Plant microbiome: Origin, composition, and functions
G.Sh. Galieva *, P.Yu. Galitskaya **, S.Yu. Selivanovskaya ***
Kazan Federal University, Kazan, 420008 Russia
E-mail: *goolnaz@rambler.ru, **gpolina33@yandex.ru, ***svetlana.selivanovskaya@kpfu.ru
Received July 12, 2022; Accepted September 28, 2022
REVIEW ARTICLE
DOI: 10.26907/2542-064X.2023.2.231-262
For citation: Galieva G.Sh., Galitskaya P.Yu., Selivanovskaya S.Yu. Plant microbiome: origin, composition, and functions. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2023, vol. 165, no. 2, pp. 231–262. doi: 10.26907/2542-064X.2023.2.231-262. (In Russian)
Abstract
Microorganisms play an important role in the growth and development of a plant throughout its entire life cycle. Recent advances in the methods of molecular biological analysis have expanded our understanding of the composition and functions of plant microbiota (epiphytic, rhizosphere, and endosphere) and the molecular mechanisms associated with specific processes that govern plant-microorganism interactions. This article reviews the types of plant microbial communities, their sources of origin, and species composition, as well as the critical role they play in modulating the plant immune response against phytopathogens, improving the elemental nutrition of plants, scaring away herbivorous animals, producing phytohormones, and enabling plants to thrive under extreme environmental conditions.
Keywords: phytobiome, rhizosphere microbiome, phyllosphere microbiome, epiphytic microbiome, endosphere microbiome, mycorrhiza, vertical and horizontal transfer of endosphere microorganisms, phytohormones, plant immune response, plant nutrition, phytopathogens
Acknowledgements. This study was funded by the subsidy allocated to Kazan Federal University for the state assignment in the sphere of scientific activities (project no. FZSM-2022-0003).
Figure Captions
Fig. 1. Plant phytobiome structure.
Fig. 2. Members of plant-associated microbial communities: main, additional, hub species, satellite species
References
1. Compant S., Samad A., Faist H., Sessitsch A. A review on the plant microbiome: Ecology, functions, and emerging trends in microbial application. J. Adv. Res., 2019, vol. 19, pp. 29–37. doi: 10.1016/j.jare.2019.03.004.
2. Leach J.E., Triplett L.R., Argueso C.T., Trivedi P. Communication in the phytobiome. Cell, 2017, vol. 169, no. 4, pp. 587–596. doi: 10.1016/j.cell.2017.04.025.
3. Zhang H., Li X., Yang Q., Sun L., Yang X., Zhou M., Deng R., Bi L. Plant growth, antibiotic uptake, and prevalence of antibiotic resistance in an endophytic system of pakchoi under antibiotic exposure. Int. J. Environ. Res. Public Health, 2017, vol. 14, no. 11, art. 1336. doi: 10.3390/ijerph14111336.
4. de Souza R., Ambrosini A., Passaglia L.M.P. Plant growth-promoting bacteria as inoculants in agricultural soils. Genet. Mol. Biol., 2015, vol. 38, no. 4, pp. 401–419. doi: 10.1590/S1415-475738420150053.
5. Gray E.J., Smith D.L. Intracellular and extracellular PGPR: Сommonalities and distinctions in the plant–bacterium signaling processes. Soil Biol. Biochem., 2005, vol. 37, no. 3, pp. 395–412. doi: 10.1016/j.soilbio.2004.08.030.
6. Bulgarelli D., Schlaeppi K., Spaepen S., van Themaat E.V.L., Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annu. Rev. Plant Biol., 2013, vol. 64, pp. 807–838. doi: 10.1146/annurev-arplant-050312-120106.
7. Hassani M.A., Durán P., Hacquard S. Microbial interactions within the plant holobiont. Microbiome, 2018, vol. 6, no. 1, art. 58. doi: 10.1186/s40168-018-0445-0.
8. Trivedi P., Leach J.E., Tringe S.G., Sa T., Singh B.K. Plant–microbiome interactions: From community assembly to plant health. Nat. Rev. Microbiol., 2020, vol. 18, no. 11, pp. 607–621. doi: 10.1038/s41579-020-0412-1.
