Unraveling root developmental programs initiated by beneficial Pseudomonas spp. bacteria.
TL;DR: The ability of selected Pseudomonas spp.
Abstract: Plant roots are colonized by an immense number of microbes, referred to as the root microbiome. Selected strains of beneficial soil-borne bacteria can protect against abiotic stress and prime the plant immune system against a broad range of pathogens. Pseudomonas spp. rhizobacteria represent one of the most abundant genera of the root microbiome. Here, by employing a germ-free experimental system, we demonstrate the ability of selected Pseudomonas spp. strains to promote plant growth and drive developmental plasticity in the roots of Arabidopsis (Arabidopsis thaliana) by inhibiting primary root elongation and promoting lateral root and root hair formation. By studying cell type-specific developmental markers and employing genetic and pharmacological approaches, we demonstrate the crucial role of auxin signaling and transport in rhizobacteria-stimulated changes in the root system architecture of Arabidopsis. We further show that Pseudomonas spp.-elicited alterations in root morphology and rhizobacteria-mediated systemic immunity are mediated by distinct signaling pathways. This study sheds new light on the ability of soil-borne beneficial bacteria to interfere with postembryonic root developmental programs.
Citations
More filters
TL;DR: This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in the understanding of ISR signaling and systemic defense priming.
Abstract: Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth–promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
1,856 citations
TL;DR: Novel knowledge and gaps on PGPR modes of action and signals are addressed, recent progress on the links between plant morphological and physiological effects induced by PGPR are highlighted, and the importance of taking into account the size, diversity, and gene expression patterns of PGPR assemblages in the rhizosphere to better understand their impact on plant growth and functioning is shown.
Abstract: The rhizosphere supports the development and activity of a huge and diversified microbial community, including microorganisms capable to promote plant growth. Among the latter, plant growth-promoting rhizobacteria (PGPR) colonize roots of monocots and dicots, and enhance plant growth by direct and indirect mechanisms. Modification of root system architecture by PGPR implicates the production of phytohormones and other signals that lead, mostly, to enhanced lateral root branching and development of root hairs. PGPR also modify root functioning, improve plant nutrition and influence the physiology of the whole plant. Recent results provided first clues as to how PGPR signals could trigger these plant responses. Whether local and/or systemic, the plant molecular pathways involved remain often unknown. From an ecological point of view, it emerged that PGPR form coherent functional groups, whose rhizosphere ecology is influenced by a myriad of abiotic and biotic factors in natural and agricultural soils, and these factors can in turn modulate PGPR effects on roots. In this paper, we address novel knowledge and gaps on PGPR modes of action and signals, and highlight recent progress on the links between plant morphological and physiological effects induced by PGPR. We also show the importance of taking into account the size, diversity, and gene expression patterns of PGPR assemblages in the rhizosphere to better understand their impact on plant growth and functioning. Integrating mechanistic and ecological knowledge on PGPR populations in soil will be a prerequisite to develop novel management strategies for sustainable agriculture.
1,028 citations
Cites background or result from "Unraveling root developmental progr..."
...Interestingly, a similar observation was made when Arabidopsis plantlets were inoculated with the PGPR Bacillus subtilis GB03 (Zhang et al., 2007), which emits volatile organic compounds (VOCs), or with Pseudomonas fluorescens WCS417 (Zamioudis et al., 2013)....
[...]
...However, minor effects on RSA were observed when plants were inoculated with an acdS bacterial mutant, or when plants affected in their ethylene signaling pathway were inoculated with wild-type PGPR (Contesto et al., 2008; Galland et al., 2012; Zamioudis et al., 2013)....
[...]
...One of the earliest transcriptomic study performed with Pseudomonas fluorescens WCS417r indicated that bacteria elicited a substantial change in the expression of 97 genes in roots whereas none of the approximately 8,000 genes tested showed a consistent change in expression in the leaves (Verhagen et al., 2004)....
[...]
...Coopération Internationale en Recherche Agronomique pour le Développement/SupAgro/Institut National de la Recherche Agronomique, Montpellier, France 5 Institut National de la Recherche Agronomique, UMR 1347, Agroécologie, Interactions Plantes-Microorganismes, Dijon, France...
[...]
TL;DR: This work highlights major recent findings in plant microbiota research using comparative community profiling and omics analyses, and discusses these approaches in light of community establishment and beneficial traits like nutrient acquisition and plant health.
