Functional Importance of the Plant Endophytic Microbiome: Implications for Agriculture, Forestry, and Bioenergy
01 Jan 2017-pp 1-5
TL;DR: The microbiome is so integral to plant survival that the microorganisms within plants can explain as much or more of the phenotypic variation as the plant genotype, with the microbiome playing a fundamental role in the adaptation of the plant to environmental challenges.
Abstract: Just as the human microbiome is important for our health [1], so too the plant microbiome is necessary for plant health, but perhaps more so. Since plants cannot move, they face more challenges in acquiring sufficient nutrients from a given site, defending against herbivores and pathogens, and tolerating abiotic stresses including drought, salinity, and pollutants. The plant microbiome may help plants overcome these challenges. Since genetic adaptation is relatively slow in plants, there is a distinct advantage to acquiring an effective microbiome able to more rapidly adapt to a changing environment. Although rhizospheric microorganisms have been extensively studied for decades, the more intimate associations of plants with endophytes, the microorganisms living fully within plants, have been only recently studied. It is now clear, though, that the plant microbiome can have profound impacts on plant growth and health. Comprising an ecosystem within plants, endophytes are involved in nutrient acquisition and cycling, interacting with each other in complex ways. The specific members of the microbiome can vary depending on the environment, plant genotype, and abiotic or biotic stresses [2–6]. The microbiome is so integral to plant survival that the microorganisms within plants can explain as much or more of the phenotypic variation as the plant genotype [7]. In plant biology research, an individual plant should thus be viewed as a whole, the plant along with intimately associated microbiota (a “holobiont”), with the microbiome playing a fundamental role in the adaptation of the plant to environmental challenges [8–10].
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25 Nov 2017
TL;DR: This review summarizes currently available knowledge about endophytic colonization by bacteria in various plant species, and specifically discusses the colonization of maize plants by Populus endophytes.
Abstract: The plant endosphere contains a diverse group of microbial communities. There is general consensus that these microbial communities make significant contributions to plant health. Both recently adopted genomic approaches and classical microbiology techniques continue to develop the science of plant-microbe interactions. Endophytes are microbial symbionts residing within the plant for the majority of their life cycle without any detrimental impact to the host plant. The use of these natural symbionts offers an opportunity to maximize crop productivity while reducing the environmental impacts of agriculture. Endophytes promote plant growth through nitrogen fixation, phytohormone production, nutrient acquisition, and by conferring tolerance to abiotic and biotic stresses. Colonization by endophytes is crucial for providing these benefits to the host plant. Endophytic colonization refers to the entry, growth and multiplication of endophyte populations within the host plant. Lately, plant microbiome research has gained considerable attention but the mechanism allowing plants to recruit endophytes is largely unknown. This review summarizes currently available knowledge about endophytic colonization by bacteria in various plant species, and specifically discusses the colonization of maize plants by Populus endophytes.
377 citations
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TL;DR: Results suggest that endophytic diazotrophic bacteria harboured by hybrid spruce trees can sustain their growth on nitrogen-limited soils via biological nitrogen fixation, indicating their wide-range ecological applications in improving the N-supply of forest stands in this region and beyond.
