New Phytologist

Plants can no longer be considered as standalone entities and a more holistic perception is needed. Indeed, plants harbor a wide diversity of microorganisms both inside and outside their tissues, in the endosphere and ectosphere, respectively. These microorganisms, which mostly belong to Bacteria and Fungi, are involved in major functions such as plant nutrition and plant resistance to biotic and abiotic stresses. Hence, the microbiota impact plant growth and survival, two key components of fitness. Plant fitness is therefore a consequence of the plant per se and its microbiota, which collectively form a holobiont. Complementary to the reductionist perception of evolutionary pressures acting on plant or symbiotic compartments, the plant holobiont concept requires a novel perception of evolution. The interlinkages between the plant holobiont components are explored here in the light of current ecological and evolutionary theories. Microbiome complexity and the rules of microbiotic community assemblage are not yet fully understood. It is suggested that the plant can modulate its microbiota to dynamically adjust to its environment. To better understand the level of plant dependence on the microbiotic components, the core microbiota need to be determined at different hierarchical scales of ecology while pan‐microbiome analyses would improve characterization of the functions displayed.

I. Introduction

The association between plants and microorganisms is known to be ancient, and arbuscular mycorrhizal (AM) mutualism is believed to have played a key role in the terrestrialization process and to have accompanied the evolution and diversification of plant phototrophs (Selosse & Le Tacon, 1998; Heckman et al., 2001). The community of mycorrhiza colonizing a plant has been extensively studied over several decades. However, it was only in 2002 that the diversity of fungi colonizing the plant root was shown to be much greater than previously believed (Vandenkoornhuyse et al., 2002), indicating a gap in our knowledge concerning microorganisms colonizing roots. Over the last few years, research into plant microbiota (i.e. the diversity of plant‐associated microorganisms within the so‐called plant microbiome) has progressed significantly. Analysis of the plant microbiome involves linking microbial ecology and the plant host's biology and functioning, and viewing microorganisms as a reservoir of additional genes and functions for their host. Even if, at first sight, the interaction might appear to be symptomless, the additive ecological functions supported by the plant microbiome are acknowledged to be a major trait extending the plant's ability to adapt to many kinds of environmental conditions and changes (Bulgarelli et al., 2013), which is of primary significance in view of the sessile lifestyle of plants. Deciphering the various types of interaction between plants and their microbiomes is a hot topic for research in ecology as well as in plant sciences and agronomy. The use of molecular approaches based on high‐throughput sequencing is dramatically extending our knowledge of plant microbiome diversity. Nevertheless, our understanding of the role of the plant microbiome, in terms of ecology and function, remains limited, although analytical studies of the interactions between plants and microorganisms have proliferated in recent years (Kiers et al., 2011; Werner et al., 2014). We are thus only just beginning to comprehend the ecological functions of the plant microbiome. The upshot of this better understanding will have substantial impacts on a variety of research investigations and applications, for example possible innovations for crop production.

We present herein a synthesis of recent research on the plant microbiome and current prospects. We first focus on knowledge of the aboveground and belowground compartments of the plant microbiome, clarifying, in the latter case, the distinction between epiphytes and the rhizosphere. We discuss differences between these plant compartments and related differences in microbiome composition and function, together with the advantages and limits of the molecular tools used to study the plant microbiome. We also explore novel theoretical and empirical ideas to better comprehend the interactions occurring between the plant and its microbiome. We limit this synthesis to the holobiont definition, the host organism and all its symbiotic microbiota (Margulis, 1993; Knowlton & Rohwer, 2003; Gordon et al., 2013) (Fig. 1). The pathogenic fraction of the plant microbiome, including bacteria, oomycetes, other protists and viruses, is not addressed in this review, although its inclusion from a holistic perspective would make sense. Where necessary, references to comprehensive reviews on specific aspects are provided.

**Figure 1**
Open in figure viewer PowerPoint

Scheme of the plant holobiont and related key interaction aspects both in term of evolution and functioning.

Caption
Scheme of the plant holobiont and related key interaction aspects both in term of evolution and functioning.

II. Plants as holobionts

Decades of research have demonstrated the importance of microorganisms in plant health. The difficulty of culturing transplants of different species in the absence of bacteria and fungi is widely known (Hardoim et al., 2008), which strongly implies the importance of such microorganisms in plant growth. It is readily acknowledged that cooperative microbial symbionts play an important role in their host's life and fitness (Kiers & van der Heijden, 2006). Thus, a plant can be regarded as a holobiont comprising the host plant and its microbiota (Zilber‐Rosenberg & Rosenberg, 2008) (Fig. 1). The concept of holobiont requires a collective view of the functions and interactions existing between a macroorganism host and its associated microorganisms (i.e. a single dynamic entity). The holobiome (i.e. the host genome and associated microbiome) can be seen as ‘the genomic reflection of the complex network of symbiotic interactions that link an individual of a given taxon with its associated microbiome’ (Guerrero et al., 2013). This supposes a novel comprehension of evolution acting on the entire holobiont, the holobiont being the unit of selection processes and adaptation (Zilber‐Rosenberg & Rosenberg, 2008) (Fig. 1). Under this theoretical framework, holobiont evolution could lead to variations in either the host or the microbiotic genomes (Zilber‐Rosenberg & Rosenberg, 2008). In addition, related implications of the holobiont concept also need to be examined.

The observed heterogeneity in the plant microbiome within a given organ is the consequence of adaptation processes and adjustments to given environmental conditions of the holobiont and allows rapid buffering of environmental changes (see Section III.). Short‐term responses related to modifications of the symbiotic microbial community (i.e. plant microbiota) can therefore be expected.
Heterogeneity in the symbiotic community could be related to transitory associations while other microbiotic components might form long‐lasting interactions and involve vertical transmission through seeds (Cankar et al., 2005) and/or pseudo‐vertical transmission (Wilkinson, 1997). If it exists, the plant ‘core microbiome’ (see Section IV.) must be functionally significant for the plant holobiont.
The diversity of the endospheric microbiota should be limited by the plant's innate immune defense system (see Section V.) and at the same time the plant microbiota also contribute to the immune system by producing antimicrobial compounds and eliciting plant defense mechanisms (Berendsen et al., 2012). Coordination of these two co‐occurring components of plant defense is assumed to occur (see Section V.).
From an evolutionary perspective, in the context of symbiosis conflicts, there must be mechanisms within the plant holobiont that allow fine‐tuning of host and symbiont behaviors. The sorting mechanisms of the cooperators need to be efficient to maximize plant holobiont fitness (see Section V.).

III. Recruitment of the plant microbiota: what are the driving factors?

We can hypothesize that interactions between plants and soil microorganisms lead to the gradual enrichment of a subset of soil microorganisms in the defined continuum of habitats (or compartments) that extends from the bulk soil to the root internal tissues.

1. The soil, a ‘seed bank’ for root microbiota

Root‐associated microorganisms are mainly recruited from the surrounding soil. The root microbiota are strongly influenced by the composition of the soil microbial species pool that is present in the vicinity of the roots. Several studies, using high‐throughput amplicon sequencing, have demonstrated the strong connection between the soil bacterial communities and root‐associated bacteria in Arabidopsis thaliana (Bulgarelli et al., 2012; Lundberg et al., 2012; Schlaeppi et al., 2014). Also, the importance of local environmental parameters, notably soil properties, as determinants of soil microbial community composition and root microbiota has been demonstrated in various studies (Shakya et al., 2013; Schreiter et al., 2014). Soil microbial community structure and the associated environmental parameters appear to be more important drivers of root‐associated bacterial community structure than plant genotype or species (Bulgarelli et al., 2012; Lundberg et al., 2012; Shakya et al., 2013; Schlaeppi et al., 2014). However, a plant's evolutionary history can significantly influence the formation of root‐inhabiting bacterial assemblages when different cultivars or species or distinct genotypes of plants are grown in the same soil (Manter et al., 2010; Ofek et al., 2013; Bouffaud et al., 2014). Similarly, the structure of fungal communities is determined more by soil origin than by plant host species (Bonito et al., 2014).

2. The rhizosphere, a ‘growth chamber’

At the periphery of the roots, the rhizosphere constitutes the first plant‐influenced habitat encountered by soil microorganisms. This thin layer of soil that surrounds roots is profoundly influenced by plant metabolism through the release of oxygen and secretion of a highly complex array of exudates including not only carbon‐rich molecules that can be used as energy sources by microorganisms but also antimicrobial compounds. Overall, this makes the rhizosphere between soil and roots a highly dynamic environment and a differentiation of microbial communities has been shown to occur accordingly (Peiffer et al., 2013; Schreiter et al., 2014). For example, the ‘recruitment’ in the rhizosphere of fungi with antagonistic activity toward the soilborne plant pathogen Verticillium dahliae has been reported (Berg et al., 2005). A recent work elegantly shows that differences between microbial communities are explained by an enrichment of microbial functional capabilities in the rhizosphere/rhizoplane which is dependent on the plant species (Ofek‐Lalzar et al., 2014). However, other recent comparisons of the microbial communities residing in the rhizosphere of A. thaliana and in the surrounding bulk soil revealed a weak ‘rhizosphere effect’, as only slight differences in taxonomic composition and community structure could be detected (Bulgarelli et al., 2012; Lundberg et al., 2012; Schlaeppi et al., 2014), and similarly in oak (Quercus sp.) (Uroz et al., 2010). In these studies, the rhizosphere microbiota appear to be largely similar to the microbial communities present in the surrounding soil. As there is no physical limit between the soil and the rhizosphere, this could be attributable to sampling methodologies that do not allow the isolation of genuine rhizospheric microorganisms from the overwhelming majority of soil microorganisms. In addition, high‐throughput amplicon sequencing does not, to date, allow detailed taxonomic affiliation of sequences, because of the relatively short 16S rRNA gene sequences obtained, which in turn prevents the detection of fine differences between the compartments. It is worth noting, nevertheless, that the specific richness of bacteria in the rhizosphere seems to be less than in the microbial communities in the surrounding soil (Bulgarelli et al., 2012).

3. The rhizoplane, a specific habitat or a transitional boundary?

The rhizoplane, or root tissue surface, is often defined as a separate habitat from the rhizosphere, colonized by microorganisms that are firmly attached to the root surface. The most well‐known root‐epiphytic microorganisms are fungi forming ectomycorrhizas (EcMs) with ligneous plants. EcMs are mostly involved in enhancing soil nutrient mobilization and uptake while, in turn, the host plant provides carbohydrates (Courty et al., 2010; Cairney, 2011). Despite the large amount of literature pertaining to EcMs, the community structure and dynamics of the root‐epiphytic compartment still need to be determined. Again, there is no obvious boundary between the rhizosphere and the rhizoplane. Hence, selective extraction and analysis of the adhering root‐epiphytic compartment using culture‐independent molecular methods and high‐throughput sequencing are very challenging from a technical point of view. Notwithstanding these methodological hindrances, it must be stressed that the rhizoplane constitutes the point of entry to the internal root tissues and that the epiphytic state can be considered as a transition stage between life outside and inside the roots. Catalyzed reporter deposition–fluorescence in situ hybridization (CARD‐FISH) has been efficiently employed to characterize the abundance and spatiotemporal dynamics of bacteria and archaea colonizing the rhizoplane in rice (Oryza sativa) (Schmidt & Eickhorst, 2013). This has led to identification of the sites of preferential colonization by microorganisms such as the root tips and lateral root cracks which can serve as portals for microorganisms to enter the roots (Hardoim et al., 2008). Also in rice, GFP‐tagged Rhizobia were used to follow the patterns of colonization of plant tissues (Chi et al., 2005). Analysis of the dissemination dynamics of Rhizobia revealed an initial colonization of the rhizoplane followed by colonization of the root endosphere. Similarly, in A. thaliana, CARD‐FISH allowed the detection of bacterial phyla at the root surface that had been shown by massive amplicon sequencing to be dominant in the endosphere compartment, therefore strengthening the hypothesis of a recruitment of endosphere microbiota from outside the roots (Bulgarelli et al., 2012).

4. The endosphere, a restricted area

Microorganisms able to penetrate and invade the root internal tissues form the endosphere microbiote. In the vast majority of land plants, the root endosphere is colonized by AM fungi (Smith & Read, 2008) along with other fungi (Vandenkoornhuyse et al., 2002), Bacteria (Reinhold‐Hurek & Hurek, 2011) and, to a lesser extent, Archaea (Sun et al., 2008). Some of these microorganisms are clearly interacting with their host plant. Vandenkoornhuyse et al. (2007) used RNA stable isotope probing to identify previously unknown root‐inhabiting microorganisms that receive and consume labeled photosynthetates from their host plants. Combining stable isotope labeling with high‐throughput sequencing now provides a powerful means of distinguishing the obligate symbionts truly interacting with their host from the facultative, transient endophytes. In contrast to the rhizosphere and the rhizoplane, the plant's endospheres feature highly specific microbial communities. In this habitat, the microbiota are very different from the microbial community in the adjacent soil. Diversity is much lower than that estimated for microbial communities outside the root (Bulgarelli et al., 2012; Schlaeppi et al., 2014). Lundberg et al. (2012) identified only 97 Operational Taxonomic Units (OTUs) of Bacteria (out of 256 OTUs whose abundances were significantly different between plant and bulk soil) that were consistently more abundant in the endosphere of A. thaliana grown in two different soils compared with the ectosphere. Comparisons of taxonomic profiles indicate broad changes in the microbial community structure as one goes from the rhizosphere to the endosphere. The above‐mentioned OTUs were mainly affiliated to a small number of bacterial families including the Streptomycetaceae (Actinobacteria), which dominate the libraries of 16S rRNA gene amplicons. Interestingly, Actinobacteria are known to be producers of a huge variety of antimicrobial compounds (Lazzarini et al., 2000). The selective enrichment of OTUs belonging to Streptomycetaceae in the endosphere of A. thaliana was also detected in another study using a similar experimental set‐up but involving controlled soils as well as soils from natural sites (Bulgarelli et al., 2012). Similarly, when wider sets of plant hosts affiliated to Arabidopsis and Cardamina species were examined, sequences assigned to Actinobacteria, Betaproteobacteria and Bacteroidetes dominated the data sets obtained for the rhizosphere and endosphere samples (Schlaeppi et al., 2014). Taken together, these findings seem to indicate that the selection of Actinobacteria within the endosphere of distinct species of Arabidopsis, as well as in the Arabidopsis relative Cardamina hirsuta, is robust against differences in soil microbial community structure, local environmental parameters or host genotypes.