Abstract: Plants do not grow as axenic organisms in nature, but host a diverse community of microorganisms, termed the plant microbiota. There is an increasing awareness that the plant microbiota plays a role in plant growth and can provide protection from invading pathogens. Apart from intense research on crop plants, Arabidopsis is emerging as a valuable model system to investigate the drivers shaping stable bacterial communities on leaves and roots and as a tool to decipher the intricate relationship among the host and its colonizing microorganisms. Gnotobiotic experimental systems help establish causal relationships between plant and microbiota genotypes and phenotypes and test hypotheses on biotic and abiotic perturbations in a systematic way. We highlight major recent findings in plant microbiota research using comparative community profiling and omics analyses, and discuss these approaches in light of community establishment and beneficial traits like nutrient acquisition and plant health.
494 citations
TL;DR: This study demonstrates that Arabidopsis thaliana specifically promotes three bacterial species in the rhizosphere upon foliar defense activation by the downy mildew pathogen Hyaloperonospora arabidopsidis, and indicates that plants can adjust their root microbiome upon pathogen infection and specifically recruit a group of disease resistance-inducing and growth-promoting beneficial microbes.
Abstract: Disease suppressive soils typically develop after a disease outbreak due to the subsequent assembly of protective microbiota in the rhizosphere. The role of the plant immune system in the assemblage of a protective rhizosphere microbiome is largely unknown. In this study, we demonstrate that Arabidopsis thaliana specifically promotes three bacterial species in the rhizosphere upon foliar defense activation by the downy mildew pathogen Hyaloperonospora arabidopsidis. The promoted bacteria were isolated and found to interact synergistically in biofilm formation in vitro. Although separately these bacteria did not affect the plant significantly, together they induced systemic resistance against downy mildew and promoted growth of the plant. Moreover, we show that the soil-mediated legacy of a primary population of downy mildew infected plants confers enhanced protection against this pathogen in a second population of plants growing in the same soil. Together our results indicate that plants can adjust their root microbiome upon pathogen infection and specifically recruit a group of disease resistance-inducing and growth-promoting beneficial microbes, therewith potentially maximizing the chance of survival of their offspring that will grow in the same soil.
478 citations
TL;DR: It is shown that wild accessions of Arabidopsis thaliana differ in their ability to associate with the root-associated bacterium Pseudomonas fluorescens, with consequences for plant fitness, and suggested that small host-mediated changes in a microbiome can have large effects on host health.
Abstract: Host-associated microbiomes influence host health. However, it is unclear whether genotypic variations in host organisms influence the microbiome in ways that have adaptive consequences for the host. Here, we show that wild accessions of Arabidopsis thaliana differ in their ability to associate with the root-associated bacterium Pseudomonas fluorescens, with consequences for plant fitness. In a screen of 196 naturally occurring Arabidopsis accessions we identified lines that actively suppress Pseudomonas growth under gnotobiotic conditions. We planted accessions that support disparate levels of fluorescent Pseudomonads in natural soils; 16S ribosomal RNA sequencing revealed that accession-specific differences in the microbial communities were largely limited to a subset of Pseudomonadaceae species. These accession-specific differences in Pseudomonas growth resulted in enhanced or impaired fitness that depended on the host's ability to support Pseudomonas growth, the specific Pseudomonas strains present in the soil and the nature of the stress. We suggest that small host-mediated changes in a microbiome can have large effects on host health.
320 citations
References
More filters
TL;DR: This review restricts itself to bacteria that are derived from and exert this effect on the root and generally designated as PGPR (plant-growth-promoting rhizobacteria), which can be direct or indirect in their effects on plant growth.
Abstract: Several microbes promote plant growth, and many microbial products that stimulate plant growth have been marketed. In this review we restrict ourselves to bacteria that are derived from and exert this effect on the root. Such bacteria are generally designated as PGPR (plant-growth-promoting rhizobacteria). The beneficial effects of these rhizobacteria on plant growth can be direct or indirect. This review begins with describing the conditions under which bacteria live in the rhizosphere. To exert their beneficial effects, bacteria usually must colonize the root surface efficiently. Therefore, bacterial traits required for root colonization are subsequently described. Finally, several mechanisms by which microbes can act beneficially on plant growth are described. Examples of direct plant growth promotion that are discussed include (a) biofertilization, (b) stimulation of root growth, (c) rhizoremediation, and (d) plant stress control. Mechanisms of biological control by which rhizobacteria can promote plant growth indirectly, i.e., by reducing the level of disease, include antibiosis, induction of systemic resistance, and competition for nutrients and niches.
