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Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants

Key Points

  • Plants establish beneficial associations with nitrogen-fixing bacteria and with arbuscular mycorrhizal fungi (AMF) to facilitate the acquisition of nutrients that are limiting to plant growth. These symbiotic associations must be newly established in each plant, and this involves the recognition of diffusible lipochitooligosaccharide (LCO) signals called nodulation factors (Nod factors) and mycorrhizal factors (Myc factors), produced by rhizobia and AMF, respectively.

  • Receptors containing oligosaccharide-binding LysM domains are involved in the recognition of LCOs from microbial symbionts. Two such receptors, Nod factor receptor 1 (NFR1) and NFR5, have been shown to bind Nod factors directly.

  • Recognition of a range of microbial oligosaccharides involves LysM-containing receptor complexes. These receptors can be involved in the promotion of symbiont infection or the restriction of pathogen colonization.

  • A common symbiosis signalling pathway is involved in the promotion of rhizobial and mycorrhizal associations. This signalling pathway uses oscillations in calcium as a secondary messenger. Despite the commonality in signalling in these symbiosis pathways, specificity must be maintained to ensure appropriate responses to each symbiont.

  • The production of symbiont-induced calcium oscillations involves a cation channel (or channels) that is most probably associated with potassium flow, a SERCA-type calcium pump and an as-yet-undefined calcium channel. Modelling suggests that these three components are sufficient for self-sustaining calcium oscillations.

  • Recognition of calcium oscillations involves calcium- and calmodulin-dependent serine/threonine protein kinase (CCaMK), which associates with and phosphorylates a transcriptional regulator. Autoactivation of this calcium-signalling complex is sufficient to promote symbiotic responses.

  • Transcription factor complexes involving a variety of GRAS domain-containing proteins are involved in regulating symbiotic gene expression. The specificity of symbiosis signalling seems to be defined by differential complexes of GRAS domain proteins, and these different complexes have specific roles in the regulation of plant gene expression associated with either rhizobia or AMF.

Abstract

Plants associate with a wide range of microorganisms, with both detrimental and beneficial outcomes. Central to plant survival is the ability to recognize invading microorganisms and either limit their intrusion, in the case of pathogens, or promote the association, in the case of symbionts. To aid in this recognition process, elaborate communication and counter-communication systems have been established that determine the degree of ingress of the microorganism into the host plant. In this Review, I describe the common signalling processes used by plants during mutualistic interactions with microorganisms as diverse as arbuscular mycorrhizal fungi and rhizobial bacteria.

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Figure 1: Rhizobial and mycorrhizal colonization.
Figure 2: Symbiotic signalling.
Figure 3: The symbiotic receptors.
Figure 4: The symbiotic machinery responsible for calcium oscillations.
Figure 5: Symbiotic signalling downstream of calcium oscillations.

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The author thanks A. Downie and J. Murray for critical reading of the manuscript.

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Glossary

Arbuscular mycorrhizal fungi

(AMF). Fungi from the phylum Glomeromycota. These fungi have the ability to associate with plant roots, leading to invasion of the root and the formation of arbuscules in root cortical cells.

Legumes

A varied group of plants that includes peas and beans. The ability to associate with nitrogen-fixing bacteria is a widespread (although not ubiquitous) feature of the family.

Rhizobial bacteria

Bacteria that can enter a nitrogen-fixing symbiosis with legumes or Parasponia spp. This ability has been acquired by a wide range of bacteria through horizontal gene transfer.

Arbuscules

Highly branched fungal hyphal networks that develop in root cells and act as the point of nutrient exchange between the mycorrhizal fungus and the host root.

Rhizosphere

The soil environment surrounding the plant root. The microbial communities within this environment are strongly influenced by the plant.

Strigolactones

Terpenoid plant hormones with a function in the suppression of shoot branching. These hormones are also released by the plant root to signal to the mycorrhizal fungus. Parasitic plants, such as Striga spp., have learnt to recognize strigolactones as a signal for the proximity of a potential plant host root.

Flavonoids

A group of polyhydroxy polyphenol plant secondary metabolites with diverse functions. Legumes release flavonoids from their roots to signal rhizobia and promote the production of nodulation factors.

Actinorhizal plants

A group of plants with the ability to associate with Frankia spp. bacteria. This association results in the production of nitrogen-fixing nodules colonized by the bacteria.

Pathogen-associated molecular pattern

(PAMP). A molecule (or part of a molecule) that is present on or in or produced by a pathogen and is recognized by the host organism as a signal of that invading pathogen.

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Oldroyd, G. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11, 252–263 (2013). https://doi.org/10.1038/nrmicro2990

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