Phyllosphere

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The plant aerial surface, mostly occupied by leaves, is inhabited by diverse microorganisms, forming the phyllosphere The plant aerial surface.png
The plant aerial surface, mostly occupied by leaves, is inhabited by diverse microorganisms, forming the phyllosphere

In microbiology, the phyllosphere is the total above-ground surface of a plant when viewed as a habitat for microorganisms. [1] [2] The phyllosphere can be further subdivided into the caulosphere (stems), phylloplane (leaves), anthosphere (flowers), and carposphere (fruits). The below-ground microbial habitats (i.e. the thin-volume of soil surrounding root or subterranean stem surfaces) are referred to as the rhizosphere and laimosphere. Most plants host diverse communities of microorganisms including bacteria, fungi, archaea, and protists . Some are beneficial to the plant, others function as plant pathogens and may damage the host plant or even kill it.

Contents

The phyllosphere microbiome

The leaf surface, or phyllosphere, harbours a microbiome comprising diverse communities of bacteria, archaea, fungi, algae and viruses. [3] [4] Microbial colonizers are subjected to diurnal and seasonal fluctuations of heat, moisture, and radiation. In addition, these environmental elements affect plant physiology (such as photosynthesis, respiration, water uptake etc.) and indirectly influence microbiome composition. [5] Rain and wind also cause temporal variation to the phyllosphere microbiome. [6]

The phyllosphere includes the total aerial (above-ground) surface of a plant, and as such includes the surface of the stem, flowers and fruit, but most particularly the leaf surfaces. Compared with the rhizosphere and the endosphere the phyllosphere is nutrient poor and its environment more dynamic.

Interactions between plants and their associated microorganisms in many of these microbiomes can play pivotal roles in host plant health, function, and evolution. [7] Interactions between the host plant and phyllosphere bacteria have the potential to drive various aspects of host plant physiology. [8] [2] [9] However, as of 2020 knowledge of these bacterial associations in the phyllosphere remains relatively modest, and there is a need to advance fundamental knowledge of phyllosphere microbiome dynamics. [10] [11]

The assembly of the phyllosphere microbiome, which can be strictly defined as epiphytic bacterial communities on the leaf surface, can be shaped by the microbial communities present in the surrounding environment (i.e., stochastic colonisation) and the host plant (i.e., biotic selection). [3] [12] [11] However, although the leaf surface is generally considered a discrete microbial habitat, [13] [14] there is no consensus on the dominant driver of community assembly across phyllosphere microbiomes. For example, host-specific bacterial communities have been reported in the phyllosphere of co-occurring plant species, suggesting a dominant role of host selection. [14] [15] [16] [11]

Conversely, microbiomes of the surrounding environment have also been reported to be the primary determinant of phyllosphere community composition. [13] [17] [18] [19] As a result, the processes that drive phyllosphere community assembly are not well understood but unlikely to be universal across plant species. However, the existing evidence does indicate that phyllosphere microbiomes exhibiting host-specific associations are more likely to interact with the host than those primarily recruited from the surrounding environment. [8] [20] [21] [22] [11]

Spatial scales matter
Trinidad map.png
Trinidad
A leaf.png
A leaf
The area of Trinidad is about 5000 sq km (2000 sq mi). Compared to the size of a human, this is about the same relative area as a typical leaf compared to the size of a bacterium. Imagine a human somewhere on Trinidad without legs to move, and neither eyes to see nor ears to hear, retaining only the ability to smell and touch. This is a parallel to how an individual bacterium perceives a leaf. There is no ability to perceive anything beyond its most immediate surroundings. Bacteria need water for movement and they perceive only "signals, such as sugars, amino acids or volatiles, diffusing to their occupied site". This microhabitat determines the experience of the individual bacterium and how it responds. [23]

Overall, there remains high species richness in phyllosphere communities. Fungal communities are highly variable in the phyllosphere of temperate regions and are more diverse than in tropical regions. [24] There can be up to 107 microbes per square centimetre present on the leaf surfaces of plants, and the bacterial population of the phyllosphere on a global scale is estimated to be 1026 cells. [25] The population size of the fungal phyllosphere is likely to be smaller. [26]

Phyllosphere microbes from different plants appear to be somewhat similar at high levels of taxa, but at the lower levels taxa there remain significant differences. This indicates microorganisms may need finely tuned metabolic adjustment to survive in phyllosphere environment. [24] Pseudomonadota seems to be the dominant colonizers, with Bacteroidota and Actinomycetota also predominant in phyllospheres. [27] Although there are similarities between the rhizosphere and soil microbial communities, very little similarity has been found between phyllosphere communities and microorganisms floating in open air (aeroplankton). [28] [5]

The search for a core microbiome in host-associated microbial communities is a useful first step in trying to understand the interactions that may be occurring between a host and its microbiome. [29] [30] The prevailing core microbiome concept is built on the notion that the persistence of a taxon across the spatiotemporal boundaries of an ecological niche is directly reflective of its functional importance within the niche it occupies; it therefore provides a framework for identifying functionally critical microorganisms that consistently associate with a host species. [29] [31] [32] [11]