5. The aboveground compartment

In addition to the studies on plant microbiota associated with belowground plant organs, evidence is accumulating to suggest substantial abundance and diversity of microbial denizens residing either inside or outside the aerial tissues of plants (Peñuelas & Terradas, 2014). Few studies have investigated the microbiome composition in reproductive organs (i.e. the anthosphere, carposphere and spermosphere), although this could have important implications for vertical transmission (Lopez‐Velasco et al., 2013). The leaf internal tissues constitute an attractive environment for a large diversity of bacteria and fungi. Analysis of A. thaliana (Bodenhausen et al., 2013) and Solanum lycopersicon L. (Romero et al., 2014) indicated very different leaf endosphere microbiotic compositions. Based on the comparison of microbial communities located in the ectosphere and endosphere of the above‐ and belowground organs of plants tissues, the colonization of the leaf internal tissues by bacteria originating from either shoots or roots (i.e. microbial endosphere continuity) has been hypothesized (Bodenhausen et al., 2013; Romero et al., 2014). In spite of evidence of within‐plant dissemination of endophytes, one cannot rule out the possibility that most endophytic dwellers found inside leaf tissues originated from the external environment and first colonized the leaf surface.

The global abundance of leaf epiphytic microorganisms has been estimated to be as high as c. 10²⁶ cells (Vorholt, 2012) as a consequence of the huge cumulated surface area represented by leaves. In contrast to root‐associated habitats, the foliar surface is characterized by much harsher conditions such as oligotrophy, exposure to UV radiation and desiccation. Microbial epiphytes, able to thrive on the leaf surface, have evolved different adaptations to cope with these extreme conditions. A phototrophic lifestyle on the leaf surface has been suggested based on the identification of microbial rhodopsins (Atamna‐Ismaeel et al., 2011; Vorholt, 2012). Some of these proteins could act as proton pumps, providing additional energy to diverse members of the phylosphere. Interestingly, these proteins could preferentially absorb green light, thus avoiding an overlap with plant pigments (Atamna‐Ismaeel et al., 2012).

Methylotrophic bacteria have repeatedly been identified on the leaf surface. About 10²⁴ g yr⁻¹ of methanol, a plant metabolic waste product, is emitted from leaves (Galbally & Kirstine, 2002). It is thus not surprising that methylotrophs such as Methylobacteriaceae (Alphaproteobacteria) often dominate the microbial communities on the leaf surface (Vorholt, 2012). Comparison of Methylobacterium communities collected on leaves of several plant species, including A. thaliania, originating from five different sites, revealed that the local environmental conditions were more important drivers of community composition than plant species (Knief et al., 2010).

Bacterial light harvesters and methylotrophs discussed above can be seen as beneficiaries of stable ecological habitat and niches provided by the host plant. Under this assumption, evolution of these microorganisms is expected to lead to the selection of specialized microorganisms able to efficiently colonize the leaf surface. Thus, these microorganisms may induce competitive exclusion of other microorganisms including plant pathogens.

IV. The plant holobiont: an existing core plant microbiota?

1. General concepts

Defining ‘core’ plant microbiota

From the ecological perspective of the plant holobiont, the results obtained from analyzing the ‘core’ microbiota (Fig. 2) can be misleading if the ecological scale of the analysis has not been clearly defined and addressed. Different dimensions of the core microbiota can be defined. The simplest dimension is the individual plant holobiont (Fig. 2), where the core microbiota represent all the microorganisms found in different samples of the given host plant (i.e. this dimension allows the control of possible microbiotic heterogeneity). The core microbiota of a plant population represent the fraction of microorganisms shared between plants of the studied population. The core microbiota of a plant species are the fraction of microorganisms shared between plants from different populations (Fig. 2). Thus, the core microbiome composition is expected to become less and less complex as the hierarchical level of ecological organization increases (i.e. from individual to ecosystem). In addition to these core microbiotic dimensions, additional layers of complexity need to be addressed, especially changes occurring through time and space.

**Figure 2**
Open in figure viewer PowerPoint

The concept of core microbiome in the light of the different hierarchical ecological levels (i.e. expected Venn diagram) (a) and at a given ecological level, changes of the core microbiome through time and space (b).

Caption
The concept of core microbiome in the light of the different hierarchical ecological levels (i.e. expected Venn diagram) (a) and at a given ecological level, changes of the core microbiome through time and space (b).

Taxonomic ranking matters in defining the core microbiota

When comparing microbiomes, the grain of observation also matters. Saying that a Poaceae community is associated with bacteria and fungi, even if true, contains less information than saying that this Poaceae community is associated with Glomus clarum and Burkolderia cepacia. This exaggerated example indicates the importance of taking into account the taxonomic ranking level in order to properly describe a microbiome and make assumptions about its functioning. Furthermore, the observation that G. clarum and B. cepacia occurred together would lead to questions about the rules governing assemblage. Thus, the lowest possible level of taxonomic ranking analysis is expected, and phylogenetic analyses of sequence data would be required to properly describe the microbiome. A clear definition of the core microbiome would be obtained by examining the intersection between sequence analyses for different samples.

A functional definition of core microbiota?

In addition to the taxonomical approach to core microbiome definition, a functional approach is also feasible. In this case, the required data are generated from metagenomic or metatranscriptomic analyses and the obtained sequences are used to predict functions. At a given core microbiome dimension (Fig. 2), the core microbiome is defined by the shared predicted functions. This makes it possible to link diversity with the functions displayed, and to compare observations with theory. Different hypotheses linking diversity and functions have been developed (Naeem et al., 2002). Among these, the hypothesis of key species (Paine, 1969) assumes that a given function is sustained by one species only. Conversely, the hypothesis of functional redundancy supposes that a diversity of organisms contributes to a function (Walker, 1992). Loss of a key species leads to a loss of function while, in the case of functional redundancy, observed differences in the taxonomic composition of the microbiome are not synonymous with function loss. These hypotheses to explain the relationships between diversity and function could account for a possible elasticity in core microbiotic community composition.

In both taxonomic and functional analyses of the core microbiome, we are making the assumption that the higher the ecological dimension, the greater the plant's dependence on the core microbiome. At high levels of ecological hierarchy, analysis of the core microbiota probably highlights key component species (i.e. high plant dependence).

2. Attempts to define the core microbiome

Analyses of plant core microbiota are still in their infancy. A finer perception of the different core microbiome dimensions is required to elucidate the possible rule(s) of organization. An initial attempt to define the core microbiome of A. thaliana has been published recently (Lundberg et al., 2012). This study identified the consistent presence of OTUs mostly affiliated to Streptomycetaceae (Actinobacteria) in the endophytic compartment, which could constitute a potential bacterial core microbiome for A. thaliana. This study focused on a taxonomically based description of the core microbiota. Although one can speculate about possible functions, a clear functional description of the core microbiome of A. thaliana remains elusive.

The presence of a common set of protein‐coding genes can reveal assembly rules based on functions rather than on species compositions, as underlined recently (Ofek‐Lalzar et al., 2014). One interesting example has emerged from the analysis of epiphytic microbial communities of the green macroalga Ulva australis (Burke et al., 2011). Community membership analysis highlighted high phylogenetic variability and low similarity in microbial taxonomic composition between the algal samples (i.e. 15% similarity), whereas they demonstrated high similarities in functional composition (70% similarity), which suggests an existing functional redundancy.

Toward a pan‐microbiome analysis?

The measured plant microbiotic compositions do show heterogeneity (i.e. Lundberg et al., 2012). This observed variance can be related, among other things, to sampling bias, heterogeneity between plant tissues and heterogeneous plant growth conditions. The definition of the core microbiome corresponds to the intersection across all the samples analyzed at a given level of ecological hierarchy. From a theoretical point of view, if the heterogeneity between samples is high, (1) a limited core microbiome can be expected and (2) the defined core microbiome composition will decline as the number of samples is increased. This theoretical reduction of the core microbiome, taken alone, could by itself result in important components of the microbiota being overlooked. To circumvent this drawback, it might be helpful to relax the definition of ‘core microbiome’ at a given ecological scale. A pan‐microbiome perspective refers to the core microbiome plus the microbiome fraction shared between different samples of a given modality (i.e. eco‐microbiome) plus the unshared fraction. According to this concept, those microorganisms and functions belonging to the core are presumed to be essential to the host taxon. Conversely, the ‘accessory’ microbiome (i.e. eco‐microbiome as defined above) would be expected to contain more dispensable functions or microorganisms whose presence is related to interactions with the surrounding environmental conditions. The pan‐microbiome concept would thus be helpful to take into account the observed heterogeneity that does exist among plant microbiota and to thereby improve our understanding of the rules of assembly governing plant microbiotic composition.

V. The plant and its microbiome: what controls what?

The question of possible control of the microbiome by the plant or, reciprocally, control of the plant by its microbiome is important to address as it impacts our understanding of fitness (i.e. survival and reproduction) at the level of the plant holobiont and of the endosphere and ectosphere microbial populations.

Likely key components for understanding what controls what in the plant holobiont include the modulation of functional plasticity of the microbiota to adjust the plant holobiont to its environment, the plant immune system and also the symbiosis behavior.

1. Functional plasticity of the plant holobiont

Trophic interactions among (micro)organisms are accepted to be key drivers controlling community assembly (Tilman, 1982; Mittelbach, 2012), which mostly takes into account competition processes. However, the positive interactions among same trophic guilds, referred to as facilitation, are key processes in ecosystems. It is now argued that facilitation (i.e. positive interactions) is an omnipresent driver of biodiversity (McIntire & Fajardo, 2014). Facilitation involves different processes such as (1) the mitigation of abiotic stresses, (2) the creation of novel habitats, (3) heterogeneity and habitat complexity, (4) service sharing, and (5) the best possible access to resources (McIntire & Fajardo, 2014). All of these phenomena help to maintain or improve spatial and local diversity. The plant holobiont concept provides a new perspective on and understanding of facilitation. In fact, the plant microbiota can be seen as a facilitator component providing additional genes to the host, which are involved in the adjustment to local environmental conditions. This view is supported by various lines of evidence. First, plant microbiome composition is more dependent on the soil type in which a given plant genotype has been grown rather than on the plant genotype per se (Bulgarelli et al., 2012), which suggests that the microbiome composition trajectory is environmentally dependent. Secondly, some host‐adapted microbes may have been selected as they provide a selective advantage for their host, and there is growing evidence of recruitment by the plant of microorganisms from the ectosphere to fight pathogens (for a review, see Berendsen et al., 2012), and/or to improve its nutrition and growth (e.g. via mycorrhiza formation). Thirdly, the colonization of a plant by particular microorganisms can lead to substantial phenotypic modifications (Streitwolf‐Engel et al., 1997, 2001; Wagner et al., 2014). Because facilitation and related plant functional plasticity embrace multiple mechanisms primed by the plant microbiota, it is clear that a plant can no longer be seen as a standalone entity. Plants require the means to dynamically adjust to biotic and abiotic constraints on account of their sessile lifestyle. The use of resources by a plant necessarily leads to an alteration in the available multidimensional niches (McIntire & Fajardo, 2014). We are proposing the hypothesis that the plant microbiome is the powerhouse of the adjustment to local conditions.

2. Plant immunity and microbiota

Plants have mechanisms to fight colonization by microorganisms. A focus on the molecular dialogue between the plant and microorganisms is important to better understand how microorganisms can live on or in their host plants.

Plant innate immunity overview

Plants rely on innate immunity. Two forms exist: (1) pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI), formerly called horizontal resistance, and (2) effector‐triggered immunity (ETI), also called R‐gene‐based immunity and previously known as vertical resistance (Jones & Dangl, 2006).

In PTI, microbe‐associated molecular patterns (MAMPs) and damage‐associated molecular patterns (DAMPs) induce corresponding pattern recognition receptors (PRRs) (i.e. host plant receptors) (Boller & Felix, 2009). MAMPs are molecular signatures of the microbe world, the best known probably being the elongation factor and flagellin, which are slowly evolving bacterial features. Bacterial flagellin elicits PTI when it is sensed as a MAMP by the leucine‐rich repeat (LRR) domains of the Flagellin‐Sensing 2 (FLS2) receptor (for a review, see Boller & Felix, 2009). The plant promptly responds by producing reactive oxygen species (ROS), activating defense genes and thickening its cell walls by callose deposition (Boller & Felix, 2009).

