Vinodkumar S, Nakkeeran S, Renukadevi P, et al. Diversity and antiviral potential of rhizospheric and endophytic Bacillus species and phyto-antiviral principles against tobacco streak virus in cotton. Agric Ecosyst Environ. 2018;267:42–51.
  • Yang F, Zhang R, Wu X, et al. An endophytic strain of the genus Bacillus isolated from the seeds of maize (Zea mays L.) has antagonistic activity against maize pathogenic strains. Microbial Pathog. 2020;142:104074.
  • Jing R, Li N, Wang W, et al. An endophytic strain JK of genus bacillus isolated from the seeds of super hybrid rice (Oryza sativa L., Shenliangyou 5814) has antagonistic activity against rice blast pathogen. Microbial Pathog. 2020;147:104422.
  • Cui L, Yang C, Wei L, et al. Isolation and identification of an endophytic bacteria Bacillus velezensis 8-4 exhibiting biocontrol activity against potato scab. Biol Control. 2020;141:104156.
  • Zhang P, Zhu Y, Ma D, et al. Screening, identification, and optimization of fermentation conditions of an antagonistic endophyte to wheat head blight. Agronomy. 2019;9(9):476.
  • Abdallah RAB, Jabnoun-Khiareddine H, Nefzi A, et al. Evaluation of the growth-promoting potential of endophytic bacteria recovered from healthy tomato plants. J Hortic For. 2018;5(2):1–10.
  • Denner W. The legislative aspects of the industrial enzymes in the manufacture of food and food ingredients. Ind Enzymol. 1996:397–411.
  • Aloo BN, Makumba B, Mbega ER. The potential of Bacilli rhizobacteria for sustainable crop production and environmental sustainability. Microbiol Res. 2019;219:26–39.
  • Caulier S, Nannan C, Gillis A, et al. Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Front Microbiol. 2019;10:302.
  • Shivaji S, Chaturvedi P, Suresh K, et al. Bacillus aerius sp. nov., Bacillus aerophilus sp. nov., Bacillus stratosphericus sp. nov. and Bacillus altitudinis sp. nov., isolated from cryogenic tubes used for collecting air samples from high altitudes. Int J Syst Evol Microbiol. 2006;56(7):1465–1473.
  • Sumpavapol P, Tongyonk L, Tanasupawat S, et al. Bacillus siamensis sp. nov., isolated from salted crab (poo-khem) in Thailand. Int J Syst Evol Microbiol. 2010;60(10):2364–2370.
  • Lai Q, Liu Y, Shao Z. Bacillus xiamenensis sp. nov., isolated from intestinal tract contents of a flathead mullet (Mugil cephalus). Antonie van Leeuwenhoek. 2014;105(1):99–107.
  • Dunlap CA, Saunders LP, Schisler DA, et al. Bacillus nakamurai sp. nov., a black-pigment-producing strain. Int J Syst Evol Microbiol. 2016;66(8):2987–2991.
  • Dunlap CA. Taxonomy of registered Bacillus spp. strains used as plant pathogen antagonists. Biol Control. 2019;134:82–86.
  • Fan B, Blom J, Klenk H-P, et al. Bacillus amyloliquefaciens, Bacillus velezensis, and Bacillus siamensis form an “operational group B. amyloliquefaciens” within the B. subtilis species complex. Front Microbiol. 2017;8:22.
  • Fira D, Dimkić I, Berić T, et al. Biological control of plant pathogens by Bacillus species. J Biotechnol. 2018;285:44–55.
  • Kushwaha P, Kashyap PL, Srivastava AK, et al. Plant growth promoting and antifungal activity in endophytic Bacillus strains from pearl millet (Pennisetum glaucum). Br J Microbiol. 2020;51(1):229–241.
  • Kaspar F, Neubauer P, Gimpel M. Bioactive secondary metabolites from Bacillus subtilis: a comprehensive review. J Nat Prod. 2019;82(7):2038–2053.
