Figure 1 - uploaded by Philippe Lemanceau
Content may be subject to copyright.
Schematic diagram representing the sources of microorganisms associated with the different plant compartments (spermosphere, rhizosphere and phyllosphere) and the continuum between them. Microorganisms in the spermosphere are recruited from flowers fruits and seeds (1) through internal, floral or external pathway and from soilborne communities (2) via trophic and signal communication; microorganisms in the rhizosphere are recruited from the spermosphere (3), and from soilborne communities via trophic and signal communication (4); microorganisms of the phyllosphere originate from the seed and rhizosphere (3, 5) but mostly from airborne communities upon their ability to adhesion to the plant surface and to resist to biotic and abiotic stresses (6). Flower scheme adapted from Maude, R.B. (1996). Seedborne diseases and their control: Principles and practice. Wallinford, Oxon, UK: CAB International. 

Schematic diagram representing the sources of microorganisms associated with the different plant compartments (spermosphere, rhizosphere and phyllosphere) and the continuum between them. Microorganisms in the spermosphere are recruited from flowers fruits and seeds (1) through internal, floral or external pathway and from soilborne communities (2) via trophic and signal communication; microorganisms in the rhizosphere are recruited from the spermosphere (3), and from soilborne communities via trophic and signal communication (4); microorganisms of the phyllosphere originate from the seed and rhizosphere (3, 5) but mostly from airborne communities upon their ability to adhesion to the plant surface and to resist to biotic and abiotic stresses (6). Flower scheme adapted from Maude, R.B. (1996). Seedborne diseases and their control: Principles and practice. Wallinford, Oxon, UK: CAB International. 

Source publication
Book
Full-text available
Plants are surrounded with microorganisms whose abundance is promoted by the release of plant organic compounds and by the presence of niches favourable to microbial development and activities. These microorganisms thrive in three main plant compartments, i.e., spermosphere, rhizosphere and phyllosphere, which are interconnected. They are recruited...

Contexts in source publication

Context 1
... seeds via the xylem or nonvascular tissue of the mother plant; (2) the floral pathway that represents microbial colonization of developing seeds through the stigma and (3) the external pathway, which corresponds to colonization of mature seeds via contact of the seed with microorganisms located on fruits or threshing residues (Maude, 1996, Fig. 1). Microorganisms transmitted by the internal and floral pathways are usually found in all seed compart- ments, while those transmitted through the external pathway are almost exclusively associated with the seed coat (Singh & Mathur, 2004). As the external pathway is more permissive than the internal or floral pathway, and the ...
Context 2
... together plant roots (including endophytic microorganisms) plus envi- ronment surrounding or attached to and influenced by the roots (Hartmann, Rothballer, & Schmid, 2008). Rhizodeposits promote the abundance and activities of microorganisms in the rhizosphere by providing nutrient sources that support their growth, persistence and physiology (Fig. 1). However, not all the populations of the soil community are favoured in the rhizosphere, as indicated by a lower biodiversity in the rhizosphere than in the corresponding bulk soil ( García-Salamanca et al., 2013;Lemanceau et al., 1995;Marilley, Vogt, Blanc, & Aragno, 1998;Semenov, van Bruggen, & Zelenev, 1999). Only the most ...
Context 3
... efficient colonizers were also able to efficiently use iron and nitrogen oxides as electron acceptors ( Ghirardi et al., 2012); this efficiency was related to the synthesis of specific siderophores and of nitrogen oxide reductases, respectively. These results confirmed the importance of the ability to adapt to iron starvation shown by Robin et al. (2007) and are in agreement with reported increased level of denitrification rates in the rhizosphere (Philippot et al., 2013). ...
Context 4
... colonization of the phyllosphere by microorganisms starts at seedling emergence and starts over every year at leaf flush in the case of perennial plant species. Most phyllosphere microorganisms are acquired horizontally, from the environment. Some of them can also be transmitted vertically, from maternal plants onto offspring via seeds (Fig. ...
