Functional Profiling of Transcription Factor Genes in<i>Neurospora crassa</i>

Carrillo, Alexander J.; Schacht, Patrick; Cabrera, Ilva E.; Blahut, Johnathon; Prudhomme, Loren; Dietrich, Sarah; Bekman, Thomas; Mei, Jennifer; Carrera, Cristian; Chen, Vivian; Clark, Isaiah; Fierro, Gerardo; Ganzen, Logan; Orellana, Jose; Wise, Shelby; Yang, Kyeongcheol; Zhong, Hui; Borkovich, Katherine A.

doi:10.1534/g3.117.043331

Cited by 55 publications

(76 citation statements)

References 78 publications

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“…An earlier study had estimated the number of TFs in Neurospora to be 182 (Borkovich et al, 2004), a number that has been recognized as larger in recent analyses (Carrillo et al, 2017; Weirauch et al, 2014). Thus, we took a conservative list comprising 253 TFs included in the previous studies and inquired for the presence of phospho-sites in the corresponding proteins.…”

Section: Resultsmentioning

confidence: 99%

Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition inNeurospora crassa

Horta

Thieme

Gao

et al. 2019

Preprint

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Fungal plant cell wall degradation processes are governed by complex regulatory mechanisms, allowing the organisms to adapt their metabolic program with high specificity to the available substrates. While the uptake of representative plant cell wall mono- and disaccharides is known to induce specific transcriptional and translational responses, the processes related to early signal reception and transduction remain largely unkown. A fast and reversible way of signal transmission are post-translational protein modifications, such as phosphorylations, which could initiate rapid adaptations of the fungal metabolism to a new condition. To elucidate how changes in the initial substrate recognition phase of Neurospora crassa affect the global phosphorylation pattern, phospho-proteomics was performed after a short (2 minutes) induction period with several plant cell wall-related mono- and disaccharides. The MS/MS-based peptide analysis revealed large-scale substrate-specific protein phosphorylation and de-phosphorylations. Using the proteins identified by MS/MS, a protein-protein-interaction (PPI) network was constructed. The variance in phosphorylation of a large number of kinases, phosphatases and transcription factors indicate the participation of many known signaling pathways, including circadian responses, two-component regulatory systems, MAP kinases as well as the cAMP-dependent and heterotrimeric G-protein pathways. Adenylate cyclase, a key component of the cAMP pathway, was identified as a potential hub for carbon source-specific differential protein interactions. In addition, four phosphorylated F-Box proteins were identified, two of which, Fbx-19 and Fbx-22, were found to be involved in carbon catabolite repression responses. Overall, these results provide unprecedented and detailed insights into a so far less well known stage of the fungal response to environmental cues and allow to better elucidate the molecular mechanisms of sensory perception and signal transduction during plant cell wall degradation.

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Section: Resultsmentioning

confidence: 99%

Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition inNeurospora crassa

Horta

Thieme

Gao

et al. 2019

Preprint

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“…Notably, out of the 17 TFs identified (S6 Table, S8 Fig), 11 were also FPR1 targets. Furthermore, Pa_1_16860 and Pa_3_1720 orthologs in N. crassa [50,51] and A. nidulans [52,53] influence sexual development (S6 Table). On the same note, the N. crassa ortholog of Pa_1_22930 plays a significant role in sexual development [51].…”

Section: Resultsmentioning

confidence: 99%

“…Furthermore, Pa_1_16860 and Pa_3_1720 orthologs in N. crassa [50,51] and A. nidulans [52,53] influence sexual development (S6 Table). On the same note, the N. crassa ortholog of Pa_1_22930 plays a significant role in sexual development [51]. Yet, we did not identify in this down-regulated CDS set, the P. anserina’s orthologs of most of the N. crassa TFs that have been found to be differentially expressed during sexual development [50,54–57].…”

Section: Resultsmentioning

confidence: 99%

A RID-like cytosine methyltransferase homologue controls sexual development in the fungusPodospora anserina

