Formation of Plant Microbiomes. Hypotheses and Controversies
DOI:
https://doi.org/10.15407/Keywords:
rhizosphere, rhizoplane, endosphere, spermosphere, soil microorganisms, seed endophytesAbstract
Microorganisms play a key role in promoting plant growth, facilitating the assimilation of biogenic element compounds, increasing resistance to biogenic and abiogenic stress factors. The vast majority of researchers believe that the source of rhizosphere and endophytic microorganisms is the soil (horizontal provision hypothesis). At the same time, today there is growing interest in the concept of the formation of the plant microbiome as a result of heredity (vertical provision рнзщеруіші). A significant number of publications indicate that seed endophytic microorganisms may play a major role in this process. The presented literature review considers existing points of view on the processes of plant microbiome assembly with an emphasis on the importance of seed endophytes.
Downloads
References
Abdelfattah, A., Wisniewski, M., Schena, L. & Tack, A. J. M. (2021)/ Experimental evidence of microbial inheritance in plants and transmission routes from seed to phyllosphere and root. Environmental Microbiology, 23(4), 2199-2214. https://doi.org/10.1111/1462-2920.15392
Adam, E., Bernhart, M., Müller, H. et al. (2018). The Cucurbita pepo seed microbiome: genotype-specific composition and implications for breeding. Plant Soil, 422, 35-49. https://doi.org/10.1007/s11104-016-3113-9
Alekseev, A. M. (1969). [Water regime of plant cells in connection with metabolism and structuring of cytoplasm]. XXIII Timiryazev reading. Moscow: Publishing House Nauka, 36. [In russian].
Arif, I., Batool, M., & Schenk, P. M. (2020). Plant microbiome engineering: expected benefits for improved crop growth and resilience. Trends Biotechnol, 38, 1385-1396. https://doi.org/10.1016/j.tibtech.2020.04.015
Bacilio-Jiménez, M., Aguilar-Flores, S., del Valle, M. V., Pérez, A., Zepeda, A., & Zenteno, E. (2001). Endophytic bacteria in rice seeds inhibit early colonization of roots by Azospirillum brasilense. Soil Biol Biochem, 33, 167-172. https://doi.org/10.1016/S0038-0717(00)00126-7
Bais, H. P., Fall, R., & Vivanco J. M. (2004). Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol, 134(1), 307-319. https://doi.org/10.1104/pp.103.028712
Bais, H. P., Weir, T. L., Perry, L. G., Gilroy, S., & Vivanco, J. M. (2006). The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol, 57, 233-266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
Barea, J. M. (2015). Future challenges and perspectives for applying microbial biotechnology in sustainable agriculture based on a better understanding of plant-microbiome interactions. J Soil Sci Plant Nutr, 15, 261-282. https://doi.org/10.4067/S0718-95162015005000021
Barret, M., Briand, M., Bonneau, S. Préveaux, A., Valière, S., Bouchez, O., Hunault, G., Simoneau, P., & Jacquesa, M. A. (2015). Emergence shapes the structure of the seed microbiota. Appl Environ Microbiol, 81, 1257-1266. https://doi.org/10.1128/AEM.03722-14
Batista, B. D., & Singh, B. K. (2021). Realities and hopes in the application of microbial tools in agriculture. Microbial biotechnol, 14(4), 1258-1268. https://doi.org/10.1111/1751-7915.13866
Behm, J. E., Geurts, R., & Kiers, E. T. (2014). Parasponia: a novel system for studying mutualism stability. Trends Plant Sci, 19(12), 757-763. https://doi.org/10.1016/j.tplants.2014.08.007
Berendsen, R. L., Pieterse, C. M. J., & Bakker, P. A. H. M. (2012). The rhizosphere microbiome and plant health. Trends Plant Sci, 17(8), 478-486. https://doi.org/10.1016/j.tplants.2012.04.001
Berg, G., & Raaijmakers, J. M. (2018). Saving seed microbiomes. ISME J,12(5), 1167-1170. https://doi.org/10.1038/s41396-017-0028-2
Berg, G., & Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol, 68, 1-13. https://doi.org/10.1111/j.1574-6941.2009.00654.x
Berg, G., Rybakova, D., Fischer, D. et al. (2020). Microbiome definition re-visited: old concepts and new challenges. Microbiome, 8(103). https://doi.org/10.1186/s40168-020-00875-0
Bergna, A., Cernava, T., Rändler, M., Grosch, R., Zachow, C., & Berg, G. (2018). Tomato seeds preferably transmit plant beneficial endophytes. Phytobiomes J, 2, 183-193. https://doi.org/10.1094/PBIOMES-06-18-0029-R
Boller, T., & Felix, G. (2009). Arenaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol, 60, 379-406. https://doi.org/10.1146/annurev.arplant.57.032905.105346