Abstract: The West Chilcotin region in British Columbia, Canada is located in the Sub-Boreal zone characterized by dry and weakly developed soils lacking essential plant nutrients, particularly nitrogen. Yet, hybrid white spruce (Picea glauca x engelmannii) trees thrive on such nitrogen-limited soils, raising a crucial question regarding their nitrogen sources. The presence of endophytic diazotrophic bacteria (nitrogen-fixing bacteria living inside the plant tissues) was reported in these spruce trees, previously. But, can these bacteria actually sustain tree growth on nitrogen-limited soils of this region? To answer this question, we tested six endophytic diazotrophic bacteria under nitrogen-poor conditions in a year-long greenhouse trial with their original host (i.e. hybrid white spruce). In a different year-long trial, we also tested these bacteria with another host native to the West Chilcotin region (i.e. lodgepole pine) to examine their interaction with a foreign host. Endophytic colonization, seedling growth promotion and the amount of nitrogen fixed in planta by each bacterium were examined. We found that each bacterium colonized one or more tissues of the spruce and pine seedlings (102–107 colonies per gram fresh tissue) and fixed significant (P 50% of the nitrogen requirements of pine and spruce seedlings via nitrogen fixation, and enhanced seedling length and biomass by nearly 1.5-fold and 5-fold, respectively. Therefore, our results suggest that endophytic diazotrophic bacteria harboured by hybrid spruce trees can sustain their growth on nitrogen-limited soils via biological nitrogen fixation. These bacteria can also provide similar benefits to a foreign host - lodgepole pine, indicating their wide-range ecological applications in improving the N-supply of forest stands in this region and beyond. In particular, C. sordidicola LS-S2r holds strong potential to be possibly used as a biofertilizer in boreal forest stands, as an economical and eco-friendly alternative to chemical fertilizers.
37 citations
03 Nov 2018
TL;DR: Diversity exists in the endophytic microbial interactions and their possible mechanisms including habitat-adapted symbiosis involved in promoting growth, development, and tolerance to abiotic stresses in crop plants.
Abstract: Plant-associated microbial interactions involve the great array of root/shoot dynamic environments known as the rhizosphere (in soil) and phyllosphere (plant aerial parts). Here, microbial communities are under multi-prolonged interactions within themselves as well as with plants to improve plant adaptation and tolerance to environmental constraints. Among the different kinds of plant-associated microbial interactions, beneficial “endophytic interactions” occur in rhizosphere as well as in phyllosphere habitats, wherein diverse group of bacterial and fungal communities colonizes plant inter- and intracellular spaces. Structural composition of endophytic microbial communities with respect to few bacterial groups and fungal species has been characterized. Identity of their large diversity and ecological functions of large majority of microbial species in the plant endophytic microbiome are remaining unknown. A variety of distinct abiotic stresses in the soil environment is known to occur singly or in combinations, causing both general and specific detrimental effects on plant growth and development. In addition to the direct negative impact on growth of the plants, abiotic stresses known to affect the rhizosphere soil as well as plant-associated beneficial microbial interactions (symbiotic and endophytic interactions) and thereby crop yield in agriculture. The so-called term induced systemic tolerance (IST) has been put forward to explain different possible mechanisms exerted by the rhizo-/endophytic bacterial and fungal- or microbe-mediated systemic tolerance against abiotic stresses in plants. Hence, there is a necessity for redefining as well as rethinking of modern agronomic practices with our current perceptive of the significance of plant-associated beneficial microbial communities (rhizosphere, symbiotic, and endophytic interactions) for plant productivity and health under abiotically stressed environments. In this present chapter, we converse the impact of abiotic stresses upon soil and plant-microbial beneficial interactions; diversity exists in the endophytic microbial interactions (rhizobacterial endophytes, Archaea, fungal endophytes, and beneficial viruses) and their possible mechanisms including habitat-adapted symbiosis involved in promoting growth, development, and tolerance to abiotic stresses in crop plants.
19 citations
01 Jan 2019
TL;DR: Advances in molecular technique, namely ITS sequencing, pyrosequencing, DNA barcoding, fatty acid methyl ester analysis (FAME), and MALDI-TOF led to the rapid and efficient identification of both culture dependent and independent fungi.
Abstract: Endophytes have profound impacts on plants, including beneficial effects on agriculturally important traits. Endophytic fungi inhabit in the internal living tissues of almost all known plants, without causing any negative effect on their host plant. Endophytic fungi are involved in the production of various bioactive natural products and are thus known for enhancing plant growth, increasing their fitness, and strengthening tolerances to various abiotic and biotic stresses. Traditionally, culture based identification of endophytic fungi in natural environments has been limited due to non-culturable and non-sporulating nature of most of the endophytic fungi. Advances in molecular technique, namely ITS sequencing, pyrosequencing, DNA barcoding, fatty acid methyl ester analysis (FAME), and MALDI-TOF led to the rapid and efficient identification of both culture dependent and independent fungi. In order to explore the potential of fungal endophytes, it is essential to identify the communal diversity as their composition is highly influenced by age, tissues, and genotype of host plants. The better understanding of endophytic diversity led to their exploration for important sources of bioactive natural products having enormous potential for the discovery of new molecules for drug discovery, industrial use, and agricultural applications.
