Skip to main content
Log in

Endophytes Modulate Plant Genes: Present Status and Future Perspectives

  • Review Article
  • Published:
Current Microbiology Aims and scope Submit manuscript

Abstract

Interactions among endophytes and plants are widespread and can vary from neutral or positive or negative. Plants are continually in a functionally dynamic state due to interactions with diverse endophytic microorganisms, which produce various metabolic substances. Through quorum sensing, these substances not only help endophytes to outcompete other host-associated pathogens or microbes but also allow them to overcome the plant immune system. Manifold interactions between endophytic microbiota cause a reflective impact on the host plant functioning and the development of ‘endobiomes,’ by synthesizing chemicals that fill the gap between host and endophytes. Despite the advances in the field, specific mechanisms for the endophytes’ precise methods to modulate plant genome and their effects on host plants remain poorly understood. Deeper genomic exploration can provide a locked away understanding of the competencies of endophytes and their conceivable function in host growth and health. Endophytes also can modify host metabolites, which could manipulate plants’ growth, adaptation, and proliferation, and can be a more exciting and puzzling topic that must be properly investigated. The consequence of the interaction of endophytes on the host genome was analyzed as it can help unravel the gray areas of endophytes about which very little or no knowledge exists. This review discusses the recent advances in understanding the future challenges in the emerging research investigating how endosymbionts affect the host’s metabolism and gene expression as an effective strategy for imparting resistance to biotic and abiotic challenges.

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

Similar content being viewed by others

Data Availability

Not applicable.

References

  1. Cui JL, Guo SX, Xiao PG (2017) Interaction between endophytes and host plant and the role of endophytes in genuineness analysis of medicinal plant. Acta Pharmaceutica Sin 52:214–221

    Google Scholar 

  2. Dubey A, Malla MA, Kumar A, Dayanandan S, Khan ML (2020) Plant endophytes: Unveiling hidden agenda for bioprospecting toward sustainable agriculture. Crit Rev Biotechnol 40(8):1210–1231. https://doi.org/10.1080/07388551.2020.1808584

    Article  CAS  PubMed  Google Scholar 

  3. Makar O, Kuzniar A, Patsula O, Kavulych Y, Kozlovskyy V, Wolinska A, Skórzynska-Polit E, Vatamaniuk O, Terek O, Romanyuk N (2021) Bacterial endophytes of spring wheat grains and the potential to acquire Fe, Cu, and Zn under their low soil bioavailability. Biology 10:409. https://doi.org/10.3390/biology10050409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Cui K, Xu T, Chen J, Yang H, Liu X, Zhuo R, Peng Y, Tang W, Wang R, Chen L, Zhang X, Zhang Z, He Z, Wang X, Liu C, Chen Y, Zhu Y (2022) Siderophores, a potential phosphate solubilizer from the endophyte Streptomyces sp. CoT10, improved phosphorus mobilization for host plant growth and rhizosphere modulation. J Cleaner Product 367:133110. https://doi.org/10.1016/j.jclepro.2022.133110

    Article  CAS  Google Scholar 

  5. Zhang X, Tong J, Dong M, Akhtar K, He B (2022) Isolation, identification and characterization of nitrogen fixing endophytic bacteria and their effects on cassava production. Peer J 10:e12677. https://doi.org/10.7717/peerj.12677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wang L, Xi N, Lang D, Zhou L, Zhang Y, Zhang X (2022) Potential biocontrol and plant growth promotion of an endophytic bacteria isolated from Glycyrrhiza uralensis seeds. Egyptian J Biol Pest Cont 32:55. https://doi.org/10.1186/s41938-022-00556-0

    Article  Google Scholar 

  7. Mengistu AA (2020) Endophytes: colonization, behaviour, and their role in defense mechanism. Int J Microbiol. https://doi.org/10.1155/2020/6927219

    Article  PubMed  PubMed Central  Google Scholar 

  8. Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kumar V, Nautiyal CS (2022) Plant abiotic and biotic stress alleviation: from an endophytic microbial perspective. Curr Microbiol 79(10):311. https://doi.org/10.1007/s00284-022-03012-2

    Article  CAS  PubMed  Google Scholar 

  10. Xu H, Gao J, Portieles R, Du L, Gao X, Borras-Hidalgo O (2022) Endophytic bacterium Bacillus aryabhattai induces novel transcriptomic changes to stimulate plant growth. PLoS ONE 17(8):e0272500. https://doi.org/10.1371/journal.pone.0272500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Nie P, Li X, Wang S, Guo J, Zhao H, Niu D (2017) Induced systemic resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET- and NPR1-dependent signaling pathway and activates PAMP-triggered immunity in Arabidopsis. Front Plant Science 8:238. https://doi.org/10.3389/fpls.2017.00238