Plant pathogens can use effectors, which are tools or weapons to manipulate their hosts by suppressing PTI mechanisms (Kamoun, 2006). Reciprocally, plants have developed the perception of danger signals through the recognition of effectors. ETI corresponds to a direct or indirect interaction between a pathogen effector and the product of a specific plant resistance gene, which leads to a strong response (i.e. hypersensitive response) consisting of cell apoptosis and local necrosis. In this case, nuclear binding sites (NBSs) interact with a variety of LRR domains to initiate cell death (Boller & Felix, 2009). It must be underlined that the knowledge corpus of plant innate immunity is mostly based on reductionist analyses focusing on one host and one microbe. The phytoprotection is also a consequence of biotic interactions where the plant microbiota are suggested to play an important role, such as the case of the fungal leaf endophyte Neotyphodium coenocephalum (Clavicipitaceae) in tall fescue (Festuca arundinacea), which provides a fitness advantage to its host. The success of this fungus‐mediated phytoprotection is so great that it has resulted in the formation of an invasive plant cultivar of tall fescue, ‘Kentucky31’, in North America (Selosse et al., 2004).

Plant defense and microbiota, ‘hand in hand’

As explained in the previous section, MAMPs and DAMPs in PTI and effectors in ETI are interpreted as danger signals by plants (Boller & Felix, 2009). Thus, it can be assumed that MAMPs, DAMPs and effectors are necessarily ‘bypassed’ by the plant microbial endosphere. In agreement with this assumption, it has been suggested that, upon attack by a pathogen, plants are able to recruit protective microorganisms from their ectosphere reservoir (for a review, see Berendsen et al., 2012), procuring a clear modulation of host plant immunity by beneficial microbes (Zamioudis & Pieterse, 2012), which induces systemic resistance primed for accelerated activation (Conrath et al., 2006; Bakker et al., 2007; Berendsen et al., 2012). To date, the recruitment mechanisms of microorganisms from the ectosphere remain poorly understood, while understanding of the mechanisms by which the plant microbiota avoid the plant's defenses is growing.

Microbiota and plant defense ‘manipulation’

Hormonal modulation of plant immunity (for a review, see Pieterse et al., 2012) is especially effective through salicylic acid (SA) and jasmonic acid (JA) acting as backbone cellular signal molecules interplaying with complex networks of regulation (Pieterse et al., 2012). Like some successful plant pathogens, certain root endophytes have been shown to be able to ‘hijack’ or manipulate plant hormone signaling in different ways, by:

synthesizing auxins and auxin analogs along with gibberellins (GAs) (Sirrenberg et al., 2007; Ben Lugtenberg & Kamilova, 2009), which probably attenuate SA signaling (Pieterse et al., 2012);
using effectors which modify the hormonal signaling pathways, as is the case for mycorrhizal fungi (Kloppholz et al., 2011; Plett et al., 2011);
transient accumulation of JA at an early stage of mycorrhiza formation and root‐nodule formation, supposedly to ‘bypass’ the SA‐triggered response (Gutjahr & Paszkowski, 2009).

Both the PTI and EPI innate immunity responses are related to the host plant encoding small RNAs involved in silencing processes of pathways leading to targeted post‐transcriptional gene silencing or transcriptional gene silencing (for a review, see Peláez & Sanchez, 2013). For example, interactions between bacteria‐responsive miRNAs and hormone signaling have been reported to occur after inoculation with symbiotic nitrogen‐fixing bacteria and during nodule development (De Luis et al., 2012; Reynoso et al., 2013). Despite this growing knowledge, the molecular bases of the signaling dialogue which allows an endophytic lifestyle within the host plant are still mostly unknown (Reinhold‐Hurek & Hurek, 2011), and progress in this fascinating research area is expected from comparative metagenomic and metatranscriptomic studies.

Plant defense and microbiota, toward emerging ideas

Because of the great complexity of the endospheric plant microbiota (Lundberg et al., 2012), we can postulate the existence of a generic mechanism across plant and microorganism species rather than specific signaling and plant defense silencing for each given pair of plant species and endospheric microorganism. Bacteria in the exosphere that are able to switch to a life within the endosphere probably possess the required key genetic machinery. It has been suggested that the mechanisms of attraction, recognition and association involve, to some extent, the ancient and widespread common symbiosis (SYM) pathway (Venkateshwaran et al., 2013) and that this root colonization is modulated by plant ethylene concentration (for a review, see Hardoim et al., 2008).

In other situations, different nonpathogenic rhizobacteria are known to be able to trigger systemic plant resistance via the activation of a variety of genes induced by pathogen attack (Conrath et al., 2006). A fraction of the plant endophytic microbiota are also known to synergistically enhance plant health by producing a variety of defensive chemicals (for a review, see Friesen et al., 2011). Thus, in addition to the plant's innate immunity systems, the idea is emerging that the actual plant microbiota can be seen as a component of plant defense.

3. Symbiosis behavior

Symbiosis and especially mutualism are usually regarded as commonplace. However, evolutionary theory predicts that cooperation should not be the norm (Schwartz & Hoeksema, 1998). If a ‘black sheep’ becomes less cooperative but keeps receiving the same advantage from its host or symbiont, a fitness gain in comparison to the ‘wild type’ should occur. From a theoretical point of view, such ‘black sheep’ cheaters thus rapidly invade the population with the result that mutualism would be unstable.

Different hypotheses have been proposed to explain the observed stability of mutualism. Luxury resource exchange, when resources are not limited and exchange is based upon emitted surplus (Kiers & van der Heijden, 2006), could provide shared advantages to the interacting (micro)organisms. Indeed, if both host and symbiont transfer resources in excess, the cost of symbiosis is lower, which is beneficial for both parties. However, it is well known that nutrients can be stored at low cost and that they do not exist in infinite amounts. A second hypothesis relates to partner choice. In this case, partners are able to discriminate based on their functional trait, which can result in an immediate fitness benefit to the interacting individuals (Sachs et al., 2004). The watermark of partner choice is the evaluation of the interaction effectiveness and a related ‘decision’ to keep interacting or to enter into an interaction (Sachs et al., 2004) requiring complex molecular signaling. This hypothesis would probably apply to the fraction of microbial endophytes selected from the rhizosphere by plants (van Overbeek & van Elsas, 2008; Berendsen et al., 2012). Conversely, a simpler process would be based on the rate of nutrient exchanges. In this context, a third hypothesis relates to the possibility of forced cooperative behavior if the interacting individuals are able to reward good partners with nutrients and simultaneously sanction the less cooperative ones. In the case of rhizobium–legume symbiosis, plants have been shown to detect and penalize Rhizobia defective in N₂ fixation by reducing resource allocation (Kiers et al., 2003). Similarly, AM symbiosis is stabilized both by the control of carbon embargo against AM fungal cheaters and by the transfer of phosphorous to plants conditioned by a plant carbon allocation (Kiers et al., 2011).

Despite this growing evidence, which supports the host and symbiont sanction hypothesis to explain cooperative behavior, it is clear that ‘free riders’ (i.e. cheaters) do exist in nature. This can be explained in several different ways.

For example, strains of Rhizobia providing little benefit to their host plant have been shown to be able to circumvent the plant's sanctions by producing rhizobitoxine, an ethylene inhibitor, which promotes an increase in lipid allocation from the host (Ratcliff & Denison, 2009). Furthermore, recent evidence has empirically confirmed the selection for cheating in the legume–rhizobium partnership (Porter & Simms, 2014).
It is hypothesized that the plant sanction trait is no longer selected in modern plant crops selected and grown in nutrient‐enriched soils using conventional agricultural practices and that, in consequence, an increase in the number of cheaters can be expected in conventionally farmed agricultural soils (Duhamel & Vandenkoornhuyse, 2013), a trend that has already been indirectly demonstrated (Johnson, 1993).
Assuming that the plant microbiota are in continuous transition, ‘free riders’ might be seen as maintainers of plant health mechanisms.

All the endophytes within the complex microorganism community could adapt their interaction behaviors (cooperator versus cheater) with the host plant in a way that ‘selfishly’ maximizes their own fitness. Thus, in addition to better understanding the ecological functions of plant endophytes, a key question is how the interaction behaviors of both the plant and microorganisms have evolved. In relation to these key issues, the question of selfishness must be meticulously addressed, especially regarding the biotic interactions within the complex microbiota. As emphasized by Kemen (2014), an improvement in fitness for different microorganisms sharing the same habitat can result from collaboration which can be achieved by sharing common goods (e.g. a detoxifying enzyme, a nutrient produced by a given (micro)organism) and genes. From a more theoretical perspective, the Black Queen Hypothesis (Morris et al., 2012) explains how possible cooperation among species can be ‘automatic’ and based upon purely selfish trajectories. This theory is based on two main assumptions: first, bacterial functions are often leaky, leading to common good production by so‐called helpers, which is consistent to some extent with the idea raised by Kemen (2014); secondly, beneficiaries, by adopting a specialist trajectory, become dependent on the presence of helpers and undergo loss of genes and functions rendered dispensable through the production of common goods. This theory, developed for free‐living microorganisms, may be extended to the interactions among microorganisms of the plant microbiota but needs experimental support.

4. Fitness of the plant holobiont

A plant can classically adapt to changing environment through changes in intrinsic plant traits. However, as described in Section III, a plant can also adapt to the perceived environment by involving different components of its microbiome. Plants can select at least part of their ecto‐ and endospheric microbiota to better adapt to environmental constraints. Partner choice corresponds to the enrollment of a cooperative partner X by an individual Y (X and Y being a microorganism and a plant, respectively), which enables Y to improve its own fitness and to promote the evolution of cooperation processes (Sachs et al., 2004). Despite the evolution of these processes of cooperation, the enrollment of X is not subjected to vertical transmission and so X is not necessarily present in the following generation of Y. Conversely, another fraction of the microbiota can be vertically transmitted. One example is the case of the fungus Epichloë festucae, in Festuca rubra, which impacts the plant's nutrient balance (Vázquez‐de‐Aldana et al., 2013). This vertical transmission allows partner fidelity feedback (Frederickson, 2013) or ‘automatic’ fitness feedback (Sachs et al., 2011), given the fact that vertical transmission tightly correlates symbiont and host reproductive interests (Sachs et al., 2004). On a broader scale, the feedback between partners in cooperative interactions is often in alignment with their respective fitness interests (Friesen, 2012; Frederickson, 2013).

The plant microbiota are complex and consist of a number of partners of different origins and evolutionary trajectories. Because of the broad diversity of microbiota, it can be speculated that each individual component of the microbiota does not have distinct functions but instead that a functional redundancy exists providing opportunities for effective and rapid adaptation.

The fitness measurement of the microbiota components is possible using specific molecular targets combined with detailed spatial and temporal dynamic analyses. Measuring plant fitness per se (i.e. the fitness of the plant alone, excluding the contribution of the microbiome) is much more difficult, even impossible, because this would require axenic growth and therefore a disconnection from most of the environmental factors. In consequence, measures of plant fitness generally include both the endosphere and ectosphere and correspond in fact to the fitness of the plant holobiont. Thus, plants are already viewed intrinsically as holobiont entities. However, the change is in our perception of this fact and our perception of the deep impact of the microbiota in the measurement of plant holobiont fitness. This perception can be extended to measures of a plant phenotypic trait (Streitwolf‐Engel et al., 2001), which is not the consequence solely of plant genome expression under particular constraints (Wagner et al., 2014). One important paper reported that a given AM fungus colonizing different host plants was able to differentially impact the aboveground biomass, a proxy of plant fitness (van der Heijden et al., 1998), thereby impacting plant community structure and productivity (van der Heijden et al., 1998; Vogelsang et al., 2006). Feedbacks between soil communities and plants drive plant community dynamics by modifying the intensity and nature of plant competition (Pendergast et al., 2013).

VI. Concluding remarks and prospects

The species richness and diversity of the plant microbiota are greater than was believed just a few years ago. A new field of research into the intricacies of the plant holobiont is opening up. Certain key issues still need to be addressed. These include: (1) description of the core microbiome and rules of community assemblage, (2) the functions of the microbiota, (3) the molecular interactions occurring between the host plant and its symbionts, and (4) the link between symbiont diversity and functions. Because of our lack of understanding of these issues, we do not yet know how and why the microbiota are so complex. It should be possible to tackle this enigma and related research questions through the use of modern tools such as metagenomics and metatranscriptomics, applying innovative strategies and performing experiments to obtain a detailed description of the microbiome and its expression along with the processes controlling plant genome expression. These molecular analyses could be combined with image analyses and the exchange processes tracked by stable isotope probing approaches, for example. A complementary analysis of the plant holobiont is to manipulate the microbial communities to elucidate the interactions involved, including synergies and exclusions, and also to better understand the ecological functions displayed. This reductionist strategy, applied under controlled conditions using gnotobiotic plants (i.e. mutants germinated in sterile conditions and manipulated microbial communities as in Bodenhausen et al. (2014)), would allow (1) identification of the genetic factors that shape the associated microbial community (Bodenhausen et al., 2014) and (2) elucidation of the importance of the microbiota in plant phenotypic plasticity (Wagner et al., 2014) and the possible adjustment of the plant holobiont to environmental conditions (Panke‐Buisse et al., 2014).

The complexity of the microbiota can be seen as a consequence of: active recruitment of microorganisms by plants; opportunist transfer of nonpathogenic microorganisms through cracks; and pseudo‐vertical and vertical transmission. For the latter, and despite the existence of a large cohort of studies mainly concerning model fungal endophytes, knowledge of the vertically transmitted microbiotic fraction is scarce, and the related co‐evolutionary processes explaining partner fidelity remain poorly investigated.