Context 5
... microorganisms can originate from various environmental sources, including soil and litter of the germination environment ( Barret et al., 2015;Copeland, Yuan, Layeghifard, Wang, & Guttman, 2015) and bioaerosols (Bulgarelli, Schlaeppi, Spaepen, Ver Loren van Themaat, & Schulze-Lefert, 2013) (Fig. 1). Bioaerosols themselves originate from various sources, including aquatic environments, soil, animals ( Bulgarelli et al., 2013) and of course neighbouring plants ( Wilson, Carroll, Roy, & Blaisdell, 2014). Raindrops, irrigation water (Morris, 2002) and leaf-dwelling insects (Osono, 2014) can also bring some microorganisms onto plant ...
Context 6
... addition, some phyllosphere microorganisms are transmitted from maternal plants onto offspring via seeds (Fig. 1). The transmission can occur via the seed tissues or the exterior of seed coats. Some beneficial bacteria inoculated on maize seeds have for instance been retrieved from leaves, after having colonized the rhizosphere, the roots and the stems (Fig. 1) and have been shown to significantly increase maize tolerance to drought (Naveed, ...
Context 7
... some phyllosphere microorganisms are transmitted from maternal plants onto offspring via seeds (Fig. 1). The transmission can occur via the seed tissues or the exterior of seed coats. Some beneficial bacteria inoculated on maize seeds have for instance been retrieved from leaves, after having colonized the rhizosphere, the roots and the stems (Fig. 1) and have been shown to significantly increase maize tolerance to drought (Naveed, Mitter, Reichenauer, Wieczorek, & Sessitsch, 2014). Such vertical transmis- sion is also common in the endophytic fungal species protecting plants against herbivory ( Hodgson et al., 2014;Rodriguez, White, Arnold, & Redman, 2009). Some species of ...
Context 8
... it colonizes the inflorescence, grows into ovules and colonizes the embryo within the seed ( Rodriguez et al., 2009). Some foliar endophytes of forbs have also been found in and on pollen grains, suggesting that the transmission to seeds can also occur via the pollen tube (Hodgson et al., 2014). ...
Context 9
... in the rhizosphere originate both from seedborne and soilborne microbial community, (3) microorganisms in the phyllosphere partly originate from the soil and the rhizosphere, as suggested by the overlap between phyllosphere and rhizosphere microbial communities ( Bai et al., 2015;Bodenhausen et al., 2013), and from airborne communities (Fig. 1). The recruitment of micro- bial communities in these different spheres (i.e., spermosphere, rhizosphere, phyllosphere) relies on a subtle communication network between plant and microorganisms. This communication plays a major role in the plant selection of specific microbial populations, and there is growing evidence that the host ...

Similar publications

Preprint
Full-text available
Plant growth-promoting bacteria (PGPB) naturally associate with plants and facilitate plant growth through a variety of mechanisms, including the ability to modulate the concentrations of these phytohormones. Ethylene, salicylate and indole-3-acetate are important phytohormones regulating several aspects of plant growth and development, as well as...

Citations

... Microbial habitats in plant and in soil encompass the bulk soil, the rhizosphere, and the endosphere ( Compant et al., 2010;Wang M. et al., 2016). The bulk soil is a meso-to oligotrophic habitat characterized by pronounced heterogeneity in physical properties, nutrient availability, and other abiotic factors ( Lemanceau et al., 2017) and therefore, may both enhance microbial diversity, and support proliferation of particular species (Gottel et al., 2011;Wang M. et al., 2016). In contrast, the rhizosphere is in immediate contact with the plant roots and is actively enriched by a complex mixture of carbon/nutrient sources, such as amino acids, sugars, and other nutrients provided by the plant, in a process known as rhizodeposition ( Hütsch et al., 2002;Bais et al., 2006). ...