    Article  Google Scholar 

  12. Khan MA, Asaf S, Khan AL, Jan R, Kang SM, Kim KM, Lee IJ (2020) Thermotolerance effect of plant growth promoting Bacillus cereus SA1 on soybean during heat stress. BMC Microbiol 20:175. https://doi.org/10.1186/s12866-020-01822-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chen XL, Sun MC, Chong SL, Si JP, Wu LS (2022) Transcriptomic and metabolomic approaches deepen our knowledge of plant-endophyte interactions. Front Plant Sci 12:00200. https://doi.org/10.3389/fpls.2021.700200

    Article  Google Scholar 

  14. Danneels B, Carlier A (2023) Whole genome sequencing of bacterial endophytes from fresh and preserved plant specimens. Methods Mol Biol 2605:133–155. https://doi.org/10.1007/978-1-0716-2871-3_7

    Article  PubMed  Google Scholar 

  15. Dalakouras A, Katsaouni A, Avramidou M, Dadami E, Tsiouri O, Vasileiadis S, Makris A, Georgopoulou ME, Papadopoulou KK (2023) A beneficial fungal root endophyte triggers systemic RNA silencing and DNA methylation of a host reporter gene. RNA Biol 20(1):20–30. https://doi.org/10.1080/15476286.2022.2159158

    Article  CAS  PubMed  Google Scholar 

  16. Tiwari P, Kang S, Bae H (2023) Plant-endophyte associations: Rich yet under-explored sources of novel bioactive molecules and applications. Microbiol Res 266:127241. https://doi.org/10.1016/j.micres.2022.127241

    Article  CAS  PubMed  Google Scholar 

  17. Pathak P, Rai VK, Can H, Singh SK, Kumar D, Bhardwaj N, Roychowdhury R, de Azevedo LCB, Kaushalendra V (2022) Plant-endophyte interaction during biotic stress management. Plants 11:2203. https://doi.org/10.3390/plants11172203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Balsanelli E, Tadra-Sfeir MZ, Faoro H, Pankievicz VC, de Baura VA, Pedrosa FO, de Souza EM, Dixon R, Monteiro RA (2016) Molecular adaptations of Herbaspirillum seropedicae during colonization of the maize rhizosphere. Environ Microbiol 18:2343–2356. https://doi.org/10.1111/1462-2920.12887

    Article  CAS  PubMed  Google Scholar 

  19. Shidore T, Dinse T, Ohrlein J, Becker A, Reinhold-Hurek B (2012) Transcriptomic analysis of responses to exudates reveal genes required for rhizosphere competence of the endophyte Azoarcus sp. strain BH72. Environ Microbiol 14:2775–2787. https://doi.org/10.1111/j.1462-2920.2012.02777.x

    Article  CAS  PubMed  Google Scholar 

  20. Camilios-Neto D, Bonato P, Wassem R, Tadra-Sfeir MZ, Brusamarello-Santos LC, Valdameri G, Donatti L, Faoro H, Weiss VA, Chubatsu LS (2014) Dual RNA-seq transcriptional analysis of wheat roots colonized by Azospirillum brasilense reveals up-regulation of nutrient acquisition and cell cycle genes. BMC Genom 15:378. https://doi.org/10.1186/1471-2164-15-378

    Article  CAS  Google Scholar 

  21. Jensen JB, Ampomah OY, Darrah R, Peters NK, Bhuvaneswari T (2005) Role of trehalose transport and utilization in Sinorhizobium meliloti alfalfa interactions. Mol Plant Microbe Interact 18:694–702. https://doi.org/10.1094/MPMI-18-0694

    Article  CAS  PubMed  Google Scholar 

  22. Ampomah OY, Avetisyan A, Hansen E, Svenson J, Huser T, Jensen JB, Bhuvaneswari T (2013) The thuEFGKAB operon of rhizobia and Agrobacterium tumefaciens code for transport of trehalose, maltitol and isomers of sucrose and their assimilation through the formation of their 3-ketoderivatives. J Bacteriol 195:3797–3807. https://doi.org/10.1128/JB.00478-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Formey D, Sallet E, Lelandais-Briere C, Ben C, Bustos-Sanmamed P, Niebel A, Frugier F, Combier JP, Debellé F, Hartmann C, Poulain J, Gavory F, Wincker P, Roux C, Gentzbittel L, Gouzy J, Crespi M (2014) The small RNA diversity from Medicago truncatula roots under biotic interactions evidences the environmental plasticity of the miRNAome. Genome Biol 15:57. https://doi.org/10.1186/s13059-014-0457-4