19 citations
01 Jan 2019
TL;DR: This chapter discusses the roles of seed-vectored microbes in modulating seedling development and increasing fitness of plants in terms of increased biotic and abiotic stress tolerance.
Abstract: This chapter discusses the roles of seed-vectored microbes in modulating seedling development and increasing fitness of plants in terms of increased biotic and abiotic stress tolerance. Particular emphasis is placed on microbes that function in the rhizophagy cycle. These microbes have been shown to enter into root cells and stimulate root growth. In some cases microbe entry into root cells results in root growth repression. The term ‘endobiome interference’ has been applied to the phenomenon of plant growth repression due to intracellular microbes. The potential application of endobiome interference to produce bioherbicides that selectively enhance growth of target crops but inhibit competitor weeds is discussed.
17 citations
References
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TL;DR: The plant microbiota emerges as a fundamental trait that includes mutualism enabled through diverse biochemical mechanisms, as revealed by studies on plant growth- Promoting and plant health-promoting bacteria.
Abstract: Plants host distinct bacterial communities on and inside various plant organs, of which those associated with roots and the leaf surface are best characterized. The phylogenetic composition of these communities is defined by relatively few bacterial phyla, including Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria. A synthesis of available data suggests a two-step selection process by which the bacterial microbiota of roots is differentiated from the surrounding soil biome. Rhizodeposition appears to fuel an initial substrate-driven community shift in the rhizosphere, which converges with host genotype–dependent finetuning of microbiota profiles in the selection of root endophyte assemblages. Substrate-driven selection also underlies the establishment of phyllosphere communities but takes place solely at the immediate leaf surface. Both the leaf and root microbiota contain bacteria that provide indirect pathogen protection, but root microbiota members appear to serve additional host functions through the acquisition of nutrients from soil for plant growth. Thus, the plant microbiota emerges as a fundamental trait that includes mutualism enabled through diverse biochemical mechanisms, as revealed by studies on plant growth–promoting and plant health–promoting bacteria.
2,169 citations
TL;DR: The pyrosequencing of the bacterial 16S ribosomal RNA gene of more than 600 Arabidopsis thaliana plants is reported to test the hypotheses that the root rhizosphere and endophytic compartment microbiota of plants grown under controlled conditions in natural soils are sufficiently dependent on the host to remain consistent across different soil types and developmental stages.
Abstract: Sequencing of the Arabidopsis thaliana root microbiome shows that its composition is strongly influenced by location, inside or outside the root, and by soil type. The association between a land plant and the soil microbes of the root microbiome is important for the plant's well-being. A deeper understanding of these microbial communities will offer opportunities to control plant growth and susceptibility to pathogens, particularly in sustainable agricultural regimes. Two groups, working separately but developing best-practice protocols in parallel, have characterized the root microbiota of the model plant Arabidopis thaliana. Working on two continents and with five different soil types, they reach similar general conclusions. The bacterial communities in each root compartment — the rhizosphere immediately surrounding the root and the endophytic compartment within the root — are most strongly influenced by soil type, and to a lesser degree by host genotype. In natural soils, Arabidopsis plants are preferentially colonized by Actinobacteria, Proteobacteria, Bacteroidetes and Chloroflexi species. And — an important point for future work — Arabidopsis root selectivity for soil bacteria under controlled environmental conditions mimics that of plants grown in a natural environment. Land plants associate with a root microbiota distinct from the complex microbial community present in surrounding soil. The microbiota colonizing the rhizosphere (immediately surrounding the root) and the endophytic compartment (within the root) contribute to plant growth, productivity, carbon sequestration and phytoremediation1,2,3. Colonization of the root occurs despite a sophisticated plant immune system4,5, suggesting finely tuned discrimination of mutualists and commensals from pathogens. Genetic principles governing the derivation of host-specific endophyte communities from soil communities are poorly understood. Here we report the pyrosequencing of the bacterial 16S ribosomal RNA gene of more than 600 Arabidopsis thaliana plants to test the hypotheses that the root rhizosphere and endophytic compartment microbiota of plants grown under controlled conditions in natural soils are sufficiently dependent on the host to remain consistent across different soil types and developmental stages, and sufficiently dependent on host genotype to vary between inbred Arabidopsis accessions. We describe different bacterial communities in two geochemically distinct bulk soils and in rhizosphere and endophytic compartments prepared from roots grown in these soils. The communities in each compartment are strongly influenced by soil type. Endophytic compartments from both soils feature overlapping, low-complexity communities that are markedly enriched in Actinobacteria and specific families from other phyla, notably Proteobacteria. Some bacteria vary quantitatively between plants of different developmental stage and genotype. Our rigorous definition of an endophytic compartment microbiome should facilitate controlled dissection of plant–microbe interactions derived from complex soil communities.
