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Comparative transcriptomics reveal different mechanisms for hyphal growth across four plant-associated dimorphic
Teeratas Kijpornyongpan1, M Catherine Aime1
1Department of Botany and Plant Pathology, Purdue University, 915 W State St, West Lafayette, IN 47907-2054, USA.
Abstract:
Fungal dimorphism is a phenomenon by which a fungus can grow both as a yeast form and a hyphal form. It is frequently related to pathogenicity as different growth forms are more suitable for different functions during a life cycle. Among dimorphic plant pathogens, the corn smut fungus Ustilago maydis serves as a model organism to understand fungal dimorphism and its effect on pathogenicity. However, there is a lack of data on whether mechanisms elucidated from model species are broadly applicable to other fungi. In this study, two non-model plant-associated species in the smut fungus subphylum (Ustilaginomycotina), Tilletiopsis washingtonensis and Meira miltonrushii, were selected to compare dimorphic mechanisms in these to those in U. maydis. We sequenced transcriptomic profiles during both yeast and hyphal growth in these two species using Tween40, a lipid mimic, as a trigger for hyphal growth. We then compared our data with previously published data from U. maydis and a fourth but unrelated dimorphic phytopathogen, Ophiostoma novo-ulmi. Comparative transcriptomics was performed to identify common genes upregulated during hyphal growth in all four dimorphic species. Intriguingly, T. washingtonensis shares the least similarities of transcriptomic alteration (hyphal growth versus yeast growth) with the others, although it is closely related to M. miltonrushii and U. maydis. This suggests that phylogenetic relatedness is not correlated with transcriptomic similarity under the same biological phenomenon. Among commonly expressed genes in the four species, genes in cell energy production and conversion, amino acid transport and metabolism and cytoskeleton are significantly enriched. Considering dimorphism genes characterized in U. maydis, as well as hyphal tip-associated genes from the literature, we found only genes encoding the cell end marker Tea4/TeaC and the kinesin motor protein Kin3 concordantly expressed in all four species. This suggests a divergence in species-specific mechanisms for dimorphic transition and hyphal growth.
Insights
Fungal dimorphism mechanisms vary across species, even closely related ones. Comparative transcriptomics reveals conserved genes in energy, metabolism, and cytoskeleton, but highlights divergent pathways for hyphal growth.
Area of Science:
- Mycology
- Plant Pathology
- Genomics
Background:
- Fungal dimorphism, the ability to switch between yeast and hyphal forms, is crucial for pathogenicity in many fungi.
- Ustilago maydis is a model organism for studying dimorphism, but its mechanisms may not apply universally to other dimorphic fungi.
- Understanding conserved and divergent dimorphic pathways is essential for broader applications in fungal biology and disease control.
Purpose of the Study:
- To investigate and compare the transcriptomic mechanisms underlying fungal dimorphism in two non-model smut fungi, Tilletiopsis washingtonensis and Meira miltonrushii.
- To identify conserved genes and pathways involved in hyphal growth across diverse dimorphic fungal species.
- To assess the correlation between phylogenetic relatedness and transcriptomic similarity in fungal dimorphism.
Main Methods:
- Transcriptomic profiling of T. washingtonensis and M. miltonrushii during yeast and hyphal growth, induced by Tween40.
- Comparative transcriptomics integrating data from Ustilago maydis and Ophiostoma novo-ulmi.
- Bioinformatic analysis to identify commonly upregulated genes during hyphal growth and enriched functional categories.
Main Results:
- Tilletiopsis washingtonensis exhibited the least transcriptomic similarity in dimorphic transition compared to other species, despite close phylogenetic relationships.
- Conserved gene enrichment was observed in cell energy, amino acid metabolism, and cytoskeleton functions across the four species.
- Only genes for cell end marker Tea4/TeaC and kinesin motor protein Kin3 were consistently upregulated in hyphal growth across all four species.
Conclusions:
- Phylogenetic relatedness does not predict transcriptomic similarity in fungal dimorphism.
- While core pathways like energy metabolism and cytoskeleton are conserved, specific mechanisms for dimorphic transition and hyphal growth diverge significantly among fungal species.
- The findings underscore the need for species-specific investigations into fungal dimorphism and pathogenicity.
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