Abstract Duplex telomere binding proteins exhibit considerable structural and functional diversity in fungi. Herein we interrogate the activities and functions of two Myb-containing, duplex telomere repeat-binding factors inUstilago maydis, a basidiomycete that is evolutionarily distant from the standard fungi. These two telomere-binding proteins,UmTay1 andUmTrf2, despite having distinct domain structures, exhibit comparable affinities and sequence specificity for the canonical telomere repeats.UmTay1 specializes in promoting telomere replication and an ALT-like pathway, most likely by modulating the helicase activity of Blm.UmTrf2, in contrast, is critical for telomere protection; transcriptional repression ofUmtrf2leads to severe growth defects and profound telomere aberrations. Comparative analysis ofUmTay1 homologs in different phyla reveals broad functional diversity for this protein family and provides a case study for how DNA-binding proteins can acquire and lose functions at various chromosomal locations. Our findings also point to stimulatory effect of telomere protein on ALT inUstilago maydisthat may be conserved in other systems. 
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                            Duplex Telomere-Binding Proteins in Fungi With Canonical Telomere Repeats: New Lessons in the Rapid Evolution of Telomere Proteins
                        
                    
    
            The telomere protein assemblies in different fungal lineages manifest quite profound structural and functional divergence, implying a high degree of flexibility and adaptability. Previous comparative analyses of fungal telomeres have focused on the role of telomere sequence alterations in promoting the evolution of corresponding proteins, particularly in budding and fission yeast. However, emerging evidence suggests that even in fungi with the canonical 6-bp telomere repeat unit, there are significant remodeling of the telomere assembly. Indeed, a new protein family can be recruited to serve dedicated telomere functions, and then experience subsequent loss in sub-branches of the clade. An especially interesting example is the Tay1 family of proteins, which emerged in fungi prior to the divergence of basidiomycetes from ascomycetes. This relatively recent protein family appears to have acquired its telomere DNA-binding activity through the modification of another Myb-containing protein. Members of the Tay1 family evidently underwent rather dramatic functional diversification, serving, e.g., as transcription factors in fission yeast while acting to promote telomere maintenance in basidiomycetes and some hemi-ascomycetes. Remarkably, despite its distinct structural organization and evolutionary origin, a basidiomycete Tay1 appears to promote telomere replication using the same mechanism as mammalian TRF1, i.e., by recruiting and regulating Blm helicase activity. This apparent example of convergent evolution at the molecular level highlight the ability of telomere proteins to acquire new interaction targets. The remarkable evolutionary history of Tay1 illustrates the power of protein modularity and the facile acquisition of nucleic acid/protein-binding activity to promote telomere flexibility. 
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                            - Award ID(s):
- 1817331
- PAR ID:
- 10283446
- Date Published:
- Journal Name:
- Frontiers in Genetics
- Volume:
- 12
- ISSN:
- 1664-8021
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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