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.
Citations
-
2 1
CrossRef
-
0
Web of Science
-
1 9
Scopus
Authors (11)
Cite as
Full text
full text is not available in portal
Keywords
Details
- 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
seen 121 times
Recommended for you
Two-step mechanism of J-domain action in driving Hsp70 function
- B. Tomiczek,
- W. Delewski,
- Ł. Nierzwicki
- + 9 authors
Analysis of Reconstituted Tripartite Complex Supports Avidity-based Recruitment of Hsp70 by Substrate Bound J-domain Protein
- M. Jelen,
- I. Grochowina,
- A. Grabinska-Rogala
- + 11 authors
Functional similarities and differences among subunits of the nascent polypeptide-associated complex (NAC) of Saccharomyces cerevisiae
- B. A. Schilke,
- T. Ziegelhoffer,
- P. Domański
- + 3 authors
Structure and evolution of the 4-helix bundle domain of Zuotin, a J-domain protein co-chaperone of Hsp70
- O. Shrestha,
- R. Sharma,
- B. Tomiczek
- + 10 authors