An RNA Recognition Motif-Containing Protein Functions in Meiotic Silencing by Unpaired DNA

Samarajeewa, Dilini A; Manitchotpisit, Pennapa; Henderson, Miranda; Xiao, Hua; Rehard, David G.; Edwards, Kevin A.; Shiu, Patrick; Hammond, Thomas M.

doi:10.1534/g3.117.041848

Cited by 11 publications

(8 citation statements)

References 59 publications

(134 reference statements)

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“…ZML2 also plays a role in wound-induced lignification as a transcriptional repressor for the lignin biosynthesis in maize ( Velezbermudez et al, 2015 ). The RNA recognition motif-containing ( RRM ), one of the largest families of RNA binding proteins gene widely detected not only in plants and animals, but also in fungus, plays an important role in RNA recognition and editing ( Fetka et al, 2000 ; Rebay et al, 2000 ; Samarajeewa et al, 2017 ). In plants, as documented in model plants of Arabidopsis and maize, RRM is required for plastid and mitochondrial RNA editing ( Sun et al, 2013 ), and previous studies showed that an organelle RRM mutant exhibits slower growth and delayed flowering time ( Shi et al, 2016 ).…”

Section: Resultsmentioning

confidence: 99%

Transcriptomes Divergence of Ricotia lunaria Between the Two Micro-Climatic Divergent Slopes at “Evolution Canyon” I, Israel

et al. 2018

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As one of the hotspot regions for sympatric speciation studies, Evolution Canyon (EC) became an ideal place for its high level of microclimatic divergence interslopes. In this study, to highlight the genetic mechanisms of sympatric speciation, phenotypic variation on flowering time and transcriptomic divergence were investigated between two ecotypes of Ricotia lunaria, which inhabit the opposite temperate and tropical slopes of EC I (Lower Nahal Oren, Mount Carmel, Israel) separated by 100 m at the bottom of the slopes. Growth chamber results showed that flowering time of the ecotype from south-facing slope population # 3 (SFS 3) was significantly 3 months ahead of the north-facing slope population # 5 (NFS 5). At the same floral development stage, transcriptome analysis showed that 1,064 unigenes were differentially expressed between the two ecotypes, which enriched in the four main pathways involved in abiotic and/or biotic stresses responses, including flavonoid biosynthesis, α-linolenic acid metabolism, plant–pathogen interaction and linoleic acid metabolism. Furthermore, based on Ka/Ks analysis, nine genes were suggested to be involved in the ecological divergence between the two ecotypes, whose homologs functioned in RNA editing, ABA signaling, photoprotective response, chloroplasts protein-conducting channel, and carbohydrate metabolism in Arabidopsis thaliana. Among them, four genes, namely, SPDS1, FCLY, Tic21 and BGLU25, also showed adaptive divergence between R. lunaria and A. thaliana, suggesting that these genes could play an important role in plant speciation, at least in Brassicaceae. Based on results of both the phenotype of flowering time and comparative transcriptome, we hypothesize that, after long-time local adaptations to their interslope microclimatic environments, the molecular functions of these nine genes could have been diverged between the two ecotypes. They might differentially regulate the expression of the downstream genes and pathways that are involved in the interslope abiotic stresses, which could further diverge the flowering time between the two ecotypes, and finally induce the reproductive isolation establishment by natural selection overruling interslope gene flow, promoting sympatric speciation.

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Section: Resultsmentioning

confidence: 99%

Transcriptomes Divergence of Ricotia lunaria Between the Two Micro-Climatic Divergent Slopes at “Evolution Canyon” I, Israel

et al. 2018

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“…Thus far, none of the known MSUD proteins are essential for cell viability (Samarajeewa et al 2017). As demonstrated in Figure 3, if sad-8 is functional during the asexual stage (a speculation based on its expression profile), it is unlikely to be a crucial factor in growth and development, as the corresponding deletion strain is proficient in linear growth and conidial production.…”

Section: Sad-8 Is Not Required For Either Vegetative Growth or Sexualmentioning

confidence: 99%

“…SAD-2 is a scaffold protein responsible for bringing SAD-1 and others to the perinuclear region (Shiu et al 2006;Decker et al 2015). The precise functions of SAD-4, SAD-5, and SAD-7 are unclear, although the first two are necessary for siRNA biogenesis and the last one may coordinate nuclear and extranuclear silencing events (Hammond et al 2013a, b;Samarajeewa et al 2017).…”