Brader, G., Compant, S., Mitter, B., Trognitz, F., & Sessitsch, A. (2014). Metabolic potential of endophytic bacteria. Curr Opin Biotechnol, 27, 30-37. https://doi.org/10.1016/j.copbio.2013.09.012
Bright, M., & Bulgheresi, S. (2010). A complex journey: Transmission of microbial symbionts. Nat Rev Microbiol, 8, 218-230. https://doi.org/10.1038/nrmicro2262
Brockett, B. F. T., Prescott, C. E., & Grayston, S. J. (2012). Soil moisture is the major factor influencing microbial community structure and enzyme activities across seven biogeoclimatic zones in western Canada. Soil Biol Biochem, 44, 9-20. https://doi.org/10.1016/j.soilbio.2011.09.003
Broeckling, C. D., Broz, A. K., Bergelson, J., Manter, D. K., & Vivanco, J. M. (2008). Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol, 74, 738-744. https://doi.org/10.1128/AEM.02188-07
Buee, M., De Boer, W., Martin, F., van Overbeek, L., & Jurkevitch, E. (2009). The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant Soil, 321, 189-212. https://doi.org/10.1007/s11104-009-9991-3
Bulgarelli, D., Rott, M., Schlaeppi, K., et al. (2012). Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature, 488, 91-95. https://doi.org/10.1038/nature11336
Bulgarelli, D., Schlaeppi, K., Spaepen, S., van Themaat, E. V. L., & Schulze-Lefert, P. (2013). Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol, 64, 807-838. https://doi.org/10.1146/annurev-arplant-050312-120106
Cankar, K., Kraigher, H., Ravnikar, M., & Rupnik, M. (2005). Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiol Lett, 244, 341-345. https://doi.org/10.1016/j.femsle.2005.02.008
Carvalhais, L. C., Dennis, P. G., & Schenk, P. M. (2014). Plant defence inducers rapidly influence the diversity of bacterial communities in a potting mix. Appl Soil Ecol, 84, 1- 5. https://doi.org/10.1016/j.apsoil.2014.06.011
Chaudhary, P., Agri, U., Chaudhary, A., Kumar, A., & Kumar, G. (2022). Endophytes and their potential in biotic stress management and crop production. Front Microbiol, 13, 933017. https://doi.org/10.3389/fmicb.2022.933017
Chimwamurombe, P. M., Groenemeyer, J. L., & Reinhold-Hurek, B. (2016). Isolation and characterization of culturable seedassociated bacterial endophytes from gnotobiotically grown Marama bean seedlings. FEMS Microbiol Ecol, 92(6), article fiw083. https://doi.org/10.1093/femsec/fiw083
Compant, S., Mitter, B., Colli-Mull, J. G., Gangl, H., & Sessitsch, A. (2011). Endophytes of Grapevine Flowers, Berries, and Seeds: Identification of Cultivable Bacteria, Comparison with Other Plant Parts, and Visualization of Niches of Colonization. Microb Ecol, 62, 188-197. https://doi.org/10.1007/s00248-011-9883-y
Compant, S., Reiter, B., Sessitsch, A., Nowak, J., Clément, C., & Barka, E. A. (2005). Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol, 71, 1685-1693. https://doi.org/10.1128/AEM.71.4.1685-1693.2005
Cope-Selby, N., Cookson, A., Squance, M., Donnison, I., Flavell, R., & Farrar, K. (2017). Endophytic bacteria in Miscanthus seed: implications for germination, vertical inheritance of endophytes, plant evolution and breeding. Glob Change Biol Bioenergy, 9, 57-77. https://doi.org/10.1111/gcbb.12364
Cottyn, B., Regalado, E., Lanoot, B., De Cleene, M., Mew, T. W., & Swings, J. (2001). Bacterial populations associated with rice seed in the tropical environment. Phytopathol, 91(3). 282-292. https://doi.org/10.1094/PHYTO.2001.91.3.282
Darrasse, A., Bureau, C., Samson, R., Morris, C. E. & Jacques, M. A. (2007). Contamination of bean seeds by Xanthomonas axonopodis pv. phaseoli associated with low bacterial densities in the phyllosphere under field and greenhouse conditions. Eur J Plant Pathol, 119, 203-215. https://doi.org/10.1007/s10658-007-9164-2
Darrasse, A., Darsonval, A., Boureau, T., Brisset, M., Durand, K., & Jacques, M. (2010). Transmission of plant-pathogenic bacteria by nonhost seeds without induction of an associated defense reaction at emergence. Appl Environ Microbiol, 76, 6787-6796. https://doi.org/10.1128/AEM.01098-10
Darriaut, R., Lailheugue, V., Masneuf-Pomar'ede, I. Marguerit, E., Martins, G., Stéphane Compant, S., Ballestra, P., Upton, S., Ollat, N., & Lauvergeat, V. (2022). Grapevine rootstock and soil microbiome interactions: keys for a resilient viticulture. Hortic Res, 9. https://doi.org/10.1093/hr/uhac019
Dawkins, R. (1989). (Original edition 1982 reprinted 1983, 1987, 1988, 1989): The extended phenotype. Oxford paperbacks, Oxford University Press, Oxford, UK. 307.
