Abstract
Mitogen activated protein kinase (MAPK) signaling pathways execute essential functions in eukaryotic organisms by transducing extracellular stimuli into adaptive cellular responses. In the fission yeast model Schizosaccharomyces pombe the cell integrity pathway (CIP) and its core effector, MAPK Pmk1, play a key role during regulation of cell integrity, cytokinesis, and ionic homeostasis. Schizosaccharomyces japonicus, another fission yeast species, shows remarkable differences with respect to S. pombe, including a robust yeast to hyphae dimorphism in response to environmental changes. We show that the CIP MAPK module architecture and its upstream regulators, PKC orthologs Pck1 and Pck2, are conserved in both fission yeast species. However, some of S. pombe’s CIP-related functions, such as cytokinetic control and response to glucose availability, are regulated differently in S. japonicus. Moreover, Pck1 and Pck2 antagonistically regulate S. japonicus hyphal differentiation through fine-tuning of Pmk1 activity. Chimeric MAPK-swapping experiments revealed that S. japonicus Pmk1 is fully functional in S. pombe, whereas S. pombe Pmk1 shows a limited ability to execute CIP functions and promote S. japonicus mycelial development. Our findings also suggest that a modified N-lobe domain secondary structure within S. japonicus Pmk1 has a major influence on the CIP signaling features of this evolutionarily diverged fission yeast.
Highlights
To explore the evolutionary conservation of the cell integrity pathway within the fission yeast clade, we obtained a S. japonicus strain deleted in Mitogen activated protein kinase (MAPK) Pmk1 by homologous recombination
We have investigated the signaling architecture and biological functions of the cell integrity MAPK signaling pathway (CIP) in the dimorphic fission yeast
Comparative phenotypic assessment of S. japonicus and S. pombe pmk1∆ mutants revealed that control of ionic homeostasis and cell wall integrity is a conserved regulatory feature of the cell integrity pathway (CIP) in both fission yeast species
Summary
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. We have recently described that the stress-responsive functions of the SAPK pathway in S. pombe are largely conserved in S. japonicus, and include regulation of G2/M progression during the cell cycle, cellular adaptation to multiple stress conditions, and the positive control of chronological lifespan and sexual differentiation [23]. The precise biological functions of the S. japonicus CIP during growth, stress, and mycelial differentiation, together with the possible role of PKC orthologs Pck and Pck as upstream regulators of this signaling cascade, are currently unknown. In this work we show that, despite the existence of some degree of functional conservation, certain biological features of CIP signaling have evolved separately in S. japonicus and S. pombe, and that Pck and Pck modulate Pmk MAPK activity during S. japonicus dimorphic switch in an opposite fashion. Pmk likely played a significant role in modulating CIP signaling to cope with the specific developmental requirements of this fission yeast species
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