Environmental signaling and regulation of mushroom formation

Abstract

Mushrooms are of great value as a food source. The Netherlands has a large share of the European white button mushroom (Agaricus bisporus) production. This market will increase in the future due to larger demand for high quality food with a growing world population. Environmental factors play a role in the initiation of mushroom formation. Mushroom formation by A. bisporus is repressed by 1-octen-3-ol and high CO2, but stimulated by low temperature. Fruiting is responsive to blue light in Schizophyllum commune and repressed by high CO2 levels. Signaling of environmental conditions leads to transcription factor activity. A set of S. commune transcription factors and a blue light sensor involved in fruiting body development have been identified. This research showed that transcription factors BriI and Hom1 stimulate vegetative growth, while biomass formation is repressed by Wc-2, Hom2, and Fst4. The transcription factor tea1 was also down-regulated in the Δwc-2Δwc-2, Δhom2Δhom2 and Δfst4Δfst4 strains. The Δtea1Δtea1 strain produced more biomass than the wild-type and was severely affected in mushroom formation. Together, these data show that transcription factors Wc-2, Hom2, Fst4, and Tea1 link mushroom initiation and repression of vegetative growth. CO2 has profound effects on functioning of organisms. Therefore, it is sensed throughout the tree of life, in most cases via the cAMP-Pka signaling pathway. Here, a clear link was shown between high CO2 and cAMP levels and repression of fruiting in S. commune. Addition of cAMP in the medium mimicked high CO2 conditions by repressing fruiting body development. Overexpression of pde2, a gene encoding phosphodiesterase that degrades cAMP, resulted in fruiting body development even at elevated CO2 levels. Furthermore, it was investigated whether the homeodomain protein Hom2 is a target for Pka. The Δhom2Δhom2 dikaryon formed more biomass than the wild-type at ambient CO2 levels, while biomass of both strains was similar at 5% CO2. Hom2 contains 4 predicted Pka RRXS phosphorylation motifs. The serine codons of these motifs were replaced by alanine. This resulted in transformant strains that showed growth inhibition and prompt fructification at low CO2. Together, it is proposed that Pka phosphorylates Hom2, thereby maintaining the mycelium in the vegetative phase. Dephosphorylation of Hom2 at low CO2 switches the dikaryon from the vegetative into the generative phase. All hom2 orthologues of Agaricomycetes contain 2-5 RRXS motifs indicating that the role of Hom2 in fruiting is conserved. The S. commune transcription factor c2h2 is involved in mushroom formation. Its inactivation results in arrest at aggregate formation. In this study, the A. bisporus c2h2 orthologue was overexpressed in this basidiomycete. Morphology, cap expansion rate, total numbers and biomass of mushrooms harvested during culturing were not affected by over-expression of c2h2. However, more class II mushrooms were formed compared to the wild-type and the yield-per-day peaked one day earlier. These data and expression analysis indicate that C2H2 functions early in fruiting body development, while it also seems to have a role in selective tissues of young mushrooms. Data indicate that c2h2 is a target for breeding of commercial mushroom strains.