Convergent evolution of heat-inducibility during subfunctionalization of the Hsp70 gene family

Abstract

BackgroundHeat-shock proteins of the 70 kDa family (Hsp70s) are essential chaperones required for key cellular functions. In eukaryotes, four subfamilies can be distinguished according to their function and localisation in different cellular compartments: cytosol, endoplasmic reticulum, mitochondria and chloroplasts. Generally, multiple cytosol-type Hsp70s can be found in metazoans that show either constitutive expression and/or stress-inducibility, arguing for the evolution of different tasks and functions. Information about the hsp70 copy number and diversity in microbial eukaryotes is, however, scarce, and detailed knowledge about the differential gene expression in most protists is lacking. Therefore, we have characterised the Hsp70 gene family of Paramecium caudatum to gain insight into the evolution and differential heat stress response of the distinct family members in protists and to investigate the diversification of eukaryotic hsp70s focusing on the evolution of heat-inducibility.ResultsEleven putative hsp70 genes could be detected in P. caudatum comprising homologs of three major Hsp70-subfamilies. Phylogenetic analyses revealed five evolutionarily distinct Hsp70-groups, each with a closer relationship to orthologous sequences of Paramecium tetraurelia than to another P. caudatum Hsp70-group. These highly diverse, paralogous groups resulted from duplications preceding Paramecium speciation, underwent divergent evolution and were subject to purifying selection. Heat-shock treatments were performed to test for differential expression patterns among the five Hsp70-groups as well as for a functional conservation within Paramecium. These treatments induced exceptionally high mRNA up-regulations in one cytosolic group with a low basal expression, indicative for the major heat inducible hsp70s. All other groups showed comparatively high basal expression levels and moderate heat-inducibility, signifying constitutively expressed genes. Comparative EST analyses for P. tetraurelia hsp70s unveiled a corresponding expression pattern, which supports a functionally conserved evolution of the Hsp70 gene family in Paramecium.ConclusionsOur analyses suggest an independent evolution of the heat-inducible cytosol-type hsp70s in Paramecium and in its close relative Tetrahymena, as well as within higher eukaryotes. This result indicates convergent evolution during hsp70 subfunctionalization and implies that heat-inducibility evolved several times during the course of eukaryotic evolution.

Identification and analysis of HSP70 from Sepiella maindroni under stress of Vibrio harveyi and Cd 2+

“…According to their apparent molecular mass, HSPs have been classified into several families: HSP90 (85-90 kDa), HSP70 (68-73 kDa), HSP60, HSP47 and low molecular mass HSPs (16-24 kDa). Heat shock protein 70 (HSP70) is an important member of the heat shock protein superfamily and appears in almost all species except for some archaea (Tavaria et al, 1996;Krenek et al, 2013). As a kind of highly conserved protein HSP70 is associated with intracellular chaperone and extracellular immunoregulatory functions to protect cells against environmental stress, and shows tissue-/time-/ dose-dependent changes (Liu et al, 2014).…”

Identification, characterisation and molecular modelling of two AP endonucleases from base excision repair pathway in sugarcane provide insights on the early evolution of green plants

“…) or even gene conversion (Krenek et al . ), respectively. However, no evidence for the latter was observed in the dataset.…”

“…Most of the x values from pair-wise sequence comparisons were below 1 (dN/ dS < 1), which is expected from sub-functionalised gene copies showing transcriptional divergence (Roulin et al 2012). A higher number of synonymous mutations and high sequence similarity can also probably be due to protein functional constraints (Yang et al 2000) or even gene conversion (Krenek et al 2013), respectively. However, no evidence for the latter was observed in the dataset.…”

Expression patterns and structural modelling of Hsp70 and Hsp90 in a fish-borne zoonotic nematode Anisakis pegreffii

“…It has been used with all monophyletic groups of the Metazoa, with available sequences consistently recovered for some species (Budin and Philippe, 1998). Hsp70 has also been used for phylogenetic analysis of different protozoan parasites (Fraga et al, 2010) with caution, because of paralogy distorting phylogenetic relationships (Krenek et al, 2013). Hsp90 is a proper phylogenetic marker analyzed in a variety of organisms and has a good balance of sequence conservation and diversity (Gupta, 1995).…”

“…2). ApHsp70 showed high amino acid sequence similarity with other known Hsp70s, especially in the regions of Hsp70 family signatures (I-III), highly conserved regions present in all Hsp70 family members (Krenek et al, 2013). The Hsp70C-terminal region of EEVD and the potential non-organelle eukaryotic consensus motif (RARFEEL) were commonly found in the five species.…”