The plant microbiota are also expected to change through time depending on abiotic and biotic environmental constraints. Among the possible explanations of plant microbiotic complexity that have received little attention is the impact of microbial viruses, which are able to provoke drastic dynamic changes (Buée et al., 2009), and the network of interactions within the microbiota (Bakker et al., 2014; Desirò et al., 2014). Improved knowledge of the microbiome component of the plant holobiont could also lead to a number of important applications in crop production (Rodriguez et al., 2008) and start‐up companies are already emerging. Nevertheless, the importance of this change in perception of the plant microbiota has, as yet, not been fully taken into account in crop selection and production. However, a ‘neodomestication’ of plants, which takes full advantage of the mutualist plant compartment and thus considers the plant holobiont as a whole, is feasible in innovative and ecologically intensive agriculture (Duhamel & Vandenkoornhuyse, 2013).

Acknowledgements

This work was supported by a grant from l'Agence Nationale de la Recherche (ANR‐10‐STRA‐0002) (http://ecs-project.univ-rennes1.fr/news.php). We warmly thank D. Warwick for comments on and suggested modifications to a previous version of the manuscript.

References

Atamna‐Ismaeel N, Finkel OM, Glaser F, Sharon I, Schneider R, Post AF, Spudich JL, von Mering C, Vorholt JA, Iluz D et al. 2011. Microbial rhodopsins on leaf surfaces of terrestrial plants. Environmental Microbiology 14: 140–146.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Atamna‐Ismaeel N, Finkel O, Glaser F, von Mering C, Vorholt JA, Koblížek M, Belkin S, Béjà O. 2012. Bacterial anoxygenic photosynthesis on plant leaf surfaces. Environmental Microbiology Reports 4: 209–216.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Bakker MG, Schlatter DC, Otto‐Hanson L, Kinkel LL. 2014. Diffuse symbioses: roles of plant–plant, plant–microbe and microbe–microbe interactions in structuring the soil microbiome. Molecular Ecology 23: 1571–1583.
Wiley Online Library PubMed Web of Science®Google Scholar
Bakker PAHM, Pieterse CMJ, van Loon LC. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97: 239–243.
Crossref PubMed Web of Science®Google Scholar
Berendsen RL, Pieterse CMJ, Bakker PAHM. 2012. The rhizosphere microbiome and plant health. Trends in Plant Science 17: 478–486.
Crossref CAS PubMed Web of Science®Google Scholar
Berg G, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K. 2005. Impact of plant species and site on rhizosphere‐associated fungi antagonistic to Verticillium dahliae Kleb. Applied and Environmental Microbiology 71: 4203–4213.
Crossref CAS PubMed Web of Science®Google Scholar
Bodenhausen N, Bortfeld‐Miller M, Ackermann M, Vorholt JA. 2014. A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genetics 10: e1004283.
Crossref CAS PubMed Web of Science®Google Scholar
Bodenhausen N, Horton MW, Bergelson J. 2013. Bacterial communities associated with the leaves and the roots of Arabidopsis thaliana. PLoS ONE 8: e56329.
Crossref CAS PubMed Web of Science®Google Scholar
Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe‐associated molecular patterns and danger signals by pattern‐recognition receptors. Annual Review of Plant Biology 60: 379–406.
Crossref CAS PubMed Web of Science®Google Scholar
Bonito G, Reynolds H, Robeson MS, Nelson J, Hodkinson BP, Tuskan G, Schadt CW, Vilgalys R. 2014. Plant host and soil origin influence fungal and bacterial assemblages in the roots of woody plants. Molecular Ecology 23: 3356–3370.
Wiley Online Library PubMed Web of Science®Google Scholar
Bouffaud M‐L, Poirier M‐A, Muller D, Moënne‐Loccoz Y. 2014. Root microbiome relates to plant host evolution in maize and other Poaceae. Environmental Microbiology 16: 2804–2814.
Wiley Online Library PubMed Web of Science®Google Scholar
Buée M, De Boer W, Martin F, van Overbeek L, Jurkevitch E. 2009. The rhizosphere zoo: an overview of plant‐associated communities of microorganisms, including phages, bacteria, archaea, and fungi, and of some of their structuring factors. Plant and Soil 321: 189–212.
Crossref CAS Web of Science®Google Scholar
Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E et al. 2012. Revealing structure and assembly cues for Arabidopsis root‐inhabiting bacterial microbiota. Nature 488: 91–95.
Crossref CAS PubMed Web of Science®Google Scholar
Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze‐Lefert P. 2013. Structure and functions of the bacterial microbiota of plants. Annual Review of Plant Biology 64: 807–838.
Crossref CAS PubMed Web of Science®Google Scholar
Burke C, Steinberg P, Rusch D, Kjelleberg S, Thomas T. 2011. Bacterial community assembly based on functional genes rather than species. Proceedings of the National Academy of Sciences, USA 108: 14288–14293.
Crossref CAS PubMed Web of Science®Google Scholar
Cairney J. 2011. Ectomycorrhizal fungi: the symbiotic route to the root for phosphorus in forest soils. Plant and Soil 344: 51–71.
Crossref CAS Web of Science®Google Scholar
Cankar K, Kraigher H, Ravnikar M, Rupnik M. 2005. Bacterial endophytes from seeds of Norway spruce (Picea abies L. Karst). FEMS Microbiology Letters 244: 341–345.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Chi F, Shen S‐H, Cheng H‐P, Jing Y‐X, Yanni YG, Dazzo FB. 2005. Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Proceedings of the National Academy of Sciences, USA 71: 7271–7278.
PubMed Web of Science®Google Scholar
Conrath U, Beckers GJM, Flors V, García‐Agustín P, Jakab G, Mauch F, Newman M‐A, Pieterse CMJ, Poinssot B, Pozo MJ et al. 2006. Priming: getting ready for battle. Molecular Plant‐Microbe Interactions 19: 1062–1071.
Crossref CAS PubMed Web of Science®Google Scholar
Courty PE, Buée M, Diedhiou AG, Frey‐Klett P. 2010. The role of ectomycorrhizal communities in forest ecosystem processes: new perspectives and emerging concepts. Soil Biology and Biochemistry 42: 679–698.
Crossref CAS Web of Science®Google Scholar
De Luis A, Markmann K, Cognat V, Holt DB, Charpentier M, Parniske M, Stougaard J, Voinnet O. 2012. Two microRNAs linked to nodule infection and nitrogen‐fixing ability in the legume Lotus japonicus. Plant Physiology 160: 2137–2154.
Crossref CAS PubMed Web of Science®Google Scholar
Desirò A, Salvioli A, Ngonkeu EL, Mondo SJ, Epis S, Faccio A, Kaech A, Pawlowska TE, Bonfante P. 2014. Detection of a novel intracellular microbiome hosted in arbuscular mycorrhizal fungi. ISME Journal 8: 257–270.
Crossref CAS PubMed Web of Science®Google Scholar
Duhamel M, Vandenkoornhuyse P. 2013. Sustainable agriculture: possible trajectories from mutualistic symbiosis and plant neodomestication. Trends in Plant Science 18: 597–600.
Crossref CAS PubMed Web of Science®Google Scholar
Frederickson ME. 2013. Rethinking mutualism stability: cheaters and the evolution of sanctions. The Quarterly Review of Biology 88: 269–295.
Crossref PubMed Web of Science®Google Scholar
Friesen ML. 2012. Widespread fitness alignment in the legume‐ rhizobium symbiosis. New Phytologist 194: 1096–1111.
Wiley Online Library PubMed Web of Science®Google Scholar
Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs JL, Martínez‐Romero E. 2011. Microbially mediated plant functional traits. Annual Review of Ecology Evolution and Systematics 42: 23–46.
Crossref Web of Science®Google Scholar
Galbally IE, Kirstine W. 2002. The production of methanol by flowering plants and the global cycle of methanol. Journal of Atmospheric Chemistry 43: 195–229.
Crossref CAS Web of Science®Google Scholar
Gordon J, Knowlton N, Relman DA, Rohwer F, Youle M. 2013. Superorganisms and holobionts. Microbe 8: 152–153.
Google Scholar
Guerrero R, Margulis L, Berlanga M. 2013. Symbiogenesis: the holobiont as a unit of evolution. International Microbiology 16: 133–143.
PubMed Web of Science®Google Scholar
Gutjahr C, Paszkowski U. 2009. Weights in the balance: jasmonic acid and salicylic acid signaling in root–biotroph interactions. Molecular Plant–Microbe Interactions 22: 763–772.
Crossref CAS PubMed Web of Science®Google Scholar
Hardoim PR, van Overbeek LS, Elsas JDV. 2008. Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiology 16: 463–471.
Crossref CAS PubMed Web of Science®Google Scholar
Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB. 2001. Molecular evidence for the early colonization of land by fungi and plants. Science 293: 1129–1133.
Crossref CAS PubMed Web of Science®Google Scholar
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf‐Engel R, Boller T, Wiemken A, Sanders IR. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72.
Crossref CAS Web of Science®Google Scholar
Johnson NC. 1993. Can fertilization of soil select less mutualistic mycorrhizae? Ecological Applications 3: 749–757.
Wiley Online Library PubMed Web of Science®Google Scholar
Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444: 323–329.
Crossref CAS PubMed Web of Science®Google Scholar
Kamoun S. 2006. A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Reviews of Phytopathology 44: 41–60.
Crossref CAS PubMed Web of Science®Google Scholar
Kemen E. 2014. Microbe‐microbe interactions determine oomycete and fungal host colonization. Current Opinion in Plant Biology 20: 75–81.
Crossref PubMed Web of Science®Google Scholar
Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333: 880–882.
Crossref CAS PubMed Web of Science®Google Scholar
Kiers ET, Rousseau RA, West SA, Denison RF. 2003. Host sanctions and the legume–rhizobium mutualism. Nature 425: 78–81.
Crossref CAS PubMed Web of Science®Google Scholar
Kiers ET, van der Heijden MGA. 2006. Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87: 1627–1636.
Wiley Online Library PubMed Web of Science®Google Scholar
Kloppholz S, Kuhn H, Requena N. 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Current Biology 21: 1204–1209.
Crossref CAS PubMed Web of Science®Google Scholar
Knief C, Ramette A, Frances L, Alonso‐Blanco C, Vorholt JA. 2010. Site and plant species are important determinants of the Methylobacterium community composition in the plant phyllosphere. ISME Journal 4: 719–728.
Crossref CAS PubMed Web of Science®Google Scholar
Knowlton N, Rohwer F. 2003. Multispecies microbial mutualisms on coral reefs: the host as a habitat. American Naturalist 162: S51–S62.
Crossref PubMed Web of Science®Google Scholar
Lazzarini A, Cavaletti L, Toppo G, Marinelli F. 2000. Rare genera of actinomycetes as potential producers of new antibiotics. Antonie van Leeuwenhoek 78: 399–405.
Crossref CAS PubMed Web of Science®Google Scholar
Lopez‐Velasco G, Carder PA, Welbaum GE, Ponder MA. 2013. Diversity of the spinach (Spinacia oleracea) spermosphere and phyllosphere bacterial communities. FEMS Microbiology Letters 346: 146–154.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Lugtenberg B, Kamilova F. 2009. Plant‐growth‐promoting rhizobacteria. Annual Review of Microbiology 63: 541–556.
Crossref CAS PubMed Web of Science®Google Scholar
