Transcriptome analyses during fruiting body formation in Fusarium graminearum and Fusarium verticillioides reflect species life history and ecology

Sikhakolli, Usha; López-Giráldez, Francesc; Li, Ning; Common, Ralph S.; Townsend, Jeffrey P.; Trail, Frances

doi:10.1016/j.fgb.2012.05.009

Cited by 73 publications

(74 citation statements)

References 30 publications

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“…Interestingly, the PUK1 ortholog in F. verticillioides (FVEG_ 01191) has a stop codon that is equivalent to the second of two tandem stop codons in its ORF. Based on published RNA-seq data (Sikhakolli et al 2012), A-to-I editing also occurs at this site and results in the UGGUAG to UGGUGG change in FVEG_ 01191 transcripts in perithecia but not in hyphae (Fig. 6B).…”

Section: None Of the Adat Genes In F Graminearum Is Specifically Expmentioning

confidence: 68%

Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes

et al. 2016

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Yeasts and filamentous fungi do not have adenosine deaminase acting on RNA (ADAR) orthologs and are believed to lack A-to-I RNA editing, which is the most prevalent editing of mRNA in animals. However, during this study with the PUK1 (FGRRES_01058) pseudokinase gene important for sexual reproduction in Fusarium graminearum, we found that two tandem stop codons, UA1831GUA1834G, in its kinase domain were changed to UG1831GUG1834G by RNA editing in perithecia. To confirm A-to-I editing of PUK1 transcripts, strand-specific RNA-seq data were generated with RNA isolated from conidia, hyphae, and perithecia. PUK1 was almost specifically expressed in perithecia, and 90% of transcripts were edited to UG1831GUG1834G. Genome-wide analysis identified 26,056 perithecium-specific A-to-I editing sites. Unlike those in animals, 70.5% of A-to-I editing sites in F. graminearum occur in coding regions, and more than two-thirds of them result in amino acid changes, including editing of 69 PUK1-like pseudogenes with stop codons in ORFs. PUK1 orthologs and other pseudogenes also displayed stage-specific expression and editing in Neurospora crassa and F. verticillioides. Furthermore, F. graminearum differs from animals in the sequence preference and structure selectivity of A-to-I editing sites. Whereas A's embedded in RNA stems are targeted by ADARs, RNA editing in F. graminearum preferentially targets A's in hairpin loops, which is similar to the anticodon loop of tRNA targeted by adenosine deaminases acting on tRNA (ADATs). Overall, our results showed that A-to-I RNA editing occurs specifically during sexual reproduction and mainly in the coding regions in filamentous ascomycetes, involving adenosine deamination mechanisms distinct from metazoan ADARs.

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Section: None Of the Adat Genes In F Graminearum Is Specifically Expmentioning

confidence: 68%

Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes

et al. 2016

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“…These patterns of mating type gene expression promise to help illuminate the biological function of mating type and pheromone genes after fertilization and hint at roles of mating type and pheromone genes in postcrossing sexual development. Although mating loci in both mat a and mat A strains have been known for a number of years for N. crassa and closely related species (57,58,82), the functions of mating loci were unknown aside from regulating homogenic incompatibility through highly regulated expression of pheromone genes and despite the distinct expression patterns of these genes at different stages in the life cycle of N. crassa and the closely related Fusarium (20).…”

Section: Figmentioning

confidence: 99%

“…However, the sexual growth of N. crassa arises as a consequence of a communion of cells of different nuclear types; the heterokaryotic reproductive cells develop into sterile paraphyses within the perithecium or undergo karyogamy and a short diploid phase prior to the production of haploid ascospores. This heterokaryosis has made it challenging to study sexual differentiation using traditional methods based on genetic screens for mutants (13,14), and genome-wide assays so far have yielded only limited information about the genetics underlying the production of multicellular sexual reproduction structures such as perithecia (13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23).…”