Dominguez-Bello, M. G., Costello, E. K., Contreras, M., Magris, M., Hidalgo, G., Fierer, N., & Knight, R. (2010). Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci USA, 107(26), 11971-11975. https://doi.org/10.1073/pnas.1002601107
Dotaniya, M. L., & Meena, V. D. (2015). Rhizosphere effect on nutrient availability in soil and its uptake by plants: a review. Proc Natl Acad Sci Ind (Sect. B Biol. Sci), 85, 1-12. https://doi.org/10.1007/s40011-013-0297-0
Dutta, B., Gitaitis, R., Sanders, H., Booth, C., Smith, S., & Langston, D. B. (2014a). Role of blossom colonization in pepper seed infestation by Xanthomonas euvesicatoria. Phytopathology, 104, 232-239. https://doi.org/10.1094/PHYTO-05-13-0138-R
Dutta, B., Gitaitis, R., Smith, S., & Langston, D. (2014b). Interactions of seedborne bacterial pathogens with host and non-host plants in relation to seed infestation and seedling transmission. Plos One, 9. https://doi.org/10.1371/journal.pone.0099215
Edwards, J., Johnson, C., Santos-Medellín, C., Lurie, E., Podishetty, N. K., Bhatnagar, S., Eisen, J. A., & Sundaresan, V. (2015). Structure, variation, and assembly of the root-associated microbiomes of rice. Plant biology, 112(8), 911-920. https://doi.org/10.1073/pnas.1414592112
Ferreira, A., Quecine, M. C., Lacava, P. T., Oda, S., Azevedo, J. L., & Araújo, W. L. (2008). Diversity of endophytic bacteria from Eucalyptus species seeds and colonization of seedlings by Pantoea agglomerans. FEMS Microbiol Lett, 287, 8-14. https://doi.org/10.1111/j.1574-6968.2008.01258.x
Fitzpatrick, C. R., Copeland, J., Wang, P. W., Guttman, D. S., Kotanen, P. M., & Johnson, M. T. J. (2018). Assembly and ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci USA, 115, 1157-1165. https://doi.org/10.1073/pnas.1717617115
Frank, A. C., Guzmán, J. P. S., & Shay, J. E. (2017). Transmission of Bacterial Endophytes. Microorganisms, 5(4), 70. https://doi.org/10.3390/microorganisms5040070
Fürnkranz, M., Lukesch, B., Müller, H., et al. (2012). Microbial Diversity Inside Pumpkins: Microhabitat-Specific Communities Display a High Antagonistic Potential against Phytopathogens. Microb Ecol, 63, 418-428. https://doi.org/10.1007/s00248-011-9942-4
Gagne-Bourgue, F., Aliferis, K. A., Seguin, P., Rani, M., Samson, R., & Jabaji, S. (2013). Isolation and characterization of indigenous endophytic bacteria associated with leaves of switchgrass (Panicum virgatum L.) cultivars. J Appl Microbiol, 114, 836-853. https://doi.org/10.1111/jam.12088
Garbeva, P.V., van Elsas, J. D., & van Veen, J. A. (2008). Rhizosphere microbial community and its response to plant species and soil history. Plant Soil, 302, 19-32. https://doi.org/10.1007/s11104-007-9432-0
Gehring, C. A., Sthultz, C. M., Flores-Rentería, L., Whipple, A. V., & Whitham, T. G. (2017). Tree genetics defines fungal partner communities that may confer drought tolerance. Proc Natl Acad Sci USA, 114, 11169-11174. https://doi.org/10.1073/pnas.1704022114
Germida, J. J., Siciliano, S. D., De Freitas, J. R., & Seib, A. M. (1998). Diversity of root-associated bacteria associated with field-grown canola (Brassica napus L.) and wheat (Triticum aestivum L.). FEMS Microbiol Ecol, 26, 43-50. https://doi.org/10.1111/j.1574-6941.1998.tb01560.x
Glassner, H., Zchori-Fein, E., Yaron, S., Sessitsch, A., Sauer, U., & Compant, S. (2017). Bacterial niches inside seeds of Cucumis melo L. Plant Soil, 422, 101-113. https://doi.org/10.1007/s11104-017-3175-3
Goggin, D. E., Emery, R. J. N., Kurepin, L.V., & Powles, S. B. (2015). A potential role for endogenous microflora in dormancy release, cytokinin metabolism and the response to fluridone in Lolium rigidum seeds. Ann Bot, 115, 293-301. https://doi.org/10.1093/aob/mcu231
Graner, G., Persson, P., Meijer, J., & Alstrom, S. (2003). A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol Lett, 224, 269-276. https://doi.org/10.1016/S0378-1097(03)00449-X
Grayston, S. J., Wang, S., Campbell, C. D., & Edwards, A. C. (1998). Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem, 30, 369-378. https://doi.org/10.1016/S0038-0717(97)00124-7