    Article  CAS  Google Scholar 

  24. Wu P, Wu Y, Liu CC, Liu LW, Ma FF, Wu XY, Wu M, Hang YY, Chen JQ, Shao ZQ, Wang B (2016) Identification of arbuscular mycorrhiza (AM)-responsive microRNAs in tomato. Front Plant Sci 7:429. https://doi.org/10.3389/fpls.2016.00429

    Article  PubMed  PubMed Central  Google Scholar 

  25. Plett JM, Martin FM (2018) Know your enemy, embrace your friend: Using omics to understand how plants respond differently to pathogenic and mutualistic microorganisms. Plant J 93:729–746. https://doi.org/10.1111/tpj.13802

    Article  CAS  PubMed  Google Scholar 

  26. Li Z, Wen W, Qin M, He Y, Xu D, Li L (2022) Biosynthetic mechanisms of secondary metabolites promoted by the interaction between endophytes and plant hosts. Front Microbiol 13:928967. https://doi.org/10.3389/fmicb.2022.928967

    Article  PubMed  PubMed Central  Google Scholar 

  27. Taghavi S, van der Lelie D (2013) Genome sequence of the plant growth-promoting endophytic bacterium Enterobacter sp. 638. In: Molecular Microbial Ecology of the Rhizosphere, 1 & 2, F. J. de Bruijn F. https://doi.org/10.1002/9781118297674.ch84

  28. Bosamia TC, Barbadikar KM, Modi A (2020) Genomic insights of plant endophyte interaction: prospective and impact on plant fitness, Editor(s): Kumar A, Radhakrishnan EK, Microbial Endophytes, Woodhead Publishing, pp 227–249 https://doi.org/10.1016/B978-0-12-819654-0.00009-0

  29. Mishra A, Singh SP, Mahfooz S, Singh SP, Bhattacharya A, Mishra N, Nautiyal CS (2018) Endophyte-mediated modulation of defense related genes and systemic resistance in Withania somnifera (L.) Dunal under Alternaria alternata stress. Appl Environ Microbiol 84:e02845-e2917. https://doi.org/10.1128/AEM.02845-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nautiyal CS, Srivastava S, Chauhan PS, Seem K, Mishra A, Sopory SK (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem 66:1–9. https://doi.org/10.1016/j.plaphy.2013.01.020

    Article  CAS  PubMed  Google Scholar 

  31. Liao HL, Bonito G, Rojas JA, Hameed K, Wu S, Schadt CW, Labbé J, Tuskan GA, Martin F, Grigoriev IV, Vilgalys R (2019) Fungal endophytes of Populus trichocarpa alter host phenotype, gene expression, and rhizobiome composition. Mol Plant Microbe Interact 32(7):853–864. https://doi.org/10.1094/MPMI-05-18-0133-R

    Article  CAS  PubMed  Google Scholar 

  32. Montejano-Ramírez V, García-Pineda E, Valencia-Cantero E (2020) Bacterial compound N, N-dimethylhexadecylamine modulates expression of iron deficiency and defense response genes in Medicago truncatula independently of the jasmonic acid pathway. Plants 9(5):624. https://doi.org/10.3390/plants9050624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang L, Wang Y, Lei S, Zhang H, Liu Z, Yang J, Niu Q (2023) Effect of volatile compounds produced by the cotton endophytic bacterial strain Bacillus sp. T6 against Verticillium wilt. BMC Microbiol 23(1):8. https://doi.org/10.1186/s12866-022-02749-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Jing M, Xu X, Peng J, Li C, Zhang H, Lian C, Chen Y, Shen Z, Chen C (2022) Comparative genomics of three Aspergillus strains reveals insights into endophytic lifestyle and endophyte-induced plant growth promotion. J Fungi 8:690. https://doi.org/10.3390/jof8070690

    Article  CAS  Google Scholar 

  35. Salvi P, Mahawar H, Agarrwal R, Kajal GV, Deshmukh R (2022) Advancement in the molecular perspective of plant-endophytic interaction to mitigate drought stress in plants. Front Microbiol 13:981355. https://doi.org/10.3389/fmicb.2022.981355

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ramos Aguila LC, Sánchez Moreano JP, Akutse KS, Bamisile BS, Liu J, Haider FU, Ashraf HJ, Wang L (2023) Comprehensive genome-wide identification and expression profiling of ADF gene family in Citrus sinensis, induced by endophytic colonization of Beauveria bassiana. Int J Biol Macromol 225:886–898. https://doi.org/10.1016/j.ijbiomac.2022.11.153

