Earth:Rhizosphere

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Short description: Region of soil or substrate comprising the root microbiome


Some rhizosphere processes in the soil
(A) Root system architecture is concerned with structural features of the root and responds to with environmental stimuli. (B) The rhizosphere produces photosynthetically fixed carbon that exudes into the soil and influences soil physicochemical gradients. (C) Free-living or parasitic nematodes interact with the rhizosphere via signaling interactions. (D) Mycorrhizal fungi create intimate relationships with the roots and engage in nutrient exchange. (E) Bacterial composition is distinct upon different parts, age, type of the roots.[1]

The rhizosphere is the narrow region of soil or substrate that is directly influenced by root secretions and associated soil microorganisms known as the root microbiome.[2] Soil pores in the rhizosphere can contain many bacteria and other microorganisms that feed on sloughed-off plant cells, termed rhizodeposition,[3] and the proteins and sugars released by roots, termed root exudates.[4] This symbiosis leads to more complex interactions, influencing plant growth and competition for resources. Much of the nutrient cycling and disease suppression by antibiotics required by plants occurs immediately adjacent to roots due to root exudates and metabolic products of symbiotic and pathogenic communities of microorganisms.[5] The rhizosphere also provides space to produce allelochemicals to control neighbours and relatives.[6]

The rhizoplane refers to the root surface including its associated soil particles which closely interact with each other.[7] The plant-soil feedback loop and other physical factors occurring at the plant-root soil interface are important selective pressures in communities and growth in the rhizosphere and rhizoplane.[8]

Background

The term "rhizosphere" was used first in 1904 by the German plant physiologist Lorenz Hiltner to describe how plant roots interface with the surrounding soil.[9][10] The prefix rhiza- comes from the Greek, meaning "root". Hiltner postulated the rhizosphere was a region surrounding the plant roots and populated with microorganisms under some degree of control by chemicals released from the plant roots.[9][8]

Chemical interactions

Chemical availability

Plant roots may exude 20-40% of the sugars and organic acids - photosynthetically fixed carbon.[11] Plant root exudates, such as organic acids, change the chemical structure and the biological communities of the rhizosphere in comparison with the bulk soil or parent soil. Concentrations of organic acids and saccharides affect the ability of the biological communities to shuttle phosphorus, nitrogen,[12][13] potassium, and water to the root cap,[4] and the total availability of iron to the plant and to its neighbors.[14] The ability of the plant's root and its associated soil microorganisms to provide specific transport proteins affects the availability of iron and other minerals for it and its neighbors. This can affect the composition of the community and its fitness.

Root exudates come in the form of chemicals released into the rhizosphere by cells in the roots and cell waste referred to as "rhizodeposition." This rhizodeposition comes in various forms of organic carbon and nitrogen that provide for the communities around plant roots and dramatically affect the chemistry surrounding the roots.[15] Exopolysaccharides, such as polyglycolide (PGA), affect the ability of roots to uptake water by maintaining the physical stability of the soil carbon sponge and controlling the flow of water.[16] For example, a tomato field study showed that exopolysaccharides extracted from the rhizosphere were different (total sugar amounts and mean infrared measurements) depending on the tomato varieties grown,[17] and that under water deficit conditions (limited irrigation), the increase in exopolysaccharide production and microbial activity affected water retention in the soil and field performance of tomato.[18] In potato cultivar root exudates, phenols and lignins comprise the greatest number of ion influencing compounds regardless of growing location; however, the intensity of different compounds was found to be influenced by soils and environmental conditions, resulting in variation amongst nitrogen compounds, lignins, phenols, carbohydrates, and amines.[19]

Allelochemicals

Although it goes beyond the rhizosphere area, it is notable that some plants secrete allelochemicals from their roots that inhibit the growth of other organisms. For example, garlic mustard produces a chemical that is believed to prevent mutualisms forming between the surrounding trees and mycorrhiza in mesic North American temperate forests where it is an invasive species.[20]

