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Progressive loss of hybrid histidine kinase genes during the evolution of budding yeasts (Saccharomycotina)

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Abstract

Two-component systems (TCSs) are widely distributed cell signaling pathways used by both prokaryotic and eukaryotic organisms to cope with a wide range of environmental cues. In fungi, TCS signaling routes, that mediate perception of stimuli, correspond to a multi-step phosphorelay between three protein families including hybrid histidine kinases (HHK), histidine phosphotransfer proteins (HPt) and response regulators (RR). The best known of these fungal transduction pathways remains the Sln1(HHK)–Ypd1(HPt)–Ssk1(RR) system that governs the high-osmolarity glycerol (HOG) mitogen-activated protein kinase (MAPK) pathway for osmo-adaptation in Saccharomyces cerevisiae. Although recent advances have provided a preliminary overview of the distribution of TCS proteins in the kingdom Fungi, underlying mechanisms that drive the remarkable diversity among HHKs and other TCS proteins in different fungal lineages remain unclear. More precisely, evolutionary paths that led to the appearance, transfer, duplication, and loss of the corresponding TCS genes in fungi have never been hitherto addressed. In the present study, we were particularly interested in studying the distribution of TCS modules across the so-called “budding yeasts clade” (Saccharomycotina) by interrogating the genome of 82 species. With the exception of the emergence of an additional RR (named Srr1) in the fungal CTG clade, TCS proteins Ypd1 (HPt), Ssk1 (RR), Skn7 (RR), and Rim15 (RR) are well conserved within the Saccharomycotina. Surprisingly, some species from the basal lineages, especially Lipomyces starkeyi, harbor several filamentous-type HHKs that appear as relict genes that have been likely retained from a common ancestor of Saccharomycotina. Overall, this analysis revealed a progressive diminution of the initial pool of HHK-encoding genes during Saccharomycotina yeast evolution.

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Acknowledgements

We acknowledge Pr. J-P Latgé and Pr. B. Dujon (Institut Pasteur, Paris, France) for fruitful discussions and critical reading of this manuscript. We would like to thank the Department of Energy Joint Genome Institute for making available a large series of yeast genomes and also J. Spatafora, J. Magnuson and D. Cullen as PIs of the MycoCosm program for allowing the use of sequences of Cephaloascus albidus, Cephaloascus fragrans, Blastobotrys (Sympodiomyces) attinorum, and Blastobotrys (Trichomonascus) petasosporus. J.L.L. thanks MINECO for the Severo Ochoa Excellence Accreditation (SEV-2016-0644). J.A.O. is supported by research project AGL2011-55971-R of the Spanish National Research Plan and by additional institutional support from the Public University of Navarre.

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Authors and Affiliations

  1. Groupe d’Etude des Interactions Hôte-Pathogène, GEIHP, EA3142, UNIV Angers, UNIV Brest, Université Bretagne-Loire, Angers, France

    Anaïs Hérivaux, Patrick Vandeputte, Jean-Philippe Bouchara, Amandine Gastebois & Nicolas Papon

  2. Genome Analysis Platform, CIC bioGUNE, Derio, Spain

    José L. Lavín

  3. Biomolécules et Biotechnologies Végétales, EA2106, Université François Rabelais de Tours, Tours, France

    Thomas Dugé de Bernonville

  4. Laboratoire de Parasitologie-Mycologie, Centre Hospitalier Universitaire d’Angers, Angers, France

    Patrick Vandeputte & Jean-Philippe Bouchara

  5. Genetics and Microbiology Research Group, Department of Agrarian Production, Public University of Navarre, Pamplona, Spain

    José A. Oguiza

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  1. Anaïs Hérivaux
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  2. José L. Lavín
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  3. Thomas Dugé de Bernonville
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  6. Amandine Gastebois
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  7. José A. Oguiza
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  8. Nicolas Papon
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Contributions

AH, TDDB and PV compiled all sequences. JLL and JAO performed phylogenetic analyses. AG and NP conceived and managed the project. NP and JPB wrote the manuscript.

Corresponding author

Correspondence to Nicolas Papon.

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Communicated by M. Kupiec.

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Hérivaux, A., Lavín, J.L., de Bernonville, T.D. et al. Progressive loss of hybrid histidine kinase genes during the evolution of budding yeasts (Saccharomycotina). Curr Genet 64, 841–851 (2018). https://doi.org/10.1007/s00294-017-0797-1

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