Tansley Review No. 45 Wall growth, protein excretion and morphogenesis in fungi

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Abstract
With the exception of the unicellular yeasts, fungi typically grow by means of hyphae that extend only at their apices and ramify into a mycelium. This mode of growth provides fungi with a certain mobility and the ability to invade dead and living organic substrata. They are thus the main decomposers of plant residues but they also have established intricate symbiotic relationships with plants, both mutualistic and parasitic. The process of apical growth of a hyphae requires the controlled expansion of the apical wall which must be transformed subsequently into a wall that resists turgor pressure and maintains the tubular shape of the hyphae. Although the driving force for hyphal extension is probably the turgor pressure, a subtle interplay between wall extension and cytoplasmic activity is necessary because only a precise gradient of wall-synthetic activity can maintain uniform wall thickness during expansion. Possibly, the presence in the plasma membrane of mechanico-sensitive proteins plays a role in conjunction with the cytoskeleton at the apex, particularly action. Although the major structural wall polysaccharides are probably manufactured directly on the expanding apical plasma membrane, proteins (and probably some wall components) are delivered to the growing surface by a continuous stream of exocytotic vesicles that fuse with the plasma membrane, at the same time extending its surface. Our analyses of the chemistry of the fungal wall and its biosynthesis and assemblage have disclosed a simple mechanism (though complex in detail) that may explain the transition from a newly formed expandable wall at the apex to a more rigid wall at the base of the hyphal extension zone. Two individual wall polymers, chitin and β-glucan, extruded at the apex are modified within the domain of the wall. Among the modifications observed are the formation of covalent crosslinks between these two polymers and hydrogen bonds between the homologous polymer chains, leading to the formation of chitin microfibrils crosslinked to a glucan matrix. This process is thought to convert an initially plastic wall into a rigid wall as the polymers fall behind the advancing tip. We have called this the steady-state growth theory for apical wall extension because a steady-state amount of plastic wall is always maintained at the growing apex. Excretion of lytic enzymes is a vital process in filamentous fungi because, in nature, they thrive on organic polymers which must be degraded extracellularly. Such enzymes are also necessary for infection processes. Cytological data suggest that such enzymes are extruded by the vesicles that continuously fuse with the plasma membrane at the growing apex. We have shown that a large portion of the excreted enzymes indeed leaves the hypha at the growing apex but another portion may be retained by the wall and is slowly released into the medium. In relation to the steady-state growth theory we hypothesize that enzymes can pass the wall at the apex by bulk flow, that is, by being carried by the flow of plastic wall material, making pores in the wall less important than previously thought. Proteins excreted by filamentous fungi not only serve dissimilatory purposes but are also important for a variety of other activities of the whole mycelium, including morphogenesis. By cloning genes abundantly expressed during formation of aerial hyphae and fruit bodies, we have discovered a class of proteins, named hydrophobins, which are only produced when the mycelium has reached a certain stage of maturity. Whilst excreted by submerged hyphae as monomers into the medium, they self-assemble as insoluble complexes in the walls of emergent hyphae. In aerial hyphae a particular hydrophobin takes the form of rodlets which probably coat the hyphae with an impermeable layer. During fruit-body formation other hydrophobins are produced which may function in the aggregation of hyphae to form a multicellular tissue. Apart from such specific morphogenetic functions, the hydrophobins may play a general role in insulating hyphae from the environment, converting the differentiating structures into sinks for translocation of water and nutrients from the assimilating mycelium. CONTENTS Summary I. Introduction 398 II. The hyphal mode of growth 399 III. Biogenesis of the wall fabric 400 IV. Wall growth until rigidification occurs 402 V. Biogenesis of the wall and protein excretion 404 VI. A role for wall proteins in morphogenesis 407 References 410.