Ecology of the rhizosphere

Sunlight and carbon dioxide from the atmosphere are absorbed by the leaves in the plant and converted to fixed carbon. This carbon travels down into the roots of the plant, where some travels back up to the leaves. The fixed carbon traveling to the root is radiated outward into the surrounding soil where microbes use it as food for growth. In return, microbes attach to the plant root where it improves the roots access to nutrients and its resistance to environmental stress and pathogens. In specific plant/root symbiotic relationships, the plant root secretes flavonoids into the soil which is sensed by microbes, where these microbes release nod factors to the plant root which promotes the infection of the plant root. These unique microbes carry out nitrogen fixation in root nodules, which supplies nutrients to the plant.
Predicted effects of elevated carbon dioxide on soil carbon reserves [21]
In the short term, plant growth is stimulated by elevated carbon dioxide, resulting in increased rhizodeposition, priming microbes to mineralize soil organic carbon (SOC) and adding CO2 to the atmosphere through respiration. But the net impact on greenhouse gas emissions will be reduced by the increased uptake of CO2 from the atmosphere by increased plant growth. However, over the long term, soil reserves of easily decomposed carbon will be depleted by the increase in microbial activity, resulting in increased catabolism of SOC reservoirs, thus increasing atmospheric CO2 concentrations beyond what is taken up by plants. This is predicted to be a particular problem in thawing permafrost that contains large reserves of SOC that are becoming increasingly susceptible to microbial degradation as the permafrost thaws.[22][23]

Rhizodeposition allows for the growth of communities of microorganisms directly surrounding and inside plant roots. This leads to complex interactions between species, including mutualism, predation/parasitism, and competition.

Predation

Predation is considered to be top-down because these interactions decrease the population, but the closeness of the interactions of species directly affects the availability of resources causing the population to also be affected by bottom-up controls.[24] Without soil fauna, microbes that directly prey upon competitors of plants and plant mutualists, interactions within the rhizosphere would be antagonistic toward the plants. Soil fauna provide the top-down component of the rhizosphere while also allowing for the bottom-up increase in nutrients from rhizodeposition and inorganic nitrogen. The complexity of these interactions has also been shown through experiments with common soil fauna, such as nematodes and protists. Predation by bacterial-feeding nematodes was shown to influence nitrogen availability and plant growth.[25] There was also an increase in the populations of bacteria to which nematodes were added. Predation upon Pseudomonas by amoeba shows predators are able to upregulate toxins produced by prey without direct interaction using supernatant.[26] The ability of predators to control the expression and production of biocontrol agents in prey without direct contact is related to the evolution of prey species to signals of high predator density and nutrient availability.

The food web in the rhizosphere can be considered as three different channels with two different sources of energy: the detritus-dependent channels are fungi and bacterial species, and the root energy-dependent channel consists of nematodes, symbiotic species, and some arthropods.[24] This food web is constantly in flux since the amount of detritus available and the rate of root sloughing changes as roots grow and age. This bacterial channel is considered to be a faster channel because of the ability of species to focus on more accessible resources in the rhizosphere and have faster regeneration times compared with the fungal channel. All three of these channels are also interrelated to the roots that form the base of the rhizosphere ecosystem and the predators, such as the nematodes and protists, that prey upon many of the same species of microflora.

Competition

The competition between plants due to released exudates is dependent upon geometrical properties, which determine the capacity of interception of exudates from any point in relation to the plants’ roots, physicochemical properties, which determine the capacity of each root to take up exudates in the area.[27] Geometrical properties are the density of roots, root diameter, and distribution of the roots. Physicochemical properties are exudation rate, decay rate of exudates, and the properties of the environment that affect diffusion. These properties define the rhizosphere of roots and the likelihood that plants can directly compete with neighbors.