Article
Full-text available
The rhizosphere of plants is enriched in nutrients facilitating growth of microorganisms, some of which are recruited as endophytes. Endophytes, especially Actinobacteria, are known to produce a plethora of bioactive compounds. We hypothesized that Leontopodium nivale subsp. alpinum (Edelweiss), a rare alpine medicinal plant, may serve as yet untapped source for uncommon Actinobacteria associated with this plant. Rhizosphere soil of native Alpine plants was used, after physical and chemical pre-treatments, for isolating Actinobacteria. Isolates were selected based on morphology and identified by 16S rRNA gene-based barcoding. Resulting 77 Actinobacteria isolates represented the genera Actinokineospora, Kitasatospora, Asanoa, Microbacterium, Micromonospora, Micrococcus, Mycobacterium, Nocardia, and Streptomyces. In parallel, Edelweiss plants from the same location were surface-sterilized, separated into leaves, roots, rhizomes, and inflorescence and pooled within tissues before genomic DNA extraction. Metagenomic 16S rRNA gene amplicons confirmed large numbers of actinobacterial operational taxonomic units (OTUs) descending in diversity from roots to rhizomes, leaves and inflorescences. These metagenomic data, when queried with isolate sequences, revealed an overlap between the two datasets, suggesting recruitment of soil bacteria by the plant. Moreover, this study uncovered a profound diversity of uncultured Actinobacteria from Rubrobacteridae, Thermoleophilales, Acidimicrobiales and unclassified Actinobacteria specifically in belowground tissues, which may be exploited by a targeted isolation approach in the future.
... Plants have evolved to cope with biotic and abiotic stresses in association with soil microorganisms ( Lemanceau et al., 2017). These microorganisms are known as plant microbiota and, together with the plant, they form an holobiont ( Liu et al., 2018). ...
... As reviewed by Philippot et al. (2013), plant roots release a huge variety of carbon-containing compounds known as rhizodeposits (nutrients, exudates, border cells, and mucilage) which make the rhizosphere more nutritive than the bulk soil, which is mostly mesotrophic/oligotrophic, inducing therefore changes on soil microbial communities. It has been reported that the biodiversity in the rhizosphere is lower than in the corresponding bulk soil (Reinhold-Hurek et al., 2015;Lemanceau et al., 2017) since carbon availability often limits microbial growth (Dennis et al., 2010). Rhizodeposits released by the plants considerably vary according to the age and development of plants, among species and even among different genotypes of the same species (InceoˇgluInceoˇglu et al., 2010;Philippot et al., 2013;Gilbert et al., 2014;Bazghaleh et al., 2015;Hacquard, 2016;Wagner et al., 2016;Lemanceau et al., 2017;Qiao et al., 2017). ...
... It has been reported that the biodiversity in the rhizosphere is lower than in the corresponding bulk soil (Reinhold-Hurek et al., 2015;Lemanceau et al., 2017) since carbon availability often limits microbial growth (Dennis et al., 2010). Rhizodeposits released by the plants considerably vary according to the age and development of plants, among species and even among different genotypes of the same species (InceoˇgluInceoˇglu et al., 2010;Philippot et al., 2013;Gilbert et al., 2014;Bazghaleh et al., 2015;Hacquard, 2016;Wagner et al., 2016;Lemanceau et al., 2017;Qiao et al., 2017). ...
Article
Full-text available
The microbiota colonizing the rhizosphere and the endorhizosphere contribute to plant growth, productivity, carbon sequestration and phytoremediation. Several studies suggested that different plants types and even genotypes of the same plant species harbor partially different microbiomes. Here, we characterize the rhizosphere bacterial and fungal microbiota across five grapevine rootstock genotypes cultivated in the same soil at two vineyards and sampling dates over two years by 16S rRNA gene and ITS high-throughput amplicon sequencing. In addition, we use quantitative PCR (qPCR) approach to measure the relative abundance and dynamic changes of fungal pathogens associated with black-foot disease. The objectives were to (1) unravel the effects of rootstock genotype on microbial communities in the rhizosphere of grapevine and (2) to compare the relative abundances of sequence reads and DNA amount of black-foot disease pathogens. Host genetic control of the microbiome was evident in the rhizosphere of the mature vineyard. Microbiome composition also shifted as year of sampling, and fungal diversity varied with sampling moments. Linear discriminant analysis identified specific bacterial (i.e., Bacillus) and fungal (i.e., Glomus) taxa associated with grapevine rootstocks. Host genotype did not predict any summary metrics of rhizosphere α- and β- diversity in the young vineyard. Regarding black-foot associated pathogens, a significant correlation between sequencing reads and qPCR was observed. In conclusion, grapevine rootstock genotypes in the mature vineyard were associated with different rhizosphere microbiomes. The latter could also have been affected by age of the vineyard, soil properties or field management practices. A more comprehensive study is needed to decipher the cause of the rootstock microbiome selection and the mechanisms by which grapevines are able to shape their associated microbial community. Understanding the vast diversity of bacteria and fungi in the rhizosphere and the interactions between microbiota and grapevine will facilitate the development of future strategies for grapevine protection.
