Iron–Sulfur Cluster Biogenesis Chaperones: Evidence for Emergence of Mutational Robustness of a Highly Specific Protein–Protein Interaction - Publication - Bridge of Knowledge

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Iron–Sulfur Cluster Biogenesis Chaperones: Evidence for Emergence of Mutational Robustness of a Highly Specific Protein–Protein Interaction

Abstract

Biogenesis of iron–sulfur clusters (FeS) is a highly conserved process involving Hsp70 and J-protein chaperones. However, Hsp70 specialization differs among species. In most eukaryotes, including Schizosaccharomyces pombe, FeS biogenesis involves interaction between the J-protein Jac1 and the multifunctional Hsp70 Ssc1. But, in Saccharomyces cerevisiae and closely related species, Jac1 interacts with the specialized Hsp70 Ssq1, which emerged through duplication of SSC1. As little is known about how gene duplicates affect the robustness of their protein interaction partners, we analyzed the functional and evolutionary consequences of Ssq1 specialization on the ubiquitous J-protein cochaperone Jac1, by comparing S. cerevisiae and S. pombe. Although deletion of JAC1 is lethal in both species, alanine substitutions within the conserved His–Pro–Asp (HPD) motif, which is critical for Jac1:Hsp70 interaction, have species-specific effects. They are lethal in S. pombe, but not in S. cerevisiae. These in vivo differences correlated with in vitro biochemical measurements. Charged residues present in the J-domain of S. cerevisiae Jac1, but absent in S. pombe Jac1, are important for tolerance of S. cerevisiae Jac1 to HPD alterations. Moreover, Jac1 orthologs from species that encode Ssq1 have a higher sequence divergence. The simplest interpretation of our results is that Ssq1’s coevolution with Jac1 resulted in expansion of their binding interface, thus increasing the efficiency of their interaction. Such an expansion could in turn compensate for negative effects of HPD substitutions. Thus, our results support the idea that the robustness of Jac1 emerged as consequence of its highly efficient and specific interaction with Ssq1.

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Authors (11)

  • Photo of  Wojciech Delewski

    Wojciech Delewski

    • Międzyuczelniany Wydział Biotechnologii UG i GUMed Katedra Biologii Molekularnej i Komórkowej
  • Photo of  Bogumiła Paterkiewicz

    Bogumiła Paterkiewicz

    • Międzyuczelniany Wydział Biotechnologii UG i GUMed Katedra Biologii Molekularnej i Komórkowej
  • Photo of  Mateusz Manicki

    Mateusz Manicki

    • Międzyuczelniany Wydział Biotechnologii UG i GUMed Katedra Biologii Molekularnej i Komórkowej
  • Photo of  Brenda Schilke

    Brenda Schilke

    • University of Wisconsin-Madison Department of Biochemistry
  • Photo of  Bartłomiej Tomiczek

    Bartłomiej Tomiczek

    • Międzyuczelniany Wydział Biotechnologii UG i GUMed Katedra Biologii Molekularnej i Komórkowej
  • Photo of  Szymon Ciesielski

    Szymon Ciesielski

    • University of Wisconsin-Madison Department of Biochemistry
  • Photo of  Rafal Dutkiewicz

    Rafal Dutkiewicz

    • Międzyuczelniany Wydział Biotechnologii UG i GUMed Katedra Biologii Molekularnej i Komórkowej
  • Photo of  Elizabeth Craig

    Elizabeth Craig

    • University of Wisconsin-Madison Department of Biochemistry
  • Photo of  Jaroslaw Marszalek

    Jaroslaw Marszalek

    • Międzyuczelniany Wydział Biotechnologii UG i GUMed Katedra Biologii Molekularnej i Komórkowej

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Category:
Articles
Type:
artykuł w czasopiśmie wyróżnionym w JCR
Published in:
MOLECULAR BIOLOGY AND EVOLUTION no. 33, edition 3, pages 643 - 656,
ISSN: 0737-4038
Language:
English
Publication year:
2016
Bibliographic description:
Delewski W., Paterkiewicz B., Manicki M., Schilke B., Tomiczek B., Ciesielski S., Nierzwicki Ł., Czub J., Dutkiewicz R., Craig E., Marszalek J.: Iron–Sulfur Cluster Biogenesis Chaperones: Evidence for Emergence of Mutational Robustness of a Highly Specific Protein–Protein Interaction// MOLECULAR BIOLOGY AND EVOLUTION. -Vol. 33, iss. 3 (2016), s.643-656
DOI:
Digital Object Identifier (open in new tab) 10.1093/molbev/msv254
Verified by:
Gdańsk University of Technology

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