Plants and soil microflora indirectly compete against one another by tying up limiting resources, such as carbon and nitrogen, into their biomass.[28] This competition can occur at varying rates due to the ratio of carbon to nitrogen in detritus and the ongoing mineralization of nitrogen in the soil. Mycorrhizae and heterotrophic soil microorganisms compete for both carbon and nitrogen, depending upon which is limiting at the time, which itself heavily depends on the species, scavenging abilities, and the environmental conditions affecting nitrogen input. Plants are less successful at the uptake of organic nitrogen, such as amino acids, than the soil microflora that exist in the rhizosphere.[29] This informs other mutualistic relationships formed by plants in relation to nitrogen uptake.

Competition over other resources, such as oxygen in limited environments, is directly affected by the spatial and temporal locations of species and the rhizosphere. In methanotrophs, proximity to higher density roots and the surface are important and help to determine where they are dominant over heterotrophs in rice paddies.[30]

The weak connection between the various channels of energy is important in the regulation of the populations of both predator and prey and the availability of resources to the biome. Strong connections between resource-consumer and consumer-consumer create coupled systems of oscillators, which are then determined by the nature of the available resources.[31] These systems can then be considered cyclical, quasi-periodic, or chaotic.

Mutualism

Plants secrete many compounds through their roots to serve symbiotic functions in the rhizosphere. Strigolactones, secreted and detected by mycorrhizal fungi, stimulate the germination of spores and initiate changes in the mycorrhiza that allow it to colonize the root. The parasitic plant, Striga also detects the presence of strigolactones and will germinate when it detects them; they will then move into the root, feeding off the nutrients present.[32][33]

Symbiotic nitrogen-fixing bacteria, such as Rhizobium species, detect compounds like flavonoids secreted by the roots of leguminous plants and then produce nod factors that signal to the plant that they are present and will lead to the formation of root nodules. Bacteria are housed in symbiosomes in these nodules, where they are sustained by nutrients from the plant and convert nitrogen gas to a form that can be used by the plant.[34] Non-symbiotic (or "free-living") nitrogen-fixing bacteria may reside in the rhizosphere just outside the roots of certain plants (including many grasses) and similarly "fix" nitrogen gas in the nutrient-rich plant rhizosphere. Even though these organisms are thought to be only loosely associated with the plants they inhabit, they may respond very strongly to the status of the plants. For example, nitrogen-fixing bacteria in the rhizosphere of the rice plant exhibit diurnal cycles that mimic plant behavior and tend to supply more fixed nitrogen during growth stages when the plant exhibits a high demand for nitrogen.[35]

In exchange for the resources and shelter that plants and roots provide, fungi and bacteria control pathogenic microbes.[36] The fungi that perform such activities also serve close relationships with species of plants in the form of mycorrhizal fungi, which are diverse in how they relate to plants. Arbuscular mycorrhizal fungi and the bacteria that make the rhizosphere their home also form close relationships in order to be more competitive.[37] which plays into the bigger cycles of nutrients that impact the ecosystem, such as biogeochemical pathways.[14]

Community structure

The rhizosphere has been referred to as an information super highway because of the proximity of data points, which include roots and organisms in the soil, and the methods for transferring data using exudates and communities.[38] This description has been used to explain the complex interactions that plants, their fungal mutualists, and the bacterial species that live in the rhizosphere have entered into over the course of their evolution. Certain species like Trichoderma are interesting because of their ability to select for species in this complex web. Trichoderma is a biological control agent because of evidence that it can reduce plant pathogens in the rhizosphere.[39] Plants themselves also affect which bacterial species in the rhizosphere are selected against because of the introduction of exudates and the relationships that they maintain. The control of which species are in these small diversity hotspots can drastically affect the capacity of these spaces and future conditions for future ecologies.[36][6]

Microbial consortium

Rhizosphere microbial consortia [40]
Main page: Biology:Microbial consortium

Although various studies have shown that single microorganisms can exert beneficial effects on plants, it is increasingly evident that when a microbial consortium — two or more interacting microorganisms — is involved, additive or synergistic results can be expected. This occurs, in part, due to the fact that multiple species can perform a variety of tasks in an ecosystem like the rhizosphere. Beneficial mechanisms of plant growth stimulation include enhanced nutrient availability, phytohormone modulation, biocontrol, and biotic and abiotic stress tolerance) exerted by different microbial players within the rhizosphere, such as plant-growth-promoting bacteria (PGPB) and fungi such as Trichoderma and mycorrhizae.[40]

