Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport

Abstract

Summary In this review we compare the structure and function of the interfaces between symbionts in biotrophic associations. The emphasis is on biotrophic fungal parasites and on mycorrhizas, although necrotrophic parasitic associations and the Rhizobium/legume symbiosis are mentioned briefly. We take as a starting point the observations that in the parasitic associations nutrient transport is polarized towards the parasite, whereas in mutualistic associations it is bidirectional. The structure and function of the interfaces are then compared. An important common feature is that in nearly all cases the heterotrophic symbiont (whether mutualistic or parasitic) is located topologically outside the cytoplasm of the host cells, in an apoplastic compartment. This means that nutrient movements across the interface must involve transport into and out of this apoplastic region through membranes of both organisms. Basic principles of membrane transport in uninfected cells are briefly reviewed to set the scene for a discussion of transport mechanisms which may operate in parasitic and mycorrhizal symbioses. The presence and possible roles of ATPases associated with membranes at the interfaces are discussed. We conclude that cytochemical techniques (used to demonstrate the activity of these enzymes) need to he extended and complemented by biochemical and biophysical studies in order to confirm that the activity is due to transport ATPases. Nevertheless, the distribution of activity appears to he in accord with polarized transport mechanisms in some pathogens and with bidirectional transport in mycorrhizas. The absence of ATPases on many fungal membranes needs re‐examination. We emphasize that transport mechanisms between mycorrhizal symbionts cannot be viewed simply as the exchange of carbon for phosphate. Additional features include provision for transport of carbon and nitrogen as amino acids or amides and for ions such as K+ and H+ involved in the maintenance of charge balance and pH regulation, processes which also occur in parasitic associations. Interplant transport of nutrients via mycorrhizal hyphae is discussed in the context of these complexities. Some suggestions for the directions of future work are made.

Diversity and classification of mycorrhizal associations

“…This process has been described as lysis or digestion, but the latter is not appropriate since it has not been established whether the plant or fungus controls it. Mycorrhizal scientists no longer consider hyphal lysis an important means of nutrient transfer in balanced mycorrhizal associations (Smith & Smith, 1990), but lysis seems to be more important in exploitative associations. Exploitative associations have unique, highly complex interfaces that function by means that are not fully understood (Burgeff, 1959;Robertson & Robertson, 1982 ;Leake, 1994;Schmid & Oberwinkler, 1994;Rasmussen, 2002).…”

Tansley Review No. 82. Strategies of arbuscular mycorrhizal fungi when infecting host plants

“…In all the different symbiotic associations, conimon features are found in the formation and structure of the interface, and studies on one association might therefore lead to better insights into others. A key role of this compartment in recognition phenomena, cellular reactions and transport events has been noted by several authors (Brewin, 1990;Smith & Smith, 1990). One common feature is the origin of the membrane, which always derives from invagination of the plant plasma membrane.…”

“…As discussed in Smith & Smith (1990) and Smith et al (1994), the interface compartments are sites where the two-way nutrient transfer occurs. The ATPase activity revealed in the perifungal membrane might be very important in terms of nutrient transport.…”

“…Although different types of interface are created during niycorrhizal interactions depending on whether the lungus does or does not penetrate the host cell, they are always composed of the membranes of both partners, separated by an apoplastic region, as described in many recent reviews (for example Bonfante & Scannerini, 1992;Smith et al, 1994). It IS assumed that their fundamental role is to allow a two-way exchange of nutrients; the type of compounds transferred and the mechanisms of transfer nave been excellently reviewed by Smith & Smith (1990) and Smith et al (1994). Here, we shall focus on the morphological aspects of one type of interface, i-e. the specialized fungal wall-plant membrane interface, which is typical of endomycorrhizas.…”

“…By contrast, no active membraneassociated ATPases were found on the membrane surrounding haustoria in plant-pathogen interactions. The absence of an active transport system on the plant perihaustorial membrane might explain the unidirectional nutrient flux towards the fungus observed in pathogenic interactions (Smith & Smith, 1990).…”