Evolution of modular intraflagellar transport from a coatomer-like progenitor
Teunis J P van Dam1, Matthew J Townsend, Martin Turk
1Radboud University Medical Centre, 6500 HB, Nijmegen, The Netherlands.
Insights
The intraflagellar transport (IFT) complex, crucial for cilia, likely evolved from vesicle coats. Its subcomplexes, particularly the BBSome, show modularity and a "last-in, first-out" evolutionary pattern.
Area of Science:
- Cell Biology
- Evolutionary Biology
- Molecular Biology
Background:
- The intraflagellar transport (IFT) complex is essential for cilium function in eukaryotic cells.
- IFT dysfunction leads to ciliopathies, a group of human diseases.
- IFT complexes are hypothesized to share ancestry with vesicle coat proteins like COPI, COPII, and clathrin.
Purpose of the Study:
- To provide phylogenetic evidence for the common ancestry of IFT subunits and COPI subunits.
- To trace the evolutionary origins of IFT-A, IFT-B, and the BBSome.
- To understand the evolutionary dynamics and modularity of the IFT system.
Main Methods:
- Phylogenetic analysis of IFT and COPI protein sequences.
- Comparative genomics across eukaryotic taxa.
- Tracing the evolutionary history and distribution of IFT subcomplexes.
Main Results:
- Phylogenetic evidence supports a common origin for IFT subunits and COPI subunits.
- IFT-A and the BBSome likely evolved from an IFT-B-like precursor through gene duplication.
- The BBSome is a modular component of IFT, frequently lost during evolution, often preceding complete cilium loss.
Conclusions:
- The IFT complex originated from protocoatomers, supporting its role in vesicle transport.
- The IFT system exhibits modularity, with subcomplexes like the BBSome being independently gained or lost.
- The BBSome's late origin and frequent loss suggest an "last-in, first-out" evolutionary model for the IFT complex.
Abstract:
The intraflagellar transport (IFT) complex is an integral component of the cilium, a quintessential organelle of the eukaryotic cell. The IFT system consists of three subcomplexes [i.e., intraflagellar transport (IFT)-A, IFT-B, and the BBSome], which together transport proteins and other molecules along the cilium. IFT dysfunction results in diseases collectively called ciliopathies. It has been proposed that the IFT complexes originated from vesicle coats similar to coat protein complex (COP) I, COPII, and clathrin. Here we provide phylogenetic evidence for common ancestry of IFT subunits and α, β', and ε subunits of COPI, and trace the origins of the IFT-A, IFT-B, and the BBSome subcomplexes. We find that IFT-A and the BBSome likely arose from an IFT-B-like complex by intracomplex subunit duplication. The distribution of IFT proteins across eukaryotes identifies the BBSome as a frequently lost, modular component of the IFT. Significantly, loss of the BBSome from a taxon is a frequent precursor to complete cilium loss in related taxa. Given the inferred late origin of the BBSome in cilium evolution and its frequent loss, the IFT complex behaves as a "last-in, first-out" system. The protocoatomer origin of the IFT complex corroborates involvement of IFT components in vesicle transport. Expansion of IFT subunits by duplication and their subsequent independent loss supports the idea of modularity and structural independence of the IFT subcomplexes.
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