    Article  CAS  PubMed  Google Scholar 

  37. Sirikantaramas S, Yamazaki M, Saito K (2009) A survival strategy: the coevolution of the camptothecin biosynthetic pathway and self-resistance mechanism. Phytochemistry 70:1894–1898. https://doi.org/10.1016/j.phytochem.2009.07.034

    Article  CAS  PubMed  Google Scholar 

  38. Camaille M, Fabre N, Clément C, Ait Barka E (2021) Advances in wheat physiology in response to drought and the role of plant growth promoting rhizobacteria to trigger drought tolerance. Microorganisms 9:687. https://doi.org/10.3390/microorganisms9040687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Wang Z, Zhu J, Li W, Li R, Wang X, Qiao H, Sun Q, Zhang H (2020) Antibacterial mechanism of the polysaccharide produced by Chaetomium globosum CGMCC 6882 against Staphylococcus aureus. Int J Biol Macromol 159:231–235. https://doi.org/10.1016/j.ijbiomac.2020.04.269

    Article  CAS  PubMed  Google Scholar 

  40. de Lamo FJ, Šimkovicová M, Fresno DH, de Groot T, Tintor N, Rep M, Takken FLW (2021) Pattern-triggered immunity restricts host colonization by endophytic fusaria, but does not affect endophyte-mediated resistance. Mol Plant Pathol 22(2):04–215. https://doi.org/10.1111/mpp.13018

    Article  CAS  Google Scholar 

  41. Shurigin V, Alaylar B, Davranov K, Wirth S, Bellingrath-Kimura SD, Egamberdieva D (2021) Diversity and biological activity of culturable endophytic bacteria associated with marigold (Calendula officinalis L.). AIMS Microbiol 7:336–353. https://doi.org/10.3934/microbiol.2021021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ray P, Guo Y, Chi M, Krom N, Boschiero C, Watson B, Huhman D, Zhao P, Singan V, Lindquist E, Yan J, Adam C, Craven K (2021) Serendipita fungi modulate the switchgrass root transcriptome to circumvent host defenses and establish a symbiotic relationship. Mol Plant-Microbe Interac 34(10):1128–1142. https://doi.org/10.1094/mpmi-04-21-0084-r

    Article  CAS  Google Scholar 

  43. Shekhawat K, Saad MM, Sheikh A, Mariappan K, Al-Mahmoudi H, Abdulhakim F, Eida AA, Jalal R, Masmoudi K, Hirt H (2021) Root endophyte induced plant thermotolerance by constitutive chromatin modification at heat stress memory gene loci. EMBO Rep 22:51049

    Article  Google Scholar 

  44. Zhu Y, Zhu S, Zhang F, Zhao Z, Christensen MJ, Nan Z, Zhang X (2022) Transcriptomic Analyses reveals molecular regulation of photosynthesis by Epichloë endophyte in Achnatherum inebrians under Blumeria graminis Infection. J Fungi 8:1201. https://doi.org/10.3390/jof8111201

    Article  CAS  Google Scholar 

  45. De Rocchis V, Jammer A, Camehl I, Franken P, Roitsch T (2022) Tomato growth promotion by the fungal endophytes Serendipita indica and Serendipita herbamans is associated with sucrose de-novo synthesis in roots and differential local and systemic effects on carbohydrate metabolisms and gene expression. J Plant Physiol 276:153755. https://doi.org/10.1016/j.jplph.2022.153755

    Article  CAS  PubMed  Google Scholar 

  46. Oviedo-Pereira DG, López-Meyer M, Evangelista-Lozano S, Sarmiento-López LG, Sepúlveda-Jiménez G, Rodríguez-Monroy M (2022) Enhanced specialized metabolite, trichome density, and biosynthetic gene expression in Stevia rebaudiana (Bertoni) Bertoni plants inoculated with endophytic bacteria Enterobacter hormaechei. Peer J 10:e13675. https://doi.org/10.7717/peerj.13675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhou H, Wang Y, Zhang Y, Xie Y, Nadeem H, Tang C (2022) Flagellin C decreases the expression of the Gossypium hirsutum cation/proton exchanger 3 gene to promote calcium ion, hydrogen peroxide, and nitric oxide and synergistically regulate the resistance of cotton to Verticillium wilt. Front Plant Sci 13:969506. https://doi.org/10.3389/fpls.2022.969506

    Article  PubMed  PubMed Central  Google Scholar 

  48. Huang X, Zeng Z, Chen Z, Tong X, Jiang J, He C, Xiang T (2022) Deciphering the potential of a plant growth promoting endophyte Rhizobium spWYJ-E13, and functional annotation of the genes involved in the metabolic pathway. Front Microbiol 13:035167. https://doi.org/10.3389/fmicb.2022.1035167