Gundel, P. E., Rudgers, J. A., & Ghersa, C. M. (2011). Incorporating the process of vertical transmission into understanding of host-symbiont dynamics. Oikos, 120, 1121-1128. https://doi.org/10.1111/j.1600-0706.2011.19299.x
Haichar, F. Z., Marol, C., Berge, O., et al. (2008). Plant host habitat and root exudates shape soil bacterial community structure. ISME J, 2, 1221-1230. https://doi.org/10.1038/ismej.2008.80
Hameed, A., Yeh, M. W., Hsieh, Y. T., et al. (2015). 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, 394, 177-197. https://doi.org/10.1007/s11104-015-2506-5
Hardoim, P. (2019). The ecology of seed microbiota. In Seed Endophytes: Biology and Biotechnology (S. K. Verma and J. J. F. White (eds). Cham: Springer International Publishing, 103-125. https://doi.org/10.1007/978-3-030-10504-4_6
Hardoim, P. R., & van Elsas, J. D. (2013). Properties of bacterial endophytes leading to maximized host fitness. F.J. de Bruijn (ed). Molecular Microbial Ecology of the Rhizosphere, vol 1. Wiley Blackwell, Hoboken, New Jersey, USA, 405-411. https://doi.org/10.1002/9781118297674.ch37
Hardoim, P. R., Hardoim, C. C., van Overbeek, L. S., & van Elsas, J. D. (2012). Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE, 7, article e30438. https://doi.org/10.1371/journal.pone.0030438
Hodgson, S., de Cates, C., Hodgson, J., Morley, N. J., Sutton, B. C, & Gange, A. C. (2014). Vertical transmission of fungal endophytes is widespread in forbs. Ecol Evol, 4, 1199-1208. https://doi.org/10.1002/ece3.953
Huang, Y. L., Kuang, Z. Y., Wang, W. F., & Cao, L. X. (2016). Exploring potential bacterial and fungal biocontrol agents transmitted from seeds to sprouts of wheat. Biol Control, 98, 27-33. https://doi.org/10.1016/j.biocontrol.2016.02.013
Hude, E. O. (1954). The function of the hilum in some Papilionaceae in relation to ripening of the seed and the permeability of the testa. Ann Bot, 18, 241-256. https://doi.org/10.1093/oxfordjournals.aob.a083393
Inceoglu, O., Van Overbeek, L. S., Salles, J. F., & van Elsas, J. D. (2013). The normal operating range of bacterial communities in soil used for potato cropping. Appl Environ Microbiol, 79, 1160-1170. https://doi.org/10.1128/AEM.02811-12
Jacoby, R., Peukert, M., Succurro, A., Koprivova, A., & Kopriva, S. (2017). The role of soil microorganisms in plant mineral nutrition-current knowledge and future directions. Front Plant Sci, 8, 1617. https://doi.org/10.3389/fpls.2017.01617
Johnston-Monje, D., & Raizada, M. N. (2011). Conservation and diversity of seed associated endophytes in Zea across boundaries of evolution, ethnography and ecology. PLoS ONE, 6, article e20396. https://doi.org/10.1371/journal.pone.0020396
Johnston-Monje, D., Lundberg, D. S., Lazarovits, G., Reis, V. M., & Raizada, M. N. (2016). Bacterial populations in juvenile maize rhizospheres originate from both seed and soil. Plant Soil, 405, 337-355. https://doi.org/10.1007/s11104-016-2826-0
Jones, J. D. G., & Dangl, J. L. (2006). The plant immune system. Nature, 444(7117), 323-329. https://doi.org/10.1038/nature05286
Kaga, H., Mano, H., Tanaka, F., Watanabe, A., Kaneko, S., & Morisaki, H. (2009). Rice seeds as sources of endophytic bacteria. Microbes Environ, 24, 154-162. https://doi.org/10.1264/jsme2.ME09113
Khan, Z., Guelich, G., Phan, H., Redman, R., & Doty, S. (2012). Bacterial and Yeast Endophytes from Poplar and Willow Promote Growth in Crop Plants and Grasses. ISRN Agron, article 890280. https://doi.org/10.5402/2012/890280
Kirk, J. L., Klironomos, J. N., Lee, H., & Trevors, J. T. (2005). The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environ Pollut, 133, 455-465. https://doi.org/10.1016/j.envpol.2004.06.002
Kong, H. G., Song, G. C., & Ryu, C. M. (2019). Inheritance of seed and rhizosphere microbial communities through plant-soil feedback and soil memory. Environ Microbiol Rep, 11, 479-486. https://doi.org/10.1111/1758-2229.12760
Krutylo, D. V. (2007). [Study of soybean seed microflora as one of the probable factors of Bradyrhizobium japonicum spread]. Agricultural Microbiology, 6, 84-91. https://doi.org/10.35868/1997-3004.6.84-91 [In Ukrainian]. https://doi.org/10.35868/1997-3004.6.84-91
