The system of pleiomorphic, motile tubules and vacuoles in growing hyphal tips of Pisolithus tinctorius

Basidiomycete fungal hyphae grow continuously by divisions of a tip cell. This results in an extensive mycelium, of which the tip cell is the final outpost. Growth of this cell requires continuous synthesis of cell wall, as well as migration of cytoplasm and organelles. Cell division produces a file of cells that, in contrast to the tip cell, grow only by branching. The result is an extensive, branched mycelium, which in some fungi may culminate in a mycorrhizal association with roots. Transport of nutrients is through the mycelium and is likely to have both symplastic and apoplastic components (Cairney, 1992). Symplastic transport is reported to occur along hyphae by diffusion, cytoplasmic streaming or osmotically generated mass flow through the fungal cytoplasm (Jennings, 1987, 1989; Thompson et al., 1987). In basidiomycetes, this symplastic continuity depends on transport through the dolipores in the septa and it is usually assumed that transport across the dolipores occurs exclusively in the cytoplasmic compartment. Recently we have shown that the fluorochrome 6-carboxyfluorescein (CF) is accumulated by a pleiomorphic system of motile tubules and vacuoles in the tip cells of the fungus Pisolithus tinctorius (Pers.) Coker and Couch (Shepherd et al., 1993). The tubules of this system, which bear a close resemblance to tubular endosomal networks of cultured cancer cells, or lysosomal networks of macrophages, can extend and retract across large intracellular distances. They can move fluorescent material by peristaltic motion between clusters of vacuoles situated at intervals along the terminal and penultimate cells. Although their movement may similarly depend on the cytoskeleton, it is independent of both the rate and direction of cytoplasmic streaming. During these observations we noted that tubules intermittently crossed the dolipore septum separating the tip and penultimate cells, indicating that this pleiomorphic tubule and vacuole system plays a role in cell-to-cell transport as well as intracellular transport. This would imply that there is a compartment additional to the cytoplasm that can, at least transiently, act as a conduit across the connecting bridges of the symplast in fungi. This contrasts with the prevailing view that transport between walled cells (higher plants and most basidiomycete fungi) occurs primarily via cytoplasm in continuities between the adjacent cells, and that any substructures in such cytoplasmic bridges are nonconducting (see Robards and Lucas, 1990). In this paper, we provide evidence that tubular elements of the tubule and vacuole system pass through the septum 1173 Journal of Cell Science 105, 1173-1178(1993) Printed in Great Britain © The Company of Biologists Limited 1993