2,097 citations
TL;DR: The individual steps of plant colonization are described and the known mechanisms responsible for rhizosphere and endophytic competence are surveyed to better predict how bacteria interact with plants and whether they are likely to establish themselves in the plant environment after field application as biofertilisers or biocontrol agents.
Abstract: In both managed and natural ecosystems, beneficial plant-associated bacteria play a key role in supporting and/or increasing plant health and growth. Plant growth-promoting bacteria (PGPB) can be applied in agricultural production or for the phytoremediation of pollutants. However, because of their capacity to confer plant beneficial effects, efficient colonization of the plant environment is of utmost importance. The majority of plant-associated bacteria derives from the soil environment. They may migrate to the rhizosphere and subsequently the rhizoplane of their hosts before they are able to show beneficial effects. Some rhizoplane colonizing bacteria can also penetrate plant roots, and some strains may move to aerial plant parts, with a decreasing bacterial density in comparison to rhizosphere or root colonizing populations. A better understanding on colonization processes has been obtained mostly by microscopic visualisation as well as by analysing the characteristics of mutants carrying disfunctional genes potentially involved in colonization. In this review we describe the individual steps of plant colonization and survey the known mechanisms responsible for rhizosphere and endophytic competence. The understanding of colonization processes is important to better predict how bacteria interact with plants and whether they are likely to establish themselves in the plant environment after field application as biofertilisers or biocontrol agents.
1,705 citations
TL;DR: Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role.
Abstract: Plants depend upon beneficial interactions between roots and microbes for nutrient availability, growth promotion, and disease suppression. High-throughput sequencing approaches have provided recent insights into root microbiomes, but our current understanding is still limited relative to animal microbiomes. Here we present a detailed characterization of the root-associated microbiomes of the crop plant rice by deep sequencing, using plants grown under controlled conditions as well as field cultivation at multiple sites. The spatial resolution of the study distinguished three root-associated compartments, the endosphere (root interior), rhizoplane (root surface), and rhizosphere (soil close to the root surface), each of which was found to harbor a distinct microbiome. Under controlled greenhouse conditions, microbiome composition varied with soil source and genotype. In field conditions, geographical location and cultivation practice, namely organic vs. conventional, were factors contributing to microbiome variation. Rice cultivation is a major source of global methane emissions, and methanogenic archaea could be detected in all spatial compartments of field-grown rice. The depth and scale of this study were used to build coabundance networks that revealed potential microbial consortia, some of which were involved in methane cycling. Dynamic changes observed during microbiome acquisition, as well as steady-state compositions of spatial compartments, support a multistep model for root microbiome assembly from soil wherein the rhizoplane plays a selective gating role. Similarities in the distribution of phyla in the root microbiomes of rice and other plants suggest that conclusions derived from this study might be generally applicable to land plants.
1,673 citations
TL;DR: It is suggested that the plant can modulate its microbiota to dynamically adjust to its environment and 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.
Abstract: 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.
1,199 citations