9. Begum N., Qin C., Ahanger M.A., Raza S., Khan M.I., Ashraf M., Ahmed M., Zhang L. Role of arbuscular mycorrhizal fungi in plant growth regulation: Implications in abiotic stress tolerance. Front. Plant Sci., 2019, vol. 10, art. 1068. doi: 10.3389/fpls.2019.01068.
10. Semenov M., Nikitin D.A., Stepanov A.L., Semenov V.M. The structure of bacterial and fungal communities in the rhizosphere and root-free loci of gray forest soil. Eurasian Soil Sci., 2019, vol. 3, pp. 355–369. doi: 10.1134/S1064229319010137.
11. Afzal I., Shinwari Z.K., Sikandar S., Shahzad S. Plant beneficial endophytic bacteria: Mechanisms, diversity, host range and genetic determinants. Microbiol. Res., 2019, vol. 221, pp. 36–49. doi: 10.1016/j.micres.2019.02.001.
12. Dong C., Wang L., Li Q., Shang Q. Epiphytic and endophytic fungal communities of tomato plants. Hortic. Plant J., 2021, vol. 7, no. 1, pp. 38–48. doi: 10.1016/j.hpj.2020.09.002.
13. Lopez-Echartea E., Strejcek M., Mukherjee S., Uhlik O., Yrjälä K. Bacterial succession in oil-contaminated soil under phytoremediation with poplars. Chemosphere, 2020, vol. 243, art. 125242. doi: 10.1016/j.chemosphere.2019.125242.
14. Hamonts K., Trivedi P., Garg A., Janitz C., Grinyer J., Holford P., Botha F.C., Anderson I.C., Singh B.K. Field study reveals core plant microbiota and relative importance of their drivers. Environ. Microbiol., 2018, vol. 20, no. 1, pp. 124–140. doi: 10.1111/1462-2920.14031.
15. Rastogi G., Sbodio A., Tech J.J., Suslow T.V., Coaker G.L., Leveau J.H.J. Leaf microbiota in an agroecosystem: Spatiotemporal variation in bacterial community composition on field-grown lettuce. ISME J., 2012, vol. 6, no. 10, pp. 1812–1822. doi: 10.1038/ismej.2012.32.
16. Ruppel S., Krumbein A., Schreiner M. Composition of the phyllospheric microbial populations on vegetable plants with different glucosinolate and carotenoid compositions. Microb. Ecol., 2008, vol. 56, no. 2, pp. 364–372. doi: 10.1007/s00248-007-9354-7.
17. Steven B., Huntley R.B., Zeng Q. The influence of flower anatomy and apple cultivar on the apple flower phytobiome. Phytobiomes J., 2018, vol. 2, no. 3, pp. 171–179. doi: 10.1094/PBIOMES-03-18-0015-R.
18. Inácio J., Pereira P., Carvalho M., Fonseca Á., Amaral-Collaço M.T., Spencer-Martins I. Estimation and diversity of phylloplane mycobiota on selected plants in a Mediterranean-type ecosystem in Portugal. Microb. Ecol., 2002, vol. 44, no. 4, pp. 344–353. doi: 10.1007/s00248-002-2022-z.
19. Preto G., Martins F., Pereira J.A., Baptista P. Fungal community in olive fruits of cultivars with different susceptibilities to anthracnose and selection of isolates to be used as biocontrol agents. Biol. Control, 2017, vol. 110, pp. 1–9. doi: 10.1016/j.biocontrol.2017.03.011.
20. Rivas-Franco F., Hampton J.G., Narciso J., Rostás M., Wessman P., Saville D.J., Jackson T.A., Glare T.A. Effects of a maize root pest and fungal pathogen on entomopathogenic fungal rhizosphere colonization, endophytism and induction of plant hormones. Biol. Control, 2020, vol. 150, art. 104347. doi: 10.1016/j.biocontrol.2020.104347.
21. Ma B., Lv X., Warren A., Gong J. Shifts in diversity and community structure of endophytic bacteria and archaea across root, stem and leaf tissues in the common reed, Phragmites australis, along a salinity gradient in a marine tidal wetland of northern China. Antonie van Leeuwenhoek, 2013, vol. 104, no. 5, pp. 759–768. doi: 10.1007/s10482-013-9984-3.
