Aquaporins in yeasts and filamentous fungi

Abstract

Recently, genome sequences from different fungi have become available. This information reveals that yeasts and filamentous fungi possess up to five aquaporins. Functional analyses have mainly been performed in budding yeast, Saccharomyces cerevisiae, which has two orthodox aquaporins and two aquaglyceroporins. Whereas Aqy1 is a spore-specific water channel, Aqy2 is only expressed in proliferating cells and controlled by osmotic signals. Fungal aquaglyceroporins often have long, poorly conserved terminal extensions and differ in the otherwise highly conserved NPA motifs, being NPX and NXA respectively. Three subgroups can be distinguished. Fps1-like proteins seem to be restricted to yeasts. Fps1, the osmogated glycerol export channel in S. cerevisiae, plays a central role in osmoregulation and determination of intracellular glycerol levels. Sequences important for gating have been identified within its termini. Another type of aquaglyceroporin, resembling S. cerevisiae Yfl054, has a long N-terminal extension and its physiological role is currently unknown. The third group of aquaglyceroporins, only found in filamentous fungi, have extensions of variable size. Taken together, yeasts and filamentous fungi are a fruitful resource to study the function, evolution, role and regulation of aquaporins, and the possibility to compare orthologous sequences from a large number of different organisms facilitates functional and structural studies.

Integrative model of the response of yeast to osmotic shock

“…Further studies can now address the relative roles of transport and gene expression on osmolyte accumulation. Interestingly, aquaglyceroporins of the characteristics of Fps1 have been found only in yeasts so far 34 . Given the importance of such osmolyte transporters in modulating the osmotic response and turgor pressure, it seems likely that proteins of similar role should exist in other organisms as well.…”

Novel stress responses facilitate Saccharomyces cerevisiae growth in the presence of the monocarboxylate preservatives

“…Resistances are induced to Acetic, but not propionic, sorbic or benzoic acids [19] Propionic, sorbic, benzoic acids, but not acetic acid [1,7] Key induced signalling pathway and activity HOG pathway signalling, leading to Hog1p MAP kinase activation [19] No evidence for a signalling pathway involvement; acid anion may act directly on the War1p transcription factor [13] Key action/target of the induced activity needed for the acquisition of resistance Phosphorylation of Fps1p, leading to Fps1p endocytosis [20] PDR12 gene induction, leading to an elevated plasma membrane level and activity of the Pdr12p ABC transporter [23,28] Probable related stress response Hog1p-directed downregulation of metalloid entry through the Fps1p channel [40] War1p activation in media containing leucine, methionine or phenylalanine as sole nitrogen source [9] Normal physiological function of the major target of the response Fps1p is the major glycerol channel of the plasma membrane, important for osmoadaptation [10,22,38] Pdr12p is also involved in export of the potentially toxic aromatic and branched-chain organic acids produced during amino acid catabolism [9] (2), a MAP kinase constitutively bound to, and that directly phosphorylates, Fps1p (3). This phosphorylation provides the signal for Fps1p endocytosis and degradation, eliminating this source of the acetic acid entry to the cell.…”

“…cerevisiae Hog1p is activated transiently both in response to hyperosmotic stress [10,22,38] and with acetic acid stress, [19] but only with the latter stress condition does it trigger a destabilization of Fps1p. [20] The Fps1p aquaglyceroporin rapidly adopts a closed channel conformation in cells shifted to high osmolarity, a Hog1p-independent response to altered cell turgor.…”

“…[20] The Fps1p aquaglyceroporin rapidly adopts a closed channel conformation in cells shifted to high osmolarity, a Hog1p-independent response to altered cell turgor. [10,22,38 There are other differences between the responses of S. cerevisiae to osmostress [10,22,38] and acetic acid stress. [19] The Hog1p activated by acetic acid in low-pH cultures does not cause GPD1 gene induction or an accumulation of intracellular glycerol, events that are characteristic of this MAP kinase becoming activated by hyperosmotic stress.…”

Stress resistance and signal fidelity independent of nuclear MAPK function

“…What cellular processes does Hog1 influence to mediate osmoresistance? If unable to counterbalance high external osmolarity, cells will plasmolyze because of loss of H 2 O through water channels (aquaporins) (28). However, lack of Hog1-dependent closure of such channels cannot be responsible for the inviability of hog1⌬ cells under hyperosmotic stress conditions because deletion of either or both of the aquaporin genes (AQY1 and AQY2) ( (Table S1).…”