    Article  Google Scholar 

  49. Nataraja KN, Dhanyalakshmi KH, Govind G, Oelmüller R (2022) Activation of drought tolerant traits in crops: endophytes as elicitors. Plant Signal Behav 17(1):2120300. https://doi.org/10.1080/15592324.2022.2120300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Fadiji AE, Babalola OO (2020) Elucidating mechanisms of endophytes used in plant protection and other bioactivities with multifunctional prospects. Front BioEng BioTechnol 8:467. https://doi.org/10.3389/fbioe.2020.00467

    Article  PubMed  PubMed Central  Google Scholar 

  51. Gururani MA, Upadhyaya CP, Baskar V, Venkatesh J, Nookaraju A, Park SW (2013) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul 32:245–258. https://doi.org/10.1007/s00344-012-9292-6

    Article  CAS  Google Scholar 

  52. Harman GE, Uphoff N (2019) Symbiotic root-endophytic soil microbes improve crop productivity and provide environmental benefits. Scientifica 2:106395. https://doi.org/10.1155/2019/9106395

    Article  CAS  Google Scholar 

  53. Ahmad I, Jiménez-Gasco MdM, Luthe DS, Barbercheck ME (2022) Endophytic Metarhizium robertsii suppresses the phytopathogen, Cochliobolus heterostrophus and modulates maize defenses. PLoS ONE 17(9):e0272944. https://doi.org/10.1371/journal.pone.0272944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Yi HS, Yang JW, Ryu CM (2013) ISR meets SAR outside: additive action of the endophyte Bacillus pumilus INR7 and the chemical inducer, benzothiadiazole, on induced resistance against bacterial spot in field-grown pepper. Front Plant Sci 4:122. https://doi.org/10.3389/fpls.2013.00122

    Article  PubMed  PubMed Central  Google Scholar 

  55. Lu H, Wei T, Lou H, Shu X, Chen Q (2021) A critical review on communication mechanism within plant-endophytic fungi interactions to cope with biotic and abiotic stresses. J Fungi (Basel) 7(9):719. https://doi.org/10.3390/jof7090719

    Article  CAS  PubMed  Google Scholar 

  56. Newman MA, Sundelin T, Nielsen JT, Erbs G (2013) MAMP (microbe-associated molecular pattern) triggered immunity in plants. Front Plant Sci 4:139. https://doi.org/10.3389/fpls.2013.00139

    Article  PubMed  PubMed Central  Google Scholar 

  57. Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma LJ, Sessitsch A (2017) Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Ann Rev Phytopathol 55(1):1–83. https://doi.org/10.1146/annurev-phyto-080516-035641

    Article  CAS  Google Scholar 

  58. Li N, Han X, Feng D, Yuan D, Huang LJ (2019) Signaling crosstalk between salicylic acid and ethylene/jasmonate in plant defense: do we understand what they are whispering? Int J Mol Sci 20:671. https://doi.org/10.3390/ijms20030671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Abdul Malik NA, Kumar IS, Nadarajah K (2020) Elicitor and receptor molecules: orchestrators of plant defense and immunity. Int J Mol Sci 21(3):963. https://doi.org/10.3390/ijms21030963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Rehman N, Khan MR, Abbas Z (2020) Functional characterization of mitogen-activated protein kinase (MAPKK) gene in halophytic Salicornia europaea against salt stress. Environ Exppt Bot 171:103934. https://doi.org/10.1016/j.envexpbot.2019.103934

    Article  CAS  Google Scholar 

  61. Kusajima M, Shima S, Fujita M, Minamisawa K, Che FS, Yamakawa H, Nakashita H (2018) Involvement of ethylene signaling in Azospirillum sp. B510-induced disease resistance in rice. Biosci Biotechnol Biochem 82(9):1522–1526. https://doi.org/10.1080/09168451.2018.1480350

    Article  CAS  PubMed  Google Scholar 

  62. Pinski A, Betekhtin A, Hupert-Kocurek K, Mur LAJ, Hasterok R (2019) Defining the genetic basis of plant–endophytic bacteria interactions. Int J Mol Sci 20:1947. https://doi.org/10.3390/ijms20081947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Levy A, Conway JM, Dangi JL, Woyke T (2018) Elucidating bacterial gene functions in the plant microbiome. Cell Host Microbe 24:475–485. https://doi.org/10.1016/j.chom.2018.09.005

    Article  CAS  PubMed  Google Scholar 

  64. Deng Y, Chen H, Li C, Xu J, Qi Q, Xu Y, Zhu Y, Zheng J, Peng D, Ruan L, Sun M (2019) Endophyte Bacillus subtilis evade plant defense by producing lantibiotic subtilomycin to mask self-produced flagellin. Commun Biol 2:368. https://doi.org/10.1038/s42003-019-0614-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Liu H, Carvalhais LC, Crawford M, Singh E, Dennis PG, Pieterse CMJ, Schenk PM (2017) Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front Microbiol 8:2552. https://doi.org/10.3389/fmicb.2017.02552

