Importance of the plant community context for the individual plant microbiota assembly

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Endophytes induced functions and phenotypic modifications

Endophytic microorganisms are involved in a variety of phenotypic changes in plants. These changes have been widely studied especially in plants of agricultural importance. Because of their sessile lifestyle plants have to cope with the environmental conditions. Abiotic conditions especially, such as light, water and others are spatially variable, so plants must cope with this heterogeneity (Hodge, 2004). There are numerous reports of fungal and bacterial symbionts conferring tolerance to a variety of stresses to host plants as well as other benefits (e.g. Friesen et al., 2011; Müller et al., 2016). The range of functions provided by roots microorganisms are reviewed in the following section.

Resources acquisition

Microorganisms living in association with plants improve the acquisition of different resources and, more especially, allow the acquisition of otherwise inaccessible ones. Leaf epiphytic cyanobacteria for example transfer atmospherically fixed nitrogen to plants that can represent 10 to 20% of the leaf nitrogen (Bentley & Carpenter, 1984). This ability to fix atmospheric nitrogen is displayed by at least six different bacterial phyla, the most common being Proteobacteria, and by several archaea lineages (Martinez-Romero, 2006; Friesen et al., 2011). Nitrogen acquisition also occurs within the tree roots in boreal forests thanks to Ectomycorrhizal fungi (Lindahl et al., 2007). In parallel, other nutrients can be more easily obtained through the help of endophytic organisms and a given organism can provide multiple resources. For instance, the arbuscular mycorrhizal fungi living in association with plants supply these plants with water, phosphorous, nitrogen, and trace elements (Smith & Read, 2008; Smith et al., 2009). In the arbuscular mycorrhizal fungi symbiosis, mineral nutrients uptake can be 5 and 25 times higher for nitrogen and phosphorus respectively, in mycorrhized as compared to non-mycorrhized roots (Van Der Heijden et al., 2003; Vogelsang et al., 2006). AM fungi acquire these resources more efficiently because hyphae can access narrower soil pores and increase the uptake of immobile resources (especially inorganic phosphate), by acquiring nutrients beyond the depletion zone of the root and stimulating the production of exudates that release immobile soil nutrients (Maiquetıáet al., 2009; Courty et al., 2010; Cairney, 2011). In addition, AM fungi are able to acquire both organic and inorganis nitrogen, which is not the case of plants (see Hodge & Storer, 2015 for a review on AM fungi nitrogen uptakes).
One example is the nitrogen in soil organic matter released by hydrolytic and oxidative enzymes produced by Ericoid mycorrhizae. This enhanced acquisition of resources not only directly affects the individual plant’s fitness but also its phenotype and competitive interactions with other plants (see section II 2.2.1 for examples; for a review see Hodge & Storer, 2015). Indeed, a phenotypic consequence of the more efficient nutrient uptake of mycorrhizae for the plant is a reduced number of fine roots together with a lower root:shoot ratio and specific root length (Smith et al. 2009). Improved resource acquisition also allows the plant to cope more efficiently with environmental constraints.

Resistance to environmental constraints

Numerous studies indicate that plant adaptation to stressful conditions may be explained by the fitness benefits conferred by mutualistic fungi (for example resources acquisition described in the section 2.1) (Stone et al., 2000; Rodriguez et al., 2004). In addition to these indirect effects of resources acquisition, fungi and bacteria also provide direct resistance to a large range of stresses through the production of certain compounds. Among the stresses alleviated by plant endophytes the main ones are salinity, extreme heat, drought and heavy metal pollutants. Salinity tolerance for example can be increased by different metabolites such as trehalose produced by bacteria like Rhizobia in nodules (Lopez et al., 2008). Such improved tolerances are not only provided by bacteria. The fungal endophyte Curvularia found on thermal soils in Yellowstone Park has been shown to increase tolerance to extreme heat (Redman et al., 2002). Fungal endophytes such as Fusarium culmorum colonizing the above- and below-ground tissues and seed coats of Leymus mollis, also confers salinity tolerance (Rodriguez et al., 2008). In addition a given microorganism can at the same increase resource acquisition and provide resistance to an abiotic stress (independently of its effect on resources acquisition). AM fungi increase stomatal conductance when they are inoculated to plants either under normal or drought conditions. This increase of stomatal conductance has been linked to greater drought tolerance of rice and tomato plants inoculated with such fungi (Lambers et al., 2008; Rodriguez et al., 2008). Following observation of the described tolerance, several microorganisms have been considered as suitable candidates for bioremediation of polluted soils. This is the case of plant growth-promoting rhizobacteria that elicite tolerance to heavy metals (Glick, 2003; Zhuang et al., 2007).