A leaf from a healthy Arabidopsis plant (left) and a leaf from a dysbiosis mutant plant (right) Healthy and unhealthy leaf.png
A leaf from a healthy Arabidopsis plant (left) and a leaf from a dysbiosis mutant plant (right)

Divergent definitions of “core microbiome” have arisen across scientific literature with researchers variably identifying “core taxa” as those persistent across distinct host microhabitats  [34] [35] and even different species. [16] [20] Given the functional divergence of microorganisms across different host species  [16] and microhabitats, [36] defining core taxa sensu stricto as those persistent across broad geographic distances within tissue- and species-specific host microbiomes, represents the most biologically and ecologically appropriate application of this conceptual framework. [37] [11] Tissue- and species-specific core microbiomes across host populations separated by broad geographical distances have not been widely reported for the phyllosphere using the stringent definition established by Ruinen. [2] [11]

Example: The manuka phyllosphere

Relative abundance of core phyllosphere taxa in manuka
Starr-010419-0063-Leptospermum scoparium-habit-Kula-Maui (24236713820).jpg
Relative abundance of core phyllosphere taxa in the manuka phyllosphere (crop).png
Manuka is a flowering scrub. The chart shows an abundance-occupancy distribution identifying core phyllosphere taxa in non-rarefied (green) and rarefied (purple) datasets. Each point represents a taxon plotted by its mean logarithmic relative abundance and occupancy. Taxa (pink) with an occupancy of 1 (i.e., detected in all 89 phyllosphere samples) were considered members of the core microbiome. [11]

The flowering tea tree commonly known as manuka is indigenous to New Zealand. [38] Manuka honey, produced from the nectar of manuka flowers, is known for its non-peroxide antibacterial properties. [39] [40] These non-peroxide antibacterial properties have been principally linked to the accumulation of the three-carbon sugar dihydroxyacetone (DHA) in the nectar of the manuka flower, which undergoes a chemical conversion to methylglyoxal (MGO) in mature honey. [41] [42] [43] However, the concentration of DHA in the nectar of manuka flowers is notoriously variable, and the antimicrobial efficacy of manuka honey consequently varies from region to region and from year to year. [44] [45] [46] Despite extensive research efforts, no reliable correlation has been identified between DHA production and climatic, [47] edaphic, [48] or host genetic factors. [49] [11]

{A} The heatmap on the left illustrates how the composition of operational taxonomic units (OTUs) in the manuka phyllosphere and associated soil communities differed significantly. No core soil microbiome was detected. (B) The chart on the right shows how OTUs in phyllosphere and associated soil communities differed in relative abundances. Differential abundance of taxa in manuka phyllosphere.png
{A} The heatmap on the left illustrates how the composition of operational taxonomic units (OTUs) in the manuka phyllosphere and associated soil communities differed significantly. No core soil microbiome was detected.
(B) The chart on the right shows how OTUs in phyllosphere and associated soil communities differed in relative abundances.

Microorganisms have been studied in the manuka rhizosphere and endosphere. [50] [51] [52] Earlier studies primarily focussed on fungi, and a 2016 study provided the first investigation of endophytic bacterial communities from three geographically and environmentally distinct manuka populations using fingerprinting techniques and revealed tissue-specific core endomicrobiomes. [53] [11] A 2020 study identified a habitat-specific and relatively abundant core microbiome in the manuka phyllosphere, which was persistent across all samples. In contrast, non-core phyllosphere microorganisms exhibited significant variation across individual host trees and populations that was strongly driven by environmental and spatial factors. The results demonstrated the existence of a dominant and ubiquitous core microbiome in the phyllosphere of manuka. [11]

See also

Related Research Articles

<i>Leptospermum scoparium</i> Species of flowering plant

Leptospermum scoparium, commonly called mānuka, mānuka myrtle, New Zealand teatree, broom tea-tree, or just tea tree, is a species of flowering plant in the myrtle family Myrtaceae, native to New Zealand and south-east Australia. Its nectar produces Mānuka honey.

<span class="mw-page-title-main">Human microbiome</span> Microorganisms in or on human skin and biofluids

The human microbiome is the aggregate of all microbiota that reside on or within human tissues and biofluids along with the corresponding anatomical sites in which they reside, including the skin, mammary glands, seminal fluid, uterus, ovarian follicles, lung, saliva, oral mucosa, conjunctiva, biliary tract, and gastrointestinal tract. Types of human microbiota include bacteria, archaea, fungi, protists, and viruses. Though micro-animals can also live on the human body, they are typically excluded from this definition. In the context of genomics, the term human microbiome is sometimes used to refer to the collective genomes of resident microorganisms; however, the term human metagenome has the same meaning.

