Rearrangement of duplicated DNA in specialized cells of Neurospora

doi:10.1016/0092-8674(87)90097-3

Cell

Volume 51, Issue 5, 4 December 1987, Pages 741-752

https://doi.org/10.1016/0092-8674(87)90097-3 Get rights and content

Abstract

Introduction of DNA into Neurospora crassa can lead to sequence instability in the sexual phase of the life cycle. Sequence instability was investigated by using a set of strains transformed with single copies of a plasmid including host sequences, Neurospora sequences deleted from the host genome, and foreign sequences. The sequences already represented in the host were rearranged at high frequency in a cross. In general, both elements of the duplication, that from the plasmid and that from the host, became rearranged, whether or not they were linked. Unique sequences were left unaltered. Cytosine residues in the rearranged sequences typically became methylated de novo. Results from tetrad analyses indicated that the rearrangements occur before meiosis, during a stage between fertilization and karyogamy. We suggest that this previously unrecognized genetic process, RIP (rearrangement induced premeiotically), may contribute diversity for evolution and also maintain the gross organization of the genome.

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Dicing of double-stranded RNA (dsRNA) into small RNA is an essential process to trigger transcriptional and post-transcriptional gene silencing. Using cell-free extracts of the model filamentous fungus Neurospora crassa, we successfully detected the dicing activity of one of two N. crassa Dicers NcDCL2. The predominant 23-nucleotide (nt) cleavage product was always detected from 30-nt to 130-nt dsRNA substrates, and additional products of approximately 18 to 28 nt were occasionally produced. The enzymatic properties of NcDCL2 are different from those of insect and plant small interfering RNA (siRNA)-producing Dicers, Drosophila melanogaster Dicer-2 and Arabidopsis thaliana DCL3 and DCL4 (AtDCL3 and AtDCL4). Whereas AtDCL3 and AtDCL4 preferentially cleave short and long dsRNAs, respectively, NcDCL2 cleaved both short and long dsRNAs. These results suggest that N. crassa has a single siRNA-producing Dicer NcDCL2, which is a prototype of plant siRNA-producing Dicers with distinct functions in diverse RNA silencing pathways. The dicing assay reported here is convenient to detect and biochemically characterize the dicing activities of both plant and fungal Dicers, and is likely applicable to other organisms.
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Citation Excerpt :
In P. biforme, 25 of 28 strains carried CheesyTer, with an identity >99.8% between strains. The identity between P. biforme and P. camemberti was also >99.8%, except in the 5-kb region at the start of CheesyTer, in which the similarity between the two species dropped to 90%, mainly due to C:G to T:A mutations in P. camemberti, corresponding to the repeat-induced point (RIP) mutations specific to fungi occurring in repeated sequences during sexual reproduction [44]. As P. camemberti was found to be clonal and no RIP footprints were detected within the rest of CheesyTer, these findings suggest that CheesyTer was transferred to an ancestor of the two P. camemberti varieties with this RIPed sequence already present.
Domestication involves recent adaptation under strong human selection and rapid diversification and therefore constitutes a good model for studies of these processes. We studied the domestication of the emblematic white mold Penicillium camemberti, used for the maturation of soft cheeses, such as Camembert and Brie, about which surprisingly little was known, despite its economic and cultural importance. Whole-genome-based analyses of genetic relationships and diversity revealed that an ancient domestication event led to the emergence of the gray-green P. biforme mold used in cheese making, by divergence from the blue-green wild P. fuscoglaucum fungus. Another much more recent domestication event led to the generation of the P. camemberti clonal lineage as a sister group to P. biforme. Penicillium biforme displayed signs of phenotypic adaptation to cheese making relative to P. fuscoglaucum, in terms of whiter color, faster growth on cheese medium under cave conditions, lower amounts of toxin production, and greater ability to prevent the growth of other fungi. The P. camemberti lineage displayed even stronger signs of domestication for all these phenotypic features. We also identified two differentiated P. camemberti varieties, apparently associated with different kinds of cheeses and with contrasted phenotypic features in terms of color, growth, toxin production, and competitive ability. We have thus identified footprints of domestication in these fungi, with genetic differentiation between cheese and wild populations, bottlenecks, and specific phenotypic traits beneficial for cheese making. This study has not only fundamental implications for our understanding of domestication but can also have important effects on cheese making.
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Gene duplication and horizontal gene transfer (HGT) are two important but different forces for adaptive genome evolution. In eukaryotic organisms, gene duplication is considered to play a more important evolutionary role than HGT. However, certain fungal lineages have developed highly efficient mechanisms that avoid the occurrence of duplicated gene sequences within their genomes. While these mechanisms likely originated as a defense against harmful mobile genetic elements, they come with an evolutionary cost. A prominent example for a genome defense system is the RIP mechanism of the ascomycete fungus Neurospora crassa, which efficiently prevents sequence duplication within the genome and functional redundancy of the subsequent paralogs. Despite this tight control, the fungus possesses two functionally redundant sterol C-5 desaturase enzymes, ERG-10a and ERG-10b, that catalyze the same step during ergosterol biosynthesis. In this study, we addressed this conundrum by phylogenetic analysis of the two proteins and supporting topology tests. We obtained evidence that a primary HGT of a sterol C-5 desaturase gene from Tremellales (an order of Basidiomycota) into a representative of the Pezizomycotina (a subphylum of Ascomycota) is the origin of the ERG-10b sequence. The reconstructed phylogenies suggest that this HGT event was followed by multiple HGT events among other members of the Pezizomycotina, thereby generating a diverse group with members in the four classes Sordariomycetes, Xylonomycetes, Eurotiomycetes and Dothideomycetes, which all harbor the second sterol C-5 desaturase or maintained in some cases only the ERG-10b version of this enzyme. These results furnish an example for a gene present in numerous ascomycetous fungi but primarily acquired by an ancestral HGT event from another fungal phylum. Furthermore, these data indicate that HGT represents one mechanism to generate functional redundancy in organisms with a strict avoidance of gene duplications.
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Abstract