    Article  PubMed  PubMed Central  Google Scholar 

  66. Zhou JU, Sun K, Chen F, Yuan J, Li X, Dai CC (2018) Endophytic Pseudomonas induces metabolic flux changes that enhance medicinal sesquiterpenoid accumulation in Atractylodes lancea. Plant Physiol Biochem 130:473–481. https://doi.org/10.1016/j.plaphy.2018.07.016

    Article  CAS  PubMed  Google Scholar 

  67. Acuña SM, Floeter-Winter LM, Muxel SM (2020) MicroRNAs: Biological regulators in pathogen-host interactions. Cells 9(1):113. https://doi.org/10.3390/cells9010113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Salamon S, Zok J, Gromadzka K, Błaszczyk L (2021) Expression Patterns of miR398, miR167, and miR159 in the interaction between bread wheat (Triticum aestivum L.) and pathogenic Fusarium culmorum and beneficial Trichoderma Fungi. Pathogens 10(11):1461. https://doi.org/10.3390/pathogens10111461

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Pentimone I, Lebrón R, Hackenberg M, Rosso LC, Colagiero M, Nigro F, Ciancio A (2018) Identification of tomato miRNAs responsive to root colonization by endophytic Pochonia chlamydosporia. Appl Microbiol Biotechnol 102:907–919. https://doi.org/10.1007/s00253-017-8608-7

    Article  CAS  PubMed  Google Scholar 

  70. Tiwari P, Bae H (2020) Horizontal gene transfer and endophytes: an implication for the acquisition of novel traits. Plants (Basel) 9(3):305. https://doi.org/10.3390/plants9030305

    Article  CAS  PubMed  Google Scholar 

  71. Maier BA, Kiefer P, Field CM, Hemmerle L, Bortfeld-Miller M, Emmenegger B, Schäfer M, Pfeilmeier S, Sunagawa S, Vogel CM, Vorholt JA (2021) A general non-self response as part of plant immunity. Nat Plants 7:696–705. https://doi.org/10.1038/s41477-021-00913-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Kaushal R, Peng L, Singh SK, Zhang M, Zhang X, Vílchez JI, Wang Z, He D, Yang Y, Lv S, Xu Z, Morcillo RJL, Wang W, Huang W, Paré PW, Song CP, Zhu JK, Liu R, Zhong W, Ma P, Zhang H (2021) Dicer-like proteins influence Arabidopsis root microbiota independent of RNA-directed DNA methylation. Microbiome 9:57. https://doi.org/10.1186/s40168-020-00966-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Pandey SS, Singh S, Babu CS, Shanker K, Srivastava NK, Kalra A (2016) Endophytes of opium poppy differentially modulate host plant productivity and genes for the biosynthetic pathway of benzylisoquinoline alkaloids. Planta 243(5):1097–1114. https://doi.org/10.1007/s00425-016-2467-9

    Article  CAS  PubMed  Google Scholar 

  74. Sun WJ, Zhu HT, Zhang TY, Zhang MY, Wang D, Yang CR, Zhang YX, Zhang YJ (2018) Two new alkaloids from Fusarium tricinctum SYPF 7082, an endophyte from the root of Panax notoginseng. Nat Prod Bioprospect 8:391–396. https://doi.org/10.1007/s13659-018-0171-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Chaudhary R, Kumar V, Gupta S, Naik B, Prasad R, Mishra S, Saris PE, Kumar V (2023) Finger Millet (Eleusine coracana) plant-endophyte dynamics: plant growth, nutrient uptake, and zinc biofortification. Microorganisms 11(4):973. https://doi.org/10.3390/microorganisms11040973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Tamošiûnë I, Stanienë G, Haimi P, Stanys V, Rugienius R, Baniulis D (2018) Endophytic Bacillus and Pseudomonas spp. modulate apple shoot growth, cellular redox balance, and protein expression under in vitro conditions. Front Plant Sci 9:889. https://doi.org/10.3389/fpls.2018.00889

    Article  PubMed  PubMed Central  Google Scholar 

  77. Hasan N, Khan IU, Farzand A, Heng Z, Moosa A, Saleem M, Canming T (2022) Bacillus altitudinis HNH7 and Bacillus velezensis HNH9 promote plant growth through upregulation of growth-promoting genes in upland cotton. J Appl Microbiol 132:3812–3824. https://doi.org/10.1111/jam.15511