<span class="mw-page-title-main">Aeroplankton</span> Tiny lifeforms floating and drifting in the air, carried by the wind

Aeroplankton are tiny lifeforms that float and drift in the air, carried by wind. Most of the living things that make up aeroplankton are very small to microscopic in size, and many can be difficult to identify because of their tiny size. Scientists collect them for study in traps and sweep nets from aircraft, kites or balloons. The study of the dispersion of these particles is called aerobiology.

<span class="mw-page-title-main">Gut microbiota</span> Community of microorganisms in the gut

Gut microbiota, gut microbiome, or gut flora, are the microorganisms, including bacteria, archaea, fungi, and viruses, that live in the digestive tracts of animals. The gastrointestinal metagenome is the aggregate of all the genomes of the gut microbiota. The gut is the main location of the human microbiome. The gut microbiota has broad impacts, including effects on colonization, resistance to pathogens, maintaining the intestinal epithelium, metabolizing dietary and pharmaceutical compounds, controlling immune function, and even behavior through the gut–brain axis.

<span class="mw-page-title-main">Oral microbiology</span>

Oral microbiology is the study of the microorganisms (microbiota) of the oral cavity and their interactions between oral microorganisms or with the host. The environment present in the human mouth is suited to the growth of characteristic microorganisms found there. It provides a source of water and nutrients, as well as a moderate temperature. Resident microbes of the mouth adhere to the teeth and gums to resist mechanical flushing from the mouth to stomach where acid-sensitive microbes are destroyed by hydrochloric acid.

<span class="mw-page-title-main">Microbiota</span> Community of microorganisms

Microbiota are the range of microorganisms that may be commensal, mutualistic, or pathogenic found in and on all multicellular organisms, including plants. Microbiota include bacteria, archaea, protists, fungi, and viruses, and have been found to be crucial for immunologic, hormonal, and metabolic homeostasis of their host.

<span class="mw-page-title-main">Oral ecology</span>

Oral ecology is the microbial ecology of the microorganisms found in mouths. Oral ecology, like all forms of ecology, involves the study of the living things found in oral cavities as well as their interactions with each other and with their environment. Oral ecology is frequently investigated from the perspective of oral disease prevention, often focusing on conditions such as dental caries, candidiasis ("thrush"), gingivitis, periodontal disease, and others. However, many of the interactions between the microbiota and oral environment protect from disease and support a healthy oral cavity. Interactions between microbes and their environment can result in the stabilization or destabilization of the oral microbiome, with destabilization believed to result in disease states. Destabilization of the microbiome can be influenced by several factors, including diet changes, drugs or immune system disorders.

<span class="mw-page-title-main">Mānuka honey</span> Type of honey

Mānuka honey is a monofloral honey produced from the nectar of the mānuka tree, Leptospermum scoparium.

Soil microbiology is the study of microorganisms in soil, their functions, and how they affect soil properties. It is believed that between two and four billion years ago, the first ancient bacteria and microorganisms came about on Earth's oceans. These bacteria could fix nitrogen, in time multiplied, and as a result released oxygen into the atmosphere. This led to more advanced microorganisms, which are important because they affect soil structure and fertility. Soil microorganisms can be classified as bacteria, actinomycetes, fungi, algae and protozoa. Each of these groups has characteristics that define them and their functions in soil.

Microbial biogeography is a subset of biogeography, a field that concerns the distribution of organisms across space and time. Although biogeography traditionally focused on plants and larger animals, recent studies have broadened this field to include distribution patterns of microorganisms. This extension of biogeography to smaller scales—known as "microbial biogeography"—is enabled by ongoing advances in genetic technologies.

<span class="mw-page-title-main">Root microbiome</span>

The root microbiome is the dynamic community of microorganisms associated with plant roots. Because they are rich in a variety of carbon compounds, plant roots provide unique environments for a diverse assemblage of soil microorganisms, including bacteria, fungi and archaea. The microbial communities inside the root and in the rhizosphere are distinct from each other, and from the microbial communities of bulk soil, although there is some overlap in species composition.

<span class="mw-page-title-main">Phycosphere</span> Microscale mucus region that is rich in organic matter surrounding a phytoplankton cel

The phycosphere is a microscale mucus region that is rich in organic matter surrounding a phytoplankton cell. This area is high in nutrients due to extracellular waste from the phytoplankton cell and it has been suggested that bacteria inhabit this area to feed on these nutrients. This high nutrient environment creates a microbiome and a diverse food web for microbes such as bacteria and protists. It has also been suggested that the bacterial assemblages within the phycosphere are species-specific and can vary depending on different environmental factors.

<span class="mw-page-title-main">Microbiome</span> Microbial community assemblage and activity

A microbiome is the community of microorganisms that can usually be found living together in any given habitat. It was defined more precisely in 1988 by Whipps et al. as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity". In 2020, an international panel of experts published the outcome of their discussions on the definition of the microbiome. They proposed a definition of the microbiome based on a revival of the "compact, clear, and comprehensive description of the term" as originally provided by Whipps et al., but supplemented with two explanatory paragraphs. The first explanatory paragraph pronounces the dynamic character of the microbiome, and the second explanatory paragraph clearly separates the term microbiota from the term microbiome.

