Full-length Chd1 of Coprinopsis cinerea is expressed after the dark period required for fruiting body maturation and impacts meiotic progression

Abstract

The maturation of the fruiting body primordia in the Agaricomycete Coprinopsis cinerea is triggered by light exposure, followed by a required dark period to complete maturation. During this maturation phase, meiosis occurs within basidia arranged on the surface of the gills (lamellae) on the underside of the cap. However, the molecular events required during the dark period for fruiting body maturation remain elusive. We identified a developmental mutant that fails to mature fruiting bodies under light/dark conditions. The mutant fruiting bodies resembled those arrested by the wild-type strains cultured under continuous light. The gene responsible for this mutant phenotype encodes a chromodomain helicase DNA-binding protein 1 (Chd1) homolog, Cc.Chd1. RNA-seq revealed a low transcriptional region (LTcR) within the Cc.chd1 gene. This suggests that a short version of Cc.Chd1 (predicted 1125 aa, Cc.Chd1S) is translated from the vegetative mycelium stage until before karyogamy. In contrast, the full-length Cc.Chd1 (predicted 1441 aa, Cc.Chd1L) is translated during or after the dark period when karyogamy occurs in the basidia. Western blot analysis confirmed these types of Cc.Chd1 at the expected stages. Microscopic observations further revealed that meiotic chromosomes in basidia become arrested at prophase I in the Cc.chd1–1 mutant and wild-type strains cultured under continuous light. These findings suggest that Cc.Chd1L is required for progression from meiotic prophase I to metaphase I. Additionally, the Cc.chd1 mutant exhibits defects in light-induced secondary knot formation, suggesting a role for Cc.Chd1S in this process.