Lareen, A., Burton, F., & Schafer, P. (2016). Plant root-microbe communication in shaping root microbiomes. Plant Mol Biol, 90, 575-587. https://doi.org/10.1007/s11103-015-0417-8
Lau, J. A., Lennon, J. T., & Heath, K. D. (2017). Trees harness the power of microbes to survive climate change. Proc Natl Acad Sci USA, 114, 11009-11011. https://doi.org/10.1073/pnas.1715417114
Lemaire, B., Janssens, S., Smets, E., & Dessein, S. (2012). Endosymbiont Transmission Mode in Bacterial Leaf Nodulation as Revealed by a Population Genetic Study of Psychotria leptophylla. Appl Environ Microbiol, 78(1), 284-287. https://doi.org/10.1128/AEM.06130-11
Links, M. G., Demeke, T., Grafenhan, T., Hill, J. E., Hemmingsen, S. M., & Dumonceaux, T. J. (2014). Simultaneous profiling of seedassociated bacteria and fungi reveals antagonistic interactions between microorganisms within a shared epiphytic microbiome on Triticum and Brassica seeds. New Phytol, 202, 542-553. https://doi.org/10.1111/nph.12693
Liu, H., Khan, M. Y., Carvalhais, L. C. Delgado-Baquerizo, M., Yan, L., Crawford, M., Dennis, P. G., Brajesh Singh, B., & Schenk P. M. (2019). Soil amendments with ethylene precursor alleviate negative impacts of salinity on soil microbial properties and productivity. Sci Rep, 9, article 6892. https://doi.org/10.1038/s41598-019-43305-4
Liu, Y., Zuo, S., Zou, Y., Wang, J., & Song, W. (2013). Investigation on diversity and population succession dynamics of endophytic bacteria from seeds of maize (Zea mays L., Nongda108) at different growth stages. Ann Microbiol, 63, 71-79. https://doi.org/10.1007/s13213-012-0446-3
Lladó, S., López-Mondéjar, R., & Baldrian, P. (2018). Drivers of microbial community structure in forest soils. Appl Microbiol Biotechnol, 102(10), 4331-4338. https://doi.org/10.1007/s00253-018-8950-4
López-López, A., Rogel, M. A., Ormeno-Orrillo, E., Martínez-Romero, J. & Martínez-Romero, E. (2010). Phaseolus vulgaris seed-borne endophytic community with novel bacterial species such as Rhizobium endophyticum sp. nov. Syst Appl Microbiol, 33, 322-327. https://doi.org/10.1016/j.syapm.2010.07.005
Lugtenberg, B. J. J., Chin-a-Woeng, T. F. C., & Bloemberg, G. V. (2002). Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek, 81, 373-383. https://doi.org/10.1023/A:1020596903142
Lundberg, D. S., Lebeis, S. L., Paredes, S. H., et al. (2012). Defining the core Arabidopsis thaliana root microbiome. Nature, 488, 86-90. https://doi.org/10.1038/nature11237
Ma, Y., Rajkumar, M., Luo, Y., & Freitas, H. (2011). Inoculation of endophytic bacteria on host and non-host plants-Effects on plant growth and Ni uptake. J Hazard Mater, 195, 230-237. https://doi.org/10.1016/j.jhazmat.2011.08.034
Maillet, F., Poinsot, V., André, O., et al. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature, 469(7328), 58-63. https://doi.org/10.1038/nature09622
Mastrett, C., Taghavi, S., van Der Lelie, D., et al. (2009). Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytoremediat, 11, 251-267. https://doi.org/10.1080/15226510802432678
Mendes, R., Kruijt, M., de Bruijn, I., Dekkers, E., van der Voort, M., Schneider, J. H. M., Piceno, Y. M., Desantis, T. Z., Andersen, G. L., Bakker, P. A. H., & Raaijmakers, J. M. (2011). Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science, 332(6033), 1097-1100. https://doi.org/10.1126/science.1203980
Mercado-Blanco, J. (2015). Life of microbes inside the plant. B. Lugtenberg (ed). Principles of Plant-Microbe Interactions. Springer International Publishing Switzerland, Heidelberg, 25-32. https://doi.org/10.1007/978-3-319-08575-3_5
Miethling, R., Wieland, G., Backhaus, H., & Tebbe, C. C. (2000). Variation in microbial rhizosphere communities in response to crop species, soil origin, and inoculation with Sinorhizobium meliloti L33. Microb Ecol, 40, 43-56. https://doi.org/10.1007/s002480000021
Miller, I. M. (1990). Bacterial Leaf Nodule Symbiosis. Advances in Botanical Research, 17, 163-234. https://doi.org/10.1016/S0065-2296(08)60134-2
Mitter, B., Pfaffenbichler, N., Flavell, R., et al. (2017). A New Approach to Modify Plant Microbiomes and Traits by Introducing Beneficial Bacteria at Flowering into Progeny Seeds. Front Microbiol, 8. https://doi.org/10.3389/fmicb.2017.00011