The initial acquisition of microbiota is the formation of an organism's microbiota immediately before and after birth. The microbiota are all the microorganisms including bacteria, archaea and fungi that colonize the organism. The microbiome is another term for microbiota or can refer to the collected genomes.

<span class="mw-page-title-main">Holobiont</span> Host and associated species living as a discrete ecological unit

A holobiont is an assemblage of a host and the many other species living in or around it, which together form a discrete ecological unit through symbiosis, though there is controversy over this discreteness. The components of a holobiont are individual species or bionts, while the combined genome of all bionts is the hologenome. The holobiont concept was initially introduced by the German theoretical biologist Adolf Meyer-Abich in 1943, and then apparently independently by Dr. Lynn Margulis in her 1991 book Symbiosis as a Source of Evolutionary Innovation. The concept has evolved since the original formulations. Holobionts include the host, virome, microbiome, and any other organisms which contribute in some way to the functioning of the whole. Well-studied holobionts include reef-building corals and humans.

<span class="mw-page-title-main">Marine microbiome</span>

All animals on Earth form associations with microorganisms, including protists, bacteria, archaea, fungi, and viruses. In the ocean, animal–microbial relationships were historically explored in single host–symbiont systems. However, new explorations into the diversity of marine microorganisms associating with diverse marine animal hosts is moving the field into studies that address interactions between the animal host and a more multi-member microbiome. The potential for microbiomes to influence the health, physiology, behavior, and ecology of marine animals could alter current understandings of how marine animals adapt to change, and especially the growing climate-related and anthropogenic-induced changes already impacting the ocean environment.

<span class="mw-page-title-main">Plant microbiome</span>

The plant microbiome, also known as the phytomicrobiome, plays roles in plant health and productivity and has received significant attention in recent years. The microbiome has been defined as "a characteristic microbial community occupying a reasonably well-defined habitat which has distinct physio-chemical properties. The term thus not only refers to the microorganisms involved but also encompasses their theatre of activity".

<span class="mw-page-title-main">Plant holobiont</span>

Since the colonization of land by ancestral plant lineages 450 million years ago, plants and their associated microbes have been interacting with each other, forming an assemblage of species that is often referred to as a holobiont. Selective pressure acting on holobiont components has likely shaped plant-associated microbial communities and selected for host-adapted microorganisms that impact plant fitness. However, the high microbial densities detected on plant tissues, together with the fast generation time of microbes and their more ancient origin compared to their host, suggest that microbe-microbe interactions are also important selective forces sculpting complex microbial assemblages in the phyllosphere, rhizosphere, and plant endosphere compartments.

<span class="mw-page-title-main">Endosphere</span>

Some microorganisms, such as endophytes, penetrate and occupy the plant internal tissues, forming the endospheric microbiome. The arbuscular mycorrhizal and other endophytic fungi are the dominant colonizers of the endosphere. Bacteria, and to some degree archaea, are important members of endosphere communities. Some of these endophytic microbes interact with their host and provide obvious benefits to plants. Unlike the rhizosphere and the rhizoplane, the endospheres harbor highly specific microbial communities. The root endophytic community can be very distinct from that of the adjacent soil community. In general, diversity of the endophytic community is lower than the diversity of the microbial community outside the plant. The identity and diversity of the endophytic microbiome of above-and below-ground tissues may also differ within the plant.

<span class="mw-page-title-main">Cetacean microbiome</span>

The cetacean microbiome is the group of communities of microorganisms that reside within whales.

