A genomewide analysis of genes for the heat shock protein 70 chaperone system in the ascidian Ciona intestinalis

Abstract

Molecular chaperones play crucial roles in various aspects of the biogenesis and maintenance of proteins in the cell. The heat shock protein 70 (HSP70) chaperone system, in which HSP70 proteins act as chaperones, is one of the major molecular chaperone systems conserved among a variety of organisms. To shed light on the evolutionary history of the constituents of the chordate HSP70 chaperone system and to identify all of the components of the HSP70 chaperone system in ascidians, we carried out a comprehensive survey for HSP70s and their cochaperones in the genome of Ciona intestinalis. We characterized all members of the Ciona HSP70 superfamily, J-proteins, BAG family, and some other types of cochaperones. The Ciona genome contains 8 members of the HSP70 superfamily, all of which have human and protostome counterparts. Members of the STCH subfamily of the HSP70 family and members of the HSPA14 subfamily of the HSP110 family are conserved between humans and protostomes but were not found in Ciona. The Ciona genome encodes 36 J-proteins, 32 of which belong to groups conserved in humans and protostomes. Three proteins seem to be unique to Ciona. J-proteins of the RBJ group are conserved between humans and Ciona but were not found in protostomes, whereas J-proteins of the DNAJC14, ZCSL3, FLJ13236, and C21orf55 groups are conserved between humans and protostomes but were not found in Ciona. J-proteins of the sacsin group seem to be specific to vertebrates. There is also a J-like protein without a conserved HPD tripeptide motif in the Ciona genome. The Ciona genome encodes 3 types of BAG family proteins, all of which have human and protostome counterparts (BAG1, BAG3, and BAT3). BAG2 group is conserved between humans and protostomes but was not found in Ciona, and BAG4 and BAG5 groups seem to be specific to vertebrates. Members for SIL1, UBQLN, UBADC1, TIMM44, GRPEL, and Magmas groups, which are conserved between humans and protostomes, were also found in Ciona. No Ciona member was retrieved for HSPBP1 group, which is conserved between humans and protostomes. For several groups of the HSP70 superfamily, J-proteins, and other types of cochaperones, multiple members in humans are represented by a single counterpart in Ciona. These results show that genes of the HSP70 chaperone system can be distinguished into groups that are shared by vertebrates, Ciona, and protostomes, ones shared by vertebrates and protostomes, ones shared by vertebrates and Ciona, and ones specific to vertebrates, Ciona, or protostomes. These results also demonstrate that the components of the HSP70 chaperone system in Ciona are similar to but simpler than those in humans and suggest that changes of the genome in the lineage leading to humans after the separation from that leading to Ciona increased the number and diversity of members of the HSP70 chaperone system. Changes of the genome in the lineage leading to Ciona also seem to have made the HSP70 chaperone system in this species slightly simpler than that in the common ancestor of humans and Ciona.

Fig 1.

Phylogenetic tree of HSP70 superfamily proteins constructed based on the full-length sequences of HSP70 superfamily proteins of humans, C intestinalis, and D melanogaster. Ciona proteins are indicated by large black dots. The number at each branch indicates the percentage of times that a node was supported in 1000 bootstrap pseudoreplications. Percentages <49% are omitted for simplicity. Proteins are named as explained in Materials and Methods. The unrooted tree is shown as a rooted tree for simplicity. The scale bar indicates an evolutionary distance of 0.2 amino acid substitutions per position. Bars on the right indicate gene groups. As for members of cytoplasmic group of DnaK subfamily, another tree was constructed to know the relationship among them more precisely (supplementary Fig S1)

Fig 2.

Phylogenetic tree of type A J-proteins constructed based on the full-length sequences of type A J-proteins of humans and C intestinalis. Ciona proteins are indicated by large black dots. The number at each branch indicates the percentage of times that a node was supported in 1000 bootstrap pseudoreplications. Proteins are named as explained in Materials and Methods. Bars on the right indicate gene groups. The unrooted tree is shown as a rooted tree for simplicity. The scale bar indicates an evolutionary distance of 0.2 amino acid substitutions per position