Moran, N. A. (2006). Symbiosis. Curr Biol, 16(20), 866-871. https://doi.org/10.1016/j.cub.2006.09.019
Moroenyane, I., Tremblay, J., & Yergeau, É. (2021). Soybean Microbiome Recovery after Disruption Is Modulated by the Seed and Not the Soil Microbiome. Phytobiomes J, 5, 418-431. https://doi.org/10.1094/PBIOMES-01-21-0008-R
Morrissey, J. P., Dow, J. M., Mark, G. L., & O'gara, F. (2004). Are microbes at the root of a solution to world food production? Rational exploitation of interactions between microbes and plants can help to transform agriculture. EMBO Rep, 5, 922-926. https://doi.org/10.1038/sj.embor.7400263
Mukhopadhyay, K., Garrison, N. K., Hinton, D. M., et al. (1996). Identification and characterization of bacterial endophytes of rice. Mycopathologia, 134, 151-159. https://doi.org/10.1007/BF00436723
Nelson, E. B. (2004). Microbial dynamics and interactions in the spermosphere. Annu Rev Phytopathol, 42, 271-309. https://doi.org/10.1146/annurev.phyto.42.121603.131041
Nelson, E. B. (2018). The seed microbiome: Origins, interactions, and impacts. Plant Soil, 422, 7-34. https://doi.org/10.1007/s11104-017-3289-7
Okunishi, S., Sako, K., Mano, H., Imamura, A., & Morisaki, H. (2005). Bacterial flora of endophytes in the maturing seed of cultivated rice (Oryza sativa). Microbes Environ, 20, 168-177. https://doi.org/10.1264/jsme2.20.168
Ovcharov, K. E. (1976). [Physiology of formation and germination of seeds]. Moscow: Publishing House Kolos, 246. [In russian].
Oucala, N., Aissat, K., & Pastor, V. (2021). Bacterial Endophytes: The Hidden Actor in Plant Immune Responses against Biotic Stress. Plants (Basel), 10(15), 1012. https://doi.org/10.3390/plants10051012
Palmer, C., Bik, E. M., Di Giulio, D. B., Relman, D. A., & Brown, P. O. (2007). Development of the human infant intestinal microbiota. PLoS Biol, 5(7), article e177. https://doi.org/10.1371/journal.pbio.0050177
Pérez-Jaramillo, J. E., Mendes, R., & Raaijmakers, J. M. (2016). Impact of plant domestication on rhizosphere microbiome assembly and functions. Plant Mol Biol, 90(6), 635-644. https://doi.org/10.1007/s11103-015-0337-7
Pitzschke, A. (2016). Developmental Peculiarities and Seed-Borne Endophytes in Quinoa: Omnipresent, Robust Bacilli Contribute to Plant Fitness. Front Microbiol, 7. https://doi.org/10.3389/fmicb.2016.00002
Poncini, L., Wyrsch, I., Tendon, V. D., Vorley, T., Boller, T., Geldner, N., Métraux, J-P., & Lehmann, S. (2017). In roots of Arabidopsis thaliana, the damage-associated molecular pattern AtPep1 is a stronger elicitor of immune signalling than flg22 or the chitin heptamer. PLoS ONE, 12(10), article e0185808. https://doi.org/10.1371/journal.pone.0185808
Porras-Alfaro, A., & Bayman, P. (2011). Hidden fungi, emergent properties: Endophytes and microbiomes. Ann Rev Phytopathol, 49, 291-315. https://doi.org/10.1146/annurev-phyto-080508-081831
Puente, M. E., Li, C. Y., & Bashan, Y. (2009a). Endophytic bacteria in cacti seeds can improve the development of cactus seedlings. Environ Exp Bot, 66(3), 402-408. https://doi.org/10.1016/j.envexpbot.2009.04.007
Puente, M. E., Li, C. Y., & Bashan, Y. (2009b). Rockdegrading endophytic bacteria in cacti. Environ Exp Bot, 66(3), 389-401. https://doi.org/10.1016/j.envexpbot.2009.04.010
Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C., & Mo€enne-Loccoz, Y. (2009). The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil, 321, 341-361. https://doi.org/10.1007/s11104-008-9568-6
Ringelberg, D., Foley, K., & Reynolds, C. M. (2012). Bacterial endophyte communities of two wheatgrass varieties following propagation in different growing media. Can J Microbiol, 58, 67-80. https://doi.org/10.1139/w11-122
Rochefort, A., Briand, M., Marais, C., et al. (2019). Influence of environment and host plant genotype on the structure and diversity of the Brassica napus seed microbiota. Phytobiomes J, 3, 326-336. https://doi.org/10.1094/PBIOMES-06-19-0031-R
Rodríguez, C. E., Antonielli, L., Mitter, B., Trognitz, F., & Sessitsch, A. (2020). Heritability and functional importance of the Setaria viridis bacterial seed microbiome. Phytobiomes J, 4, 40-52. https://doi.org/10.1094/PBIOMES-04-19-0023-R