The diagram on the right illustrates that rhizosphere microorganisms like plant-growth-promoting bacteria (PGPB), arbuscular mycorrhizal fungi (AMF), and fungi from the genus Trichoderma spp. can establish beneficial interactions with plants, promoting plant growth and development, increasing the plant defense system against pathogens, promoting nutrient uptake, and enhancing tolerance to different environmental stresses. Rhizosphere microorganisms can influence one another, and the resulting consortia of PGPB + PGPB (e.g., a nitrogen-fixing bacterium such as Rhizobium spp. and Pseudomonas fluorescens), AMF + PGPB, and Trichoderma + PGPB may have synergetic effects on plant growth and fitness, providing the plant with enhanced benefits to overcome biotic and abiotic stress. Dashed arrows indicate beneficial interactions between AMF and Trichoderma.[40]

Formation of N-fixing nodules induced by rhizobia[40]
Plant responses to bacteria in the rhizosphere[40]

Communication

Communication in the rhizosphere [41]
Actors and interactions in the rhizosphere: Inter-kingdom and intra-kingdom communication involving plants and microbes in the rhizosphere, including the consistent role of rhizobia.
VOCs = volatile organic compounds; PGP = plant growth promoting; AMF = arbuscular mycorrhizal fungi

Communication is often the basis of biotic interactions. Frequently, more than two organisms can take part in the communication, resulting in a complex network of crosstalking. Recent advances in plant-microbe interactions research have shown that communication, both inter-kingdom and intra-kingdom, is shaped by a broad spectrum of factors. In this context, the rhizosphere (i.e., the soil close to the root surface) provides a specific microhabitat where complex interactions occur. The complex environment that makes up the rhizosphere can select for certain microbial populations, which are adapted to this unique niche. Among them, rhizobia have emerged as an important component of the rhizospheric microbiome. Rhizospheric crosstalk is found in rhizobium-legume interactions. This symbiosis is a complex process that involves signalling that can be shaped by plant rhizospheric exudates and microbiome composition. The relationship established by rhizobia with other rhizospheric organisms, together with the influence of environmental factors, results in their beneficial role on host plant health.[41]

Prokaryotes and eukaryotes have interacted for millions of years, evolving and refining over time their communication systems. As proposed by Hauser in 1996,[10] biological signals and the exchange of information are part of the definition of communication, while the signals themselves are considered as "every structure able to shape the behavior of the organisms".[42][43] Consequently, the signals can evolve and persist thanks to the interaction between signal producers and receivers. Then, cooperation and fitness improvement are the basis of biological communication.[44][41]

In a particular environment, individuals can communicate and interact with multiple partners, and the nature of interaction can determine variable costs and benefits to the partner, as a biological market.[45] A large number of signals can be exchanged involving the plant itself, insects, fungi, and microbes. This all takes place in a high-density environmental niche. Usually, communication is the result of chemical responses of cells to signatory molecules coming from other cells. These signals affect both the metabolism and transcription of genes activating several regulatory mechanisms.[41]

Root nodules, each containing billions of Rhizobiaceae bacteria

Frequently in the rhizosphere, more than two organisms (and species) can take part in the communication, resulting in a complex network of interactions and cross-talks which influence the fitness of all participating partners. Thus, this environment can be considered a hot spot for numerous inter-kingdom signals exchange, which involves plant-associated microbial communities (rhizobiome). The microbial community's composition is mainly shaped and recruited by hundreds of metabolites released in the soil by plant roots, which normally facilitate interactions with the biotic and abiotic environment. Often the plant can modulate their diversity based on the benefits in terms of growth and health, such as with plant growth-promoting rhizobacteria.[46] Nevertheless, a large number of nutrients issued by the plant can be of interest to pathogenic organisms, which can take advantage of plant products for their survival in the rhizosphere.[47][41]

