Molecular and comparative genomic analyses reveal evolutionarily conserved and unique features of the Schizosaccharomyces japonicus mycelial growth and the underlying genomic changes

Abstract

Fungal pathogens, from phytopathogenic fungus to human pathogens, are able to alternate between the yeast-like form and filamentous forms. This morphological transition (dimorphism) is in close connection with their pathogenic lifestyles and with their responses to changing environmental conditions. The mechanisms governing these morphogenetic conversions are still not fully understood. Therefore, we studied the filamentous growth of the less-known, non-pathogenic dimorphic fission yeast, S. japonicus, which belongs to an ancient and early evolved branch of the Ascomycota. Its RNA sequencing revealed that several hundred genes were up- or down-regulated in the hyphae compared to the yeast-phase cells. These genes belonged to different GO categories, confirming that mycelial growth is a rather complex process. The genes of transport- and metabolic processes appeared especially in high numbers among them. High expression of genes involved in glycolysis and ethanol production was found in the hyphae, while other results pointed to the regulatory role of the protein kinase A (PKA) pathway. The homologues of 49 S. japonicus filament-associated genes were found by sequence alignments also in seven distantly related dimorphic and filamentous species. The comparative genomic analyses between S. japonicus and the closely related but non-dimorphic S. pombe shed some light on the differences in their genomes. All these data can contribute to a better understanding of hyphal growth and those genomic rearrangements that underlie it.

Telomere‐to‐telomere Schizosaccharomyces japonicus genome assembly reveals hitherto unknown genome features

“…Despite being closely related and relying on many conserved genes, several major differences with S. japonicus has made this pair of sister species emerge as a powerful evolutionary cell biology system (Alam et al, 2023; Gu et al, 2015; Makarova et al, 2016, 2020; Yam et al, 2011). Furthermore, S. japonicus has become a standalone model organism for study of processes not present or tractable in other model yeasts, such as mitotic nuclear envelope breakdown and reassembly, cellular geometry scaling and the RNA interference pathway controlling both post‐transcriptional gene silencing and heterochromatin formation (Aoki et al, 2011; Chapman et al, 2022; Furuya & Niki, 2010, 2012; Gomez‐Gil et al, 2019; Gu & Oliferenko, 2019; Kinnaer et al, 2019; Klar, 2013; Lee et al, 2020; Nozaki et al, 2018; Papp et al, 2021; Pieper et al, 2020; Rutherford et al, 2022; Wang et al, 2021; Yam et al, 2013).…”

Telomere-to-telomereSchizosaccharomyces japonicusgenome assembly reveals hitherto unknown genome features

“…Despite being closely related and relying on many conserved genes, several major differences with S. japonicus has made this pair of sister species emerge as a powerful evolutionary cell biology system (Alam, Gu, Reichert, Bahler, & Oliferenko, 2023 ; Gu, Yam, & Oliferenko, 2015; Makarova et al, 2016; Makarova et al, 2020; Yam, He, Zhang, Chiam, & Oliferenko, 2011). Furthermore, S. japonicus has become a standalone model organism for study of processes not present or tractable in other yeasts (Aoki et al, 2011; Chapman, Taglini, & Bayne, 2022; Furuya & Niki, 2010, 2012; Gomez-Gil et al, 2019; Gu & Oliferenko, 2019; Kinnaer, Dudin, & Martin, 2019; Lee et al, 2020; Nozaki, Furuya, & Niki, 2018; Papp, Acs-Szabo, Batta, & Miklos, 2021; Pieper, Sprenger, Teis, & Oliferenko, 2020; Rutherford et al, 2022; Wang et al, 2021; Yam, Gu, & Oliferenko, 2013).…”

Schizosaccharomyces versatilis represents a distinct evolutionary lineage of fission yeast

“…Schizosaccharomyces pombe is a widely used model organism in diverse fields of molecular cellular biology research, which has provided fundamental insights into the regulation of cell growth and cell cycle, mitosis, meiosis, chromosome biology, RNA processing, epigenetics, cellular organisation, polarity establishment and maintenance, cytoskeleton function, and so on (Wood et al, 2002; Wood et al, 2012). More recently, another fission yeast species, Schizosaccharomyces japonicus , has emerged both as a part of a powerful composite evolutionary cell biology model system used alongside S. pombe (Gu et al, 2015; Makarova et al, 2016, 2020; Yam et al, 2011) and as a valuable standalone model organism for the study of processes not apparent or tractable in other yeasts (Aoki et al, 2011; Chapman et al, 2022; Furuya & Niki, 2010, 2012; Gomez‐Gil et al, 2019; Gu & Oliferenko, 2019; Kinnaer et al, 2019; Klar, 2013; Lee et al, 2020; Nozaki et al, 2018; Papp et al, 2021; Pieper et al, 2020; Rutherford et al, 2022; Wang et al, 2021; Yam et al, 2013).…”