Rosenblueth, M., Lopez-Lopez, A., Martinez, J., Rogel, M. A., Toledo, I., & Martínez-Romero, E. (2012). Seed bacterial endophytes: common genera, seed-to-seed variability and their possible role in plants. Acta Hortic, 938, 39-48. https://doi.org/10.17660/ActaHortic.2012.938.4
Rosier, A., Medeiros, F. H., & Bais, H. P. (2018). Defining plant growth promoting rhizobacteria molecular and biochemical networks in beneficial plant-microbe interactions. Plant Soil, 428(1-2), 35-55. https://doi.org/10.1007/s11104-018-3679-5
Rovira, A. D. (1969). Plant root exudates. Bot Rev, 35, 17-34. https://doi.org/10.1007/BF02859887
Rousk, J., Baath, E., Brookes, P. C., Lauber, C. L., Lozupone, C., Caporaso, J. G., Knight, R., & Fierer, N. (2010). Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J, 4, 1340-1351. https://doi.org/10.1038/ismej.2010.58
Rout, M. E., Chrzanowski, T. H., Westlie, T. K., DeLuca, T. H., Callaway, R. M., & Holben, W. E. (2013). Bacterial endophytes enhance competition by invasive plants. Am J Bot, 100, 1726-1737. https://doi.org/10.3732/ajb.1200577
Ruiz, D., Agaras, B., Werra, P., Wall, L. G., & Valverde, C. (2011). Characterization and screening of plant probiotic traits of bacteria isolated from rice seeds cultivated in Argentina. J Microbiol, 49(6), 902-912. https://doi.org/10.1007/s12275-011-1073-6
Rybakova, D., Mancinelli, R., Wikström, M., Birch-Jensen, A-S., Joeke Postma, J., Ralf-Udo Ehlers, R-U., Simon Goertz, S., & Berg, G. (2017). The structure of the Brassica napus seed microbiome is cultivar-dependent and affects the interactions of symbionts and pathogens. Microbiome, 5, 104. https://doi.org/10.1186/s40168-017-0310-6
Saikkonen, K., Saari, S., & Helander, M. (2010). Defensive mutualism between plants and endophytic fungi? Fungal Divers, 41, 101-113. https://doi.org/10.1007/s13225-010-0023-7
Santos, L. F., & Olivares, F. L. (2021). Plant microbiome structure and benefits for sustainable agriculture. Curr Plant Biol, 26, article 100198. https://doi.org/10.1016/j.cpb.2021.100198
Santoyo, G., Moreno-Hagelsieb, G., Orozco-Mosqueda, M. D. C., & Glick, B. R. (2016). Plant growth-promoting bacterial endophytes. Microbiol Res, 183, 92-99. https://doi.org/10.1016/j.micres.2015.11.008
Schardl, C. L. (2001). Epichloë festucae and related mutualistic symbionts of grasses. Fungal Genet Biol, 33, 69-82. https://doi.org/10.1006/fgbi.2001.1275
Schiltz, S., Gaillard, I., Pawlicki-Jullian, N., Thiombiano, B., Mesnard, F., & Gontier, E. (2015). A review: what is the spermosphere and how can it be studied? J Appl Microbiol, 119. https://doi.org/10.1111/jam.12946
Shade, A., Jacques, M.-A., & Barret, M. (2017). Ecological patterns of seed microbiome diversity, transmission, and assembly. Curr Opin Microbiol, 37, 15-22. https://doi.org/10.1016/j.mib.2017.03.010
Shahzad, R., Khan, A. L., Bilal, S., Asaf, S., & Lee, I.-J. (2018). What is there in seeds? Vertically transmitted endophytic resources for sustainable improvement in plant growth. Front Plant Sci, 9, 24. https://doi.org/10.3389/fpls.2018.00024
Sheth, R. U., Cabral, V., Chen, S. P., & Wang, H. H. (2016). Manipulating bacterial communities by in situ microbiome engineering. Trends Genet, 32, 189-200. https://doi.org/10.1016/j.tig.2016.01.005
Singh, B. K. (2010). Exploring microbial diversity for biotechnology: the way forward. Trends Biotechnol, 28, 111-116. https://doi.org/10.1016/j.tibtech.2009.11.006
Smalla, K., Wieland, G., Buchner, A., Zock, A., Parzy, J., Kaiser, S., Roskot, N., Heuer, H., & Berg, G. (2001). Bulk and rhizosphere soil bacterial communities studied by denaturing gradient gel electrophoresis: plant-dependent enrichment and seasonal shifts revealed. Appl Environ Microbiol, 67, 4742-4751. https://doi.org/10.1128/AEM.67.10.4742-4751.2001
Truyens, S., Beckers, B., Thijs, S., Weyens, N., Cuypers, A., & Vangronsveld, J. (2016). The effects of the growth substrate on cultivable and total endophytic assemblages of Arabidopsis thaliana. Plant Soil, 405, 325-336. https://doi.org/10.1007/s11104-015-2761-5
