Comparison of Xrn1 and Rat1 5' → 3' exoribonucleases in budding yeast supports the specific role of Xrn1 in cotranslational mRNA decay.

IF 2.2 4区 生物学 Q4 BIOCHEMISTRY & MOLECULAR BIOLOGY
Yeast Pub Date : 2024-07-01 Epub Date: 2024-06-14 DOI:10.1002/yea.3968
José E Pérez-Ortín, Antonio Jordán-Pla, Yujie Zhang, Jorge Moreno-García, Claudio Bassot, Marina Barba-Aliaga, Leire de Campos-Mata, Mordechai Choder, Juana Díez, Ilaria Piazza, Vicent Pelechano, José García-Martínez
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引用次数: 0

Abstract

The yeast Saccharomyces cerevisiae and most eukaryotes carry two 5' → 3' exoribonuclease paralogs. In yeast, they are called Xrn1, which shuttles between the nucleus and the cytoplasm, and executes major cytoplasmic messenger RNA (mRNA) decay, and Rat1, which carries a strong nuclear localization sequence (NLS) and localizes to the nucleus. Xrn1 is 30% identical 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, a process referred to as "cotranslational mRNA decay." The division of labor between the two enzymes is still enigmatic and serves as a paradigm for the subfunctionalization of many other paralogs. 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 physical segregation of the two paralogs plays roles in their specific functions. However, reversing segregation is not sufficient to fully complement the Xrn1 function. Specifically, cRat1 can partially restore the cell volume, mRNA stability, the proliferation rate, and 5' → 3' decay alterations that characterize xrn1Δ cells. Nevertheless, cotranslational decay is only slightly complemented by cRat1. The use of the AlphaFold prediction for cRat1 and its subsequent docking with the ribosome complex and the sequence conservation between cRat1 and Xrn1 suggest that the tight interaction with the ribosome observed for Xrn1 is not maintained in cRat1. Adding the Xrn1 C-terminal domain to Rat1 does not improve phenotypes, which indicates that lack of the C-terminal is not responsible for partial complementation. Overall, during evolution, it appears that the two paralogs have acquired specific characteristics to make functional partitioning beneficial.

比较了芽殖酵母中的 Xrn1 和 Rat1 5' → 3' 外切核酸酶,证明了 Xrn1 在共翻译 mRNA 衰变中的特殊作用。
酵母和大多数真核生物都携带两种 5' → 3' 外切核酸酶旁系亲属。在酵母中,它们被称为 Xrn1 和 Rat1,前者在细胞核和细胞质之间穿梭,执行主要的细胞质信使 RNA(mRNA)衰变;后者携带强核定位序列(NLS),定位在细胞核中。Xrn1 与 Rat1 有 30% 的相同之处,但在 C 端延伸了约 500 个氨基酸。在细胞质中,Xrn1 可以在核糖体翻译的最后一轮过程中降解脱帽 mRNA,这一过程被称为 "共翻译 mRNA 降解"。这两种酶的分工仍是一个谜,也是许多其他旁系亲属亚功能化的范例。在这里,我们证明了 Rat1 能够在细胞质 mRNA 降解中发挥作用,前提是 Rat1 因其 NLS 中断(cRat1)而保持细胞质状态。这表明这两个同源物的物理分离在其特定功能中发挥了作用。然而,逆转分离并不足以完全补充 Xrn1 的功能。具体来说,cRat1能部分恢复xrn1Δ细胞的细胞体积、mRNA稳定性、增殖率和5'→3'衰变。不过,cRat1 只对共翻译衰变起到了轻微的补充作用。利用 AlphaFold 对 cRat1 进行预测,随后将其与核糖体复合体对接,以及 cRat1 和 Xrn1 之间的序列保守表明,在 Xrn1 中观察到的与核糖体的紧密相互作用在 cRat1 中并没有得到维持。在 Rat1 中添加 Xrn1 C 端结构域并不能改善表型,这表明缺乏 C 端结构域并不是部分互补的原因。总之,在进化过程中,这两个同源物似乎获得了特定的特征,使功能分区变得有益。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Yeast
Yeast 生物-生化与分子生物学
CiteScore
5.30
自引率
3.80%
发文量
55
审稿时长
3 months
期刊介绍: Yeast publishes original articles and reviews on the most significant developments of research with unicellular fungi, including innovative methods of broad applicability. It is essential reading for those wishing to keep up to date with this rapidly moving field of yeast biology. Topics covered include: biochemistry and molecular biology; biodiversity and taxonomy; biotechnology; cell and developmental biology; ecology and evolution; genetics and genomics; metabolism and physiology; pathobiology; synthetic and systems biology; tools and resources
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