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      Neurospora Heterokaryons with Complementary Duplications and Deficiencies in Their Constituent Nuclei Provide an Approach to Identify Nucleus-Limited Genes

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          Abstract

          Introgression is the transfer of genes or genomic regions from one species into another via hybridization and back-crosses. We have introgressed four translocations ( EB4, IBj5, UK14-1, and B362i) from Neurospora crassa into N. tetrasperma. This enabled us to construct two general types of heterokaryons with mat-A and mat-a nuclei of different genotypes: one type is [ T + N] (with one translocation nucleus and one normal sequence nucleus), and the other is [ Dp + Df] (with one nucleus carrying a duplication of the translocation region and the other being deleted for the translocation region). Self-crossing these heterokaryons again produced [ T + N] and [ Dp + Df] progeny. From conidia (vegetative spores) produced by the heterokaryotic mycelia, we obtained self-fertile (heterokaryotic) and self-sterile (homokaryotic) derivative strains. [ T + N] heterokaryons produced homokaryotic conidial derivatives of both mating types, but [ Dp + Df] heterokaryons produced viable conidial homokaryons of only the mating type of the Dp nucleus. All four [ T + N] heterokaryons and three [ Dp + Df] heterokaryons produced both self-sterile and self-fertile conidial derivatives, but the [ Dp(B362i) + Df(B362i)] heterokaryons produced only self-sterile ones. Conceivably, the Df(B362i) nuclei may be deleted for a nucleus-limited gene required for efficient mitosis or nuclear division, and whose deficit is not complemented by the neighboring Dp(B362i) nuclei. A cross involving Dp(EB4) showed repeat-induced point mutation (RIP). Because RIP can occur in self-crosses of [ Dp + Df] but not [ T + N] heterokaryons, RIP alteration of a translocated segment would depend on the relative numbers of [ Dp + Df] vs. [ T + N] ancestors.

          Most cited references25

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          Meiotic silencing by unpaired DNA.

          The silencing of gene expression by segments of DNA present in excess of the normal number is called cosuppression in plants and quelling in fungi. We describe a related process, meiotic silencing by unpaired DNA (MSUD). DNA unpaired in meiosis causes silencing of all DNA homologous to it, including genes that are themselves paired. A semidominant Neurospora mutant, Sad-1, fails to perform MSUD. Sad-1 suppresses the sexual phenotypes of many ascus-dominant mutants. MSUD may provide insights into the function of genes necessary for meiosis, including genes for which ablation in vegetative life would be lethal. It may also contribute to reproductive isolation of species within the genus Neurospora. The wild-type allele, sad-1(+), encodes a putative RNA-directed RNA polymerase.
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            Premeiotic instability of repeated sequences in Neurospora crassa.

            E Selker (1989)
            Maintenance of a steamlined genome is probably important to a free-living fungus. The period between fertilization and karyogamy in the life cycle of Neurospora and related fungi provides an ideal time for "genome-cleaning". Premeiotic intrachromosomal recombination deletes tandem repeats at high frequency in both homothallic and heterothallic filamentous ascomycetes. This eliminates excess copies of tandemly repeated genes and at the same time favors their homogenization. Heterothallic fungi such as Neurospora also take the bolder steps of mutating and modifying both copies of duplicated sequences, linked or unlinked, by RIP. Because these organisms are outbreeders, and because RIP operates immediately prior to meiosis in cells having nuclei from both parents, the process does not cause much lethality or loss of genetic information. RIP should effectively counter selfish and redundant DNA, and at the same time generate raw material for evolution. In addition, RIP should both prevent chromosomal rearrangements by causing divergence of dispersed repeated sequences and rid a population of duplication-generating rearrangements. Thus, this form of genetic instability potentially stabilizes the gross organization of the genome.
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              Massive Changes in Genome Architecture Accompany the Transition to Self-Fertility in the Filamentous Fungus Neurospora tetrasperma

              A large region of suppressed recombination surrounds the sex-determining locus of the self-fertile fungus Neurospora tetrasperma. This region encompasses nearly one-fifth of the N. tetrasperma genome and suppression of recombination is necessary for self-fertility. The similarity of the N. tetrasperma mating chromosome to plant and animal sex chromosomes and its recent origin (<5 MYA), combined with a long history of genetic and cytological research, make this fungus an ideal model for studying the evolutionary consequences of suppressed recombination. Here we compare genome sequences from two N. tetrasperma strains of opposite mating type to determine whether structural rearrangements are associated with the nonrecombining region and to examine the effect of suppressed recombination for the evolution of the genes within it. We find a series of three inversions encompassing the majority of the region of suppressed recombination and provide evidence for two different types of rearrangement mechanisms: the recently proposed mechanism of inversion via staggered single-strand breaks as well as ectopic recombination between transposable elements. In addition, we show that the N. tetrasperma mat a mating-type region appears to be accumulating deleterious substitutions at a faster rate than the other mating type (mat A) and thus may be in the early stages of degeneration.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                20 April 2015
                June 2015
                : 5
                : 6
                : 1263-1272
                Affiliations
                [* ]Centre for DNA Fingerprinting and Diagnostics, Hyderabad 500001, India
                []Graduate Studies, Manipal University, Manipal 576104, Karnataka, India
                Author notes
                [1 ]Corresponding author: Centre for DNA Fingerprinting and Diagnostics, Tuljaguda Complex, Nampally, Hyderabad 500001, India. E-mail: kas@ 123456cdfd.org.in
                Author information
                http://orcid.org/0000-0002-5269-8020
                Article
                GGG_017616
                10.1534/g3.115.017616
                4478554
                25897010
                2dd5fe27-b330-4f36-933b-2db666e44ffb
                Copyright © 2015 Giri et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License ( http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 22 February 2015
                : 15 April 2015
                Page count
                Pages: 10
                Categories
                Investigations

                Genetics
                chromosome translocation,introgression,pseudohomothallism,rip,msud
                Genetics
                chromosome translocation, introgression, pseudohomothallism, rip, msud

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