22. Zuo Y., Hu Q., Zhang K., He X. Host and tissue affiliations of culturable endophytic fungi associated with xerophytic plants in the desert region of Northwest China. Agronomy, 2022, vol. 12, no. 3, art. 727. doi: 10.3390/agronomy12030727.
23. Liu H., Carvalhais L.C., Crawford M., Singh E., Dennis P.G., Pieterse C.M.J., Schenk P.M. Inner plant values: Diversity, colonization and benefits from endophytic bacteria. Front. Microbiol., 2017, vol. 8, art. 2552. doi: 10.3389/fmicb.2017.02552.
24. Chebotar V.K., Malfanova N.V., Shcherbakov A.V., Ahtemova G.A., Borisov A.Y., Lugtenberg B., Tikhonovich I.A. Endophytic bacteria in microbial drugs that improve plant development (Review). Appl. Biochem. Microbiol., 2015, vol. 51, no. 3, pp. 271–277. doi: 10.1134/S0003683815030059.
25. Durán M., San Emeterio L., Canals R.M. Comparison of culturing and metabarcoding methods to describe the fungal endophytic assemblage of Brachypodium rupestre growing in a range of anthropized disturbance regimes. Biology, 2021, vol. 10, no. 12, art. 1246. doi: 10.3390/biology10121246.
26. Duan M., Li H., Gu J., Tuo X., Sun W., Qian X., Wang X. Effects of biochar on reducing the abundance of oxytetracycline, antibiotic resistance genes, and human pathogenic bacteria in soil and lettuce. Environ. Pollut., 2017, vol. 224, pp. 787–795. doi: 10.1016/j.envpol.2017.01.021.
27. Taye Z.M., Helgason B.L., Bell J.K., Norris C.E., Vail S., Robinson S.J., Parkin I.A.P., Arcand M., Mamet S., Links M.G., Dowhy T., Siciliano S., Lamb E.G. Core and differentially abundant bacterial taxa in the rhizosphere of field grown Brassica napus genotypes: Implications for canola breeding. Front. Microbiol., 2020, vol. 10, art. 3007. doi: 10.3389/fmicb.2019.03007.
28. Toju H., Peay K.G., Yamamichi M., Narisawa K., Hiruma K., Naito K., Fukuda S., Ushio M., Nakaoka S., Onoda Y., Yoshida K., Schlaeppi K., Bai Y., Sugiura R., Ichihashi Y., Minamisawa K., Kiers E.T. Core microbiomes for sustainable agroecosystems. Nat. Plants, 2018, vol. 4, no. 5, pp. 247–257. doi: 10.1038/s41477-018-0139-4.
29. Jousset A., Bienhold C., Chatzinotas A., Gallien L., Gobet A., Kurm V., Küsel K., Rillig M.C., Rivett D.W., Salles J.F., van der Heijden M.G.A., Youssef N.H., Zhang X., Wei Z., Hol W.H.G. Where less may be more: How the rare biosphere pulls ecosystems strings. ISME J., 2017, vol. 11, no. 4, pp. 853–862. doi: 10.1038/ismej.2016.174.
30. Hanski I. Dynamics of regional distribution: The core and satellite species hypothesis. Oikos, 1982, vol. 38, no. 2, pp. 210–221. doi: 10.2307/3544021.
31. Chambers L.G., Guevara R., Boyer J.N., Troxler T.G., Davis S.E. Effects of salinity and inundation on microbial community structure and function in a mangrove peat soil. Wetlands, 2016, vol. 36, no. 2, pp. 361–371. doi: 10.1007/s13157-016-0745-8.
32. Lemanceau P., Blouin M., Muller D., Moënne-Loccoz Y. Let the core microbiota be functional. Trends Plant Sci., 2017, vol. 22, no. 7, pp. 583–595. doi: 10.1016/j.tplants.2017.04.008.
33. Hol W.H.G., de Boer W., de Hollander M., Kuramae E.E., Meisner A., van der Putten W.H. Context dependency and saturating effects of loss of rare soil microbes on plant productivity. Front. Plant Sci., 2015, vol. 6, art. 485. doi: 10.3389/fpls.2015.00485.