Truyens, S., Weyens, N., Cuypers, A., & Vangronsveld, J. (2015). Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep, 7, 40-50. https://doi.org/10.1111/1758-2229.12181
Vandenkoornhuyse, P., Quaiser, A., Duhame, M., Le Van, A., & Dufresne, A. (2015). The importance of the microbiome of the plant holobiont. New Phytol, 206, 1196-1206. https://doi.org/10.1111/nph.13312
van der Heijden, M. G. A., & Schlaeppi, K. (2015). Root surface as a frontier for plant microbiome research. Biol Sci, 112(8), 2299-2300. https://doi.org/10.1073/pnas.1500709112
van Opstal, E. J., & Bordenstein, S. R. (2015). Rethinking heritability of the microbiome. Science, 349, 1172-1173. https://doi.org/10.1126/science.aab3958
van Overbeek, L. S., Franke, A. C., Nijhuis, E. H. M., Groeneveld, R. M. W., da Rocha, U. N., & Lotz, L. A. P. (2011). Bacterial communities associated with Chenopodium album and Stellaria media seeds from arable soils. Microb Ecol, 62, 257-264. https://doi.org/10.1007/s00248-011-9845-4
Vega, F. E., Pava-Ripoll, M., Posada, F., & Buyer, J. S. (2005). Endophytic bacteria in Coffea arabica L. J Basic Microbiol, 45, 371-380. https://doi.org/10.1002/jobm.200410551
Verma, S. K., Kingsley, K., Irizarry, I., Bergen, M., Kharwar, R. N., & White Jr, J. F., et al. (2017). Seed vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol, 122, 1680-1691. https://doi.org/10.1111/jam.13463
Volkogon, V. V. (1994). [Associative nitrogen fixers of the root zone of forage cereals]. Mikrobiol Z, 56(2), 40-41. [In russian].
Volkogon, V. V. (1999). Nitrogen-fixing microorganisms of the root zone and seeds of cereal grasses. Bull Institute of Agricultural Microbiology, 4, 6-14.
Volkogon, V. V., Mamchur, A. E., Lemeshko, S. V., & Minyailo, V. G. (1995). [Azospirillum-endophytes of seeds of cereal plants]. Mikrobiol Z, 57(1), 14-19. [In russian].
Volkogon, V. V., Dulnev, P. G., Kovtun, E. P., Nosovets E. I., & Shevchuk E. N. (1996). [Effect of phytohormones and their synthetic analogues on the activity of associative nitrogen fixation]. Microbiology, 65(6), 850-854. [In russian].
Volkogon, V. V., Khalchytsky, A. E., Minyailo, V. G., Onishchenko, L. I., & Lemeshko, S. V. (1991). [Nitrogen-fixing microorganisms of the root zone of ryegrass and sedge]. Mikrobiol Z, 53(6), 3-8. [In russian].
Walker, T. S., Bais, H. P., Déziel, E., Schweizer, H. P., Rahme, L. G., Fall, R., & Vivanco J. M. (2004). Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol, 134(1), 320-331. https://doi.org/10.1104/pp.103.027888
Wassermann, B., Cernava, T., Müller, H., Berg, C. & Berg, G. (2019). Seeds of native alpine plants host unique microbial communities embedded in cross-kingdom networks. Microbiome, 7, 108. https://doi.org/10.1186/s40168-019-0723-5
Wiesel, L., Newton, A. C., Elliott, I., Booty D., Girloy E. M., Birch P. R. J., & Hein, I. (2014). Molecular effects of resistance elicitors from biological origin and their potential for crop protection. Front Plant Sci, 5, article 655. https://doi.org/10.3389/fpls.2014.00655
Wood, C. W., & Stinchcombe, J. R. (2017). A window into the transcriptomic basis of genotype-by-genotype interactions in the legume-rhizobia mutualism. Mol Ecol, 26(21), 5869-5871. https://doi.org/10.1111/mec.14370
Zamioudis, C., & Pieterse, C. M. (2012). Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact, 25, 139-150. https://doi.org/10.1094/MPMI-06-11-0179
Zawoznik, M. S., Vázquez, S. C., Díaz Herrera, S. M., & Groppa, M. D. (2014). Search for endophytic diazotrophs in barley seeds. Braz J Microbiol, 45, 621-625. https://doi.org/10.1590/S1517-83822014000200033
Zhou, J., Xia, B., Treves, D. S., Wu, L-Y., Marsh, T. L., O'Neill, R. V., Palumbo, A. V., & Tiedje, J. M. (2002). Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol, 68, 326-334. https://doi.org/10.1128/AEM.68.1.326-334.2002
Zolla, G., Badri, D. V., Bakker, M. G., Manter, D. K., & Vivanco J. M. (2013). Soil microbiomes vary in their ability to confer drought tolerance to Arabidopsis. Appl Soil Ecol, 68, 1-9. https://doi.org/10.1016/j.apsoil.2013.03.007
Downloads
Published
Issue
Section
License
Copyright (c) 2025 Mikrobiolohichnyi Zhurnal

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.