References

  1. ↑ Last, F.T. (1955). "Seasonal incidence of Sporobolomyces on cereal leaves". Trans Br Mycol Soc. 38 (3): 221–239. doi:10.1016/s0007-1536(55)80069-1.
  2. 1 2 3 Cid, Fernanda P.; Maruyama, Fumito; Murase, Kazunori; Graether, Steffen P.; Larama, Giovanni; Bravo, Leon A.; Jorquera, Milko A. (2018). "Draft genome sequences of bacteria isolated from the Deschampsia antarctica phyllosphere". Extremophiles. 22 (3): 537–552. doi:10.1007/s00792-018-1015-x. PMID   29492666. S2CID   4320165.
  3. 1 2 Leveau, Johan HJ (2019). "A brief from the leaf: Latest research to inform our understanding of the phyllosphere microbiome". Current Opinion in Microbiology. 49: 41–49. doi:10.1016/j.mib.2019.10.002. PMID   31707206. S2CID   207946690.
  4. ↑ Ruinen, J. (1956) "Occurrence of Beijerinckia species in the 'phyllosphere'". Nature, 177(4501): 220–221.
  5. 1 2 Dastogeer, K.M., Tumpa, F.H., Sultana, A., Akter, M.A. and Chakraborty, A. (2020) "Plant microbiome–an account of the factors that shape community composition and diversity". Current Plant Biology: 100161. doi : 10.1016/j.cpb.2020.100161. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
  6. ↑ Lindow, Steven E. (1996). "Role of Immigration and Other Processes in Determining Epiphytic Bacterial Populations". Aerial Plant Surface Microbiology. pp. 155–168. doi:10.1007/978-0-585-34164-4_10. ISBN   978-0-306-45382-3.
  7. ↑ Friesen, Maren L.; Porter, Stephanie S.; Stark, Scott C.; von Wettberg, Eric J.; Sachs, Joel L.; Martinez-Romero, Esperanza (2011). "Microbially Mediated Plant Functional Traits". Annual Review of Ecology, Evolution, and Systematics. 42: 23–46. doi:10.1146/annurev-ecolsys-102710-145039.
  8. 1 2 Vogel, Christine; Bodenhausen, Natacha; Gruissem, Wilhelm; Vorholt, Julia A. (2016). "The Arabidopsis leaf transcriptome reveals distinct but also overlapping responses to colonization by phyllosphere commensals and pathogen infection with impact on plant health" (PDF). New Phytologist. 212 (1): 192–207. doi:10.1111/nph.14036. hdl: 20.500.11850/117578 . PMID   27306148.
  9. ↑ Kumaravel, Sowmya; Thankappan, Sugitha; Raghupathi, Sridar; Uthandi, Sivakumar (2018). "Draft Genome Sequence of Plant Growth-Promoting and Drought-Tolerant Bacillus altitudinis FD48, Isolated from Rice Phylloplane". Genome Announcements. 6 (9). doi:10.1128/genomeA.00019-18. PMC   5834328 . PMID   29496824.
  10. ↑ Laforest‐Lapointe, Isabelle; Whitaker, Briana K. (2019). "Decrypting the phyllosphere microbiota: Progress and challenges". American Journal of Botany. 106 (2): 171–173. doi: 10.1002/ajb2.1229 . PMID   30726571.
  11. 1 2 3 4 5 6 7 8 9 10 11 12 Noble, Anya S.; Noe, Stevie; Clearwater, Michael J.; Lee, Charles K. (2020). "A core phyllosphere microbiome exists across distant populations of a tree species indigenous to New Zealand". PLOS ONE. 15 (8): e0237079. Bibcode:2020PLoSO..1537079N. doi: 10.1371/journal.pone.0237079 . PMC   7425925 . PMID   32790769. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License. CC-BY icon.svg Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License.
  12. ↑ Vorholt, Julia A. (2012). "Microbial life in the phyllosphere". Nature Reviews Microbiology. 10 (12): 828–840. doi:10.1038/nrmicro2910. hdl: 20.500.11850/59727 . PMID   23154261. S2CID   10447146.
  13. 1 2 Stone, Bram W. G.; Jackson, Colin R. (2016). "Biogeographic Patterns Between Bacterial Phyllosphere Communities of the Southern Magnolia (Magnolia grandiflora) in a Small Forest". Microbial Ecology. 71 (4): 954–961. doi:10.1007/s00248-016-0738-4. PMID   26883131. S2CID   17292307.
  14. 1 2 Redford, Amanda J.; Bowers, Robert M.; Knight, Rob; Linhart, Yan; Fierer, Noah (2010). "The ecology of the phyllosphere: Geographic and phylogenetic variability in the distribution of bacteria on tree leaves". Environmental Microbiology. 12 (11): 2885–2893. doi:10.1111/j.1462-2920.2010.02258.x. PMC   3156554 . PMID   20545741.
