A gene associated with filamentous growth in Ophiostoma novo-ulmi has RNA-binding motifs and is similar to a yeast gene involved in mRNA splicing

Pereira, Verónica; Royer, John C.; Hintz, William E.; Field, Deborah J.; Bowden, Christine G.; Kokurewicz, Karl; Hubbes, M.; Horgen, Paul A.

doi:10.1007/s002940050015

Cited by 17 publications

(24 citation statements)

References 51 publications

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“…In addition, research in other fungi could unveil further support for the connection between mRNA traYcking and polar growth. Promising examples are the elm pathogen Ophiostoma novo-ulmi or A. nidulans where defects in polar growth were observed due to loss of RRM-containing proteins Col1 or SwoK, respectively (Pereira et al 2000;Shaw and Upadhyay 2005). Furthermore, loss of SwoC1 from A. nidulans caused defects in endocytosis and polarity.…”

Section: Discussionmentioning

confidence: 99%

mRNA trafficking in fungi

Zarnack

Feldbrügge

2007

Mol Genet Genomics

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Fungal growth depends on active transport of macromolecules along the actin and/or microtubule cytoskeleton. Thereby, molecular cargo such as proteins, lipids, and mRNAs is targeted to defined subcellular regions. Active transport and localisation of mRNAs mediate localised translation so that protein synthesis occurs where protein function is required. In Saccharomyces cerevisiae, actomyosin-dependent mRNA trafficking participates in polar growth, asymmetric cell division, targeting of membrane proteins and import of mitochondrial proteins. The best-understood example is transport of ASH1 mRNA to the distal pole of the incipient daughter cell. cis-acting RNA sequences are recognised by the RNA-binding protein She2p that is connected via the adaptor She3p to the molecular motor Myo4p. Local translation at the poles of daughter cells causes Ash1p to accumulate predominantly in nuclei of daughter cells, where this transcription factor inhibits mating-type switching. Recently, it was also shown that actomyosin-dependent ASH1 mRNA transport directs tip cell-specific gene expression in filaments of the human pathogen Candida albicans. Furthermore, in the plant pathogen Ustilago maydis microtubule-dependent shuttling of the RNA-binding protein Rrm4 is essential to determine the axis of polarity in infectious filaments. Thus, mRNA trafficking appears to be universally required for polar growth of fungi.

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Section: Discussionmentioning

confidence: 99%

mRNA trafficking in fungi

Zarnack

Feldbrügge

2007

Mol Genet Genomics

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“…Moreover, quorum sensing has been shown in O. ulmi, O. piceae and O. floccosum [15, 17, 18]. Until now, only two genes have been identified as being involved in the dimorphism in O. novo-ulmi , namely COL1 [19] and an as yet uncharacterized gene that also affects asexual sporulation (synnematospores) and pathogenicity [20, 21]. The knockout col1 mutant exhibits reduced mycelial growth, whereas yeast growth is barely affected by the mutation [19].…”

Section: Introductionmentioning

confidence: 99%

From yeast to hypha: defining transcriptomic signatures of the morphological switch in the dimorphic fungal pathogen Ophiostoma novo-ulmi

Nigg

Bernier

2016

BMC Genomics

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BackgroundYeast-to-hypha transition is a major morphological change in fungi. Molecular regulators and pathways that are involved in this process have been extensively studied in model species, including Saccharomyces cerevisiae. The Mitogen-Actived Protein Kinase (MAPK) cascade, for example, is known to be involved in the yeast-to-pseudohypha switch. Yet the conservation of mechanisms regulating such morphological changes in non-model fungi is still poorly understood. Here, we investigate cell remodeling and transcriptomic modifications that occur during this morphological switch in the highly aggressive ascomycete fungus Ophiostoma novo-ulmi, the causal agent of Dutch elm disease.ResultsUsing a combination of light microscopy, scanning electron microscopy and flow cytometry, we demonstrate that the morphological switch occurs in less than 27 h, with phenotypic cell modifications being detected within the first 4 h. Using RNAseq, we found that over 22% of the genome of O. novo-ulmi is differentially expressed during the transition. By performing clustering analyses of time series gene expression data, we identified several sets of genes that are differentially expressed according to distinct and representative temporal profiles. Further, we found that several genes that are homologous to S. cerevisiae MAPK genes are regulated during the yeast-to-hypha transition in O. novo-ulmi and mostly over-expressed, suggesting convergence in gene expression regulation.ConclusionsOur results are the first report of a time-course experiment monitoring the morphological transition in a non-model Sordariomycota species and reveal many genes of interest for further functional investigations of fungal dimorphism.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3251-8) contains supplementary material, which is available to authorized users.

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“…Currently, only a few critical RNA-binding proteins have been identified, such as the RRM (RNA recognition motif) proteins Col1 and Rrm4 from the elm pathogen Ophiostoma novo-ulmi and U. maydis, respectively. Deletion of the corresponding genes leads to reduced virulence in both fungi (Pereira et al 2000;Becht et al 2005). A key step toward understanding the function of these regulatory factors is a detailed knowledge of their RNA binding capacity.…”

Section: Discussionmentioning

confidence: 99%

Tandem KH domains of Khd4 recognize AUACCC and are essential for regulation of morphology as well as pathogenicity inUstilago maydis

Vollmeister¹,

Haag²,

Zarnack³

et al. 2009

RNA

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RNA-binding proteins constitute key factors of the post-transcriptional machinery. These regulatory proteins recognize specific elements within target transcripts to promote, for example, maturation, translation, or stability of mRNAs. In Ustilago maydis, evidence is accumulating that post-transcriptional processes are important to determine pathogenicity. Deletion of khd4, encoding a predicted RNA-binding protein with five K homology (KH) domains, causes aberrant cell morphology and reduced virulence. Here, we demonstrate that Khd4 recognizes the sequence AUACCC in vivo via its tandem KH domains 3 and 4. This sequence most likely functions as a regulatory RNA element in U. maydis, since it accumulates in 39 untranslated regions. Consistently, an independent mRNA expression profiling approach revealed that the binding motif is significantly enriched in transcripts showing altered expression levels in khd4D strains. Since the vast majority of potential Khd4 target mRNAs exhibit increased amounts in deletion mutants, Khd4 might promote mRNA instability. Mutants that fail to bind AUACCC resemble deletion mutants, which exhibit altered cell morphology, disturbed filamentous growth, and severely reduced virulence. Hence, RNA binding is essential for function of Khd4, stressing the importance of post-transcriptional control in regulating morphology and pathogenicity.

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A gene associated with filamentous growth in Ophiostoma novo-ulmi has RNA-binding motifs and is similar to a yeast gene involved in mRNA splicing

Cited by 17 publications

References 51 publications

mRNA trafficking in fungi

mRNA trafficking in fungi

From yeast to hypha: defining transcriptomic signatures of the morphological switch in the dimorphic fungal pathogen Ophiostoma novo-ulmi

Tandem KH domains of Khd4 recognize AUACCC and are essential for regulation of morphology as well as pathogenicity inUstilago maydis

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