  • Ding T, Su B, Chen X, et al. An endophytic bacterial strain isolated from Eucommia ulmoides inhibits southern corn leaf blight. Front Microbiol. 2017;8:903.
  • Xie S, Liu J, Gu S, et al. Antifungal activity of volatile compounds produced by endophytic Bacillus subtilis DZSY21 against Curvularia lunata. Ann Microbiol. 2020;70(1):1–10.
  • Rabbee MF, Ali M, Choi J, et al. Bacillus velezensis: a valuable member of bioactive molecules within plant microbiomes. Molecules. 2019;24(6):1046.
  • Dhouib H, Zouari I, Abdallah DB, et al. Potential of a novel endophytic Bacillus velezensis in tomato growth promotion and protection against Verticillium wilt disease. Biol Control. 2019;139:104092.
  • Lopes R, Tsui S, Gonçalves PJ, et al. A look into a multifunctional toolbox: endophytic Bacillus species provide broad and underexploited benefits for plants. World J Microbiol Biotechnol. 2018;34(7):94.
  • Pršić J, Ongena M. Elicitors of plant immunity triggered by beneficial bacteria. Front Plant Sci. 2020;11:594530.
  • Andrić S, Meyer T, Ongena M. Bacillus responses to plant-associated fungal and bacterial communities. Front Microbiol. 2020;11:1350.
  • Yamamoto S, Shiraishi S, Suzuki S. Are cyclic lipopeptides produced by Bacillus amyloliquefaciens S13‐3 responsible for the plant defence response in strawberry against Colletotrichum gloeosporioides? Lett Appl Microbiol. 2015;60(4):379–386.
  • Gond SK, Bergen MS, Torres MS, et al. Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res. 2015;172:79–87.
  • Hasan N, Farzand A, Heng Z, et al. Antagonistic potential of novel endophytic bacillus strains and mediation of plant defense against verticillium wilt in upland cotton. Plants. 2020;9(11):1438.
  • Köhl J, Kolnaar R, Ravensberg WJ. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci. 2019;10:845.
  • Ray P, Lakshmanan V, Labbé JL, et al. Microbe to microbiome: a paradigm shift in the application of microorganisms for sustainable agriculture. Front Microbiol. 2020;11:3323.
  • Rajamanickam S, Karthikeyan G, Kavino M, et al. Biohardening of micropropagated banana using endophytic bacteria to induce plant growth promotion and restrain rhizome rot disease caused by Pectobacterium carotovorum subsp. Carotovorum. Sci Hortic. 2018;231:179–187.
  • Egamberdieva D, Wirth SJ, Shurigin VV, et al. Endophytic bacteria improve plant growth, symbiotic performance of chickpea (Cicer arietinum L.) and induce suppression of root rot caused by Fusarium solani under salt stress. Front Microbiol. 2017;8:1887.
  • Saha C, Mukherjee G, Agarwal‐Banka P, et al. A consortium of non‐rhizobial endophytic microbes from Typha angustifolia functions as probiotic in rice and improves nitrogen metabolism. Plant Biol. 2016;18(6):938–946.
  • Bradáčová K, Florea AS, Bar-Tal A, et al. Microbial consortia versus single-strain inoculants: an advantage in PGPM-assisted tomato production? Agronomy. 2019;9(2):105.
  • Wang Q, Zhou Q, Huang L, et al. Cadmium phytoextraction through Brassica juncea L. under different consortia of plant growth-promoting bacteria from different ecological niches. Ecotoxicol Environ Saf. 2022;237:113541.
  • Rosier A, Beauregard PB, Bais HP. Quorum quenching activity of the PGPR Bacillus subtilis UD1022 alters nodulation efficiency of Sinorhizobium meliloti on Medicago truncatula. Front Microbiol. 2021;11(3476):1–13.