  15. ↑ Vokou, Despoina; Vareli, Katerina; Zarali, Ekaterini; Karamanoli, Katerina; Constantinidou, Helen-Isis A.; Monokrousos, Nikolaos; Halley, John M.; Sainis, Ioannis (2012). "Exploring Biodiversity in the Bacterial Community of the Mediterranean Phyllosphere and its Relationship with Airborne Bacteria". Microbial Ecology. 64 (3): 714–724. doi:10.1007/s00248-012-0053-7. PMID   22544345. S2CID   17291303.
  16. 1 2 3 Laforest-Lapointe, Isabelle; Messier, Christian; Kembel, Steven W. (2016). "Host species identity, site and time drive temperate tree phyllosphere bacterial community structure". Microbiome. 4 (1): 27. doi: 10.1186/s40168-016-0174-1 . PMC   4912770 . PMID   27316353.
  17. ↑ Zarraonaindia, Iratxe; Owens, Sarah M.; Weisenhorn, Pamela; West, Kristin; Hampton-Marcell, Jarrad; Lax, Simon; Bokulich, Nicholas A.; Mills, David A.; Martin, Gilles; Taghavi, Safiyh; Van Der Lelie, Daniel; Gilbert, Jack A. (2015). "The Soil Microbiome Influences Grapevine-Associated Microbiota". mBio. 6 (2). doi:10.1128/mBio.02527-14. PMC   4453523 . PMID   25805735.
  18. ↑ Finkel, Omri M.; Burch, Adrien Y.; Lindow, Steven E.; Post, Anton F.; Belkin, Shimshon (2011). "Geographical Location Determines the Population Structure in Phyllosphere Microbial Communities of a Salt-Excreting Desert Tree". Applied and Environmental Microbiology. 77 (21): 7647–7655. doi:10.1128/AEM.05565-11. PMC   3209174 . PMID   21926212.
  19. ↑ Finkel, Omri M.; Burch, Adrien Y.; Elad, Tal; Huse, Susan M.; Lindow, Steven E.; Post, Anton F.; Belkin, Shimshon (2012). "Distance-Decay Relationships Partially Determine Diversity Patterns of Phyllosphere Bacteria on Tamrix Trees across the Sonoran Desert". Applied and Environmental Microbiology. 78 (17): 6187–6193. doi:10.1128/AEM.00888-12. PMC   3416633 . PMID   22752165.
  20. 1 2 Kembel, S. W.; O'Connor, T. K.; Arnold, H. K.; Hubbell, S. P.; Wright, S. J.; Green, J. L. (2014). "Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest". Proceedings of the National Academy of Sciences. 111 (38): 13715–13720. Bibcode:2014PNAS..11113715K. doi: 10.1073/pnas.1216057111 . PMC   4183302 . PMID   25225376. S2CID   852584.
  21. ↑ Innerebner, Gerd; Knief, Claudia; Vorholt, Julia A. (2011). "Protection of Arabidopsis thaliana against Leaf-Pathogenic Pseudomonas syringae by Sphingomonas Strains in a Controlled Model System". Applied and Environmental Microbiology. 77 (10): 3202–3210. doi:10.1128/AEM.00133-11. PMC   3126462 . PMID   21421777.
  22. ↑ Lajoie, Geneviève; Maglione, Rémi; Kembel, Steven W. (2020). "Adaptive matching between phyllosphere bacteria and their tree hosts in a neotropical forest". Microbiome. 8 (1): 70. doi: 10.1186/s40168-020-00844-7 . PMC   7243311 . PMID   32438916.
  23. ↑ Compant, Stéphane; Cambon, Marine C.; Vacher, Corinne; Mitter, Birgit; Samad, Abdul; Sessitsch, Angela (2020). "The plant endosphere world – bacterial life within plants". Environmental Microbiology. 23 (4): 1812–1829. doi: 10.1111/1462-2920.15240 . ISSN   1462-2912. PMID   32955144.
  24. 1 2 Finkel, Omri M.; Burch, Adrien Y.; Lindow, Steven E.; Post, Anton F.; Belkin, Shimshon (2011). "Geographical Location Determines the Population Structure in Phyllosphere Microbial Communities of a Salt-Excreting Desert Tree". Applied and Environmental Microbiology. 77 (21): 7647–7655. doi:10.1128/AEM.05565-11. PMC   3209174 . PMID   21926212.
  25. ↑ Vorholt, Julia A. (2012). "Microbial life in the phyllosphere". Nature Reviews Microbiology. 10 (12): 828–840. doi:10.1038/nrmicro2910. hdl: 20.500.11850/59727 . PMID   23154261. S2CID   10447146.
  26. ↑ Lindow, Steven E.; Brandl, Maria T. (2003). "Microbiology of the Phyllosphere". Applied and Environmental Microbiology. 69 (4): 1875–1883. doi:10.1128/AEM.69.4.1875-1883.2003. PMC   154815 . PMID   12676659. S2CID   2304379.
  27. ↑ Bodenhausen, Natacha; Horton, Matthew W.; Bergelson, Joy (2013). "Bacterial Communities Associated with the Leaves and the Roots of Arabidopsis thaliana". PLOS ONE. 8 (2): e56329. doi: 10.1371/journal.pone.0056329 . PMC   3574144 . PMID   23457551.