It stands to reason that the plants play a fundamental role in the rhizosphere scene.[48] Indeed, because of the chemical signals conveyed by nutrient-rich exudates released by the plant roots, a large variety of microbes can first colonize the rhizosphere and then gradually penetrate the root and the overall plant tissue (endophytes).[49] Otherwise, they can colonize the host plant establishing a lasting and beneficial symbiotic relationship.[50] To date, numerous investigations on root exudates composition have been performed.[46][51][52][41]

The most known plant-microbe dialogue on the rhizosphere scene, which determines direct and indirect advantages to the partners, was properly addressed as early as 1904 when Hiltner described the symbiotic interaction among legumes and rhizobia.[10] This symbiosis is a highly specific process in which the genetic and chemical communication signals are strictly plant-bacterium specific. In this mutualistic interaction, rhizobia positively influence the host's growth thanks to the nitrogen fixation process and at the same time can benefit from the nutrients provided by the plant.[41]

This symbiosis has been extensively studied in recent decades, and many studies on the communication and the signaling between the two partners at different steps of the symbiosis (from root infection to nodule development) have been elucidated.[53][54] However, the knowledge about the earlier steps of rhizosphere colonization, namely the opening line at the root surface, remains poorly characterized. Nonetheless, increasing data have shown the importance of intraspecies and multispecies communications among rhizospheric biotic components for the improvement of rhizobia–legumes interaction. In addition, it has been shown that rhizobia are part of the rhizosphere of a wide variety of non-legume plants where they can play a role as plant growth promoting components, recovering a central role in plant core microbiome.[55][41]

Methods

The following are some methods commonly used or of interest in rhizosphere research. Many of these methods include both field testing of the root systems and in lab testing using simulated environments to perform experiments, such as pH determination.[56]

  • High-throughput screening
  • High-Throughput Sequencing: 16S rRNA Amplicon, Metagenomics, Metatranscriptomics
  • Culture Depend Approaches
  • Root Imaging
  • Isotopic labeling
  • Enzyme Assays
  • Mini rhizotron camera
  • Various methods used to determine water movement in the rhizosphere e.g. microelectrodes and agar techniques for pH and microsampling of rhizosphere materials[56]
  • Pyrolysis–field ionization mass spectrometry allows for spectrometry of agricultural fields to find fulvic and humic acids and the extraction residues (humins) in certain studies and expanded to general organic compounds in other recent work.[57][19]
Illustration of the rhizosphere[58]
A = amoeba consuming bacteria; BL = energy limited bacteria; BU = non-energy limited bacteria; RC = root derived carbon; SR = sloughed root hair cells; F = fungal hyphae; N = nematode worm.[56]
Growth chamber designs for studying rhizosphere interactions
(A) Rhizotron/Rhizobox set up, (B) Rhizobox with side-compartment, (C) vertical root mat chambers; a modular option is show where the plant can be pre-grown in a separate compartment and transplanted afterward onto the main examination chamber, inset shows a modular set up option, (D) horizontal root mat in rhizobox, (E) Mycorrhizal compartments, (F) split-root systems shown here in a rhizobox set up; (G) Nylon bag to separate root and root-free soil; roots may be restricted in the bag or the soil may be protected from root penetration by the bag.[1]