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG et al. 2012. Defining the core Arabidopsis thaliana root microbiome. Nature 488: 86–90.
Crossref CAS PubMed Web of Science®Google Scholar
Manter DK, Delgado JA, Holm DG, Stong RA. 2010. Pyrosequencing reveals a highly diverse and cultivar‐specific bacterial endophyte community in potato roots. Microbial Ecology 60: 157–166.
Crossref PubMed Web of Science®Google Scholar
Margulis L. 1993. Symbiosis in cell evolution, 2nd edn. New York, NY, USA: W. H. Freeman & Co.
Google Scholar
McIntire EJB, Fajardo A. 2014. Facilitation as a ubiquitous driver of biodiversity. New Phytologist 201: 403–416.
Wiley Online Library PubMed Web of Science®Google Scholar
Mittelbach GG. 2012. Community Ecology. Sunderland, MA, USA: Sinauer Associates.
Google Scholar
Morris JJ, Lenski RE, Zinser ER. 2012. The black queen hypothesis: evolution of dependencies through adaptive gene loss. mBio 3: e00036–12.
Crossref PubMed Web of Science®Google Scholar
Naeem S, Loreau M, Inchausti P. 2002. Biodiversity and Ecosystem Functioning: the emergence of a synthetic ecological framework. In: Loreau M, Naeem S, Inchausti P, eds. Biodiversity and ecosystem functioning: synthesis and perspectives, 1st edn. Oxford, UK: Oxford University Press, 3–11.
Google Scholar
Ofek M, Voronov‐Goldman M, Hadar Y, Minz D. 2013. Host signature effect on plant root‐associated microbiomes revealed through analyses of resident vs. active communities. Environmental Microbiology 16: 2157–2167.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Ofek‐Lalzar M, Sela N, Goldman‐Voronov M, Green SJ, Hadar Y, Minz D. 2014. Niche and host‐associated functional signatures of the root surface microbiome. Nature Communications 5: 4950.
Crossref CAS PubMed Web of Science®Google Scholar
van Overbeek L, van Elsas JD. 2008. Effects of plant genotype and growth stage on the structure of bacterial communities associated with potato (Solanum tuberosum L.). FEMS Microbiology Ecology 64: 283–296.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Paine RT. 1969. A note on trophic complexity and community stability. The American Naturalist 103: 91–93.
Crossref Web of Science®Google Scholar
Panke‐Buisse K, Poole AC, Goodrich JK, Ley RE, Kao‐Kniffin J. 2014. Selection on soil microbiomes reveals reproducible impacts on plant function. ISME Journal. doi:10.1038/ismej.2014.196.
CrossrefGoogle Scholar
Peiffer JA, Spor A, Koren O, Jin Z, Green TringeS, Dangl JL, Buckler ES, Ley RE. 2013. Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences, USA 16: 6548–6553.
Crossref Web of Science®Google Scholar
Peláez P, Sanchez F. 2013. Small RNAs in plant defense responses during viral and bacterial interactions: similarities and differences. Frontiers in Plant Science 4: 343.
Crossref PubMed Web of Science®Google Scholar
Pendergast TH IV, Burke DJ, Carson WP. 2013. Belowground biotic complexity drives aboveground dynamics: a test of the soil community feedback model. New Phytologist 197: 1300–1310.
Wiley Online Library PubMed Web of Science®Google Scholar
Peñuelas J, Terradas J. 2014. The foliar microbiome. Trends in Plant Science 19: 278–280.
Crossref CAS PubMed Web of Science®Google Scholar
Pieterse CMJ, Van der Does D, Zamioudis C, Leon‐Reyes A, Van Wees SCM. 2012. Hormonal modulation of plant immunity. Annual Review of Cell and Developmental Biology 28: 489–521.
Crossref CAS PubMed Web of Science®Google Scholar
Plett JM, Kemppainen M, Kale SD, Kohler A, Legu eVER, Brun A, Tyler BM, Pardo AG, Martin F. 2011. A secreted effector protein of laccaria bicolor is required for symbiosis development. Current Biology 21: 1197–1203.
Crossref CAS PubMed Web of Science®Google Scholar
Porter SS, Simms EL. 2014. Selection for cheating across disparate environments in the legume–rhizobium mutualism. Ecology Letters 17: 1121–1129.
Wiley Online Library PubMed Web of Science®Google Scholar
Ratcliff WC, Denison RF. 2009. Rhizobitoxine producers gain more poly‐3‐hydroxybutyrate in symbiosis than do competing rhizobia, but reduce plant growth. ISME Journal 3: 870–872.
Crossref CAS PubMed Web of Science®Google Scholar
Reinhold‐Hurek B, Hurek T. 2011. Living inside plants: bacterial endophytes. Current Opinion in Plant Biology 14: 435–443.
Crossref PubMed Web of Science®Google Scholar
Reynoso MA, Blanco FA, Bailey‐Serres J, Crespi MIN, Zanetti MIAE. 2013. Selective recruitment of mRNAs and miRNAs to polyribosomes in response to rhizobia infection in Medicago truncatula. Plant Journal 73: 289–301.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim Y‐O, Redman RS. 2008. Stress tolerance in plants via habitat‐adapted symbiosis. ISME Journal 2: 404–416.
Crossref PubMed Web of Science®Google Scholar
Romero FM, Marina MIA, Pieckenstain FL. 2014. The communities of tomato (Solanum lycopersicum L.) leaf endophytic bacteria, analyzed by 16S‐ribosomal RNA gene pyrosequencing. FEMS Microbiology Letters 351: 187–194.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Sachs JL, Mueller UG, Wilcox TP, Bull JJ. 2004. The evolution of cooperation. Quarterly Review of Biology 79: 135–160.
Crossref PubMed Web of Science®Google Scholar
Sachs JL, Skophammer RG, Regus JU. 2011. Evolutionary transitions in bacterial symbiosis. Proceedings of the National Academy of Sciences, USA 108: 10800–10807.
Crossref CAS PubMed Web of Science®Google Scholar
Schlaeppi K, Dombrowski N, Oter RG, Ver Loren van Themaat E, Schulze‐Lefert P. 2014. Quantitative divergence of the bacterial root microbiota in Arabidopsis thaliana relatives. Proceedings of the National Academy of Sciences, USA 111: 585–592.
Crossref CAS PubMed Web of Science®Google Scholar
Schmidt H, Eickhorst T. 2013. Detection and quantification of native microbial populations on soil‐grown rice roots by catalyzed reporter deposition‐fluorescence in situ hybridization. FEMS Microbiology Ecology 87: 390–402.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Schreiter S, Ding G‐C, Heuer H, Neumann G, Sandmann M, Grosch R, Kropf S, Smalla K. 2014. Effect of the soil type on the microbiome in the rhizosphere of field‐grown lettuce. Frontiers in Microbiology 5: 144.
Crossref PubMed Web of Science®Google Scholar
Schwartz MW, Hoeksema JD. 1998. Specialization and resource trade: biological markets as a model of mutualisms. Ecology 79: 1029–1038.
Wiley Online Library Web of Science®Google Scholar
Selosse MA, Baudoin E, Vandenkoornhuyse P. 2004. Symbiotic microorganisms, a key for ecological success and protection of plants. Comptes Rendus Biologies 327: 639–648.
Crossref PubMed Web of Science®Google Scholar
Selosse MA, Le Tacon F. 1998. The land flora: a phototroph–fungus partnership? Trends in Ecology & Evolution 13: 15–20.
Crossref CAS PubMed Web of Science®Google Scholar
Shakya M, Gottel N, Castro H, Yang ZK, Gunter L, Labbé J, Muchero W, Bonito G, Vilgalys R, Tuskan G et al. 2013. A multifactor analysis of fungal and bacterial community structure in the root microbiome of mature Populus deltoides trees. PLoS ONE 8: e76382.
Crossref CAS PubMed Web of Science®Google Scholar
Sirrenberg A, Göbel C, Grond S, Czempinski N, Ratzinger A, Karlovsky P, Santos P, Feussner I, Pawlowski K. 2007. Piriformospora indica affects plant growth by auxin production. Physiologia Plantarum 131: 581–589.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Smith SE, Read DJ. 2008. Mycorrhizal symbiosis. New Phytologist 137: 563–568.
Google Scholar
Streitwolf‐Engel R, Boller T, Wiemken A, Sanders IR. 1997. Clonal growth traits of two Prunella species are determined by co‐occurring arbuscular mycorrhizal fungi from a calcareous grassland. Journal of Ecology 85: 181–191.
Crossref Web of Science®Google Scholar
Streitwolf‐Engel R, van der Heijden MGA, Wiemken A, Sanders IR. 2001. The ecological significance of arbuscular mycorrhizal fungal effects on clonal reproduction in plants. Ecology 82: 2846–2859.
Wiley Online Library Web of Science®Google Scholar
Sun L, Qiu F, Zhang X, Dai X, Dong X, Song W. 2008. Endophytic bacterial diversity in rice (Oryza sativa L.) roots estimated by 16S rDNA sequence analysis. Microbial Ecology 55: 415–424.
Crossref CAS PubMed Web of Science®Google Scholar
Tilman D. 1982. Resource competition and community structure. Monographs in Population Biology 17: 1–296.
CAS PubMedGoogle Scholar
Uroz S, Buée M, Murat C, Frey‐Klett P, Martin F. 2010. Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. Environmental Microbiology Reports 2: 281–288.
Wiley Online Library CAS PubMed Web of Science®Google Scholar
Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW. 2002. Extensive fungal diversity in plant roots. Science 295: 2051.
Crossref PubMed Web of Science®Google Scholar
Vandenkoornhuyse P, Mahé S, Ineson P, Staddon P, Ostle N, Cliquet J‐B, Francez A‐J, Fitter AH, Young JPW. 2007. Active root‐inhabiting microbes identified by rapid incorporation of plant‐derived carbon into RNA. Proceedings of the National Academy of Sciences, USA 104: 16970–16975.
Crossref CAS PubMed Web of Science®Google Scholar
Vázquez‐de‐Aldana BR, García‐Ciudad A, García‐Criado B, Vicente‐Tavera S, Zabalgogeazcoa I. 2013. Fungal endophyte (Epichloë festucae) alters the nutrient content of Festuca rubra regardless of water availability. PLoS ONE 8: e84539.
Crossref PubMed Web of Science®Google Scholar
Venkateshwaran M, Volkening JD, Sussman MR, Ané J‐M. 2013. Symbiosis and the social network of higher plants. Current Opinion in Plant Biology 16: 118–127.
Crossref CAS PubMed Web of Science®Google Scholar
Vogelsang KM, Reynolds HL, Bever JD. 2006. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytologist 172: 554–562.
Wiley Online Library PubMed Web of Science®Google Scholar
Vorholt JA. 2012. Microbial life in the phyllosphere. Nature Reviews Microbiology 10: 828–840.
Crossref CAS PubMed Web of Science®Google Scholar
Wagner MR, Lundberg DS, Coleman‐Derr D, Tringe SG, Dangl JL, Mitchell‐Olds T. 2014. Natural soil microbes alter flowering phenology and the intensity of selection on flowering time in a wild Arabidopsis relative. Ecology Letters 17: 717–726.
Wiley Online Library PubMed Web of Science®Google Scholar
Walker BH. 1992. Biodiversity and Ecological Redundancy. Conservation Biology 6: 18–23.
Wiley Online Library Web of Science®Google Scholar
Werner GDA, Strassmann JE, Ivens ABF, Engelmoer DJP, Verbruggen E, Queller DC, Noë R, Johnson NC, Hammerstein P, Kiers ET. 2014. Evolution of microbial markets. Proceedings of the National Academy of Sciences, USA 111: 1237–1244.
Crossref CAS PubMed Web of Science®Google Scholar
Wilkinson DM. 1997. The role of seed dispersal in the evolution of mycorrhizae. Oikos 78: 394–396.
Crossref Web of Science®Google Scholar
Zamioudis C, Pieterse CMJ. 2012. Modulation of host immunity by beneficial microbes. Molecular Plant–Microbe Interactions 25: 139–150.
Crossref CAS PubMed Web of Science®Google Scholar
Zilber‐Rosenberg I, Rosenberg E. 2008. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiology Reviews 32: 723–735.
Wiley Online Library CAS PubMed Web of Science®Google Scholar