34. Zhang Y.-J., Hu H.-W., Chen Q.-L., Singh B.K., Yan H., Chen D., He J.-Z. Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes. Environ. Int., 2019, vol. 130, art. 104912. doi: 10.1016/j.envint.2019.104912.
35. Mendes R., Garbeva P., Raaijmakers J.M. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol. Rev., 2013, vol. 37, no. 5, pp. 634–663. doi: 10.1111/1574-6976.12028.
36. Gans J., Wolinsky M., Dunbar J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science, 2005, vol. 309, no. 5739, pp. 1387–1390. doi: 10.1126/science.1112665.
37. Zarraonaindia I., Owens S.M., Weisenhorn P., West K., Hampton-Marcell J., Lax S., Bokulich N.A., Mills D.A., Martin G., Taghavi S., van der Lelie D., Gilbert J.A. The soil microbiome influences grapevine-associated microbiota. mBio, 2015, vol. 6, no. 2, art. e02527-14. doi: 10.1128/mBio.02527-14.
38. Coleman-Derr D., Desgarennes D., Fonseca-Garcia C., Gross S., Clingenpeel S., Woyke T., North G., Visel A., Partida-Martinez L.P., Tringe S.G. Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species. New Phytol., 2016, vol. 209, no. 2, pp. 798–811. doi: 10.1111/nph.13697.
39. de Souza R.S.C., Okura V.K., Armanhi J.S.L., Jorrín B., Lozano N., da Silva M.J., González-Guerrero M., de Araújo L.M., Verza N.C., Bagheri H.C., Imperial J., Arruda P. Unlocking the bacterial and fungal communities assemblages of sugarcane microbiome. Sci. Rep., 2016, vol. 6, no. 1, art. 28774. doi: 10.1038/srep28774.
40. Rozpądek P., Domka A.M., Nosek M., Ważny R., Jędrzejczyk R.J., Wiciarz M., Turnau K. The role of strigolactone in the cross-talk between Arabidopsis thaliana and the endophytic fungus Mucor sp. Front. Microbiol., 2018, vol. 9, art. 441. doi: 10.3389/fmicb.2018.00441.
41. Arora N.K., Mishra J. Prospecting the roles of metabolites and additives in future bioformulations for sustainable agriculture. Appl. Soil Ecol., 2016, vol. 107, pp. 405–407. doi: 10.1016/j.apsoil.2016.05.020.
42. Oldroyd G.E.D. Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol., 2013, vol. 11, no. 4, pp. 252–263. doi: 10.1038/nrmicro2990.
43. Adebajo S.O., Akintokun P.O., Ojo A.E., Akintokun A.K., Badmos O.A. Recovery of biosurfactant using different extraction solvent by rhizospheric bacteria isolated from rice-husk and poultry waste biochar amended soil. Egypt. J. Basic Appl. Sci., 2020, vol. 7, no. 1, pp. 252–266. doi: 10.1080/2314808X.2020.1797377.
44. Goswami M., Deka S. Biosurfactant production by a rhizosphere bacteria Bacillus altitudinis MS16 and its promising emulsification and antifungal activity. Colloids Surf., B, 2019, vol. 178, pp. 285–296. doi: 10.1016/j.colsurfb.2019.03.003.
45. Pessione E., Garcia-Contreras R. Non-conventional antimicrobial agents. In: Rezaei N. (Ed.) Encyclopedia of Infection and Immunity. Vol. 4. Elsevier, 2022. pp. 586–607. doi: 10.1016/B978-0-12-818731-9.00136-1.
46. Wang F., Fu Y.-H., Sheng H.-J., Topp E., Jiang X., Zhu Y.-G., Tiedje J.M. Antibiotic resistance in the soil ecosystem: A One Health perspective. Curr. Opin. Environ. Sci. Health, 2021, vol. 20, art. 100230. doi: 10.1016/j.coesh.2021.100230.
47. Malfanova N., Franzil L., Lugtenberg B., Chebotar V., Ongena M. Cyclic lipopeptide profile of the plant-beneficial endophytic bacterium Bacillus subtilis HC8. Arch. Microbiol., 2012, vol. 194, no. 11, pp. 893–899. doi: 10.1007/s00203-012-0823-0.