Section: Introductionmentioning

confidence: 99%

An NCBP3-Domain Protein Mediates Meiotic Silencing by Unpaired DNA

Boone

Xiao

Vierling

et al. 2020

G3 Genes|Genomes|Genetics

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In the filamentous fungus Neurospora crassa, genes unpaired during meiosis are silenced by a process known as meiotic silencing by unpaired DNA (MSUD). MSUD utilizes common RNA interference (RNAi) proteins, such as Dicer and Argonaute, to target homologous mRNAs for silencing. Previously, we demonstrated that nuclear cap-binding proteins NCBP1 and NCBP2 are involved in MSUD. We report here that SAD-8, a protein similar to human NCBP3, also mediates silencing. Although SAD-8 is not essential for either vegetative or sexual development, it is required for MSUD. SAD-8 localizes predominantly in the nucleus and interacts with both NCBP1 and NCBP2. Similar to NCBP1 and NCBP2, SAD-8 interacts with a component (Argonaute) of the perinuclear meiotic silencing complex (MSC), further implicating the involvement of cap-binding proteins in silencing.

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“…The 6-day-old perithecia were fixed in a solution of 100 mM PIPES (pH 6.9), 10 mM EGTA, 5 mM MgSO4 and 4% paraformaldehyde for 20 minutes at room temperature as previously described (32). Perithecia were subsequently washed and stored in sodium phosphate buffer (80 mM Na2HPO4 + 20 mM NaH2PO4).…”

Section: Assaying Hh1-gfp Expressionmentioning

confidence: 99%

Recombination-independent recognition of DNA homology for meiotic silencing in Neurospora crassa

Rhoades

Cecere

Hammond

et al. 2019

Preprint

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Pairing of homologous chromosomes represents a key aspect of meiosis in nearly all sexually reproducing species. While meiotic pairing requires the formation of double-strand DNA breaks in some organisms, in many others it can proceed in the apparent absence of DNA breakage and recombination. The mechanistic nature of such recombination-independent pairing represents a fundamental question in molecular biology.Using "meiotic silencing by unpaired DNA" (MSUD) in the fungus Neurospora crassa as a model system, we demonstrate the existence of a cardinally new solution to the problem of inter-chromosomal homology recognition during meiosis. Here we take advantage of the unique ability of MSUD to efficiently detect and silence (by RNA interference) any relatively short DNA fragment lacking a homologous allelic partner. We show that MSUD does not require the function of eukaryotic RecA proteins and the type II topoisomeraselike protein Spo11. We further show that MSUD can recognize patterns of weak interspersed homology in which short units of sequence identity are arrayed with a periodicity of 11 base-pairs (bp). Taken together, these results reveal the function of a recombination-independent homology-directed process in guiding the expression of small interfering RNAs and suggest that meiotic chromosomes can be evaluated for sequence homology at base-pair resolution by a mechanism that operates on intact DNA molecules. MAIN TEXTProper pairing of homologous chromosomes in meiosis is essential for ensuring fertility and preventing birth defects. While the general role of recombination during meiosis has been firmly established (1), many organisms (including the fruit fly D. melanogaster and the roundworm C. elegans) feature "non-canonical" programs in which homologous chromosomes can identify one another in the apparent absence of DNA breakage and recombination (1). Such recombination-independent pairing was previously suggested to rely on various forms of "bar-coding" by transcription, proteins, RNAs, or landmark genomic features such as centromeres and telomeres (2-6). Alternatively, there exists a possibility that recombination-independent pairing may be guided directly at the level of DNA homology (7, 8), but the experimental evidence for this type of homologous inter-chromosomal communication in meiosis remains sparse (9).In the model fungus Neurospora crassa, a process known as meiotic silencing by unpaired DNA (MSUD) can identify non-homologous DNA sequences present at allelic chromosomal positions (10). Once detected, such sequences undergo transient post-transcriptional silencing by RNA interference (10). The ability of MSUD to detect non-homologous sequences as short as ~1 kbp, irrespective of nucleotide composition and transcriptional capacity, strongly suggests that a general homology search is involved (11). Furthermore, because MSUD occurs within a relatively short time interval (a few hours at the beginning of prophase I), the underlying search mechanism must be very efficient.Previous studies have ident...

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An RNA Recognition Motif-Containing Protein Functions in Meiotic Silencing by Unpaired DNA

Cited by 11 publications

References 59 publications

Transcriptomes Divergence of Ricotia lunaria Between the Two Micro-Climatic Divergent Slopes at “Evolution Canyon” I, Israel

Transcriptomes Divergence of Ricotia lunaria Between the Two Micro-Climatic Divergent Slopes at “Evolution Canyon” I, Israel

An NCBP3-Domain Protein Mediates Meiotic Silencing by Unpaired DNA

Recombination-independent recognition of DNA homology for meiotic silencing in Neurospora crassa

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