ICE1 of Poncirus trifoliata functions in cold tolerance by modulating polyamine levels through interacting with arginine decarboxylase

Huang, Xiaosan; Zhang, Qinghua; Zhu, Dexin; Fu, Xing-Zheng; Wang, Min; Zhang, Qian; Moriguchi, Takaya; Liu, Jihong

doi:10.1093/jxb/erv138

Cited by 81 publications

(73 citation statements)

References 73 publications

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“…Higher SOD, CAT, APX and GR activities were measured in cold-treated DX indicating that higher efficiency in the balance of ROS production. Furthermore, the transriptome results also showed the up-regulation of nonenzymic antioxidants in DX, including tocopherol, GSH, and polyamine, which have been reported to function in elevating stress tolerance [9, 32]. These results will help in broader understanding of the enhanced cold tolerance in DX partially resulted from ROS pathways modulation.…”

Section: Discussionmentioning

confidence: 77%

De novo transcriptome sequencing and gene expression profiling of Elymus nutans under cold stress

Miao

Shao

et al. 2016

BMC Genomics

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Background Elymus nutans Griseb., is an important alpine perennial forage of Pooideae subfamily with strong inherited cold tolerance. To get a deeper insight into its molecular mechanisms of cold tolerance, we compared the transcriptome profiling by RNA-Seq in two genotypes of Elymus nutans Griseb. the tolerant Damxung (DX) and the sensitive Gannan (GN) under cold stress.ResultsThe new E. nutans transcriptomes were assembled and comprised 200,520 and 181,331 transcripts in DX and GN, respectively. Among them, 5436 and 4323 genes were differentially expressed in DX and GN, with 170 genes commonly expressed over time. Early cold responses involved numerous genes encoding transcription factors and signal transduction in both genotypes. The AP2/EREBP famliy of transcription factors was predominantly expressed in both genotypes. The most significant transcriptomic changes in the later phases of cold stress are associated with oxidative stress, primary and secondary metabolism, and photosynthesis. Higher fold expressions of fructan, trehalose, and alpha-linolenic acid metabolism-related genes were detected in DX. The DX-specific dehydrins may be promising candidates to improve cold tolerance. Twenty-six hub genes played a central role in both genotypes under cold stress. qRT-PCR analysis of 26 genes confirmed the RNA-Seq results.ConclusionsThe stronger transcriptional differentiation during cold stress in DX explains its better cold tolerance compared to GN. The identified fructan biosynthesis, alpha-linolenic acid metabolism, and DX-specific dehydrin-related genes may provide genetic resources for the improvement of cold-tolerant characters in DX. Our findings provide important clues for further studies of the molecular mechanisms underlying cold stress responses in plants.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3222-0) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 77%

De novo transcriptome sequencing and gene expression profiling of Elymus nutans under cold stress

Miao

Shao

et al. 2016

BMC Genomics

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“…It is also demonstrated that putrescine plays a role in maintaining ROS homeostasis by regulating the antioxidant system to elevate abiotic stress tolerance (Liu et al ., ; Wang et al ., ; Song et al ., ). Accumulation of putrescine activates antioxidant enzymes such as superoxidase dismutase and catalase to eliminate redundant ROS under cold stress in tobacco and lemon (Huang et al ., ). In potato, freezing‐tolerant genotypes accumulated more putrescine to response to cold stress, while sensitive genotypes did not (Figure ), suggesting that putrescine is involved in freezing tolerance of potato.…”

Section: Discussionmentioning

confidence: 97%

The arginine decarboxylase gene ADC1, associated to the putrescine pathway, plays an important role in potato cold‐acclimated freezing tolerance as revealed by transcriptome and metabolome analyses

Kou

Chen

et al. 2018

The Plant Journal

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These authors contributed equally to this work. SUMMARYLow temperature severely influences potato production as the cultivated potato (Solanum tuberosum) is frost sensitive, however the mechanism underlying the freezing tolerance of the potato is largely unknown. In the present research, we studied the transcriptome and metabolome of the freezing-tolerant wild species Solanum acaule (Aca) and freezing-sensitive cultivated S. tuberosum (Tub) to identify the main pathways and important factors related to freezing tolerance. Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway annotation indicated that polyamine and amino acid metabolic pathways were specifically upregulated in Aca under cold treatment. The transcriptome changes detected in Aca were accompanied by the specific accumulation of putrescine, saccharides, amino acids and other metabolites. The combination of transcriptome and metabolome analyses revealed that putrescine exhibited an accumulative pattern in accordance with the expression of the arginine decarboxylase gene ADC1. The primary role of putrescine was further confirmed by analyzing all three polyamines (putrescine, spermidine, and spermine) and the genes encoding the corresponding enzymes in two sets of potato genotypes with distinct freezing tolerance, implying that only putrescine and ADC1 were uniquely enhanced by cold in the freezingtolerant genotypes. The function of putrescine was further analyzed by its exogenous application and the overexpression of SaADC1 in S. tuberosum cv. E3, indicating its important role(s) in cold-acclimated freezing tolerance, which was accompanied with the activation of C-repeat binding factor genes (CBFs). The present research has identified that the ADC1-associated putrescine pathway plays an important role in coldacclimated freezing tolerance of potato, probably by enhancing the expression of CBF genes.

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“…These findings support the inference that ICE1 has a function in regulating the expression of CBF and COR genes under cold stress, and that ICE1 and ICE2 together contribute even more to the cold‐induced gene expression and freezing tolerance. In addition, a role of ICE1 homologs in cold stress response has been observed in many plant species such as rice, tomato, Zea mays, Chrysanthemum dichrum , Chinese wild Vitis amurensis, Pyrus ussuriensis, Poncirus trifoliata , and Cucumis sativus (Liu et al 2010; Feng et al 2013; Xu et al 2014; Huang et al 2015a, 2015b; Lu et al 2017; Zhang et al 2017).…”

Section: Accession Numbermentioning

confidence: 99%

The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes

Tang

Zhao

Ren

et al. 2020

JIPB

111

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A recent paper by Kidokoro et al. (2020) in The Plant Cell reported a transgene‐dependent transcriptional silencing phenomenon in the dominant ice1‐1 Arabidopsis mutant containing the CBF3‐LUC reporter, and questioned whether ICE1 may regulate CBF genes and may be involved in plant cold response. Here, we evaluate available evidence supporting the involvement of ICE1 in plant cold response, and provide ChIP‐seq data showing ICE1 binding to the promoters of CBF genes and other regulatory genes known to be critical for cold response as well as to the promoters of some COR genes.

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ICE1 of Poncirus trifoliata functions in cold tolerance by modulating polyamine levels through interacting with arginine decarboxylase

Abstract: Highlight: ICE1 of Poncirus trifoliata (L.) Raf. plays a positive role in cold tolerance and modulates polyamine synthesis by interacting with arginine decarboxylase.

Cited by 81 publications

References 73 publications

De novo transcriptome sequencing and gene expression profiling of Elymus nutans under cold stress

De novo transcriptome sequencing and gene expression profiling of Elymus nutans under cold stress

The arginine decarboxylase gene ADC1, associated to the putrescine pathway, plays an important role in potato cold‐acclimated freezing tolerance as revealed by transcriptome and metabolome analyses

The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes

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