Meiotic trans-Sensing and Silencing in Neurospora

Rodolfo Aramayo; Robert J. Pratt

doi:10.1128/9781555816636.ch11

Chapter 11 : Meiotic trans-Sensing and Silencing in Neurospora

Authors: Rodolfo Aramayo¹, Robert J. Pratt²

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Affiliations: 1: Department of Biology, Texas A&M University, College Station, TX; 2: Department of Biology, Texas A&M University, College Station, TX

Content Type: Monograph

Publication Year: 2010

Category: Microbial Genetics and Molecular Biology; Fungi and Fungal Pathogenesis

Book DOI: 10.1128/9781555816636

Chapter DOI: 10.1128/9781555816636.ch11

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Abstract:

Before any genetic exchange can take place between the chromosomes participating in meiosis, the molecules must first physically pair. The process of meiotic long-distance pairing must involve trans-sensing between chromosomal segments, but the relationship between these kinds of sensing and that of the trans-sensing that activates meiotic silencing is unknown. This chapter considers the trans-sensing that is involved in the early evaluation of every chromosomal DNA segment and the one involved in meiotic silencing as being the same. The trans-sensing between the genomes participating in meiosis occurs concomitantly with the coalignment of homologous chromosomes and requires extensive searching and satisfaction of stringent molecular homology criteria before recombination is allowed. Understanding meiotic silencing in Neurospora requires knowledge about the life cycle of N. crassa. The pairs of homologous chromosomes of N. crassa will first undergo premeiotic DNA replication, generating sister chromatids attached along their length by cohesin. The participating parental nuclei will then fuse at karyogamy, generating a diploid nucleus. In Neurospora, testing the involvement of genes in meiotic silencing is not straightforward. The diploid nature of the meiotic cell makes it difficult to identify recessive alleles in genes involved in the process. The ancient origins of meiotic silencing in all of its current manifestations are likely grounded in RNAi-mediated genome defense mechanisms. The study of meiotic trans-sensing and meiotic silencing is important not only from a mechanistic perspective but also from an evolutionary point of view.

Citation: Aramayo R, Pratt R. 2010. Meiotic trans-Sensing and Silencing in Neurospora, p 132-144. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch11

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Meiotic trans-Sensing and Silencing in Neurospora

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FIGURE 1

Genome defense mechanisms in the life cycle of N. crassa. Neurospora has two mating types, A and a. Sexual spores (ascospores) are formed when strains of opposite mating type mate and undergo sex. Germinated ascospores form mycelia from which asexual spores (conidia) are produced. Mating occurs when, in response to nitrogen starvation, a strain (either A or a) forms a protoperithecium (female element) that is fertilized by a male element of the opposite mating type to initiate perithecium development. After fertilization, the male- and the female-derived nuclei coexist in a heterokaryotic tissue and divide mitotically until they are sorted into a dikaryotic tissue (dikaryotic cells contain only one nucleus of each mating type). The nuclei then pair and undergo a series of synchronous mitoses until the tip of the hyphal cell in which they reside bends to form a hook-shaped cell called a crozier. One crozier will originate one ascus, containing eight ascospores. The time and places in the life cycle where quelling, RIP, meiotic trans-sensing, and meiotic silencing occur are indicated. Homologs pair inside the only diploid nucleus present in the zygote, immediately after karyogamy. The oval representing a diploid nucleus shows only one pair of chromosomes in the process of sensing. (Adapted from Chromosome Research 15: 633–651, 2007.)

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FIGURE 1

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FIGURE 2

Meiosis, meiotic trans-sensing, and meiotic silencing. (A) Homologous chromosomes are represented by the squiggly lines contained inside the dashed rectangles. The temporal stage during which the prekaryogamic events occur inside the haploid A and a nuclei is represented by the horizontal dashed line. The stages where cell division occurs are indicated by vertical lines. The active comparison between chromosomal regions that occurs during meiotic trans-sensing and recombination is represented by the vertical dashed lines connecting the homologous chromosomes participating in the process. The clear region located on one chromosome represents a transposable or an insertion element. The small squiggly lines represent a hypothetical diffusible signal containing the sequence information from the unpaired region. Meiotic silencing uses this sequence information to silence homologous regions. (B) Depiction of the close connection seen in Neurospora between meiotic trans-sensing and silencing. The resultant phenotypic output, which may or may not reveal the result of meiotic gene silencing, can be detected by the use of appropriate reporters, which, according to their nature can affect the color and/or the shape of the ascospores product of the cross. The close temporal and developmental connection between meiosis and spore formation makes of Neurospora one of the most, if not the most powerful model system available for studying the molecular mechanisms behind meiotic trans-sensing. See the text for more details.

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FIGURE 2

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FIGURE 3

Meiotic silencing in Neurospora: detection and suppression. Simplified views of the genetic composition of the participants in, and of the predicted phenotypic outputs of, several different crosses are presented using Rsp as a reporter gene. (A) In crosses where the diploid is sad-1 +/sad-1 + rsp +/rsp frameshift (fs), silencing of the reporter gene Rsp is not activated due to the lack of unpaired chromatin/DNA. As a result, the sole functional copy of Rsp can complement the heterozygous Rsp condition, which results in the production of wild-type spindle-shaped ascospores. This observation establishes that the product of Rsp acts before cellularization and that all spores, regardless of their individual genotypes, are spindle shaped. (B) As expected, in crosses where the diploid is sad-1 +/sad-1 + rsp fs/rsp fs, all spores are round, which establishes that it is the product of Rsp that controls spore shape. (C to F) A box represents the diploid stage. Inside it, only one homologous chromosome pair is depicted with the Sad-1 and the Rsp loci indicated. A predicted ascus product of the cross is shown to the right of the diploid cell. Arrows represent SAD-1 activity, and bars represent silencing. The thickness of these lines represents relative levels of silencing or activity. (C) Unpaired rsp + resulting in cis- silencing. (D) Unpaired ectopic rsp + resulting in trans-silencing. (E) In the absence of functional product of Sad-1, development stops at the pachytene stage of meiosis I. This makes the evaluation of the presence or absence of silencing by use of Rsp impossible. (F) The dominance of the Rsp Δ allele can be suppressed in crosses heterozygous for Sad-1. See the text for details.

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FIGURE 3

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FIGURE 4

A model for meiotic silencing. An ascus at the pachytene stage of meiosis I is presented. Inside this cell, the meiotic nucleus, delineated by its nuclear membrane, apparently remains intact and is surrounded by a perinuclear structure that supports the attachment of components of the meiotic silencing apparatus. Inside the nucleus unpaired DNA (not paired DNA) induces meiotic silencing of homologous regions. The degree of unpairing determines the strength of the induction step, which presumably involves the synthesis of aberrant RNA (aRNA) and its conversion to double-stranded RNA (dsRNA) by the SAD-1 RdRP. The presence of dsRNA triggers the initiation of the meiotic RNA silencing process, which is composed of the following steps: the conversion of the dsRNA trigger into siRNAs via the SMS-3 Dicer (initiation step); the use of guide RNAs (gRNAs) as primers and single-stranded RNA (ssRNA) as a template by SAD-1 RdRP to generate dsRNA (amplification cycle); the incorporation of the gRNAs generated by both the initiation step and the amplification cycles into the RNA-inducing silencing complex (RISC), to direct the endonucleolytic cleavage of mRNA or ssRNA (effector cycle). It is possible that SAD-1 and SMS-2 maintain the silencing by participating in complexes related to the RdRP and the RNA-induced transcriptional silencing complexes detected in S. pombe, respectively.

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FIGURE 4

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