How membranes shape plant symbioses: signaling and transport in nodulation and arbuscular mycorrhiza

Abstract

As sessile organisms that cannot evade adverse environmental conditions, plants have evolved various adaptive strategies to cope with environmental stresses. One of the most successful adaptations is the formation of symbiotic associations with beneficial microbes. In these mutualistic interactions the partners exchange essential nutrients and improve their resistance to biotic and abiotic stresses. In arbuscular mycorrhiza (AM) and in root nodule symbiosis (RNS), AM fungi and rhizobia, respectively, penetrate roots and accommodate within the cells of the plant host. In these endosymbiotic associations, both partners keep their plasma membranes intact and use them to control the bidirectional exchange of signaling molecules and nutrients. Intracellular accommodation requires the exchange of symbiotic signals and the reprogramming of both interacting partners. This involves fundamental changes at the level of gene expression and of the cytoskeleton, as well as of organelles such as plastids, endoplasmic reticulum (ER), and the central vacuole. Symbiotic cells are highly compartmentalized and have a complex membrane system specialized for the diverse functions in molecular communication and nutrient exchange. Here, we discuss the roles of the different cellular membrane systems and their symbiosis-related proteins in AM and RNS, and we review recent progress in the analysis of membrane proteins involved in endosymbiosis.

Keywords: LysM receptor; SYMRK; VAPYRIN; arbuscule; mycorrhiza; rhizobium; root nodules; symbiosis.

Figure 1

Transmission electron micrograph of a cortical cell of P. hybrida colonized by G. intraradices (Rhizophagus irregularis). For clarity, cellular components are pseudocolored as follows: green, fragmented plant vacuole; blue, plant mitochondria and plastids; light brown, fungal vacuoles; red, symbiotic interface. Note the very close contact of the periarbuscular membrane (PAM) with fungal hyphae (white arrows), and the proximity of the tonoplast with the PAM (black arrows).

Figure 2

Schematic representation of a cortex cell with an arbuscule. The arbuscule takes most of the space that is normally occupied by the central vacuole. Cellular compartments are colored in light green (plant vacuole), dark green (plant plastids), blue (plant mitochondria), yellow (plant cytoplasm), gray (nucleus), red (symbiotic interface), purple (trunc portion of the symbiotic interface), and brown (plant cell wall). The cellular constituents of the host are marked with letters as follows: c, cytoplasm; m, mitochondria; n, nucleus; p, plastids; v, vacuole. The fungal arbuscule is marked as well (a).

Figure 3

Schematic representation of a plant cell with the major components involved in symbiotic signaling and defense signaling. The central vacuole has been omitted for clarity. Solid arrows indicate transport fluxes whereas dashed arrows represent signaling pathways. Receptor complexes involving LysM proteins originate from different plant species. Perception of bacterial peptidoglycan (PGN) is represented by CERK1, LYM1, and LYM3 of Arabidopsis. Chitin perception is represented by rice proteins CERK1 and CEBiP. The nod factor receptors (NFR1 and NFR5) are from L. japonicus, whereas the elusive nature of the myc factor receptors (MFR1 and MFR2) is shown with question marks. The common SYM pathway is represented by SYMRK, NENA, NUP85, NUP133, CASTOR, POLLUX, CCAMK, and CYCLOPS from L. japonicus. The remaining components (MCA8, SIP2, FLOT4, PUB1, SYMREM1, SINA4, and HMGR1) were described in M. truncatula or L. japonicus, except for PDR1 that was discovered in petunia. See Table A1 and the main text for more information on the respective genes and their function in symbiosis.