Biotic stresses

In addition to their role in the resistance against abiotic stresses plant-associated microorganisms also mediate plant resistance against biotic constraints among which the most studied are aggressions by pathogens. Indeed, endophytes are able to secrete defensive chemicals in plant tissues (Arnold et al. 2003; Clay & Schardl 2002). Different studies have identified chemicals providing defense against pathogens and produced by a myriad of microorganisms associated with plants. The range of compounds produced by symbionts consists of antimicrobials with direct effects on the pathogen or indirect effects such as a diminution of its pathogenicity. Compounds with a direct and immediate antibacterial effect include antimicrobial auxin and other phytohormones (Morshed et al., 2005). Compounds with indirect effects are for example nonanoic acid produced by the fungus Trichoderma harzianum that inhibits mycelial growth and spore germination of two pathogens in the tissues of Theobroma cacao (Aneja et al. 2005). Alternatively, microorganisms can also produce compounds such as AHL -degrading lactonases that are able to alter the communication between pathogens and thus prevent the expression of virulence genes (Reading & Sperandio, 2006). In addition, different strains and species can produce different compounds and each endophyte can itself produce several compounds. Even within a species, each strain can produce multiple antibiotics as in Bacillus where these antibiotics have synergistic interactions against pathogens (Haas et al., 2000). Such protection against biotic aggressors can also be mediated by stimulation of the plant immune system. Boller & Felix (2009) highlighted mutualist-induced signaling pathways initiated by flagellin/FLS2 and EF-Tu/EFR recognition receptors, allowing plants to respond to virus, pests and pathogens. The defensive responses induced by mutualists are not always localized and given microorganisms like the fungus Trichoderma may induce both systemic and localized resistances to a variety of plant pathogens (Harman et al., 2004). Such resistances often protect against crop damage and many plant-associated microorganisms like the latter can be used for biocontrol (Harman et al., 2004). Biotic constraints are not limited to pathogens and many other aggressors or competitors can affect plants. One of the most studied biotic stresses alleviated by plant-associated microorganisms is herbivory. Mutualist-induced resistance to herbivory has been identified and described for various plant feeding herbivores. Such resistance often involves the production by the endophyte of compounds that are toxic for herbivores or thatdiminish plant palatability. For example, Tanaka et al., (2005) showed that the fungal endophyte Neotyphodium produces the secondary metabolite peramine that protects Epichloë festucae from insect herbivory. Like for abiotic stress tolerance (see above section 2.2.1) a single microorganism can produce various compounds. For instance, clavicipitaceous endophytes such as Neotyphodium induce the production of alkaloids, lolitrems, lolines, and peramines allowing grasses to defend against herbivores (Rowan, 1993; Siegel et al., 1989; Clay, 1990; Clay & Schardl 2002). Such patterns of defense against herbivores have been mostly evidenced in grasses and also comprise other endophytes limiting mammalian herbivory through the production of lysergic acid amide (White, 1987; Gentile et al., 1999; Zhang et al., 2012). Non-toxic compounds conferring antifeeding properties include for example alkaloids that reduce rabbit herbivory on plants (Panaccione et al., 2006).

Growth and reproductive strategy

As has been shown in other hosts such as insects with Wolbachia, endophytes can also alter plant growth and reproductive strategy. In clonal plants, Streitwolf-Engel et al., (1997, 2001) showed that colonization of the roots by Arbuscular Mycorrhizal Fungi could alter the growth and reproduction of clonal plants. In this experiment, the authors found that ramets (i.e. clonal units composed of roots and shoots) production by Prunella vulgaris was differentially affected by the inoculation of three AM fungi isolates (see figure 3 for clonal growth plant description). The number of ramets produced changed by a factor of up to 1.8 independently of the isolates’effects on plant biomass. AM fungi can thus alter the trade-off between growth and reproduction. In addition, microorganisms can also alter the trade-off between different compartments of plant growth. In the above-described experiment the authors also found that branching (lateral ramification) was affected by the inoculation, suggesting that foraging by the plant (i.e., the strategy for resources acquisition) was modified by Arbuscular Mycorrhizal Fungi inoculation. In another experiment conducted, Sudova (2009) showed that growth and reproductive strategy modifications induced by the AM fungi vari both with the fungi identity and the plant species. Using five co-occurring plant species with 3 AM fungal isolates the authors showed that plant growth response to inoculation varied widely from negative to positive depending on the inoculum. AM inoculation led to changes in clonal growth traits such as an increase in stolon number and length only in some plant species.
The effects of microorganisms on growth and reproductive strategy of plants appear thus to depend on the matching between plant and microorganisms identities although this idea has not been extensively tested.
As shown in this section the vast diversity of plant-associated microorganisms ensures essential functions impacting plant growth, development, survival and resistance to environmental constraints in general. However, the described studies tended to focus on describing the effects of the microbiota but not on the use of this microbiota by the plant. Considering the benefits of symbiotic associations, evolution should favorize a plant that optimizes its interactions with microbes. However, the extent to which plants might forage for microorganisms has not been investigated to date.