    Article  CAS  PubMed  Google Scholar 

  78. Qin L, Tian P, Cui Q, Hu S, Jian W, Xie C, Yang X, Shen H (2021) Bacillus circulans GN03 alters the microbiota, promotes cotton seedling growth and disease resistance, and increases the expression of phytohormone synthesis and disease resistance-related genes. Front Plant Sci 12:644597. https://doi.org/10.3389/fpls.2021.644597

    Article  PubMed  PubMed Central  Google Scholar 

  79. da Silva Santos SDS, da Silva AA, Polonio JC, Polli AD, Orlandelli RC, Dos Santos Oliveira JADS, Brandão Filho JUT, Azevedo JL, Pamphile JA (2022) Influence of plant growth-promoting endophytes Colletotrichum siamense and Diaporthe masirevici on tomato plants (Lycopersicon esculentum Mill.). Mycology 13(4):257–270. https://doi.org/10.1080/21501203.2022.2050825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Jahn L, Storm-Johannsen L, Seidler D, Noack J, Gao W, Schafhauser T, Wohlleben W, van Berkel WJH, Jacques P, Kar T, Piechulla B, Ludwig-Muller J (2022) The endophytic fungus Cyanodermella asteris influences growth of the nonnatural host plant Arabidopsis thaliana. Mol Plant Microbe Interact 35(1):49–63. https://doi.org/10.1094/MPMI-03-21-0072-R

    Article  CAS  PubMed  Google Scholar 

  81. Mousa WK, Schwan A, Davidson J, Strange P, Liu H, Zhou T, Auzanneau F-I, Raizada MN (2015) An endophytic fungus isolated from finger millet (Eleusine coracana) produces antifungal natural products. Front Microbiol 6:1157. https://doi.org/10.3389/fmicb.2015.01157

    Article  PubMed  PubMed Central  Google Scholar 

  82. Oviedo-Pereira DG, López-Meyer M, Evangelista-Lozano S, Sarmiento-López LG, Sepúlveda-Jiménez G, Rodríguez-Monroy M (2022) Enhanced specialized metabolite, trichome density, and biosynthetic gene expression in Stevia rebaudiana (Bertoni) Bertoni plants inoculated with endophytic bacteria Enterobacter hormaechei. PeerJ 10:e13675. https://doi.org/10.7717/peerj.13675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Fuchs B, Krischke M, Mueller MJ, Krauss J, Biere A (2017) Herbivore specific induction of defence metabolites in a grass-endophyte association. Funct Ecol 31:318–324. https://doi.org/10.1111/1365-2435.12755

    Article  Google Scholar 

  84. García-Latorre C, Rodrigo S, Marin-Felix Y, Stadler M, Santamaria O (2023) Plant-growth promoting activity of three fungal endophytes isolated from plants living in dehesas and their effect on Lolium multiflorum. Sci Rep 13:7354. https://doi.org/10.1038/s41598-023-34036-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Sun BT, Akutse KS, Xia XF, Chen JH, Ai X, Tang Y, Wang Q, Feng BW, Goettel MS, You MS (2018) Endophytic effects of Aspergillus oryzae on radish (Raphanus sativus) and its herbivore, Plutella xylostella. Planta 248(3):705–714. https://doi.org/10.1007/s00425-018-2928-4

    Article  CAS  PubMed  Google Scholar 

  86. Waqas M, Khan AL, Hamayun M, Shahzad R, Kang SM, Kim JG, Lee IJ (2015) Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum and Aspergillus terreus. J Plant Interact 10:280–287. https://doi.org/10.1080/17429145.2015.1079743

    Article  CAS  Google Scholar 

  87. Yuan J, Zhang W, Sun K, Tang MJ, Chen PX, Li X, Dai CC (2019) Comparative transcriptomics and proteomics of Atractylodes lancea in response to endophytic fungus Gilmaniella sp. AL12 reveals regulation in plant metabolism. Front Microbiol 10:1208. https://doi.org/10.3389/fmicb.2019.01208

    Article  PubMed  PubMed Central  Google Scholar 

  88. Bilal S, Shahzad R, Imran M, Jan R, Kim KM, Lee IJ (2020) Synergistic association of endophytic fungi enhances Glycine max L. resilience to combined abiotic stresses: Heavy metals, high temperature and drought stress. Ind Crop Prod 143:111931. https://doi.org/10.1016/j.indcrop.2019.111931

    Article  CAS  Google Scholar 

  89. Bilal S, Shahzad R, Khan AL, Al-Harrasi A, Kim CK, Lee IJ (2019) Phytohormones enabled endophytic Penicillium funiculosum LHL06 protects Glycine max L. from synergistic toxicity of heavy metals by hormonal and stress-responsive proteins modulation. J Hazard Mater 379:11. https://doi.org/10.1016/j.jhazmat.2019.120824

