RNA Chaperone Function of a Universal Stress Protein in Arabidopsis Confers Enhanced Cold Stress Tolerance in Plants.

Sarah Mae Boyles Melencion,Yong Hun Chi,Changyu Lee,Seol Ki Paeng,Seong Dong Wi,Sung Sun Koo,Thuy Thi Pham,Sang Yeol Lee,Seoung Woo Ryu

doi:10.3390/ijms18122546

Sarah Mae Boyles Melencion, Yong Hun Chi + Show 7 more

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https://doi.org/10.3390/ijms18122546

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Abstract

The physiological function of Arabidopsis thaliana universal stress protein (AtUSP) in plant has remained unclear. Thus, we report here the functional role of the Arabidopsis universal stress protein, AtUSP (At3g53990). To determine how AtUSP affects physiological responses towards cold stress, AtUSP overexpression (AtUSP OE) and T-DNA insertion knock-out (atusp, SALK_146059) mutant lines were used. The results indicated that AtUSP OE enhanced plant tolerance to cold stress, whereas atusp did not. AtUSP is localized in the nucleus and cytoplasm, and cold stress significantly affects RNA metabolism such as by misfolding and secondary structure changes of RNA. Therefore, we investigated the relationship of AtUSP with RNA metabolism. We found that AtUSP can bind nucleic acids, including single- and double-stranded DNA and luciferase mRNA. AtUSP also displayed strong nucleic acid-melting activity. We expressed AtUSP in RL211 Escherichia coli, which contains a hairpin-loop RNA structure upstream of chloramphenicol acetyltransferase (CAT), and observed that AtUSP exhibited anti-termination activity that enabled CAT gene expression. AtUSP expression in the cold-sensitive Escherichia coli (E. coli) mutant BX04 complemented the cold sensitivity of the mutant cells. As these properties are typical characteristics of RNA chaperones, we conclude that AtUSP functions as a RNA chaperone under cold-shock conditions. Thus, the enhanced tolerance of AtUSP OE lines to cold stress is mediated by the RNA chaperone function of AtUSP.

Highlights

Plants are continually exposed to detrimental environmental factors such as extreme temperature, water deficit, salinity, heavy metals, pathogens, and herbivore attack
We show that Arabidopsis thaliana universal stress protein (AtUSP) OE plants exhibit enhanced cold stress tolerance compared to wild type (WT) and atusp plants
We used the Bio-Analytic Resource (BAR) for plant biology bioinformatics database (Available online: http://bar.utoronto.ca/) to analyze AtUSP mRNA transcript levels in Arabidopsis, and found that they are significantly up-regulated by cold treatment (4 ◦C) (Figure S1 of Supplemental Materials)

Summary

Introduction

Plants are continually exposed to detrimental environmental factors such as extreme temperature, water deficit, salinity, heavy metals, pathogens, and herbivore attack. Many stress-responsive genes have been identified that have essential roles in defense responses against environmental stresses. The first universal stress protein (USP) identified was C13.5 protein in bacteria; its gene expression was stimulated by a wide variety of stresses. USPs have essential roles for bacterial survival under abiotic stresses such as nutrient starvation, high salinity, extreme temperatures, and chemical exposure [4]. Bacterial USPs are involved in processes such as cell motility, cell adhesion, iron scavenging, and oxidative stress resistance [5]. USPs have been identified in fungi, archaebacteria, eubacteria, protozoa, metazoans, and plants [6]

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