  • Niu B, Wang W, Yuan Z, et al. Microbial interactions within multiple-strain biological control agents impact soil-borne plant disease. Front Microbiol. 2020;11(2452):1–16.
  • Qiu Z, Egidi E, Liu H, et al. New frontiers in agriculture productivity: optimised microbial inoculants and in situ microbiome engineering. Biotechnology advances. 2019;37(6):107371.
  • Vannier N, Agler M, Hacquard S. Microbiota-mediated disease resistance in plants. PLoS Pathog. 2019;15(6):e1007740.
  • Sessitsch A, Pfaffenbichler N, Mitter B. Microbiome applications from lab to field: facing complexity. Trends Plant Sci. 2019;24(3):194–198.
  • Xiong C, Zhu YG, Wang JT, et al. Host selection shapes crop microbiome assembly and network complexity. New Phytol. 2021;229(2):1091–1104.
  • Fitzpatrick CR, Salas-González I, Conway JM, et al. The plant microbiome: from ecology to reductionism and beyond. Annu Rev Microbiol. 2020;74:81–100.
  • Cordovez V, Dini-Andreote F, Carrión VJ, et al. Ecology and evolution of plant microbiomes. Annu Rev Microbiol. 2019;73:69–88.
  • Feng H, Zhang N, Du W, et al. Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol Plant Microbe Interact. 2018;31(10):995–1005.
  • Cregger M, Veach A, Yang Z, et al. The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome. 2018;6(1):31.
  • Yu P, Wang C, Baldauf JA, et al. Root type and soil phosphate determine the taxonomic landscape of colonizing fungi and the transcriptome of field‐grown maize roots. New Phytol. 2018;217(3):1240–1253.
  • Hartman K, van der Heijden MG, Wittwer RA, et al. Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming. Microbiome. 2020;8(1):66.
  • Hiruma K, Gerlach N, Sacristán S, et al. Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell. 2016;165(2):464–474.
  • Stringlis IA, Yu K, Feussner K, et al. MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci U S A. 2018;115(22):5213–5222.
  • Ganin H, Kemper N, Meir S, et al. Indole derivatives maintain the status quo between beneficial biofilms and their plant hosts. Mol Plant Microbe Interact. 2019;32(8):1013–1025.
  • Tewari S, Shrivas VL, Hariprasad P, et al. Harnessing endophytes as biocontrol agents. In: Plant health under biotic stress. Singapore: Springer; 2019. p. 189–218.
  • Munir S, Li Y, He P, et al. Unraveling the metabolite signature of citrus showing defense response towards Candidatus Liberibacter asiaticus after application of endophyte Bacillus subtilis L1-21. Microbiol Res. 2020;234:126425.
  • Yadav A, Yadav K. Exploring the potential of endophytes in agriculture: a minireview. Adv Plants Agric Res. 2017;6(4):102–106.
  • Christakis CA, Daskalogiannis G, Chatzakis A, et al. Halophytic bacterial endophytome: a potential source of beneficial microbes for a sustainable agriculture. bioRxiv. 2020;7:1–54.
  • Sarhan MS, Patz S, Hamza MA, et al. G3 PhyloChip analysis confirms the promise of plant-based culture media for unlocking the composition and diversity of the maize root microbiome and for recovering unculturable candidate divisions/phyla. Microb Environ. 2018;33(3):317–325.
  • Elsawey H, Patz S, Nemr RA, et al. Plant broth-(not bovine-) based culture media provide the most compatible vegan nutrition for in vitro culturing and in situ probing of plant microbiota. Diversity. 2020;12(11):418.
  • Yousaf S, Bulgari D, Bergna A, et al. Pyrosequencing detects human and animal pathogenic taxa in the grapevine endosphere. Front Microbiol. 2014;5:327.
  • Singh M, Kumar A, Singh R, et al. Endophytic bacteria: a new source of bioactive compounds. 3 Biotech. 2017;7(5):315.