    Article  CAS  Google Scholar 

  90. Khan AL, Waqas M, Hussain J, Al-Harrasi A, Hamayun M, Lee IJ (2015) Phytohormones enabled endophytic fungal symbiosis improve aluminum phytoextraction in tolerant Solanum lycopersicum: An example of Penicillium janthinellum LK5 and comparison with exogenous GA3. J Hazard Mater 295:70–78. https://doi.org/10.1016/j.jhazmat.2015.04.008

    Article  CAS  PubMed  Google Scholar 

  91. Fu WQ, Xu M, Sun K, Chen XL, Dai CC, Jia Y (2020) Remediation mechanism of endophytic fungus Phomopsis liquidambaris on phenanthrene in vivo. Chemosphere 243:125305. https://doi.org/10.1016/j.chemosphere.2019.125305

    Article  CAS  PubMed  Google Scholar 

  92. Abdelaziz ME, Kim D, Ali S, Fedoroff NV, Al-Babili S (2017) The endophytic fungus Piriformospora indica enhances Arabidopsis thaliana growth and modulates Na (+)/K (+) homeostasis under salt stress conditions. Plant Sci 263:107–115. https://doi.org/10.1016/j.plantsci.2017.07.006

    Article  CAS  PubMed  Google Scholar 

  93. Zachow C, Jahanshah G, de Bruijn I, Song C, Ianni F, Pataj Z, Gerhardt H, Pianet I, Lämmerhofer M, Berg G, Gross H (2015) The novel lipopeptide poaeamide of the endophyte Pseudomonas poae RE* 1–1-14 is involved in pathogen suppression and root colonization. Mol Plant Microbe Interact 28(7):800–810. https://doi.org/10.1094/mpmi-12-14-0406-r

    Article  CAS  PubMed  Google Scholar 

  94. Deja-Sikora E, Kowalczyk A, Trejgell A, Szmidt-Jaworska A, Baum C, Mercy L, Hrynkiewicz K (2020) Arbuscular mycorrhiza changes the impact of Potato Virus Y on growth and stress tolerance of Solanum tuberosum L. in vitro. Front Microbiol 10:2971. https://doi.org/10.3389/fmicb.2019.02971

    Article  PubMed  PubMed Central  Google Scholar 

  95. Tavares M, Nascimento F, Glick B, Rossi M (2018) The expression of an exogenous ACC deaminase by the endophyte Serratia grimesii BXF1 promotes the early nodulation and growth of common bean. Lett Appl Microbiol 66:252–259. https://doi.org/10.1111/lam.12847

    Article  CAS  PubMed  Google Scholar 

  96. Jaemsaeng R, Jantasuriyarat C, Thamchaipenet A (2018) Molecular interaction of 1-aminocyclopropane-1-carboxylate deaminase (ACCD)-producing endophytic Streptomyces sp. GMKU 336 towards salt-stress resistance of Oryza sativa L. cv. KDML105. Sci Rep 8:1–15. https://doi.org/10.1038/s41598-018-19799-9

    Article  CAS  Google Scholar 

  97. Tseng Y-H, Rouina H, Groten K, Rajani P, Furch ACU, Reichelt M, Baldwin IT, Nataraja KN, Uma Shaanker R, Oelmüller R (2020) An Endophytic Trichoderma strain promotes growth of its hosts and defends against pathogen attack. Front Plant Sci 11:573670. https://doi.org/10.3389/fpls.2020.573670

    Article  PubMed  PubMed Central  Google Scholar 

  98. Miranda V, Silva-Castro GA, Ruiz-Lozano JM, Fracchia S (2023) García-Romera I (2023) Fungal endophytes enhance wheat and tomato drought tolerance in terms of plant. J Fungi 9(3):384

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Thanks to Dr. Vijay Dhasmana, Chancellor, Swami Rama Himalayan University, Jolly Grant, Dehradun, Uttarakhand, for providing the necessary facilities to contribute to this article.

Funding

This research received no specific grant from public, commercial, or not-for-profit funding agencies.

Author information

Authors and Affiliations

Authors

Contributions

VK conceptualized the article, original draft preparation, and data curation; CSN intellectualized, reviewed, edited, and made final changes to the manuscript. Both authors checked and certified the final article.

Corresponding author

Correspondence to Vivek Kumar.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Code Availability

Not applicable.

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kumar, V., Nautiyal, C.S. Endophytes Modulate Plant Genes: Present Status and Future Perspectives. Curr Microbiol 80, 353 (2023). https://doi.org/10.1007/s00284-023-03466-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00284-023-03466-y

Navigation