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Plant–microbiome interactions: from community assembly to plant health

An Author Correction to this article was published on 23 November 2020

This article has been updated

Abstract

Healthy plants host diverse but taxonomically structured communities of microorganisms, the plant microbiota, that colonize every accessible plant tissue. Plant-associated microbiomes confer fitness advantages to the plant host, including growth promotion, nutrient uptake, stress tolerance and resistance to pathogens. In this Review, we explore how plant microbiome research has unravelled the complex network of genetic, biochemical, physical and metabolic interactions among the plant, the associated microbial communities and the environment. We also discuss how those interactions shape the assembly of plant-associated microbiomes and modulate their beneficial traits, such as nutrient acquisition and plant health, in addition to highlighting knowledge gaps and future directions.

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Fig. 1: General structure of the bacterial and fungal communities from various plant-associated niches.
Fig. 2: Plant colonization and microbiome assembly.
Fig. 3: Beneficial effects of the plant-associated microbiome.

Change history

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Acknowledgements

P.T and J.E.L. were partially supported by funding from Colorado Agricultural Experiment Station; S.G.T. works at the US Department of Energy Joint Genome Institute and is supported by contract no. DE-AC02-05CH11231; B.K.S. is supported by the Australian Research Council (DP170104634). T.S. is supported by National Research Foundation of Korea (2015R1A2A1A05001885).

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P.T. researched data for the article. P.T., J.E.L., S.G.T., T.S. and B.K.S. contributed substantially to the discussion of the content. P.T., J.E.L., S.G.T., T.S. and B.K.S. wrote the article.

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Correspondence to Pankaj Trivedi.

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Glossary

Holobiont

A plant and the members of its associated microbiota considered as a single entity; this represents the ‘unit of selection’ at which plant–microbiome interactions have probably co-evolved in order to maintain host functionality and fitness over ecological and even evolutionary timescales.

Core microbiota

The group of microorganisms commonly found within a microbiota; recurrence of an association between microorganisms is used as the criterion to select the microorganisms that potentially provide critical functions within the habitat in which they are found.

Genome-wide association studies

(GWASs). A method to survey entire genomes of the genetic variants of many individuals for genetic polymorphisms, single-nucleotide polymorphisms, that are associated with a particular trait.

Multi-‘omics’

An approach (also known as integrative omics) to combine sets of different omic groups — such as the genome, proteome, transcriptome and metabolome — to study biological entities in a concerted way.

Microeukaryotes

Any microscopic eukaryotes, mainly protists, fungi, nematodes and small zooplankton.

Synthetic communities

(SynComs). Communities that comprise individually isolated microorganisms for controlled studies of microbial communities.

Rhizosphere

The region of soil in the vicinity of plant roots that is influenced by plant-derived nutrients and oxygen availability; it is not a region of definable size or shape, but instead consists of a gradient in chemical, biological and physical properties that change both radially and longitudinally along the root.

Endophytes

The microorganisms residing within plant tissues (the endosphere), such as leaves, roots or stems.

Phyllosphere

All the aboveground organs of plants, including the leaf, flower, stem and fruit.

Hub microorganisms

Microbial groups that are substantially more connected within a co-occurrence network than other groups on the basis of centrality measurements, such as degree, between-ness centrality and closeness centrality.

Keystone species

Highly connected microbial taxa that individually or in a guild show great explanatory power for network structure and functioning, irrespective of their abundance; not all hub species are keystone species, as a high number of direct correlations (a requirement for hubs) is not a requirement for keystone species.

Chemotaxis

Movement of organisms in response to a chemical stimulus in the direction of a higher concentration of beneficial substances or a lower concentration of toxins.

Plant exudates

Complex mixtures of soluble organic substances — which may contain sugars, amino acids, organic acids, enzymes and other substances — that are secreted by living plants, along with microbially modified products of these substances.

Biofilm

An assemblage of microbial cells that is irreversibly associated with a surface and is enclosed in a matrix of primarily polysaccharide material.

Carbohydrate-active enzymes

Enzymes involved in the biosynthesis, modification, binding and breakdown of carbohydrates.

Siderophores

Low-molecular-weight organic chelators with a very high and specific affinity for ferric iron, which scavenge iron from the environment and make the element available to microbial cells and/or a plant host.

Effector proteins

Proteins produced by plant-associated microorganisms that modify plant functioning in order to promote microbial colonization.

Quorum sensing

Population-density-dependent regulation of gene expression, mediated by the production of signal molecules called autoinducers.

Carotenoid

An organic pigment produced by plants, algae and several groups of bacteria and fungi.

Induced systemic resistance

(ISR). A physiological ‘state of enhanced defensive capacity’ of the entire plant against diverse pathogens and herbivores that is induced by local stimulation through beneficial microorganisms.

Phytobiome

Plants, their environment and all microorganisms and macroorganisms living in, on or around the plants.

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Trivedi, P., Leach, J.E., Tringe, S.G. et al. Plant–microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18, 607–621 (2020). https://doi.org/10.1038/s41579-020-0412-1

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