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Arbuscular mycorrhiza: the mother of plant root endosymbioses

Key Points

  • The arbuscular mycorrhiza (AM) symbiosis is formed by a monophyletic group of fungi from the phylum Glomeromycota and the roots of 70–90% of land plant species.

  • AM fungi are considered to be 'living fossils' and 'ancient asexuals', because structurally identical fungi were detected in association with the oldest land plant fossils and sexual stages or mechanisms are unknown.

  • A class of terpenoids, strigolactones, has recently been identified that functions as signalling compounds in symbiosis and as endogenous plant hormones. The same compounds have been known for decades to trigger seed germination of parasitic plants, such as Striga.

  • AM fungi induce a signal transduction process in root cells that overlaps with the root-nodule symbiosis and involves the induction and decoding of calcium signatures. Seven plant genes have been cloned that are required for these signalling processes in AM and root-nodule symbiosis.

  • Plant cells respond to fungal signals by forming a tunnel-like structure in anticipation and preparation for penetration by fungal hyphae. The underlying cellular developmental programme was recruited during the evolution of the root-nodule symbiosis with rhizobia and species of Frankia

  • Long-distance transport through the coenocytic mycelium uses cargo packages for carbon, phosphate and nitrogen transport that can be actively moved by the cytoplasm and includes lipid droplets, glycogen and polyphosphate granules (probably in a complex with arginine and trace metals).

Abstract

Arbuscular mycorrhiza (AM), a symbiosis between plants and members of an ancient phylum of fungi, the Glomeromycota, improves the supply of water and nutrients, such as phosphate and nitrogen, to the host plant. In return, up to 20% of plant-fixed carbon is transferred to the fungus. Nutrient transport occurs through symbiotic structures inside plant root cells known as arbuscules. AM development is accompanied by an exchange of signalling molecules between the symbionts. A novel class of plant hormones known as strigolactones are exuded by the plant roots. On the one hand, strigolactones stimulate fungal metabolism and branching. On the other hand, they also trigger seed germination of parasitic plants. Fungi release signalling molecules, in the form of 'Myc factors' that trigger symbiotic root responses. Plant genes required for AM development have been characterized. During evolution, the genetic programme for AM has been recruited for other plant root symbioses: functional adaptation of a plant receptor kinase that is essential for AM symbiosis paved the way for nitrogen-fixing bacteria to form intracellular symbioses with plant cells.

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Figure 1: Arbuscular mycorrhiza (AM) fungi form an independent phylum, the Glomeromycota.
Figure 2: The arbuscule.
Figure 3: Different hyphal growth and branching strategies in arbuscular mycorrhiza (AM) fungi.
Figure 4: Steps in arbuscular mycorrhiza (AM) development.
Figure 5: Comparison of intracellular accommodation structures in bacterial and fungal root endosymbioses.
Figure 6: Common symbiosis signalling components for arbuscular mycorrhiza (AM) and root-nodule symbiosis.
Figure 7: Metabolic fluxes and long-distance transport in arbuscular mycorrhiza (AM).

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Acknowledgements

I thank A. Schüßler for helpful discussions and for adapting Fig. 1, and K. Haage for compiling Table 1. I apologize to all those colleagues whose work was not cited owing to space restrictions.

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DATABASES

Entrez Genome Project

Lotus japonicus

Medicago truncatula

Mesorhizobium loti

Sinorhizobium meliloti

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Glossary

Aseptate

Not containing septae.

Coenocytic

Multiple nuclei within the same cell.

Anastomosis

A hyphal fusion with a cytoplasmic connection.

Obligate biotroph

An organism that is unable to complete a reproductive cycle in the absence of a living host.

Mycoheterotrophic

Obtains carbon sources from a fungal symbiont.

Nod factors

The bacterial symbionts of legumes (rhizobia) produce signalling molecules named Nod factors. They consist of an N-acetylglucosamine backbone that carries various strain-specific decorations including a lipid side chain.

Calcium spiking

A sharp periodic increase in calcium concentration around the nucleus of symbiotically stimulated root cells.

Appressorium

A flattened, hyphal organ that facilitates the penetration of cells or tissues of other organisms.

Microfilament

Strong, but flexible, linear polymer of actin subunits and component of the cytoskeleton.

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Parniske, M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6, 763–775 (2008). https://doi.org/10.1038/nrmicro1987

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