  • Gadhave KR, Devlin PF, Ebertz A, et al. Soil inoculation with Bacillus spp. modifies root endophytic bacterial diversity, evenness, and community composition in a context-specific manner. Microbial Ecol. 2018;76(3):741–750.
  • Prasannakumar M, Mahesh H, Desai RU, et al. Metagenome sequencing of fingermillet-associated microbial consortia provides insights into structural and functional diversity of endophytes. 3 Biotech. 2020;10(1):15.
  • Paolinelli M, Escoriaza G, Cesari C, et al. Metatranscriptomic approach for microbiome characterization and host gene expression evaluation for “Hoja de malvón” disease in Vitis vinifera cv. Malbec. 2020.
  • Liu D, Li K, Hu J, et al. Biocontrol and action mechanism of Bacillus amyloliquefaciens and Bacillus subtilis in soybean phytophthora blight. Int J Mol Sci. 2019;20(12):2908.
  • Asaf S, Khan AL, Khan MA, et al. Complete genome sequencing and analysis of endophytic Sphingomonas sp. LK11 and its potential in plant growth. 3 Biotech. 2018;8(9):389.
  • Frank AC. The genomes of endophytic bacteria. In: Endophytes of forest trees. Cham: Springer; 2018. p. 141–176.
  • Dahmani MA, Desrut A, Moumen B, et al. Unearthing the plant growth-promoting traits of Bacillus megaterium RmBm31, an endophytic bacterium isolated from root nodules of Retama monosperma. Front Plant Sci. 2020;11:124.
  • Chen C, Yue Z, Chu C, et al. Complete genome sequence of bacillus sp. strain wr11, an endophyte isolated from wheat root providing genomic insights into its plant growth-promoting effects. Mol Plant Microbe Interact. 2020:876–879.
  • Naik S, Tsang A, Ramanan US, et al. Genome sequence resource of Bacillus velezensis EB14, a native endophytic bacterial strain with biocontrol potential against the poplar stem canker causative pathogen, Sphaerulina musiva. Phytopathology. 2020;111(5):890–892.
  • Pérez-Equihua A, Santoyo G. Draft genome sequence of Bacillus sp. strain E25, a biocontrol and plant growth-promoting bacterial endophyte isolated from Mexican Husk Tomato Roots (Physalis ixocarpa Brot. Ex Horm.). Microbiol Resour Announc. 2021;10(1):e01112-20.
  • Chen L, Shi H, Heng J, et al. Antimicrobial, plant growth-promoting and genomic properties of the peanut endophyte Bacillus velezensis LDO2. Microbiol Res. 2019;218:41–48.
  • Utturkar SM, Cude WN, Robeson MS, et al. Enrichment of root endophytic bacteria from Populus deltoides and single-cell-genomics analysis. Appl Environ Microbiol. 2016;82(18):5698–5708.
  • Murphy BR, Doohan FM, Hodkinson TR. From concept to commerce: developing a successful fungal endophyte inoculant for agricultural crops. J Fungi. 2018;4(1):24.
  • Morelli M, Bahar O, Papadopoulou KK, et al. Role of endophytes in plant health and defense against pathogens. Front Plant Sci. 2020;11(2020):1312.
  • Rao HY, Mohana NC, Satish S. Biocommercial aspects of microbial endophytes for sustainable agriculture. In: Microbial endophytes. UK: Woodhead Publishing; 2020. p. 323–347.
  • Santos URd, Costa MC, de Freitas GJ, et al. Exposition to biological control agent Trichoderma stromaticum increases the development of cancer in mice injected with murine melanoma. Front Cell Infect Microbiol. 2020;10:252.
  • Whitaker BK, Bakker MG. Bacterial endophyte antagonism toward a fungal pathogen in vitro does not predict protection in live plant tissue. FEMS Microbiol Ecol. 2019;95(2):fiy237.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.