Transcellular ionic currents studied by intracellular potential recordings in Neurospora crassa hyphae Transfer of energy from proximal to apical cells

Abstract

Membrane potentials, input resistances, and electric coupling in the apical parts of N.crassa growing hyphae were recorded with the aid of intracellular microelectrodes. It was revealed that the apical cells were always depolarized by 10 to 30 mV as compared to the adjacent proximal cells. The septal pore maintained an electrical resistance of 4 to 6 MQ. The calculated values of the endogenous electrical current passing through the septal pore varied between 0.5 and 1 nA. Electrical isolation of the apical cells resulted in their depolarization from 120-150 mV to 40-60 mV, characteristics of the membrane potential value of N.crassa adult hypbae with completely blocked electrogenic pumps. A simultaneous increase in the input resistance value from 15-20 MI2 to 40-80 Ms'2 was observed. The above data can be explained assuming that H+-ATPase activity was greatly lowered in the apical cells. Thus in the intact hyphae with electrically coupled cells energy is transferred from the proximal hyphal compartments to the apical ones.

The Plasma Membrane Proton Pump PMA-1 Is Incorporated into Distal Parts of the Hyphae Independently of the Spitzenkörper in Neurospora crassa

“…This electrochemical gradient has been studied in several fungal species by diverse methods, including vibrating probes, microelectrodes, and pH indicators. The results showed that current normally flows inward at the hyphal apical regions and flows outward at distal areas (3,4,(6)(7)(8)(9).…”

“…One of the most widely accepted models for fungal growth, the vesicle supply center for fungal morphogenesis, postulates a unidirectional traffic of vesicles to the hyphal apex, where they aggregate temporarily at an apical structure, the Spitzenkörper, prior to fusion with the apical plasma membrane (PM) by the process of exocytosis (1). However, some PM proteins, such as the H ϩ -ATPases, essential for hyphal growth, have been previously predicted to be absent or inactive at the hyphal apex (2)(3)(4), suggesting the existence of vesicle delivery routes other than the above and independent of the Spitzenkörper that reach nonapical regions of the hyphal PM. H ϩ -ATPases are involved in pumping protons out of the cell, generating a large electrochemical gradient and supplying energy to H ϩ -coupled nutrient uptake systems (5).…”

Energy transfer via cell‐to‐cell junctions

“…The local electric currents were really demonstrated for some animal and plant cells, but their functional significance remained virtually obscure [1,10,11,18,19,21]. We have once more obtained evidence (see also [6,9]) that ionic interactions through permeable intercellular junctions might be involved in the energy redistribution between the adjacent cells. These observations might be useful for the study of the energy budget of the tissue cells.…”

“…Previously, we have revealed with the aid of intracellular microelectrodes that the apical cells of Neurospora crassa hyphae electrically coupled with other hyphae compartments maintain high membrane potential levels due to the intercellular ion fluxes which are comparable with the ion fluxes generated by the primary ionic pump [9]. Thus, the membrane potential in apical cell with inactive H+-ATPase (see [lO,l 11) is supported by the trunk cells where the ATPase is active.…”

Primary basidiospore charge and taxonomy of Agaricomycetes

“…Electrophysiological studies made by Tatiana Belozerskaya with coworkers show that, in mycelial fungi, energy transfer takes place in the electrically coupled cells via ionic fluxes, that these ionic fluxes promote local metabolic specialization of individual hyphal segments and favor their functional heterogeneity, and that integration of cells takes place via local intercellular interactions due to a non-uniform distribution of ionic pumps and secondary transport systems in the apical and proximal hyphal cells [26][27][28][29][30]. As most basidia are hyphal end cells [6], the bioelectrical activity might be involved in the formation of both the sterigmata and the basidiospores.…”