Plant microbiota assembly

The additive ecological functions supplied by the plant mutualists described in the previous section extend the plant’s adaptation ability (e.g., Vandenkoornhuyse et al., 2015), leading to fitness benefits for the host in highly variable environments (Conrath et al., 2006) and therefore can affect evolutionary trajectories (e.g., Brundrett, 2002). In addition, because microbial communities may produce a mixture of antipathogen molecules that are potentially synergistic (see section 2.2.2), we can predict that plant hosts will be better protected against biotic stresses in the presence of more diverse microbial communities (Friesen et al., 2011). The same idea has been proposed for resources acquisition following results showing complementarity between symbionts in the acquisition of resources (Van der Heijden et al., 1998b). Thus the composition of the plant microbiota is of major importance in determining the ecological success (the fitness) of plants. In this context, the assembly rules shaping microbiota diversity and composition have only started to be described in recent years, and the current knowledge is reviewed in the following section (see figure 4 for an overview of the factors shaping microbiota assembly).

Table of contents :

INT R ODUC T ION GE NE R AL E
General context of the thesis
I. Scientific context
II. Structure of the PhD thesis
L iterature review
1. Microbiota composition
1.1 Plants and microorganisms, an ubiquitous alliance
1.2 Plant-microorganisms symbiosis
1.3 The root microbiota: Diversity and composition
2. Endophytes induced functions and phenotypic modifications
2.1 Resources acquisition
2.2 Resistance to environmental constraints
2.2.1 A biotic stresses
2.2.2 Biotic stresses
2.3 Growth and reproductive strategy
3. Plant microbiota assembly
3.1 Microbiota recruitment
3.1.1 The soil as a microbial reservoir
3.1.2 Rhizosphere
3.1.3 Endosphere
3.2 Controls of the plant over its microbiota
3.2.1 Microorganisms recruitment through compounds secretion
3.2.2 The immune system
3.2.3 Regulation of symbiotic interactions
3.2.4 The host plant effect: genetics and biogeography
3.3 Biotic interactions
3.3.1 Microbe-microbe interactions
3.3.2 The plant community context
3.4 Microbiota transmission
3.4.1 Horizontal or pseudo-vertical transmission
3.4.2 Vertical transmission or heritability
4. The plant is a “holobiont”
5. Objectives of the thesis
C hapter I: C onsequences of mutualist-induced plasticity
I.1. Introduction
Scientific context
Objectives of the chapter
Methods
Main results
I.2 A rticle I: Epigenetic mechanisms and microbiota as a toolbox for plant phenotypic adjustment to environment
I.3 A rticle II: A M fungi patchiness and the clonal growth of Glechoma hederacea in heterogeneous environments
Chapter II: T he heritability of the plant microbiota, toward the meta-holobiont
II.1 Introduction
Scientific context
Objectives of the chapter
Methods
Main results
II.2 Article III: A microorganisms journey between plant generations
II.3 Article IV: Introduction of the metaholobiont concept for clonal plants.
Chapter III:Importance of the plant community context for the individual plant microbiota assembly
III.1 Introduction
Scientific Context
Objectives of the chapter
Methods
Main results
III.2 A rticle V: Plant-plant interactions mediated by fungi impact plant fitness
GE NE R A L DISC USSION A ND PE R SPE C T IV E S
I. Plants and microorganism: a tight association
II. Redefining the individual plant : from holobiont to meta-holobiont
III. From individuals to community
IV. Microbiota assembly and agricultural practices
Bibliography

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