Grognet

Timpano

Carlier

et al. 2019

Preprint

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21DNA methyltransferases are ubiquitous enzymes conserved in bacteria, plants and 22 opisthokonta. These enzymes, which methylate cytosines, are involved in numerous 23 biological processes, notably development. In mammals and higher plants, methylation 24 patterns established and maintained by the cytosine DNA methyltransferases (DMTs) are 25 essential to zygotic development. In fungi, some members of an extensively conserved 26 fungal-specific DNA methyltransferase class are both mediators of the Repeat Induced Point 27 mutation (RIP) genome defense system and key players of sexual reproduction. Yet, no DNA 28 methyltransferase activity of these purified RID (RIP deficient) proteins could be detected in 29 vitro. These observations led us to explore how RID-like DNA methyltransferase encoding 30 genes would play a role during sexual development of fungi showing very little genomic DNA 31 methylation, if any. 32To do so, we used the model ascomycete fungus P. anserina. We identified the 33 PaRid gene, encoding a RID-like DNA methyltransferase and constructed knocked-out 34ΔPaRid defective mutants. Crosses involving P. anserina ΔPaRid mutants are sterile. Our 35 results show that, although gametes are readily formed and fertilization occurs in a ΔPaRid 36 background, sexual development is blocked just before the individualization of the dikaryotic 37 cells leading to meiocytes. Complementation of ΔPaRid mutants with ectopic alleles of 38 PaRid, including 39 demonstrated that the catalytic motif of the putative PaRid methyltransferase is essential to 40 ensure proper sexual development and that the expression of PaRid is spatially and 41 temporally restricted. A transcriptomic analysis performed on mutant crosses revealed an 42 overlap of the PaRid-controlled genetic network with the well-known mating-types gene 43 developmental pathway common to an important group of fungi, the Pezizomycotina. 44 45 46 3 Author Summary 47Sexual reproduction is considered to be essential for long-term persistence of 48 eukaryotic species. Sexual reproduction is controlled by strict mechanisms governing which 49 haploids can fuse (mating) and which developmental paths the resulting zygote will follow. In 50 mammals, differential genomic DNA methylation patterns of parental gametes, known as 51 'DNA methylation imprints' are essential to zygotic development, while in plants, global 52 genomic demethylation often results in female-sterility. Although animal and fungi are 53 evolutionary related, little is known about epigenetic regulation of gene expression and 54 development in multicellular fungi. Here, we report on a gene of the model fungus Podospora 55 anserina, encoding a protein called PaRid that looks like a DNA methyltrasferase. We 56 showed that expression of the catalytically functional version of the PaRid protein is required 57 in the maternal parental strain to form zygotes. By establishing the transcriptional profile of 58PaRid mutant strain, we identified a set of PaRid direct and/or indirect target genes. Half o...

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“…Linear growth rates for the transcription factor knockouts reported by Carrillo et al (2017) were compared via T-test for knockouts showing altered cold shock responses vs those showing no alteration to the response. One possible association between growth rate and altered cold shock phenotype was found for the knockouts displaying a dense phenotype which showed statistically faster growth rates than those with no alterations to cold shock (T-test, p=0.019).…”

Section: Resultsmentioning

confidence: 99%

Cold shock as a screen for genes involved in cold acclimatization in Neurospora crassa

Watters

Manzanilla

Howell

et al. 2018

Preprint

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13When subjected to rapid drops of temperature (cold shock), Neurospora responds with a 14 dramatic, but temporary shift in its branching pattern. While the cold shock response has been 15 described morphologically, it has yet to be examined genetically. This project aims to begin the 16 genetic characterization of the cold shock response and the associated acclimatization to cold 17 environments. We report here the results of a screen of mutants from the Neurospora knockout 18 library for alterations in their morphological response to cold shock and thus, their ability to 19 acclimatize to the cold. Three groups of knockouts were selected to be subject to this screen: 20 genes previously suspected to be involved in hyphal development as well as knockouts resulting 21 in morphological changes; transcription factors; and genes homologous to E. coli genes known to showed altered cold shock responses in Neurospora -suggesting that the response in these two 26 organisms is largely shared in common. . CC-BY 4.0 International license peer-reviewed) is the author/funder. It is made available under a The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/259580 doi: bioRxiv preprint first posted online Feb. 4, 2018; 2 The environmental conditions that life must contend with can vary widely. Organisms have 1 evolved a wide range of mechanisms for contending with these changing conditions. For the 2 filamentous fungus Neurospora, growth continues through nearly the entire range of 3 temperatures (above freezing) that is observed in this environment. Although the rate of tip 4 extension varies linearly with temperature (Watters et al 2000), the branch density (the statistical 5 distribution of distances between branch sites along a linear growing hypha) remains constant 6 across this range (Watters et al. 2000) allowing the fungus to continue to infiltrate its 7 environment at the same density. Temperatures progressing through this range would be 8 expected to have dramatic impacts on enzyme activity generally (and thus overall metabolism), 9 but also directly on features critical to growth such as membrane fluidity, DNA/RNA stability 10 and the rates of transcription and translation. 12Response to cold shock 13 When the apparent independence of branching and temperature is tested by rapid temperature temperature, the colony returns to lateral branching, termed the "Recovery" phase. Growth in 22 this phase of the response resembles that which would be seen had the colony been grown at 4°C 23 continuously. The same density is observed for growth subjected to constant incubation at 4°C 24(or any other fixed temperature) as well (Watters et al 2000). Thus, the cold shock response 25 appears to be a temporary disturbance to a homeostatic system which maintains branch density at 26 a constant, evolutionarily favored, value. 28Thus, Neurospora appears to incorporate a system which has the effect of maintaining 29 homeostasis for critical cellular characteristics. At least one impact of this...

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Functional Profiling of Transcription Factor Genes inNeurospora crassa

Cited by 55 publications

References 78 publications

Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition inNeurospora crassa

Broad substrate-specific phosphorylation events are associated with the initial stage of plant cell wall recognition inNeurospora crassa

A RID-like cytosine methyltransferase homologue controls sexual development in the fungusPodospora anserina

Cold shock as a screen for genes involved in cold acclimatization in Neurospora crassa

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