Two Classes of Homeodomain Proteins Specify the Multiple A Mating Types of the Mushroom Coprinus cinereus

Abstract

The A mating type locus of the mushroom Coprinus cinereus regulates essential steps in sexual development. The locus is complex and contains several functionally redundant, multiallelic genes that encode putative transcription factors. Here, we compare four genes from an A locus designated A42. Overall, the DNA sequences are very different (approximately 50% homology), but two classes of genes can be distinguished on the basis of a conserved homeodomain motif in their predicted proteins (HD1 and HD2). Development is postulated to be triggered by an HD1 and an HD2 gene from different A loci. Thus, proteins encoded by genes of the same locus must be distinguished from those encoded by another locus. Individual proteins of both classes recognize each other using the region N-terminal to the homeodomain. These N-terminal specificity regions (COP1 and COP2) are predicted to be helical and are potential dimerization interfaces. The amino acid composition of the C-terminal regions of HD1 proteins suggests a role in activation, and gene truncations indicate that this region is essential for function in vivo. A corresponding C-terminal region in HD2 proteins can be dispensed with in vivo. We will discuss these predicted structural features of the C. cinereus A proteins, their proposed interactions following a compatible cell fusion, and their similarities to the a1 and alpha 2 mating type proteins of the yeast Saccharomyces cerevisiae.

Life History and Developmental Processes in the BasidiomyceteCoprinus cinereus

“…It is not known whether the A mating-type products are positive or negative regulators of development, since morphological observations do not show whether a regulatory effect is direct or indirect. Analysis of monokaryons transformed with A genes of another specificity ("A on" transformants) revealed a negative function of compatible A genes on the production of oidia and positive effects not only on the formation of clamp cells but also on the formation of chlamydospores, hyphal knots, and fruiting-body initials (232,258,261,307,358,477), consistent with the earlier observations with common B heterokaryons and Amut homokaryons (see above) ( Table 1). The mating-type-encoded transcription factors of C. cinereus and other basidiomycetes (S. commune and Ustilago spp.)…”

“…Other, nondiscriminating dimerization domains were predicted to localize directly C-terminal to the HD1 homeodomains (131,254). Remarkably, there is a significant identity between a short sequence downstream of the homeodomain in HD1 proteins to the 20-aa C-terminal tail of the homologous matingtype protein ␣2 of S. cerevisiae (172,258) (Fig. 14).…”

“…Paralogous genes from the same A haplotype and also allelic versions from other A haplotype are very different in sequence, with the highest conservation in the regions containing the homeodomain motifs. Paralogous genes have a DNA sequence identity between 40 and 50%, allelic genes DNA homologies between 60 and 70% (16,131,258,308,477). Domain swaps indicated that allele specificity resides within the highly variable N termini of the proteins and subsequent in vitro studies on Cterminally truncated proteins showed that the 120-to 150-aa N termini are indeed discriminating HD1-HD2 protein dimerization domains (22,258).…”

“…Paralogous genes have a DNA sequence identity between 40 and 50%, allelic genes DNA homologies between 60 and 70% (16,131,258,308,477). Domain swaps indicated that allele specificity resides within the highly variable N termini of the proteins and subsequent in vitro studies on Cterminally truncated proteins showed that the 120-to 150-aa N termini are indeed discriminating HD1-HD2 protein dimerization domains (22,258). The N-terminal ends of HD1 and HD2 proteins from allelic gene pairs interact strongly, but N-terminal dimerization is ineffective in all other combinations (proteins of the same kind, or HD1 and HD2 proteins encoded within the same or in paralogous gene pairs) (22).…”

Wood production, wood technology, and biotechnological impacts

“…Next to eliciting typical features of the dikaryotic mycelium (e.g. clamps cells and clamp cell fusion; Kües et al 1992, 1994a,c, Badalyan et al 2004), the A mating type genes were shown to induce hyphal knot and primordia development ) and the B mating type genes to support the A mating type genes in initiation of fruiting body development and to act in fruiting body maturation at the stage of karyogamy (Kües et al 2002b). Therefore not surprisingly, certain mutations in the mating type loci (Kües et al 1994b, Pardo et al 1996, Olesnicky et al 1999, Srivilai et al 2006b) make fruiting body development independent from dikaryon formation (Swamy et al 1984).…”