See also

References

  1. ↑ 1.0 1.1 Yee, Mon Oo; Kim, Peter; Li, Yifan; Singh, Anup K.; Northen, Trent R.; Chakraborty, Romy (26 March 2021). "Specialized Plant Growth Chamber Designs to Study Complex Rhizosphere Interactions". Frontiers in Microbiology (Frontiers Media SA) 12: 625752. doi:10.3389/fmicb.2021.625752. ISSN 1664-302X. PMID 33841353.  50px Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
  2. ↑ "Microbial Health of the Rhizosphere". http://uwstudentweb.uwyo.edu/T/Twhite/. 
  3. ↑ Hütsch, Birgit W.; Augustin, Jürgen; Merbach, Wolfgang (2002). "Plant rhizodeposition – an important source for carbon turnover in soils". Journal of Plant Nutrition and Soil Science 165 (4): 397–407. doi:10.1002/1522-2624(200208)165:4<397::AID-JPLN397>3.0.CO;2-C. https://www.researchgate.net/publication/230290633. 
  4. ↑ 4.0 4.1 Walker, Travis S.; Bais, Harsh Pal; Grotewold, Erich; Vivanco, Jorge M. (2003). "Root exudation and rhizosphere biology". Plant Physiology 132 (1): 44–51. doi:10.1104/pp.102.019661. PMID 12746510. 
  5. ↑ Ingham, Elaine R.. "The Soil Food Web". USDA-NRCS. https://www.nrcs.usda.gov/wps/portal/nrcs/detailfull/soils/health/biology/?cid=nrcs142p2_053868. 
  6. ↑ 6.0 6.1 Grayston, Susan J.; Wang, Shenquiang; Campbell, Colin D.; Edwards, Anthony C. (March 1998). "Selective influence of plant species on microbial diversity in the rhizosphere". Soil Biology and Biochemistry 30 (3): 369–378. doi:10.1016/S0038-0717(97)00124-7. 
  7. ↑ Estermann, Eva F.; McLaren, A. D. (1961). "Contribution of rhizoplane organisms to the total capacity of plants to utilize organic nutrients". Plant and Soil 15 (3): 243–260. doi:10.1007/BF01400458. 
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  24. ↑ 24.0 24.1 Moore, John C.; McCann, Kevin; Setälä, Heikki; De Ruiter, Peter C. (2003). "Top-Down is Bottom-Up: Does Predation in the Rhizosphere Regulate Aboveground Dynamics?". Ecology 84 (4): 846. doi:10.1890/0012-9658(2003)084[0846:TIBDPI2.0.CO;2]. 
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  30. ↑ Bodegom, Peter van; Stams, Fons; Mollema, Liesbeth; Boeke, Sara; Leffelaar, Peter (August 2001). "Methane Oxidation and the Competition for Oxygen in the Rice Rhizosphere". Applied and Environmental Microbiology 67 (8): 3586–3597. doi:10.1128/AEM.67.8.3586-3597.2001. PMID 11472935. Bibcode: 2001ApEnM..67.3586V. 
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  35. ↑ Sims, GK; Dunigan, EP (1984). "Diurnal and seasonal variations in nitrogenase activity (C2H2 reduction) of rice roots". Soil Biology and Biochemistry 16 (1): 15–18. doi:10.1016/0038-0717(84)90118-4. 
  36. ↑ 36.0 36.1 Weller, D. M. (1988). "Biological Control of Soilborne Plant Pathogens in the Rhizosphere with Bacteria". Annual Review of Phytopathology 26 (1): 379–407. doi:10.1146/annurev.py.26.090188.002115. https://zenodo.org/record/1235057. 
  37. ↑ Bianciotto, V.; Minerdi, D.; Perotto, S.; Bonfante, P. (1996). "Cellular interactions between arbuscular mycorrhizal fungi and rhizosphere bacteria". Protoplasma 193 (1–4): 123–131. doi:10.1007/BF01276640. 
  38. ↑ Bais, Harsh Pal; Park, Sang-Wook; Weir, Tiffany L; Callaway, Ragan M; Vivanco, Jorge M (2004). "How plants communicate using the underground information superhighway". Trends in Plant Science 9 (1): 26–32. doi:10.1016/j.tplants.2003.11.008. PMID 14729216. 
  39. ↑ Howell, C. R. (2003). "Mechanisms Employed by Trichoderma Species in the Biological Control of Plant Diseases: The History and Evolution of Current Concepts". Plant Disease 87 (1): 4–10. doi:10.1094/PDIS.2003.87.1.4. PMID 30812698. 