Citing Literature

Number of times cited: 143

Kyriaki Glynou, Bora Nam, Marco Thines and Jose G. Maciá‐Vicente, Facultative root‐colonizing fungi dominate endophytic assemblages in roots of nonmycorrhizal Microthlaspi species, New Phytologist, 217, 3, (1190-1202), (2017).
Wiley Online Library
Jessica M. Nelson, Duncan A. Hauser, Rosemary Hinson and A. Jonathan Shaw, A novel experimental system using the liverwort Marchantia polymorpha and its fungal endophytes reveals diverse and context‐dependent effects, New Phytologist, 218, 3, (1217-1232), (2018).
Wiley Online Library
Denis Faure, Jean‐Christophe Simon and Thierry Heulin, Holobiont: a conceptual framework to explore the eco‐evolutionary and functional implications of host–microbiota interactions in all ecosystems, New Phytologist, 218, 4, (1321-1324), (2018).
Wiley Online Library
Tatsuya Nobori, Akira Mine and Kenichi Tsuda, Molecular networks in plant–pathogen holobiont, FEBS Letters, 592, 12, (1937-1953), (2018).
Wiley Online Library
Kelly Hamonts, Pankaj Trivedi, Anshu Garg, Caroline Janitz, Jasmine Grinyer, Paul Holford, Frederik C. Botha, Ian C. Anderson and Brajesh K. Singh, Field study reveals core plant microbiota and relative importance of their drivers, Environmental Microbiology, 20, 1, (124-140), (2018).
Wiley Online Library
Melanie Sapp, Sebastian Ploch, Anna M. Fiore‐Donno, Michael Bonkowski and Laura E. Rose, Protists are an integral part of the Arabidopsis thaliana microbiome, Environmental Microbiology, 20, 1, (30-43), (2017).
Wiley Online Library
Bruno H. P. Rosado, Lidiane C. Almeida, Luciana F. Alves, Marcio R. Lambais and Rafael S. Oliveira, The importance of phyllosphere on plant functional ecology: a phyllo trait manifesto, New Phytologist, 219, 4, (1145-1149), (2018).
Wiley Online Library
Justine Karst, Cole Burns, Jonathan A. Cale, Pedro M. Antunes, Michaela Woods, Louis J. Lamit, Jason D. Hoeksema, Catherine Zabinski, Catherine A. Gehring, Marc La Flèche, Megan A. Rúa and Sally Keith, Tree species with limited geographical ranges show extreme responses to ectomycorrhizas, Global Ecology and Biogeography, 27, 7, (839-848), (2018).
Wiley Online Library
Amit K. Jaiswal, Yigal Elad, Eddie Cytryn, Ellen R. Graber and Omer Frenkel, Activating biochar by manipulating the bacterial and fungal microbiome through pre‐conditioning, New Phytologist, 219, 1, (363-377), (2018).
Wiley Online Library
Fonseca-García Citlali, Damaris Desgarennes, Víctor M. Flores-Núñez and Laila P. Partida-Martínez, The Microbiome of Desert CAM Plants: Lessons From Amplicon Sequencing and Metagenomics, Metagenomics, 10.1016/B978-0-08-102268-9.00012-4, (231-254), (2018).
Crossref
Roman Gonzalez-Escobedo, Carlos I. Briones-Roblero, Rosa M. Pineda-Mendoza, Flor N. Rivera-Orduña and Gerardo Zúñiga, Bacteriome from Pinus arizonica and P. durangensis: Diversity, Comparison of Assemblages, and Overlapping Degree with the Gut Bacterial Community of a Bark Beetle That Kills Pines, Frontiers in Microbiology, 9, (2018).
Crossref
Gabriele Berg and Jos M. Raaijmakers, Saving seed microbiomes, The ISME Journal, (2018).
Crossref
Eric B. Nelson, The seed microbiome: Origins, interactions, and impacts, Plant and Soil, 10.1007/s11104-017-3289-7, 422, 1-2, (7-34), (2017).
Crossref
Ariadna S. Sánchez-López, Sofie Thijs, Bram Beckers, Ma. Carmen González-Chávez, Nele Weyens, Rogelio Carrillo-González and Jaco Vangronsveld, Community structure and diversity of endophytic bacteria in seeds of three consecutive generations of Crotalaria pumila growing on metal mine residues, Plant and Soil, 10.1007/s11104-017-3176-2, 422, 1-2, (51-66), (2017).
Crossref
Arielle Woznica and Nicole King, Lessons from simple marine models on the bacterial regulation of eukaryotic development, Current Opinion in Microbiology, 43, (108), (2018).
Crossref
Thangasamy Saminathan, Marleny García, Bandana Ghimire, Carlos Lopez, Abiodun Bodunrin, Padma Nimmakayala, Venkata L. Abburi, Amnon Levi, Nagamani Balagurusamy and Umesh K. Reddy, Metagenomic and Metatranscriptomic Analyses of Diverse Watermelon Cultivars Reveal the Role of Fruit Associated Microbiome in Carbohydrate Metabolism and Ripening of Mature Fruits, Frontiers in Plant Science, 9, (2018).
Crossref
Allison L. H. Jack and Eric B. Nelson, A seed-recruited microbiome protects developing seedlings from disease by altering homing responses of Pythium aphanidermatum zoospores, Plant and Soil, 422, 1-2, (209), (2018).
Crossref
Roberta Fulthorpe, J. Scott MacIvor, Pu Jia and Simone-Louise E. Yasui, The Green Roof Microbiome: Improving Plant Survival for Ecosystem Service Delivery, Frontiers in Ecology and Evolution, 6, (2018).
Crossref
Kyle Hartman, Marcel G. A. van der Heijden, Raphaël A. Wittwer, Samiran Banerjee, Jean-Claude Walser and Klaus Schlaeppi, Cropping practices manipulate abundance patterns of root and soil microbiome members paving the way to smart farming, Microbiome, 6, 1, (2018).
Crossref
Zhong Wei, Jie Hu, Yi'an Gu, Shixue Yin, Yangchun Xu, Alexandre Jousset, Qirong Shen and Ville-Petri Friman, Ralstonia solanacearum pathogen disrupts bacterial rhizosphere microbiome during an invasion, Soil Biology and Biochemistry, 118, (8), (2018).
Crossref
Gayathri Ilangumaran, John R. Lamont and Donald L. Smith, THE ROLE OF THE PHYTOMICROBIOME IN MAINTAINING BIOFUEL CROP PRODUCTION IN A CHANGING CLIMATE, Microbes for Climate Resilient Agriculture, (1-24), (2017).
Wiley Online Library
Jay Prakash Verma, Functional importance of the plant microbiome: Implications for agriculture, forestry and bioenergy: A book review, Journal of Cleaner Production, 178, (877), (2018).
Crossref
Harihar Jaishree Subrahmaniam, Cyril Libourel, Etienne‐Pascal Journet, Jean‐Benoît Morel, Stéphane Muños, Andreas Niebel, Sylvain Raffaele and Fabrice Roux, The genetics underlying natural variation of plant–plant interactions, a beloved but forgotten member of the family of biotic interactions, The Plant Journal, 93, 4, (747-770), (2018).
Wiley Online Library
Pasquale Alibrandi, Massimiliano Cardinale, MD Mahafizur Rahman, Francesco Strati, Paolo Ciná, Marta L. de Viana, Eugenia M. Giamminola, Giuseppe Gallo, Sylvia Schnell, Carlotta De Filippo, Mirella Ciaccio and Anna Maria Puglia, The seed endosphere of Anadenanthera colubrina is inhabited by a complex microbiota, including Methylobacteriumspp. and Staphylococcus spp. with potential plant-growth promoting activities, Plant and Soil, 422, 1-2, (81), (2018).
Crossref
Leticia Pérez‐Izquierdo, Mario Zabal‐Aguirre, Dulce Flores‐Rentería, Santiago C. González‐Martínez, Marc Buée and Ana Rincón, Functional outcomes of fungal community shifts driven by tree genotype and spatial‐temporal factors in Mediterranean pine forests, Environmental Microbiology, 19, 4, (1639-1652), (2017).
Wiley Online Library
Srisailam Marupakula, Shahid Mahmood, Johanna Jernberg, Srivathsa Nallanchakravarthula, Zaenab A. Fahad and Roger D. Finlay, Bacterial microbiomes of individual ectomycorrhizal Pinus sylvestris roots are shaped by soil horizon and differentially sensitive to nitrogen addition, Environmental Microbiology, 19, 11, (4736-4753), (2017).
Wiley Online Library
Jonathan W. Leff, Ryan C. Lynch, Nolan C. Kane and Noah Fierer, Plant domestication and the assembly of bacterial and fungal communities associated with strains of the common sunflower, Helianthus annuus, New Phytologist, 214, 1, (412-423), (2016).
Wiley Online Library
Stefan Krause, Jörg Lewandowski, Nancy B. Grimm, David M. Hannah, Gilles Pinay, Karlie McDonald, Eugènia Martí, Alba Argerich, Laurent Pfister, Julian Klaus, Tom Battin, Scott T. Larned, Jacob Schelker, Jan Fleckenstein, Christian Schmidt, Michael O. Rivett, Glenn Watts, Francesc Sabater, Albert Sorolla and Valentina Turk, Ecohydrological interfaces as hot spots of ecosystem processes, Water Resources Research, 53, 8, (6359-6376), (2017).
Wiley Online Library
Laila P. Partida‐Martínez, The fungal holobiont: Evidence from early diverging fungi, Environmental Microbiology, 19, 8, (2919-2923), (2017).
Wiley Online Library
Philippe Lemanceau, Manuel Blouin, Daniel Muller and Yvan Moënne-Loccoz, Let the Core Microbiota Be Functional, Trends in Plant Science, 22, 7, (583), (2017).
Crossref
P. Lemanceau, M. Barret, S. Mazurier, S. Mondy, B. Pivato, T. Fort and C. Vacher, Plant Communication With Associated Microbiota in the Spermosphere, Rhizosphere and Phyllosphere, How Plants Communicate with their Biotic Environment, 10.1016/bs.abr.2016.10.007, (101-133), (2017).
Crossref
Nadia Riera, Utpal Handique, Yunzeng Zhang, Megan M. Dewdney and Nian Wang, Characterization of Antimicrobial-Producing Beneficial Bacteria Isolated from Huanglongbing Escape Citrus Trees, Frontiers in Microbiology, 8, (2017).
Crossref
Valerio Mezzasalma, Anna Sandionigi, Ilaria Bruni, Antonia Bruno, Gianni Lovicu, Maurizio Casiraghi, Massimo Labra and Monica Scali, Grape microbiome as a reliable and persistent signature of field origin and environmental conditions in Cannonau wine production, PLOS ONE, 12, 9, (e0184615), (2017).
Crossref
Matthew D. Wallenstein, Managing and manipulating the rhizosphere microbiome for plant health: A systems approach, Rhizosphere, 10.1016/j.rhisph.2017.04.004, 3, (230-232), (2017).
Crossref
Michael James Van Oosten, Olimpia Pepe, Stefania De Pascale, Silvia Silletti and Albino Maggio, The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants, Chemical and Biological Technologies in Agriculture, 4, 1, (2017).
Crossref
Sagar Chhabra and David N. Dowling, Endophyte-Promoted Nutrient Acquisition: Phosphorus and Iron, Functional Importance of the Plant Microbiome, 10.1007/978-3-319-65897-1_3, (21-42), (2017).
Crossref
Alice Checcucci, Isabel Maida, Giovanni Bacci, Cristina Ninno, Anna Rita Bilia, Sauro Biffi, Fabio Firenzuoli, Guido Flamini, Renato Fani and Alessio Mengoni, Is the plant-associated microbiota of Thymus spp. adapted to plant essential oil?, Research in Microbiology, 168, 3, (276), (2017).
Crossref
Yupei Liu, Lixiang Cao, Hongming Tan and Renduo Zhang, Surface display of ACC deaminase on endophytic Enterobacteriaceae strains to increase saline resistance of host rice sprouts by regulating plant ethylene synthesis, Microbial Cell Factories, 16, 1, (2017).
Crossref
Ignacio Belda, Iratxe Zarraonaindia, Matthew Perisin, Antonio Palacios and Alberto Acedo, From Vineyard Soil to Wine Fermentation: Microbiome Approximations to Explain the “terroir” Concept, Frontiers in Microbiology, 8, (2017).
Crossref
Isabelle Laforest-Lapointe, Alain Paquette, Christian Messier and Steven W. Kembel, Leaf bacterial diversity mediates plant diversity and ecosystem function relationships, Nature, 546, 7656, (145), (2017).
Crossref
Rose A. Marks, Jeramiah J. Smith, Quentin Cronk and D. Nicholas McLetchie, Variation in the bacteriome of the tropical liverwort, Marchantia inflexa, between the sexes and across habitats, Symbiosis, (2017).
Crossref
B. R. MURPHY, T. R. HODKINSON and F. M. DOOHAN, A fungal endophyte consortium counterbalances the negative effects of reduced nitrogen input on the yield of field-grown spring barley, The Journal of Agricultural Science, 155, 08, (1324), (2017).
Crossref
David A Baltrus, Adaptation, specialization, and coevolution within phytobiomes, Current Opinion in Plant Biology, 38, (109), (2017).
Crossref
G. Rodríguez-Caballero, F. Caravaca, A.J. Fernández-González, M.M. Alguacil, M. Fernández-López and A. Roldán, Arbuscular mycorrhizal fungi inoculation mediated changes in rhizosphere bacterial community structure while promoting revegetation in a semiarid ecosystem, Science of The Total Environment, 584-585, (838), (2017).
Crossref
Amir H. Ahkami, Richard Allen White, Pubudu P. Handakumbura and Christer Jansson, Rhizosphere engineering: Enhancing sustainable plant ecosystem productivity, Rhizosphere, 3, (233), (2017).
Crossref
Pierre Hohmann and Monika M. Messmer, Breeding for mycorrhizal symbiosis: focus on disease resistance, Euphytica, 10.1007/s10681-017-1900-x, 213, 5, (2017).
Crossref
Ashley Shade, Marie-Agnès Jacques and Matthieu Barret, Ecological patterns of seed microbiome diversity, transmission, and assembly, Current Opinion in Microbiology, 10.1016/j.mib.2017.03.010, 37, (15-22), (2017).