3,761 citations
"Unraveling root developmental progr..." refers background in this paper
...…fungi (PGPF), have long been demonstrated to promote plant growth, improve host nutrition, and protect plants from various forms of abiotic stress and soil-borne diseases (Ryu et al., 2003; Lugtenberg and Kamilova, 2009; Yang et al., 2009; Blom et al., 2011; Schwachtje et al., 2011)....
[...]
TL;DR: Recent advances in elucidating the role of root exudates in interactions between plant roots and other plants, microbes, and nematodes present in the rhizosphere are described.
Abstract: The rhizosphere encompasses the millimeters of soil surrounding a plant root where complex biological and ecological processes occur. This review describes recent advances in elucidating the role of root exudates in interactions between plant roots and other plants, microbes, and nematodes present in the rhizosphere. Evidence indicating that root exudates may take part in the signaling events that initiate the execution of these interactions is also presented. Various positive and negative plant-plant and plant-microbe interactions are highlighted and described from the molecular to the ecosystem scale. Furthermore, methodologies to address these interactions under laboratory conditions are presented.
3,674 citations
"Unraveling root developmental progr..." refers background in this paper
...…mediated by root exudates, such as communication with symbiotic microorganisms (via secretion of semiochemicals) and alterations in the chemical and physical properties of the soil (via secretion of organic and inorganic substances) justify such an energy investment (Bais et al., 2004, 2006)....
[...]
...Importantly, most of the root exudation is considered to occur in the elongation zone of newly formed roots (Bais et al., 2006)....
[...]
...The composition of microbial communities in the rhizosphere significantly differs from that in the bulk soil and is highly dependent on low- and high-Mr compounds secreted from the roots, collectively referred to as root exudates (Bais et al., 2006)....
[...]
TL;DR: In this article, the authors discuss evidence that upon pathogen or insect attack, plants are able to recruit protective microorganisms, and enhance microbial activity to suppress pathogens in the rhizosphere.
3,228 citations
TL;DR: Evidence is emerging that beneficial root-inhabiting microbes also hijack the hormone-regulated immune signaling network to establish a prolonged mutualistic association, highlighting the central role of plant hormones in the regulation of plant growth and survival.
Abstract: Plant hormones have pivotal roles in the regulation of plant growth, development, and reproduction. Additionally, they emerged as cellular signal molecules with key functions in the regulation of immune responses to microbial pathogens, insect herbivores, and beneficial microbes. Their signaling pathways are interconnected in a complex network, which provides plants with an enormous regulatory potential to rapidly adapt to their biotic environment and to utilize their limited resources for growth and survival in a cost-efficient manner. Plants activate their immune system to counteract attack by pathogens or herbivorous insects. Intriguingly, successful plant enemies evolved ingenious mechanisms to rewire the plant’s hormone signaling circuitry to suppress or evade host immunity. Evidence is emerging that beneficial root-inhabiting microbes also hijack the hormone-regulated immune signaling network to establish a prolonged mutualistic association, highlighting the central role of plant hormones in the regulation of plant growth and survival.
2,132 citations
"Unraveling root developmental progr..." refers background in this paper
...The crucial role of ET and JA signaling in systemic immune responses that are triggered by beneficial Pseudomonas spp. bacteria, including WCS417, is well documented (Van Wees et al., 2008; Van der Ent et al., 2009; Pieterse et al., 2012)....
[...]
...The essential role of the ET and JA signaling pathways in systemic immune responses activated upon root colonization by soil-borne beneficial microbes is well documented (Van Wees et al., 2008; Van der Ent et al., 2009; Pieterse et al., 2012)....
[...]
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
"Unraveling root developmental progr..." refers background in this paper
...Exciting new discoveries combining metagenomics, PhyloChip analysis, and quantitative plant genetics have revealed a core microbiome within the roots and rhizosphere of plants (Mendes et al., 2011; Brown et al., 2012; Bulgarelli et al., 2012; Lundberg et al., 2012; Sessitsch et al., 2012)....
[...]
...Soil-borne Pseudomonas spp. represent one of the most abundant genera of the root microbiome (Mendes et al., 2011; Brown et al., 2012; Bulgarelli et al., 2012; Lundberg et al., 2012; Sessitsch et al., 2012)....
[...]