48. Awasthi N., Kumar A., Makkar R., Cameotra S.S. Biodegradation of soil-applied endosulfan in the presence of a biosurfactant. J. Environ. Sci. Health, Part B, 1999, vol. 34, no. 5, pp. 793–803. doi: 10.1080/03601239909373226.
49. Dobrovol’skaya T.G. Struktura bakterial’nykh soobshchestv pochv [The Structure of Soil Bacterial Communities]. Moscow, IKTs Akademkniga, 2002. 282 p. (In Russian)
50. Feoktistova N.V., Mardanova A.M., Hadieva G.F., Sharipova M.R. Rhizosphere bacteria. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2016, vol. 158, no. 2, pp. 207–224. (In Russian)
51. Matilla M.A., Espinosa-Urgel M., Rodríguez-Herva J.J., Ramos J.L., Ramos-González M.I. Genomic analysis reveals the major driving forces of bacterial life in the rhizosphere. Genome Biol., 2007, vol. 8, no. 9, art. R179. doi: 10.1186/gb-2007-8-9-r179.
52. Gamalero E., Lingua G., Berta G., Lemanceau P. Methods for studying root colonization by introduced beneficial bacteria. In: Lichtfouse E., Navarrete M., Debaeke P., Véronique S., Alberola C. (Eds.) Sustainable Agriculture. Dordrecht, Springer, 2009, pp. 601–615. doi: 10.1007/978-90-481-2666-8_37.
53. Compant S., Clément C., Sessitsch A. Plant growth-promoting bacteria in the rhizo- and endosphere of plants: Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol. Biochem., 2010, vol. 42, no. 5, pp. 669–678. doi: 10.1016/j.soilbio.2009.11.024.
54. Jiménez-Bremont J.F., Marina M., Guerrero-González M. de la L., Rossi F.R., Sánchez-Rangel D., Rodríguez-Kessler M., Ruiz O.A., Gárriz A. Physiological and molecular implications of plant polyamine metabolism during biotic interactions. Front. Plant Sci., 2014, vol. 5, art. 95. doi: 10.3389/fpls.2014.00095.
55. Labutova N.M. Interactions between endomycorrhizal fungi and rhizosphere microorganisms. Mikol. Fitopatol., 2009, vol. 43, no. 1, pp. 3–19. (In Russian)
56. Pattnaik S.S., Busi S. Rhizospheric fungi: Diversity and potential biotechnological applications. In: Yadav A., Mishra S., Singh S., Gupta A. (Eds) Recent Advancement in White Biotechnology Through Fungi. Vol. 1: Diversity and enzymes perspectives. Ser.: Fungal Biology. Cham, Springer, 2019, pp. 63–84. doi: 10.1007/978-3-030-10480-1_2.
57. Kennedy A.C., de Luna L.Z. Rhizosphere. In: Hillel D. (Ed.) Encyclopedia of Soils in the Environment. Vol. 4. Acad. Press, 2005, pp. 399–406. doi: 10.1016/B0-12-348530-4/00163-6.
58. Poveda J., Eugui D., Abril-Urías P., Velasco P. Endophytic fungi as direct plant growth promoters for sustainable agricultural production. Symbiosis, 2021, vol. 85, no. 1, pp. 1–19. doi: 10.1007/s13199-021-00789-x.
59. Rajkumar H.G., Seema H.S., Sunil Kumar C.P. Diversity of arbuscular mycorrhizal fungi associated with some medicinal plants in Western Ghats of Karnataka region, India. World J. Nucl. Sci. Technol., 2012, vol. 2, no. 1, pp. 13–20.
60. Coutinho T.A., Bophela K.N. Chapter 7 – Tree leaves as a habitat for phyllobacteria. In: Asiegbu F.O., Kovalchuk A. (Eds.) Forest Microbiology. Vol. 1: Tree microbiome: Phyllosphere, endosphere and rhizosphere. Acad. Press, 2021, pp. 133–144. doi: 10.1016/B978-0-12-822542-4.00001-2.
For other references see (total number of references: 115) 
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