Global Characterization of XRN 5′-3′ Exoribonucleases and Their Responses to Environmental Stresses in Plants

Weimeng Song,Yue Niu,You Wu,Yanjie Li,Yan Bao,Xiang Yu

doi:10.3390/d13120612

Abstract

The XRN family of 5′-3′ Exoribonucleases is functionally conserved in eukaryotic organisms. However, the molecular evolution of XRN proteins in plants and their functions in plant response to environment stresses remain largely unexplored. In this study, we identified 23 XRN proteins in 6 representative plant species. Polygenetic analysis revealed that XRN2 was Arabidopsis-specific among these species, and additional branches outside the clades of XRN3 and XRN4 proteins, which we named as XRN5, were found in rice, maize, and soybean. However, XRN5 in soybean lost their entire 5′-3′ XRN Exoribonuclease domain. Protein conserved sequence analysis showed that XRN3/XRN2 contained potential bipartite nuclear-localization signals (NLS) while all the XRN4 proteins lost their second KR/RR motif of NLS, potentially leading to their cytoplasm localization. SIXRN3-2 contained one mutation in this second KR/RR motif, which may change their sub-cellular localization. The promoter cis-element analysis indicated that these XRN genes responded to multiple stresses and plant hormones diversely at transcriptional level. Finally, transcriptomic analysis suggested that OsXRN3 and ZmXRN3-1 were induced by low temperature, SIXRN4 and ZmXRN4 was inhibited by heat shock, and OsXRN5 and GmXRN5-2 were repressed by drought. However, in general, the expression patterns revealed the response diversity of XRNs to environment stimuli in different plant species. Taken together, this study characterized 23 XRNs with NLS variation that contributed to their sub-cellular localization and provided an overview of the XRNs response diversity to multiple environmental stresses, suggesting that XRNs could be used as potential gene editing candidates for precise stress-tolerant crop breeding.

Highlights

RNA degradation plays a critical role in RNA quantity and quality control
To characterize XRNs in plant species, the protein sequences of AtXRN2, AtXRN3 and AtXRN4 was used to identify potential homologs based on hmmsearch in Phytozome
We found that XRN3 proteins were conserved from moss to angiosperm plants and triplicated in soybean, XRN2 protein only existed in Arabidopsis among these 6 species, and XRN4 proteins were conserved in flowering plants, but not in moss; XRN5 proteins were uncovered in monocot rice and maize and dicot soybean

Summary

Introduction

RNA degradation plays a critical role in RNA quantity and quality control. RNA turnover is triggered by 30 polyA tail shortening and 50 cap removal, followed by Exoribonucleases cleavage from 50 to 30 and/or from 30 to 50 [1]. There are two XRNs of 50 -30 exoribonucleases: cytoplasmic enzyme XRN1 and nuclear enzyme XRN2 [2]. XRN1 plays a role in cytoplasmic RNA decay, whose substrates include mRNAs, noncoding. RNAs and products from Nonsense-mediated mRNA decay, while XRN2 (Rat1) functions in nuclear RNA decay with its activating partner RAI1 [3,4]. Current studies suggested that yeast XRN1 can degrade the mRNA following the last ribosome in a co-translational. In Arabidopsis, 50 -30 Exoribonucleases include three XRNs: AtXRN2, AtXRN3 and

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