Article
Full-text available
Modern agriculture faces several challenges due to climate change, limited resources, and land degradation. Plant-associated soil microbes harbor beneficial plant growth-promoting (PGP) traits that can be used to address some of these challenges. These microbes are often formulated as inoculants for many crops. However, inconsistent productivity can be a problem since the performance of individual inoculants/microbes vary with environmental conditions. Over the past decade, the ability to utilize Next Generation Sequencing (NGS) approaches with soil microbes has led to an explosion of information regarding plant associated microbiomes. Although this type of work has been predominantly sequence-based and often descriptive in nature, increasingly it is moving towards microbiome functionality. The synthetic microbial communities (SynCom) approach is an emerging technique that involves co-culturing multiple taxa under well-defined conditions to mimic the structure and function of a microbiome. The SynCom approach hopes to increase microbial community stability through synergistic interactions between its members. This review will focus on plant-soil-microbiome interactions and how they have the potential to improve crop production. Current approaches in the formulation of synthetic microbial communities will be discussed, and its practical application in agriculture will be considered.
Article
To explore the effects of elevated ozone (O3) on microbial communities inhabiting phyllo- and endo-spheres of Japonica rice leaves, cultivars Nangeng 5055 (NG5055) and Wuyujing 27 (WYJ27) were grown in either charcoal-filtered air (CF) or elevated O3 (ambient O3 + 40 ppb, E-O3) in field open-top chambers (OTCs) during a growing season. E-O3 increased the values of the Shannon (43–80%) and Simpson (34–51%) indexes of the phyllo-and endo-spheric bacterial communities in NG5055. E-O3 also increased the values of the phyllosphere Simpson index by 58% and the endosphere Shannon index by 54% in WYJ27. Both diversity indexes positively correlated with the contents of nitrogen, phosphorus, magnesium, and soluble sugar, and negatively correlated with the contents of starch and condensed tannins. The leaf-associated bacterial community composition significantly changed in both rice cultivars under E-O3. Moreover, the leaf-associated bacterial communities in NG5055 were more sensitive to E-O3 than those in WYJ27. The chemical properties explained 70% and 98% of variations in the phyllosphere and endosphere bacterial communities, respectively, suggesting a predominant role of chemical status for the endospheric bacterial community. Most variation (57.3%) in the endosphere bacterial community assembly was explained by phosphorus. Gammaproteobacteria and Pantoea were found to be the most abundant class (63–76%) and genus (38–48%) in the phyllosphere and endosphere, respectively. E-O3 significantly increased the relative abundance of Bacteroidetes in the phyllosphere bacterial community and decreased the relative abundance of Gammaproteobacteria in the endophytic community. In conclusion, elevated O3 increased the diversity of bacterial communities of leaf phyllosphere and endosphere, and leaf chemical properties had a more pronounced effect on the endosphere bacterial community.
Article
Seagrasses and associated microbial communities constitute a functional unit (holobiont) which responds as a whole to environmental changes. However, it is still unclear how the microbial colonizers are selected. In this study we compared the epiphytic microbial communities associated with Posidonia oceanica and Halophila stipulacea, Mediterranean native and exotic seagrass species, respectively, growing side by side in monospecific patches within the port of Limassol (Cyprus, Eastern Mediterranean Sea). To evaluate whether the environment rather than the host species and/or its physiological condition play a role in shaping the seagrass epiphytic microbial community, the environmental microbial communities (seawater and sediment) and seagrass associated ones were determined by using 16S rRNA gene amplicon sequencing. Plant ecological status was evaluated by morphological (biometry), structural (density) and biochemical (pigment/phenol content) descriptors. In both species, leaf associated microbial communities are clearly similar to seawater microbes; conversely, microbes associated with H. stipulacea roots/rhizomes differ from the microbial communities in surrounding sediment. In both seagrasses, Pseudomonadaceae was the most abundant family on leaves, but each species harboured unique microbial families. To our best knowledge, this is the first study on these two neighbouring seagrass species, coupling plant ecological status with associated microbial communities. Results demonstrated that each seagrass responded differently to the same environmental conditions and selected different epiphytic microbial communities, supporting their putative use as ecological indicators.
