Academic journal article Genetics

Novel Sexual-Cycle-Specific Gene Silencing in Aspergillus Nidulans

Academic journal article Genetics

Novel Sexual-Cycle-Specific Gene Silencing in Aspergillus Nidulans

Article excerpt

ABSTRACT We report a novel sexual-cycle-specific gene-silencing system in the genetic model Aspergillus nidulans. Duplication of the mating type matA^sup HMG^ gene in this haploid organism triggers Mat-induced silencing (MatIS) of both endogenous and transgenic matA genes, eliminates function of the encoded SRY structural ortholog, and results in formation of barren fruiting bodies. MatIS is spatiotemporally restricted to the prezygotic stage of the sexual cycle and does not interfere with vegetative growth, asexual reproduction, differentiation of early sexual tissues, or fruiting body development. MatIS is reversible upon deletion of the matA transgene. In contrast to other sex-specific silencing phenomena, MatIS silencing has nearly 100% efficiency and appears to be independent of homologous duplicated DNA segments. Remarkably, transgene-derived matA RNA might be sufficient to induce MatIS. A unique feature of MatIS is that RNA-mediated silencing is RNA interference/Argonaute-independent and is restricted to the nucleus having the duplicated gene. The silencing phenomenon is recessive and does not spread between nuclei within the common cytoplasm of a multinucleate heterokaryon. Gene silencing induced by matA gene duplication emerges as a specific feature associated with matAHMG regulation during sexual development.

DISCOVERY of homology-dependent gene silencing (HDGS) has opened a new dimension to our understanding of eukaryotic genome integrity, structure, and expression. HDGS as a consequence of gene duplication is a ubiquitous phenomenon that has been reported across the kingdoms in various species of fungi, plants, and animals. Transgene-mediated gene duplication often triggers simultaneous silencing of both the transgene and the homologous endogenous gene at the transcriptional and/or posttranscriptional level (Bingham 1997; Cogoni and Macino 1999b; Cogoni 2001).The basic molecular machinery for gene silencing shares common mechanistic features with plants, animals, and fungal species (Bingham 1997; Selker 1997; Cogoni and Macino 1999b; Cogoni 2001; Vaucheret and Fagard 2001). Silencing is usually induced by duplicated homologous coding sequences that trigger RNA-mediated post-transcriptional degradation of the gene-specific messenger RNA (mRNA) or RNA/DNA-mediated DNA methylation and/or chromatin modification resulting in transcriptional inhibition of gene expression (Cogoni and Macino 1999b; Moazed 2009). Gene silencing is believed to be an ancient phenomenon that evolved as a genome defense mechanism responding to virus infection or transposon invasion. It plays a major role in genome stability, maintenance, and regulation of chromatin structure and gene expression (Cogoni and Macino 1999b; Moazed 2009).

Several components of gene-silencing pathways are conserved. RNAse III (Dicer), RNA-dependent RNA polymerase (RdRP), Argonaute proteins, RNA-silencing complexes [RNAinduced silencing complexes (RISCs) and RNA-induced transcriptional silencing complexes (RITS)], and chromatinremodeling complexes have been characterized in various eukaryotic species from protists to humans (Cerutti and Casas-Mollano 2006; Moazed 2009). However, precise molecular mechanisms and mechanistic details underlying HDGS pathways are still poorly defined and remain largely unknown (Cogoni and Macino 1999b; Vaucheret and Fagard 2001; Catalanotto et al. 2004; Chicas et al. 2004; Forrest et al. 2004; Hammond and Keller 2005; Wassenegger 2005).

In fungi, a variety of different HDGS phenomena have been reported, all demonstrating conserved but also unique features. HDGS processes have been observed in Neurospora (Cogoni and Macino 1997a,b), Ascobolous (Barry et al. 1993; Malagnac et al. 1997), Schizophyllum (Schuurs et al. 1997), Coprinus (Freedman and Pukkila 1993), Phytophthora (van West et al. 1999), and Cryptococcus (Wang et al. 2010). The most studied and best characterized are premeiotic repeatinduced point mutation (RIP) in Neurospora crassa and methylation induced premeiotically (MIP) in Ascobolous immersus. …

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