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

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. CONTENTS Summary 1 I. Introduction 2 II. The availability of nutrients to the symbionts 3 III. Structure of interfaces between symbionts 4 IV. Identity of nutrients transferred: an overview 12 V. Membrane transport: basic principles 14 VI. Transport at the interface of biotrophic symbioses 15 VII. Regulation of pH in biotrophic symbioses 25 VIII. Conclusions: 26