Structurally distinct telomere-binding proteins in Ustilago maydis execute non-overlapping functions in telomere replication, recombination, and protection

Eun Young Yu,Swapna Ganduri,William K Holloman,Jeanette H Sutherland,Neal F Lue,Syed S Zahid,Min Hsu

doi:10.1038/s42003-020-01505-z

Eun Young Yu, Swapna Ganduri + Show 5 more

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https://doi.org/10.1038/s42003-020-01505-z

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Journal: Communications Biology	Publication Date: Dec 1, 2020
Citations: 9	License type: open-access

Affiliation: Cornell University, Hearst (United States)

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 in Ustilago maydis, a basidiomycete that is evolutionarily distant from the standard fungi. These two telomere-binding proteins, UmTay1 and UmTrf2, 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 of Umtrf2 leads to severe growth defects and profound telomere aberrations. Comparative analysis of UmTay1 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 in Ustilago maydis that may be conserved in other systems.

Highlights

Duplex telomere binding proteins exhibit considerable structural and functional diversity in fungi
We showed in a published report that this protein has high affinity and sequence specificity for the cognate telomere repeats, and that it interacts directly with Blm helicase, just like mammalian TRF1/220
The CgTEL oligo, another G-rich repeat that lacks the GGGTTA sequence, was unable to compete. This binding preference is similar to that reported for Y. lipolytica Tay[1], with regard to the strong preference for DNA with canonical repeats[11,12], and indicates that UmTay[1] has the requisite DNAbinding properties to act at U. maydis telomeres

Summary

Introduction

Duplex telomere binding proteins exhibit considerable structural and functional diversity in fungi. We interrogate the activities and functions of two Myb-containing, duplex telomere repeat-binding factors in Ustilago maydis, a basidiomycete that is evolutionarily distant from the standard fungi These two telomere-binding proteins, UmTay[1] and UmTrf[2], despite having distinct domain structures, exhibit comparable affinities and sequence specificity for the canonical telomere repeats. Special mechanisms are required to retain and replenish telomere DNA owing to (i) the propensity of telomere DNA to form barriers that block replication forks[3]; and (ii) the “end-replication” problem that prevents the complete synthesis of lagging strand duplex[4] Both the protective and DNA maintenance functions of telomeres are mediated by specific proteins within the dynamic assembly, often through direct physical interactions between telomere proteins and functionally relevant downstream targets.

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