  28. ↑ Vokou, Despoina; Vareli, Katerina; Zarali, Ekaterini; Karamanoli, Katerina; Constantinidou, Helen-Isis A.; Monokrousos, Nikolaos; Halley, John M.; Sainis, Ioannis (2012). "Exploring Biodiversity in the Bacterial Community of the Mediterranean Phyllosphere and its Relationship with Airborne Bacteria". Microbial Ecology. 64 (3): 714–724. doi:10.1007/s00248-012-0053-7. PMID   22544345. S2CID   17291303.
  29. 1 2 Shade, Ashley; Handelsman, Jo (2012). "Beyond the Venn diagram: The hunt for a core microbiome". Environmental Microbiology. 14 (1): 4–12. doi: 10.1111/j.1462-2920.2011.02585.x . PMID   22004523.
  30. ↑ Berg, Gabriele; Rybakova, Daria; Fischer, Doreen; Cernava, Tomislav; Vergès, Marie-Christine Champomier; Charles, Trevor; Chen, Xiaoyulong; Cocolin, Luca; Eversole, Kellye; Corral, Gema Herrero; Kazou, Maria; Kinkel, Linda; Lange, Lene; Lima, Nelson; Loy, Alexander; MacKlin, James A.; Maguin, Emmanuelle; Mauchline, Tim; McClure, Ryan; Mitter, Birgit; Ryan, Matthew; Sarand, Inga; Smidt, Hauke; Schelkle, Bettina; Roume, Hugo; Kiran, G. Seghal; Selvin, Joseph; Souza, Rafael Soares Correa de; Van Overbeek, Leo; et al. (2020). "Microbiome definition re-visited: Old concepts and new challenges". Microbiome. 8 (1): 103. doi: 10.1186/s40168-020-00875-0 . PMC   7329523 . PMID   32605663.
  31. ↑ Turnbaugh, Peter J.; Hamady, Micah; Yatsunenko, Tanya; Cantarel, Brandi L.; Duncan, Alexis; Ley, Ruth E.; Sogin, Mitchell L.; Jones, William J.; Roe, Bruce A.; Affourtit, Jason P.; Egholm, Michael; Henrissat, Bernard; Heath, Andrew C.; Knight, Rob; Gordon, Jeffrey I. (2009). "A core gut microbiome in obese and lean twins". Nature. 457 (7228): 480–484. Bibcode:2009Natur.457..480T. doi:10.1038/nature07540. PMC   2677729 . PMID   19043404.
  32. ↑ Lundberg, Derek S.; Lebeis, Sarah L.; Paredes, Sur Herrera; Yourstone, Scott; Gehring, Jase; Malfatti, Stephanie; Tremblay, Julien; Engelbrektson, Anna; Kunin, Victor; Rio, Tijana Glavina del; Edgar, Robert C.; Eickhorst, Thilo; Ley, Ruth E.; Hugenholtz, Philip; Tringe, Susannah Green; Dangl, Jeffery L. (2012). "Defining the core Arabidopsis thaliana root microbiome". Nature. 488 (7409): 86–90. Bibcode:2012Natur.488...86L. doi:10.1038/nature11237. PMC   4074413 . PMID   22859206.
  33. ↑ He, Sheng Yang (2020) When plants and their microbes are not in sync, the results can be disastrous The Conversation, 28 August 2020.
  34. ↑ Hamonts, Kelly; Trivedi, Pankaj; Garg, Anshu; Janitz, Caroline; Grinyer, Jasmine; Holford, Paul; Botha, Frederik C.; Anderson, Ian C.; Singh, Brajesh K. (2018). "Field study reveals core plant microbiota and relative importance of their drivers". Environmental Microbiology. 20 (1): 124–140. doi: 10.1111/1462-2920.14031 . PMID   29266641. S2CID   10650949.
  35. ↑ Cernava, Tomislav; Erlacher, Armin; Soh, Jung; Sensen, Christoph W.; Grube, Martin; Berg, Gabriele (2019). "Enterobacteriaceae dominate the core microbiome and contribute to the resistome of arugula (Eruca sativa Mill.)". Microbiome. 7 (1): 13. doi: 10.1186/s40168-019-0624-7 . PMC   6352427 . PMID   30696492.
  36. ↑ Leff, Jonathan W.; Del Tredici, Peter; Friedman, William E.; Fierer, Noah (2015). "Spatial structuring of bacterial communities within individual Ginkgo bilobatrees". Environmental Microbiology. 17 (7): 2352–2361. doi:10.1111/1462-2920.12695. PMID   25367625.
  37. ↑ Hernandez-Agreda, Alejandra; Gates, Ruth D.; Ainsworth, Tracy D. (2017). "Defining the Core Microbiome in Corals' Microbial Soup". Trends in Microbiology. 25 (2): 125–140. doi:10.1016/j.tim.2016.11.003. PMID   27919551.
  38. ↑ Stephens, J. M. C.; Molan, P. C.; Clarkson, B. D. (2005). "A review of Leptospermum scoparium(Myrtaceae) in New Zealand". New Zealand Journal of Botany. 43 (2): 431–449. doi: 10.1080/0028825X.2005.9512966 . S2CID   53515334.
  39. ↑ Cooper, R.A.; Molan, P.C.; Harding, K.G. (2002). "The sensitivity to honey of Gram-positive cocci of clinical significance isolated from wounds". Journal of Applied Microbiology. 93 (5): 857–863. doi: 10.1046/j.1365-2672.2002.01761.x . PMID   12392533. S2CID   24517001.