Crossref
Evelyn M Molloy and Christian Hertweck, Antimicrobial discovery inspired by ecological interactions, Current Opinion in Microbiology, 10.1016/j.mib.2017.09.006, 39, (121-127), (2017).
Crossref
Abdul Latif Khan, Sajjad Asaf, Ahmed Al-Rawahi, In-Jung Lee, Ahmed Al-Harrasi and Raffaella Balestrini, Rhizospheric microbial communities associated with wild and cultivated frankincense producing Boswellia sacra tree, PLOS ONE, 12, 10, (e0186939), (2017).
Crossref
Rashid Nazir, Sylvie Mazurier, Pu Yang, Philippe Lemanceau and Jan Dirk van Elsas, The Ecological Role of Type Three Secretion Systems in the Interaction of Bacteria with Fungi in Soil and Related Habitats Is Diverse and Context-Dependent, Frontiers in Microbiology, 8, (2017).
Crossref
Juliana Almario, Ganga Jeena, Jörg Wunder, Gregor Langen, Alga Zuccaro, George Coupland and Marcel Bucher, Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition , Proceedings of the National Academy of Sciences, 10.1073/pnas.1710455114, 114, 44, (E9403-E9412), (2017).
Crossref
Kevin Walsh, J. Matthew Haggerty, Michael P. Doane, John J. Hansen, Megan M. Morris, Ana Paula B. Moreira, Louisi de Oliveira, Luciana Leomil, Gizele D. Garcia, Fabiano Thompson and Elizabeth A. Dinsdale, Aura-biomes are present in the water layer above coral reef benthic macro-organisms, PeerJ, 5, (e3666), (2017).
Crossref
Tyler J. Carrier and Adam M. Reitzel, The Hologenome Across Environments and the Implications of a Host-Associated Microbial Repertoire, Frontiers in Microbiology, 8, (2017).
Crossref
Natalie Christian, Briana K. Whitaker and Keith Clay, Chapter 5 A Novel Framework for Decoding Fungal Endophyte Diversity, The Fungal Community, 10.1201/9781315119496-6, (63-78), (2017).
Crossref
B.J. Hawkins and J.M. Kranabetter, Quantifying inorganic nitrogen uptake capacity among ectomycorrhizal fungal species using MIFE microelectrode ion flux measurements: theory and applications, Botany, 10.1139/cjb-2017-0028, 95, 10, (963-969), (2017).
Crossref
Achim Quaiser, Alexis Dufresne, Sophie Michon-Coudouel, Marine Biget and Philippe Vandenkoornhuyse, Large-Scale Sequence-Based Information, Terrestrial Ecosystem Research Infrastructures, 10.1201/9781315368252-8, (165-192), (2017).
Crossref
Mohamed Mounir Saggaï, Abdelkader Ainouche, Mark Nelson, Florence Cattin and Abdelhak El Amrani, Long-term investigation of constructed wetland wastewater treatment and reuse: Selection of adapted plant species for metaremediation, Journal of Environmental Management, 201, (120), (2017).
Crossref
Abida Sultan, Jens C. Frisvad, Birgit Andersen, Birte Svensson and Christine Finnie, Investigation of the indigenous fungal community populating barley grains: Secretomes and xylanolytic potential, Journal of Proteomics, 169, (153), (2017).
Crossref
Lin Chen, Xiuli Xin, Jiabao Zhang, Marc Redmile-Gordon and Guangsen Nie, Soil Characteristics Overwhelm Cultivar Effects on the Structure and Assembly of Root-Associated Microbiomes of Modern Maize, Pedosphere, (2017).
Crossref
Pious Thomas and Aparna Chandra Sekhar, Cultivation Versus Molecular Analysis of Banana (Musa sp.) Shoot-Tip Tissue Reveals Enormous Diversity of Normally Uncultivable Endophytic Bacteria, Microbial Ecology, 10.1007/s00248-016-0877-7, 73, 4, (885-899), (2016).
Crossref
Sharon Lafferty Doty, Functional Importance of the Plant Endophytic Microbiome: Implications for Agriculture, Forestry, and Bioenergy, Functional Importance of the Plant Microbiome, 10.1007/978-3-319-65897-1_1, (1-5), (2017).
Crossref
S. B. Miguel Paulo, C. Delvaux Julio, N. V. de Oliveira Marcelo, C. Moreira Bruno, C. Borges Arnaldo, R. Totola Marcos, C. L. Neves Julio and D. Costa Mauricio, Diversity and distribution of the endophytic fungal community in eucalyptus leaves, African Journal of Microbiology Research, 11, 3, (92), (2017).
Crossref
Franziska Wemheuer, Kristin Kaiser, Petr Karlovsky, Rolf Daniel, Stefan Vidal and Bernd Wemheuer, Bacterial endophyte communities of three agricultural important grass species differ in their response towards management regimes, Scientific Reports, 7, (40914), (2017).
Crossref
Lilia C Carvalhais, Peer M Schenk and Paul G Dennis, Jasmonic acid signalling and the plant holobiont, Current Opinion in Microbiology, 37, (42), (2017).
Crossref
Sebastiàn Lòpez-Fernàndez, Valerio Mazzoni, Federico Pedrazzoli, Ilaria Pertot and Andrea Campisano, A Phloem-Feeding Insect Transfers Bacterial Endophytic Communities between Grapevine Plants, Frontiers in Microbiology, 8, (2017).
Crossref
Britt Koskella, Lindsay J. Hall and C. Jessica E. Metcalf, The microbiome beyond the horizon of ecological and evolutionary theory, Nature Ecology & Evolution, 10.1038/s41559-017-0340-2, 1, 11, (1606-1615), (2017).
Crossref
Nian Wang, Lukasz L. Stelinski, Kirsten S. Pelz-Stelinski, James H. Graham and Yunzeng Zhang, Tale of the Huanglongbing Disease Pyramid in the Context of the Citrus Microbiome, Phytopathology, 107, 4, (380), (2017).
Crossref
Carmen Sánchez-Cañizares, Beatriz Jorrín, Philip S Poole and Andrzej Tkacz, Understanding the holobiont: the interdependence of plants and their microbiome, Current Opinion in Microbiology, 38, (188), (2017).
Crossref
Sharon L. Doty, John L. Freeman, Christopher M. Cohu, Joel G. Burken, Andrea Firrincieli, Andrew Simon, Zareen Khan, J. G. Isebrands, Joseph Lukas and Michael J. Blaylock, Enhanced Degradation of TCE on a Superfund Site Using Endophyte-Assisted Poplar Tree Phytoremediation, Environmental Science & Technology, 51, 17, (10050), (2017).
Crossref
Hongwei Liu, Lilia C. Carvalhais, Mark Crawford, Eugenie Singh, Paul G. Dennis, Corné M. J. Pieterse and Peer M. Schenk, Inner Plant Values: Diversity, Colonization and Benefits from Endophytic Bacteria, Frontiers in Microbiology, 8, (2017).
Crossref
Mari Pent, Kadri Põldmaa and Mohammad Bahram, Bacterial Communities in Boreal Forest Mushrooms Are Shaped Both by Soil Parameters and Host Identity, Frontiers in Microbiology, 8, (2017).
Crossref
Zhong Wei and Alexandre Jousset, Plant Breeding Goes Microbial, Trends in Plant Science, 22, 7, (555), (2017).
Crossref
Kevin Panke-Buisse, Stacey Lee and Jenny Kao-Kniffin, Cultivated Sub-Populations of Soil Microbiomes Retain Early Flowering Plant Trait, Microbial Ecology, 73, 2, (394), (2017).
Crossref
Aiqun Chen, Mian Gu, Shuangshuang Wang, Jiadong Chen and Guohua Xu, Transport properties and regulatory roles of nitrogen in arbuscular mycorrhizal symbiosis, Seminars in Cell & Developmental Biology, 10.1016/j.semcdb.2017.06.015, (2017).
Crossref
Pious Thomas, Aparna C. Sekhar and Sadiq Pasha Shaik, High taxonomic diversity of cultivation-recalcitrant endophytic bacteria in grapevine field shoots, their in vitro introduction, and unsuspected persistence, Planta, 246, 5, (879), (2017).
Crossref
Prasun Bandyopadhyay and Ajit Varma, Co-cultivation of Piriformospora indica with Azotobacter sp., Mycorrhiza - Eco-Physiology, Secondary Metabolites, Nanomaterials, 10.1007/978-3-319-57849-1_8, (135-148), (2017).
Crossref
Irene Cordero, Beatriz Ruiz-Díez, Luis Balaguer, Andreas Richter, José J. Pueyo and Ana Rincón, Rhizospheric microbial community of Caesalpinia spinosa (Mol.) Kuntze in conserved and deforested zones of the Atiquipa fog forest in Peru, Applied Soil Ecology, 10.1016/j.apsoil.2017.02.015, 114, (132-141), (2017).
Crossref
Adrien Lies, Yves Prin, Robin Duponnois and Hicham Ferhout, The Management of the Mycorrhizal Soil Infectivity: Ecological and Technical Approaches, Mycorrhiza - Eco-Physiology, Secondary Metabolites, Nanomaterials, 10.1007/978-3-319-57849-1_11, (209-221), (2017).
Crossref
Prasun Bandyopadhyay, Soubhagya Kumar Bhuyan, Pramod Kumar Yadava, Ajit Varma and Narendra Tuteja, Emergence of plant and rhizospheric microbiota as stable interactomes, Protoplasma, 254, 2, (617), (2017).
Crossref
Yunzeng Zhang, Jin Xu, Nadia Riera, Tao Jin, Jinyun Li and Nian Wang, Huanglongbing impairs the rhizosphere-to-rhizoplane enrichment process of the citrus root-associated microbiome, Microbiome, 5, 1, (2017).
Crossref
Giuseppe Colla, Lori Hoagland, Maurizio Ruzzi, Mariateresa Cardarelli, Paolo Bonini, Renaud Canaguier and Youssef Rouphael, Biostimulant Action of Protein Hydrolysates: Unraveling Their Effects on Plant Physiology and Microbiome, Frontiers in Plant Science, 8, (2017).
Crossref
Julia A. Vorholt, Christine Vogel, Charlotte I. Carlström and Daniel B. Müller, Establishing Causality: Opportunities of Synthetic Communities for Plant Microbiome Research, Cell Host & Microbe, 10.1016/j.chom.2017.07.004, 22, 2, (142-155), (2017).
Crossref
Silma L. Rocha, Harry C. Evans, Vanessa L. Jorge, Lucimar A. O. Cardoso, Fernanda S. T. Pereira, Fabiano B. Rocha, Robert W. Barreto, Adam G. Hart and Simon L. Elliot, Recognition of endophyticTrichodermaspecies by leaf-cutting ants and their potential in a Trojan-horse management strategy, Royal Society Open Science, 4, 4, (160628), (2017).
Crossref
Pedro E. Gundel, Jennifer A. Rudgers and Kenneth D. Whitney, Vertically transmitted symbionts as mechanisms of transgenerational effects, American Journal of Botany, 104, 5, (787-792), (2017).
Wiley Online Library
Linda S. Thomashow, Induced systemic resistance: a delicate balance, Environmental Microbiology Reports, 8, 5, (560-563), (2016).
Wiley Online Library
Binoy Ambika Manirajan, Stefan Ratering, Volker Rusch, Andreas Schwiertz, Rita Geissler‐Plaum, Massimiliano Cardinale and Sylvia Schnell, Bacterial microbiota associated with flower pollen is influenced by pollination type, and shows a high degree of diversity and species‐specificity, Environmental Microbiology, 18, 12, (5161-5174), (2016).
Wiley Online Library
Pascal Eusemann, Martin Schnittler, R. Henrik Nilsson, Ari Jumpponen, Mathilde B. Dahl, David G. Würth, Allan Buras, Martin Wilmking and Martin Unterseher, Habitat conditions and phenological tree traits overrule the influence of tree genotype in the needle mycobiome–icea glauca system at an arctic treeline ecotone, New Phytologist, 211, 4, (1221-1231), (2016).
Wiley Online Library
Stéphane Hacquard, Disentangling the factors shaping microbiota composition across the plant holobiont, New Phytologist, 209, 2, (454-457), (2015).
Wiley Online Library
Devin Coleman‐Derr, Damaris Desgarennes, Citlali Fonseca‐Garcia, Stephen Gross, Scott Clingenpeel, Tanja Woyke, Gretchen North, Axel Visel, Laila P. Partida‐Martinez and Susannah G. Tringe, Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species, New Phytologist, 209, 2, (798-811), (2015).
Wiley Online Library
Joel E. Kostka, David J. Weston, Jennifer B. Glass, Erik A. Lilleskov, A. Jonathan Shaw and Merritt R. Turetsky, The Sphagnum microbiome: new insights from an ancient plant lineage, New Phytologist, 211, 1, (57-64), (2016).
Wiley Online Library
Daniel Revillini, Catherine A. Gehring, Nancy Collins Johnson and Joseph Bailey, The role of locally adapted mycorrhizas and rhizobacteria in plant–soil feedback systems, Functional Ecology, 30, 7, (1086-1098), (2016).
Wiley Online Library
Amaia Nogales, Tânia Nobre, Vera Valadas, Carla Ragonezi, Matthias Döring, Alexios Polidoros and Birgit Arnholdt-Schmitt, Can functional hologenomics aid tackling current challenges in plant breeding?, Briefings in Functional Genomics, 10.1093/bfgp/elv030, 15, 4, (288-297), (2015).
Crossref
Dániel G. Knapp, Gábor M. Kovács and Angela Sessitsch, Interspecific metabolic diversity of root-colonizing endophytic fungi revealed by enzyme activity tests, FEMS Microbiology Ecology, 10.1093/femsec/fiw190, 92, 12, (fiw190), (2016).
Crossref
F. Roux and J. Bergelson, The Genetics Underlying Natural Variation in the Biotic Interactions of Arabidopsis thaliana, Genes and Evolution, 10.1016/bs.ctdb.2016.03.001, (111-156), (2016).
Crossref
Lin Chen, Philip C. Brookes, Jianming Xu, Jiabao Zhang, Congzhi Zhang, Xiaoyu Zhou and Yu Luo, Structural and functional differentiation of the root-associated bacterial microbiomes of perennial ryegrass, Soil Biology and Biochemistry, 98, (1), (2016).
Crossref