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confidence: 99%

Global Gene Expression and Focused Knockout Analysis Reveals Genes Associated with Fungal Fruiting Body Development in Neurospora crassa

et al. 2014

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Fungi can serve as highly tractable models for understanding genetic basis of sexual development in multicellular organisms. Applying a reverse-genetic approach to advance such a model, we used random and multitargeted primers to assay gene expression across perithecial development in Neurospora crassa. We found that functionally unclassified proteins accounted for most upregulated genes, whereas downregulated genes were enriched for diverse functions. Moreover, genes associated with developmental traits exhibited stage-specific peaks of expression. Expression increased significantly across sexual development for mating type gene mat a-1 and for mat A-1 specific pheromone precursor ccg-4. In addition, expression of a gene encoding a protein similar to zinc finger, stc1, was highly upregulated early in perithecial development, and a strain with a knockout of this gene exhibited arrest at the same developmental stage. A similar expression pattern was observed for genes in RNA silencing and signaling pathways, and strains with knockouts of these genes were also arrested at stages of perithecial development that paralleled their peak in expression. The observed stage specificity allowed us to correlate expression upregulation and developmental progression and to identify regulators of sexual development. Bayesian networks inferred from our expression data revealed previously known and new putative interactions between RNA silencing genes and pathways. Overall, our analysis provides a finescale transcriptomic landscape and novel inferences regarding the control of the multistage development process of sexual crossing and fruiting body development in N. crassa. S hifts in gene expression over the course of development have been attributed a primary role in the unfolding of the developmental program of animals and plants (1-4). However, the genomic basis of development in a third multicellular clade, the fungi, is arguably very different and the least well understood. Estimated as comprising 1.5 to 7.1 million species, fungi have deep evolutionary origins (5-7) and diverse body plans, ranging from highly reduced unicellular species such as microsporidia and yeasts to notoriously large hyphal mats that produce multicellular fruiting bodies such as mushrooms, which feature specialized cell types (8). To address multicellular fruiting body development from a reverse-genetic approach, model fungi can provide ideal systems, as they are easily manipulated, develop fruiting structures with a few well-characterized tissue types, and have relatively small genome sizes, so numerous fungal genomes have been sequenced.Neurospora crassa is a multicellular ascomycete fungus in the family Sordariomycetes, which has been used as a genetic model organism due to its simple filamentous asexual stage (9, 10), and which exhibits promise for revealing the molecular basis of the more complex sexual development of fungi. N. crassa has 28 morphologically distinct cell types, including 14 that are finely differentiated during the development of...

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“…Fruiting body mutants are now available for many fungi other than P. anserina, including Sordaria macrospora [27], N. crassa [28], A. nidulans [29] and Coprinopsis cinerea (formely Coprinus cinereus) [30,31] and could be analyzed using similar methods. They are complementary to the now more widespread large scale analyses of transcriptomes during fruiting body development as performed in the ascomycetes Fusarium graminearum and Fusarium verticilloides [32][33][34], N. crassa [35,36], S. macrospora [37], Pyronema confluens [38], Tuber melanosporum [39][40][41], Cordyceps militaris [42] and Ophiocordyceps sinensis [43], as well as in the basidiomycetes C. cinerea [44], Moniliophthora perniciosa [45], Agrocybe aegerita [46], Lentinula edodes [47,48], Auricularia polytricha [49] and Ganoderma lucidum [50].…”

Section: Resultsmentioning

confidence: 99%

Simple Genetic Tools to Study Fruiting Body Development in Fungi

Silar¹

2014

TOMYCJ

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Unlike for animal and plant development, the molecular processes involved in shaping the multicellular fruiting bodies of fungi are almost unknown. Especially, the interplay between the mycelium, the maternal tissues and zygotic ones are seldom investigated. Here, I summarized simple genetic methods that permit to allocate site(s) of action for genes whose mutations block fruiting body development. These involve the formation of genetic mosaics and grafting, as used for many decades to study embryo development in animals and plants. They are easily implemented without the requirement of complex equipment. Yet, they provide useful information when one wants to order genes into pathways acting during fruiting body production. Examples taken from the study of the model ascomycete Podospora anserina illustrate how they can be interpreted.

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Transcriptome analyses during fruiting body formation in Fusarium graminearum and Fusarium verticillioides reflect species life history and ecology

Cited by 73 publications

References 30 publications

Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes

Genome-wide A-to-I RNA editing in fungi independent of ADAR enzymes

Global Gene Expression and Focused Knockout Analysis Reveals Genes Associated with Fungal Fruiting Body Development in Neurospora crassa

Simple Genetic Tools to Study Fruiting Body Development in Fungi

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