  40. ↑ Rabie, Erika; Serem, June Cheptoo; Oberholzer, Hester Magdalena; Gaspar, Anabella Regina Marques; Bester, Megan Jean (2016). "How methylglyoxal kills bacteria: An ultrastructural study". Ultrastructural Pathology. 40 (2): 107–111. doi:10.3109/01913123.2016.1154914. hdl: 2263/52156 . PMID   26986806. S2CID   13372064.
  41. ↑ Adams, Christopher J.; Manley-Harris, Merilyn; Molan, Peter C. (2009). "The origin of methylglyoxal in New Zealand manuka (Leptospermum scoparium) honey". Carbohydrate Research. 344 (8): 1050–1053. doi:10.1016/j.carres.2009.03.020. PMID   19368902.
  42. ↑ Atrott, Julia; Haberlau, Steffi; Henle, Thomas (2012). "Studies on the formation of methylglyoxal from dihydroxyacetone in Manuka (Leptospermum scoparium) honey". Carbohydrate Research. 361: 7–11. doi:10.1016/j.carres.2012.07.025. PMID   22960208.
  43. ↑ Mavric, Elvira; Wittmann, Silvia; Barth, Gerold; Henle, Thomas (2008). "Identification and quantification of methylglyoxal as the dominant antibacterial constituent of Manuka (Leptospermum scoparium)honeys from New Zealand". Molecular Nutrition & Food Research. 52 (4): 483–489. doi: 10.1002/mnfr.200700282 . PMID   18210383.
  44. ↑ Hamilton, G., Millner, J., Robertson, A. and Stephens, J. (2013) "Assessment of manuka provenances for production of high 'unique manuka factor' honey". Agronomy New Zealand, 43: 139–144.
  45. ↑ Williams, Simon; King, Jessica; Revell, Maria; Manley-Harris, Merilyn; Balks, Megan; Janusch, Franziska; Kiefer, Michael; Clearwater, Michael; Brooks, Peter; Dawson, Murray (2014). "Regional, Annual, and Individual Variations in the Dihydroxyacetone Content of the Nectar of Ma̅nuka (Leptospermum scoparium) in New Zealand". Journal of Agricultural and Food Chemistry. 62 (42): 10332–10340. doi:10.1021/jf5045958. PMID   25277074.
  46. ↑ Stephens, J.M.C. (2006) "The factors responsible for the varying levels of UMF® in manuka (Leptospermum scoparium) honey", Doctoral dissertation, University of Waikato.
  47. ↑ Noe, Stevie; Manley-Harris, Merilyn; Clearwater, Michael J. (2019). "Floral nectar of wild manuka (Leptospermum scoparium) varies more among plants than among sites". New Zealand Journal of Crop and Horticultural Science. 47 (4): 282–296. doi:10.1080/01140671.2019.1670681. S2CID   204143940.
  48. ↑ Nickless, Elizabeth M.; Anderson, Christopher W. N.; Hamilton, Georgie; Stephens, Jonathan M.; Wargent, Jason (2017). "Soil influences on plant growth, floral density and nectar yield in three cultivars of manuka (Leptospermum scoparium)". New Zealand Journal of Botany. 55 (2): 100–117. doi:10.1080/0028825X.2016.1247732. S2CID   88657399.
  49. ↑ Clearwater, Michael J.; Revell, Maria; Noe, Stevie; Manley-Harris, Merilyn (2018). "Influence of genotype, floral stage, and water stress on floral nectar yield and composition of manuka (Leptospermum scoparium)". Annals of Botany. 121 (3): 501–512. doi:10.1093/aob/mcx183. PMC   5838834 . PMID   29300875.
  50. ↑ Johnston, Peter R. (1998). "Leaf endophytes of manuka (Leptospermum scoparium)". Mycological Research. 102 (8): 1009–1016. doi:10.1017/S0953756297005765.
  51. ↑ McKenzie, E. H. C.; Johnston, P. R.; Buchanan, P. K. (2006). "Checklist of fungi on teatree (Kunzeaand Leptospermumspecies) in New Zealand". New Zealand Journal of Botany. 44 (3): 293–335. doi: 10.1080/0028825X.2006.9513025 . S2CID   84538904.
  52. ↑ Wicaksono, Wisnu Adi; Sansom, Catherine E.; Eirian Jones, E.; Perry, Nigel B.; Monk, Jana; Ridgway, Hayley J. (2018). "Arbuscular mycorrhizal fungi associated with Leptospermum scoparium (Manuka): Effects on plant growth and essential oil content". Symbiosis. 75: 39–50. doi:10.1007/s13199-017-0506-3. S2CID   4819178.
  53. ↑ Wicaksono, Wisnu Adi; Jones, E. Eirian; Monk, Jana; Ridgway, Hayley J. (2016). "The Bacterial Signature of Leptospermum scoparium (Manuka) Reveals Core and Accessory Communities with Bioactive Properties". PLOS ONE. 11 (9): e0163717. Bibcode:2016PLoSO..1163717W. doi: 10.1371/journal.pone.0163717 . PMC   5038978 . PMID   27676607.
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