Zhilin Yuan, Irina S. Druzhinina, Jessy Labbé, Regina Redman, Yuan Qin, Russell Rodriguez, Chulong Zhang, Gerald A. Tuskan and Fucheng Lin, Specialized Microbiome of a Halophyte and its Role in Helping Non-Host Plants to Withstand Salinity, Scientific Reports, 10.1038/srep32467, 6, 1, (2016).
Crossref
Daniel B. Müller, Christine Vogel, Yang Bai and Julia A. Vorholt, The Plant Microbiota: Systems-Level Insights and Perspectives, Annual Review of Genetics, 10.1146/annurev-genet-120215-034952, 50, 1, (211-234), (2016).
Crossref
Behnam Khatabi, Neda Maleki Tabrizi and Ghasem Hosseini Salekdeh, Holistic Sequencing: Moving Forward from Plant Microbial Proteomics to Metaproteomics, Agricultural Proteomics Volume 1, 10.1007/978-3-319-43275-5_5, (87-103), (2016).
Crossref
Nathan Vannier, Anne-Kristel Bittebiere, Philippe Vandenkoornhuyse and Cendrine Mony, AM fungi patchiness and the clonal growth of Glechoma hederacea in heterogeneous environments, Scientific Reports, 6, 1, (2016).
Crossref
Robert J. Robbins, Leonard Krishtalka and John C. Wooley, Advances in biodiversity: metagenomics and the unveiling of biological dark matter, Standards in Genomic Sciences, 11, 1, (2016).
Crossref
Jeremiah A. Henning, David J. Weston, Dale A. Pelletier, Collin M. Timm, Sara S. Jawdy and Aimée T. Classen, Root bacterial endophytes alter plant phenotype, but not physiology, PeerJ, 4, (e2606), (2016).
Crossref
Paulo Sérgio Balbino Miguel, Marcelo Nagem Valério de Oliveira, Júlio César Delvaux, Guilherme Luiz de Jesus, Arnaldo Chaer Borges, Marcos Rogério Tótola, Júlio César Lima Neves and Maurício Dutra Costa, Diversity and distribution of the endophytic bacterial community at different stages of Eucalyptus growth, Antonie van Leeuwenhoek, 109, 6, (755), (2016).
Crossref
Kezia Goldmann, Kristina Schröter, Rodica Pena, Ingo Schöning, Marion Schrumpf, François Buscot, Andrea Polle and Tesfaye Wubet, Divergent habitat filtering of root and soil fungal communities in temperate beech forests, Scientific Reports, 6, 1, (2016).
Crossref
Murali Gopal and Alka Gupta, Microbiome Selection Could Spur Next-Generation Plant Breeding Strategies, Frontiers in Microbiology, 7, (2016).
Crossref
Tim Richter-Heitmann, Thilo Eickhorst, Stefan Knauth, Michael W. Friedrich and Hannes Schmidt, Evaluation of Strategies to Separate Root-Associated Microbial Communities: A Crucial Choice in Rhizobiome Research, Frontiers in Microbiology, 7, (2016).
Crossref
Sonia Szymańska, Tomasz Płociniczak, Zofia Piotrowska-Seget and Katarzyna Hrynkiewicz, Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L. – community structure and metabolic potential, Microbiological Research, 10.1016/j.micres.2016.05.012, 192, (37-51), (2016).
Crossref
Matthew T. Agler, Jonas Ruhe, Samuel Kroll, Constanze Morhenn, Sang-Tae Kim, Detlef Weigel, Eric M. Kemen and Matthew K. Waldor, Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation, PLOS Biology, 14, 1, (e1002352), (2016).
Crossref
Janine Haueisen and Eva H Stukenbrock, Life cycle specialization of filamentous pathogens — colonization and reproduction in plant tissues, Current Opinion in Microbiology, 32, (31), (2016).
Crossref
Yves Dessaux, Catherine Grandclément and Denis Faure, Engineering the Rhizosphere, Trends in Plant Science, 21, 3, (266), (2016).
Crossref
Catherine Grandclément, Mélanie Tannières, Solange Moréra, Yves Dessaux, Denis Faure and Miguel Camara, Quorum quenching: role in nature and applied developments, FEMS Microbiology Reviews, 40, 1, (86), (2016).
Crossref
Citlali Fonseca-García, Devin Coleman-Derr, Etzel Garrido, Axel Visel, Susannah G. Tringe and Laila P. Partida-Martínez, The Cacti Microbiome: Interplay between Habitat-Filtering and Host-Specificity, Frontiers in Microbiology, 7, (2016).
Crossref
Kelly Justin da Silva, Rafael Dutra de Armas, Cláudio Roberto F. S. Soares and Juliana Bernardi Ogliari, Communities of endophytic microorganisms in different developmental stages from a local variety as well as transgenic and conventional isogenic hybrids of maize, World Journal of Microbiology and Biotechnology, 32, 11, (2016).
Crossref
Sarah C. Watkinson, Molecular Ecology, The Fungi, 10.1016/B978-0-12-382034-1.00006-2, (189-203), (2016).
Crossref
Corinne Vacher, Arndt Hampe, Annabel J. Porté, Ursula Sauer, Stéphane Compant and Cindy E. Morris, The Phyllosphere: Microbial Jungle at the Plant–Climate Interface, Annual Review of Ecology, Evolution, and Systematics, 10.1146/annurev-ecolsys-121415-032238, 47, 1, (1-24), (2016).
Crossref
Amanda Rosier, Usha Bishnoi, Venkatachalam Lakshmanan, D. Janine Sherrier and Harsh P. Bais, A perspective on inter-kingdom signaling in plant–beneficial microbe interactions, Plant Molecular Biology, 90, 6, (537), (2016).
Crossref
Collin M. Timm, Dale A. Pelletier, Sara S. Jawdy, Lee E. Gunter, Jeremiah A. Henning, Nancy Engle, Jayde Aufrecht, Emily Gee, Intawat Nookaew, Zamin Yang, Tse-Yuan Lu, Timothy J. Tschaplinski, Mitchel J. Doktycz, Gerald A. Tuskan and David J. Weston, Two Poplar-Associated Bacterial Isolates Induce Additive Favorable Responses in a Constructed Plant-Microbiome System, Frontiers in Plant Science, 7, (2016).
Crossref
Alexander Schouten, Mechanisms Involved in Nematode Control by Endophytic Fungi, Annual Review of Phytopathology, 10.1146/annurev-phyto-080615-100114, 54, 1, (121-142), (2016).
Crossref
Yuan Qin, Irina S. Druzhinina, Xueyu Pan and Zhilin Yuan, Microbially Mediated Plant Salt Tolerance and Microbiome-based Solutions for Saline Agriculture, Biotechnology Advances, 10.1016/j.biotechadv.2016.08.005, 34, 7, (1245-1259), (2016).
Crossref
Gabriele Berg, Daria Rybakova, Martin Grube and Martina Köberl, The plant microbiome explored: implications for experimental botany, Journal of Experimental Botany, 10.1093/jxb/erv466, 67, 4, (995-1002), (2015).
Crossref
Anastasia Bragina, Christian Berg and Gabriele Berg, The core microbiome bonds the Alpine bog vegetation to a transkingdom metacommunity, Molecular Ecology, 24, 18, (4795-4807), (2015).
Wiley Online Library
Etienne Yergeau, Terrence H. Bell, Julie Champagne, Christine Maynard, Stacie Tardif, Julien Tremblay and Charles W. Greer, Transplanting Soil Microbiomes Leads to Lasting Effects on Willow Growth, but not on the Rhizosphere Microbiome, Frontiers in Microbiology, 6, (2015).
Crossref
Patrick Brown and Sebastian Saa, Biostimulants in agriculture, Frontiers in Plant Science, 6, (2015).
Crossref
Aimée T. Classen, Maja K. Sundqvist, Jeremiah A. Henning, Gregory S. Newman, Jessica A. M. Moore, Melissa A. Cregger, Leigh C. Moorhead and Courtney M. Patterson, Direct and indirect effects of climate change on soil microbial and soil microbial‐plant interactions: What lies ahead?, Ecosphere, 6, 8, (1-21), (2015).
Wiley Online Library
U.G. Mueller and J.L. Sachs, Engineering Microbiomes to Improve Plant and Animal Health, Trends in Microbiology, 10.1016/j.tim.2015.07.009, 23, 10, (606-617), (2015).
Crossref
Christine Strullu‐Derrien, Marc‐André Selosse, Paul Kenrick and Francis M. Martin, The origin and evolution of mycorrhizal symbioses: from palaeomycology to phylogenomics, New Phytologist, , (2018).
Wiley Online Library
J. Marty Kranabetter, Rachael Harman‐Denhoed and Barbara J. Hawkins, Saprotrophic and ectomycorrhizal fungal sporocarp stoichiometry (C : N : P) across temperate rainforests as evidence of shared nutrient constraints among symbionts, New Phytologist, , (2018).
Wiley Online Library
Lukas Wille, Monika M. Messmer, Bruno Studer and Pierre Hohmann, Insights to plant–microbe interactions provide opportunities to improve resistance breeding against root diseases in grain legumes, Plant, Cell & Environment, , (2018).
Wiley Online Library
Raheem Shahzad, Abdul L. Khan, Saqib Bilal, Sajjad Asaf and In-Jung Lee, What Is There in Seeds? Vertically Transmitted Endophytic Resources for Sustainable Improvement in Plant Growth, Frontiers in Plant Science, 10.3389/fpls.2018.00024, 9, (2018).
Crossref
Ariadna Sánchez-López, Isabel Pintelon, Vincent Stevens, Valeria Imperato, Jean-Pierre Timmermans, Carmen González-Chávez, Rogelio Carrillo-González, Jonathan Van Hamme, Jaco Vangronsveld and Sofie Thijs, Seed Endophyte Microbiome of Crotalaria pumila Unpeeled: Identification of Plant-Beneficial Methylobacteria, International Journal of Molecular Sciences, 10.3390/ijms19010291, 19, 1, (291), (2018).
Crossref
Pragya Adhikari, Yeonyee Oh and Dilip Panthee, Current Status of Early Blight Resistance in Tomato: An Update, International Journal of Molecular Sciences, 10.3390/ijms18102019, 18, 10, (2019), (2017).
Crossref
Francesco Dovana, Marco Mucciarelli, Maurizio Mascarello, Anna Fusconi and Massimo Labra, In Vitro Morphogenesis of Arabidopsis to Search for Novel Endophytic Fungi Modulating Plant Growth, PLOS ONE, 10.1371/journal.pone.0143353, 10, 12, (e0143353), (2015).
Crossref
Amandine Lê Van, Achim Quaiser, Marie Duhamel, Sophie Michon-Coudouel, Alexis Dufresne and Philippe Vandenkoornhuyse, Ecophylogeny of the endospheric root fungal microbiome of co-occurring Agrostis stolonifera , PeerJ, 10.7717/peerj.3454, 5, (e3454), (2017).
Crossref
Sharon L. Doty, Andrew W. Sher, Neil D. Fleck, Mahsa Khorasani, Roger E. Bumgarner, Zareen Khan, Andrew W. K. Ko, Soo-Hyung Kim, Thomas H. DeLuca and Benedicte Riber Albrectsen, Variable Nitrogen Fixation in Wild Populus, PLOS ONE, 10.1371/journal.pone.0155979, 11, 5, (e0155979), (2016).
Crossref
Ying Zhao, Zhixiao Gao, Binnian Tian, Kai Bi, Tao Chen, Huiquan Liu, Jiatao Xie, Jiasen Cheng, Yanping Fu, Daohong Jiang and Seon-Woo Lee, Endosphere microbiome comparison between symptomatic and asymptomatic roots of Brassica napus infected with Plasmodiophora brassicae, PLOS ONE, 10.1371/journal.pone.0185907, 12, 10, (e0185907), (2017).
Crossref
Jennifer E. Schmidt, Timothy M. Bowles and Amélie C. M. Gaudin, Using Ancient Traits to Convert Soil Health into Crop Yield: Impact of Selection on Maize Root and Rhizosphere Function, Frontiers in Plant Science, 10.3389/fpls.2016.00373, 7, (2016).
Crossref
Posy E. Busby, Chinmay Soman, Maggie R. Wagner, Maren L. Friesen, James Kremer, Alison Bennett, Mustafa Morsy, Jonathan A. Eisen, Jan E. Leach and Jeffery L. Dangl, Research priorities for harnessing plant microbiomes in sustainable agriculture, PLOS Biology, 10.1371/journal.pbio.2001793, 15, 3, (e2001793), (2017).
Crossref
Fanny Rohrbacher and Marc St-Arnaud, Root Exudation: The Ecological Driver of Hydrocarbon Rhizoremediation, Agronomy, 10.3390/agronomy6010019, 6, 1, (19), (2016).
Crossref
Elodie Blanchet, Soizic Prado, Didier Stien, Jocivânia Oliveira da Silva, Yoan Ferandin, Nicole Batailler, Laurent Intertaglia, Alexandre Escargueil and Raphaël Lami, Quorum Sensing and Quorum Quenching in the Mediterranean Seagrass Posidonia oceanica Microbiota, Frontiers in Marine Science, 10.3389/fmars.2017.00218, 4, (2017).
Crossref
Salvatore Alaimo, Gioacchino P. Marceca, Rosalba Giugno, Alfredo Ferro and Alfredo Pulvirenti, Current Knowledge and Computational Techniques for Grapevine Meta-Omics Analysis, Frontiers in Plant Science, 10.3389/fpls.2017.02241, 8, (2018).
Crossref
Manuel González-Guerrero, Viviana Escudero, Ángela Saéz and Manuel Tejada-Jiménez, Transition Metal Transport in Plants and Associated Endosymbionts: Arbuscular Mycorrhizal Fungi and Rhizobia, Frontiers in Plant Science, 10.3389/fpls.2016.01088, 7, (2016).
Crossref
Kelly Ugarelli, Seemanti Chakrabarti, Peeter Laas and Ulrich Stingl, The Seagrass Holobiont and Its Microbiome, Microorganisms, 10.3390/microorganisms5040081, 5, 4, (81), (2017).
Crossref
Martina Cerri, Rumakanta Sapkota, Andrea Coppi, Valentina Ferri, Bruno Foggi, Daniela Gigante, Lorenzo Lastrucci, Roberta Selvaggi, Roberto Venanzoni, Mogens Nicolaisen, Francesco Ferranti and Lara Reale, Oomycete Communities Associated with Reed Die-Back Syndrome, Frontiers in Plant Science, 10.3389/fpls.2017.01550, 8, (2017).
Crossref
Nathan Vannier, Cendrine Mony, Anne-Kristel Bittebière and Philippe Vandenkoornhuyse, Epigenetic Mechanisms and Microbiota as a Toolbox for Plant Phenotypic Adjustment to Environment, Frontiers in Plant Science, 10.3389/fpls.2015.01159, 6, (2015).
Crossref

Volume206, Issue4

Special Issue: Featured papers on ‘Eucalyptus genome’

June 2015

Pages 1196-1206

New Phytologist

The importance of the microbiome of the plant holobiont