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Comparison of Xrn1 and Rat1 5′→3′ exoribonucleases in budding yeast supports the unique role of Xrn1 in co-translational mRNA decay
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  • Jose Perez-Ortin,
  • A. Jordán-Pla,
  • Y. Zhang,
  • J. Moreno-García,
  • L. Campos-Mata,
  • Juana Diez,
  • V. Pelechano,
  • Jose Garcia-Martinez,
  • Mordechai Choder
Jose Perez-Ortin
Universitat de València

Corresponding Author:[email protected]

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A. Jordán-Pla
Universitat de València
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Y. Zhang
Karolinska Institutet Institutionen for mikrobiologi tumor- och cellbiologi
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J. Moreno-García
Universitat de València
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L. Campos-Mata
Universitat Pompeu Fabra
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Juana Diez
Universitat Pompeu Fabra
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V. Pelechano
Karolinska Institutet Institutionen for mikrobiologi tumor- och cellbiologi
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Jose Garcia-Martinez
Universitat de València
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Mordechai Choder
Technion Israel Institute of Technology
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Abstract

The yeast Saccharomyces cerevisiae and most eukaryotes carry two 5’→3’ exoribonuclease paralogues that are very similar. In yeast, they are called Xrn1, which shuttles between the nucleus and cytoplasm and executes major cytoplasmic mRNA decay, and Rat1, which carries a strong nuclear localization sequence (NLS) and localizes in the nucleus. Xrn1 is 40% homologous to Rat1 but has an extra ~500 amino acids C-terminal extension. In the cytoplasm, Xrn1 can degrade decapped mRNAs during the last round of translation by ribosomes “co-translational mRNA decay”. The division of labor between the two enzymes is still enigmatic and can serve as a paradigm for division of labor of many other paralogues. Here we show that Rat1 is capable of functioning in cytoplasmic mRNA decay, provided that Rat1 remains cytoplasmic due to its NLS disruption (cRat1). This indicates that the actual segregation of the two paralogues plays roles in their specific functions. However, segregation is not sufficient for fully complementing Xrn1 function. Specifically, cRat1 can only partially recover cell volume, mRNA stability, proliferation rate, 5’→3’ decay alterations that characterize xrn1Δ cells. In particular, co-translational decay is only little complemented by cRat1. Adding the Xrn1 C-terminal domain to Rat1 does not improve the phenotypes indicating that lack of C-terminal is not the reason for the partial complementation. Collectively, it seems that during evolution the two paralogues acquire unique features that make the division of work beneficial.
25 Jul 2023Submitted to Yeast
25 Jul 2023Submission Checks Completed
25 Jul 2023Assigned to Editor
25 Jul 2023Review(s) Completed, Editorial Evaluation Pending
03 Aug 2023Reviewer(s) Assigned
11 Sep 2023Editorial Decision: Revise Major
11 Apr 20242nd Revision Received
11 Apr 2024Submission Checks Completed
11 Apr 2024Assigned to Editor
11 Apr 2024Review(s) Completed, Editorial Evaluation Pending
14 May 2024Editorial Decision: Revise Minor
26 May 2024Review(s) Completed, Editorial Evaluation Pending