  40. ↑ 40.0 40.1 40.2 40.3 40.4 Santoyo, Gustavo; Guzmán-Guzmán, Paulina; Parra-Cota, Fannie Isela; Santos-Villalobos, Sergio de los; Orozco-Mosqueda, Ma. del Carmen; Glick, Bernard R. (2021). "Plant Growth Stimulation by Microbial Consortia". Agronomy 11 (2): 219. doi:10.3390/agronomy11020219.  CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
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  42. ↑ Maynard-Smith, John; Harper, David (6 November 2003). Animal Signals. New York: Oxford University Press. ISBN 978-0-19-852685-8. OCLC 54460090. https://books.google.com/books?id=SUA51MeG1lcC&pg=PA1. 
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  44. ↑ Zahavi, Amotz (2008). "The handicap principle and signalling in collaborative systems". in Hughes, David P.. Sociobiology of Communication. Oxford University Press. pp. 1–10. https://books.google.com/books?id=aJkSDAAAQBAJ&pg=PA1. 
  45. ↑ Werner, Gijsbert D. A.; Cornwell, William K.; Cornelissen, Johannes H. C.; Kiers, E. Toby (2015). "Evolutionary signals of symbiotic persistence in the legume–rhizobia mutualism". Proceedings of the National Academy of Sciences 112 (33): 10262–10269. doi:10.1073/pnas.1424030112. PMID 26041807. Bibcode: 2015PNAS..11210262W. 
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  47. ↑ Rasmann, Sergio; Turlings, Ted CJ (2016). "Root signals that mediate mutualistic interactions in the rhizosphere". Current Opinion in Plant Biology 32: 62–68. doi:10.1016/j.pbi.2016.06.017. PMID 27393937. 
  48. ↑ Bending, G.D. (2017). "The Rhizopshere and Its Microorganisms". Encyclopedia of Applied Plant Sciences. pp. 347–351. doi:10.1016/B978-0-12-394807-6.00165-9. ISBN 9780123948083. 
  49. ↑ Hardoim, Pablo R.; Van Overbeek, Leo S.; Elsas, Jan Dirk van (2008). "Properties of bacterial endophytes and their proposed role in plant growth". Trends in Microbiology 16 (10): 463–471. doi:10.1016/j.tim.2008.07.008. PMID 18789693. 
  50. ↑ Chi, Feng; Shen, Shi-Hua; Cheng, Hai-Ping; Jing, Yu-Xiang; Yanni, Youssef G.; Dazzo, Frank B. (2005). "Ascending Migration of Endophytic Rhizobia, from Roots to Leaves, inside Rice Plants and Assessment of Benefits to Rice Growth Physiology". Applied and Environmental Microbiology 71 (11): 7271–7278. doi:10.1128/AEM.71.11.7271-7278.2005. PMID 16269768. Bibcode: 2005ApEnM..71.7271C. 
  51. ↑ Bulgarelli, Davide; Schlaeppi, Klaus; Spaepen, Stijn; Van Themaat, Emiel Ver Loren; Schulze-Lefert, Paul (2013). "Structure and Functions of the Bacterial Microbiota of Plants". Annual Review of Plant Biology 64: 807–838. doi:10.1146/annurev-arplant-050312-120106. PMID 23373698. 
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  53. ↑ Oldroyd, Giles E.D.; Murray, Jeremy D.; Poole, Philip S.; Downie, J. Allan (2011). "The Rules of Engagement in the Legume-Rhizobial Symbiosis". Annual Review of Genetics 45: 119–144. doi:10.1146/annurev-genet-110410-132549. PMID 21838550. 
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  55. ↑ Yeoh, Yun Kit; Paungfoo-Lonhienne, Chanyarat; Dennis, Paul G.; Robinson, Nicole; Ragan, Mark A.; Schmidt, Susanne; Hugenholtz, Philip (2016). "The core root microbiome of sugarcanes cultivated under varying nitrogen fertilizer application". Environmental Microbiology 18 (5): 1338–1351. doi:10.1111/1462-2920.12925. PMID 26032777. 
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