References (20)

Cloning of the am (glutamate dehydrogenase) gene of Neurospora crassa through the use of a synthetic DNA probe

Gene

The cytogenetics of Neurospora

Dispersed 5S RNA genes in N. crassa: structure, expression and evolution

Cell

Enhancement of methotrexate resistance and dihydrofolate reductase gene amplification by treatment of mouse 3T6 cells with hydroxyurea

Mol. Cell. Biol.

Genetical and molecular analyses of qa-2 transformants in Neurospora crassa

Genetics

Efficient transformation of Neurospora crassa utilizing hybrid plasmid DNA

Cellular DNA rearrangements and early developmental arrest caused by DNA insertion in transgenic mouse embryos

Mol. Cell. Biol.

Genetic and microbial research techniques for Neurospora crassa

Meth. Enzymol.

Mechanisms of inheritance. 1. Mendelian

Transformation of Neurospora crassa with recombinant plasmids containing the cloned glutamate dehydrogenase (am) gene: evidence for autonomous replication of the transforming plasmid

Mol. Cell. Biol.

Cited by (276)

Biochemical characterization of the dicing activity of Dicer-like 2 in the model filamentous fungus Neurospora crassa

Domestication of the Emblematic White Cheese-Making Fungus Penicillium camemberti and Its Diversification into Two Varieties

Evidence of repeated horizontal transfer of sterol C-5 desaturase encoding genes among dikarya fungi

Sexual development, its determinants, and regulation in Trichoderma reesei

Off the wall: The rhyme and reason of Neurospora crassa hyphal morphogenesis

DNA Methylation: Shared and Divergent Features across Eukaryotes

Cell

ArticleRearrangement of duplicated DNA in specialized cells of Neurospora

Abstract

Gene

Cell

Enhancement of methotrexate resistance and dihydrofolate reductase gene amplification by treatment of mouse 3T6 cells with hydroxyurea

Mol. Cell. Biol.

Genetical and molecular analyses of qa-2 transformants in Neurospora crassa

Genetics

Efficient transformation of Neurospora crassa utilizing hybrid plasmid DNA

Cellular DNA rearrangements and early developmental arrest caused by DNA insertion in transgenic mouse embryos

Mol. Cell. Biol.

Genetic and microbial research techniques for Neurospora crassa

Meth. Enzymol.

Mechanisms of inheritance. 1. Mendelian

Transformation of Neurospora crassa with recombinant plasmids containing the cloned glutamate dehydrogenase (am) gene: evidence for autonomous replication of the transforming plasmid

Mol. Cell. Biol.

Article
Rearrangement of duplicated DNA in specialized cells of Neurospora