Chapter
The plant root is an adaptive organ that both affects and is affected by the physical, chemical, and biological properties of the surrounding soil. The rhizosphere is the zone of soil immediately influenced by the root with altered microbial diversity, increased activity and number of organisms, and complex interactions between soil microorganisms and the root. The significance of the rhizosphere arises from the release of organic material from the root and the subsequent effect of increased microbial activity on nutrient cycling and plant growth. The unique assemblage of microorganisms in the rhizosphere, known as the rhizosphere microbiome, where microbial community composition, abundance, and functional attributes are distinct from the bulk soil microbiome of the surrounding environment, can both influence and be influenced by plant growth. This chapter explores the rhizosphere habitat, how roots and microbes interact, and ways that this relationship is affected by environmental conditions and management.
Article
Full-text available
Plants have always grown and evolved surrounded by numerous microorganisms that inhabit their environment, later termed microbiota. To enhance food production, humankind has relied on various farming practices such as irrigation, tilling, fertilization, and pest and disease management. Over the past few years, studies have highlighted the impacts of such practices, not only in terms of plant health or yields but also on the microbial communities associated with plants, which have been investigated through microbiome studies. Because some microorganisms exert beneficial traits that improve plant growth and health, understanding how to modulate microbial communities will help in developing smart farming and favor plant growth-promoting (PGP) microorganisms. With tremendous cost cuts in NGS technologies, metagenomic approaches are now affordable and have been widely used to investigate crop-associated microbiomes. Being able to engineer microbial communities in ways that benefit crop health and growth will help decrease the number of chemical inputs required. Against this background, this review explores the impacts of agricultural practices on soil- and plant-associated microbiomes, focusing on plant growth-promoting microorganisms from a metagenomic perspective.
Article
The phyllosphere is considered a key site for the transfer of both naturally and anthropogenically selected antimicrobial resistance genes (ARGs) to humans. Consequently, the development of green building systems may pose an, as yet, unexplored pathway for ARGs and pathogens to transfer from the environment to outdoor plants. We collected leaves from plants climbing up buildings at 1, 2, 4 and 15 m above ground level and collected associated dust samples from adjacent windowsills to determine the diversity and relative abundance of microbiota and ARGs. Overall, a total of 143 ARGs from 11 major classes and 18 mobile genetic elements (MGEs) were detected. The relative abundance of ARGs within the phyllosphere decreased with increasing height above ground level. Fast expectation–maximization microbial source tracking (FEAST) suggested that the contribution of soil and aerosols to the phyllosphere microbiome was limited. A culture-dependent method to isolate bacteria from plant tissues identified a total of 91 genera from root, stem, and leaf samples as well as endophytes isolated from leaves. Of those bacteria, 20 isolates representing 9 genera were known human pathogenic members to humans. Shared bacterial from culture-dependent and culture-independent methods suggest microorganisms may move from soil to plant, potentially through an endophytic mechanism and thus, there is a clear potential for movement of ARGs and human pathogens from the outdoor environment.
Article
Full-text available
Microbes and seagrass establish symbiotic relationships constituting a functional unit called the holobiont that reacts as a whole to environmental changes. Recent studies have shown that the seagrass microbial associated community varies according to host species, environmental conditions and the host’s health status, suggesting that the microbial communities respond rapidly to environmental disturbances and changes. These changes, dynamics of which are still far from being clear, could represent a sensitive monitoring tool and ecological indicator to detect early stages of seagrass stress. In this review, the state of art on seagrass holobiont is discussed in this perspective, with the aim of disentangling the influence of different factors in shaping it. As an example, we expand on the widely studied Halophila stipulacea’s associated microbial community, highlighting the changing and the constant components of the associated microbes, in different environmental conditions. These studies represent a pivotal contribution to understanding the holobiont’s dynamics and variability pattern, and to the potential development of ecological/ecotoxicological indices. The influences of the host’s physiological and environmental status in changing the seagrass holobiont, alongside the bioinformatic tools for data analysis, are key topics that need to be deepened, in order to use the seagrass-microbial interactions as a source of ecological information.