Research articleCyclophilin AtROC1S58F confers Arabidopsis cold tolerance by modulating jasmonic acid signaling and antioxidant metabolism
Introduction
Cold stress is one of the most devastating abiotic stresses that affect plant growth, productivity, and distribution. Extremely low temperature could disrupt cellular homeostasis and induce the accumulation of reactive oxygen species (ROS), such as hydrogen peroxide (H2O2), superoxide anion (O2−), and hydroxyl radical (Sinha et al., 2015). Correspondingly, plants have evolved sophisticated mechanisms to mitigate cellular oxidative damages caused by cold stress, including physiological and biochemical modifications and the activation of cold-responsive genes and transcription factors (TFs). Specifically, antioxidant enzymes (e.g., superoxide dismutase [SOD], peroxidase [POD], monodehydroascorbate reductase [MDHAR], glutathione reductase [GR]) and non-enzymatic antioxidants including ascorbic acid (ASA) and glutathione (GSH) accumulate to detoxify ROS accumulation (Mittler et al., 2004).
Cyclophilins (CYPs), a class of proteins that contain the conserved peptidyl-prolyl isomerase (PPIase) domain, are involved in protein folding and are known to play essential roles in various processes of plant growth and development (Dipesh Kumar et al., 2012). For example, AtCYP40 interacts with Hsp 90 to regulate the number of juvenile leaves and the morphology of inflorescence in Arabidopsis (Berardini et al., 2001). The Arabidopsis CYP71 (AtCYP71) and rice CYP2 (OsCYP2) both participate in lateral development, while the former being a histone remodeling factor that affects meristem cell organization in Arabidopsis (Li and Luan, 2011) and the latter regulating the stability of OsIAA11 (Indole-3-acetic acid) to control lateral root development in rice (Oryza sativa) (Jing et al., 2015; Kang et al., 2013). In addition, overexpression of AtCYP20-2 and TaCYP20-2 alters Arabidopsis flowering time (Zhang et al., 2013). The chloroplast stroma-localized protein AtCYP20-3 interacts with serine acetyltransferase to respond to high light and oxidative stress in Arabidopsis (Dominguez-Solis et al., 2008) and overexpression of OsCYP20-2 confers tobacco (Nicotiana tabacum) resistance to osmotic stress and high light (Kim et al., 2012). Furthermore, OsCYP19-4 exerts cold-tolerance and is associated with increased tiller and spike numbers in rice (Yoon et al., 2016). Despite their importance in cold tolerance and growth regulation, the detailed mechanisms employed by CYPs in response to cold stress are still unclear.
Jasmonic acids (JAs) are a class of plant phytohormones essential for plant development and stress tolerance (Sharma and Laxmi, 2016). Previous studies have shown that CYPs likely confer plant cold tolerance through JA signaling, which is known to participate in the response to a broad spectrum of stress conditions (Chen et al., 2007; Trivedi et al., 2013). In plants, JAs are synthesized from theα-linolenlic acid (18:3) in the chloroplasts membranes, which was then catalyzed mainly by lipoxygenases, allene oxide synthase (AOS), allene oxide cyclase (AOC), and 12-oxophytodienoate reductase 3 (OPR3), in plastids and peroxisomes (Santino et al., 2013). JA signaling is initiated by the formation of a co-receptor complex consisting of JA receptor coronatine insensitive 1 (COI1) and jasmonate-ZIM domain (JAZ) repressor, where JAZ is ubiquitinated and degraded by the 26S proteasome, thereby allowing for the binding of MYC transcriptional factors to the G-box element that functions downstream of JA-responsive genes (Per et al., 2018). In cold-stressed rice plants, endogenous JA level and the transcript levels of JA biosynthetic genes OsIOX2, OsAOC, and OsAOS1 were significantly increased (Du et al., 2013); and exogenous methyl jasmonate application significantly enhances the freezing tolerance of Arabidopsis plants (Hu et al., 2013). Further research indicated that exogenous applied JA could increase ASA content and POD enzymatic activity in carambola (Averrhoa carambola) during cold storage (Mustafa et al., 2016). These results suggest that jasmonate might play important roles in imparting cold tolerance in plants.
AtCYP18-3 (ROC1, Rotamase CYP 1) is a member of the CYP family. In our previous study, we identified a gain-of-function Arabidopsis roc1 mutant ROC1S58F, which exhibited substantially increased sensitivity to temperature (Ma et al., 2013). The ROC1S58F mutant does not bolt and sets only a few flowers from the center of the rosette under normal growth conditions, but produces an increasing number of flowers and normal siliques at a low temperature (16 °C) (Ma et al., 2013). Here, we investigated the underlying molecular mechanisms for these phenotypic changes under different temperatures, and hypothesized that abiotic stress level in the mutant was alleviated, likely associated with increases in endogenous hormone levels and antioxidant activities.
Section snippets
Microarray data analysis
Total RNA was isolated from 30 d-old ROC1S58F and WT leaves according to Ma et al. (2013). The Affymetrix Arabidopsis ATH1 Genome Array (ATLAS Niolabs GmbH, Berlin, Germany) was used to contrast the transcriptomes of these plants. Differentially expressed genes (DEGs) were identified based on |fold change| >2 and P-value <0.05. For DEGs classification and functional analysis, gene ontology (GO) was categorized against the agriGO database (http://bioinfo.cau.edu.cn/agriGO/index.php) for
The ROC1S58F affects JA signaling and antioxidant metabolism
Based on the Arabidopsis ATH1 chip, a total of 1040 DEGs were identified between ROC1S58F and WT under normal growth condition (Supplemental file1). GO enrichment analysis found 107 enriched GO terms in ‘biological process’ (mainly including cellular process, metabolic process, and response to stimulus), 14 in ‘cellular’ component (mainly including endomembrane system, plasma membrane, and cell wall), and 32 in ‘molecular function’ (mainly including catalytic activity, hydrolase activity, and
Discussion
In a previous study of our lab, we identified a ROC1S58F mutant, in which ROC1S58F transcript level was significantly reduced but the protein abundance was substantially increased with cold stress treatment (Ma et al., 2013). Transcriptome analysis revealed that GO terms ‘response to jasmonic acid stimulus’ and ‘response to oxidative stress’ were significantly enriched in ROC1S58F mutant compared with WT under normal growth conditions. Therefore, in the current study, we performed a systematic
Contributions
Y.W. designed and performed the experiments; Y.W. and X.M. wrote the manuscript; X.M. and P.M. conceived the study, supervised the project, and edited the manuscript; L.G. and S.J. assisted in performing the experiments. All authors read and approved the final manuscript.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
This work was supported by the Fundamental Research Funds for the Central Universities of China (Grant No. CAU-2018QC144). The authors thanks Liangsheng Wang and Stephanie Rossi for critical review and editing the manuscript.
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