Temperature signaling

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    OsCIPK7 point-mutation leads to conformation and kinase-activity change for sensing cold response
    Dajian Zhang, Xiaoyu Guo, Yunyuan Xu, Hao Li, Liang Ma, Xuefeng Yao, Yuxiang Weng, Yan Guo, Chun-Ming Liu and Kang Chong
    J Integr Plant Biol 2019, 61 (12): 1194-1200.  
    doi: 10.1111/jipb.12800
    Abstract (Browse 995)  |   Save
    Calcineurin B‐like interacting protein kinases (CIPKs) play important roles via environmental stress. However, less is known how to sense the stress in molecular structure conformation level. Here, an OsCIPK7 mutant via TILLING procedure with a point mutation in the kinase domain showed increased chilling tolerance, which could be potentially used in the molecular breeding. We found that this point mutation of OsCIPK7 led to a conformational change in the activation loop of the kinase domain, subsequently with an increase of protein kinase activity, thus conferred an increased tolerance to chilling stress.
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    Proteomic and metabolomic profiling underlines the stage- and time-dependent effects of high temperature on grape berry metabolism
    David Lecourieux, Christian Kappel, Stéphane Claverol, Philippe Pieri, Regina Feil, John E. Lunn, Marc Bonneu, Lijun Wang, Eric Gomès, Serge Delrot and Fatma Lecourieux
    J Integr Plant Biol 2020, 62 (8): 1132-1158.  
    DOI: 10.1111/jipb.12894
    Abstract (Browse 372)  |   Save

    Climate change scenarios predict an increase in mean air temperatures and in the frequency, intensity, and length of extreme temperature events in many wine‐growing regions worldwide. Because elevated temperature has detrimental effects on berry growth and composition, it threatens the economic and environmental sustainability of wine production. Using Cabernet Sauvignon fruit‐bearing cuttings, we investigated the effects of high temperature (HT) on grapevine berries through a label‐free shotgun proteomic analysis coupled to a complementary metabolomic study. Among the 2,279 proteins identified, 592 differentially abundant proteins were found in berries exposed to HT. The gene ontology categories “stress,” “protein,” “secondary metabolism,” and “cell wall” were predominantly altered under HT. High temperatures strongly impaired carbohydrate and energy metabolism, and the effects depended on the stage of development and duration of treatment. Transcript amounts correlated poorly with protein expression levels in HT berries, highlighting the value of proteomic studies in the context of heat stress. Furthermore, this work reveals that HT alters key proteins driving berry development and ripening. Finally, we provide a list of differentially abundant proteins that can be considered as potential markers for developing or selecting grape varieties that are better adapted to warmer climates or extreme heat waves.

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    Aldehyde dehydrogenase ALDH3F1 involvement in flowering time regulation through histone acetylation modulation on FLOWERING LOCUS C
    Danyun Xu, Qing Liu, Gang Chen, Zhiqiang Yan and Honghong Hu
    J Integr Plant Biol 2020, 62 (8): 1080-1092.  
    DOI: 10.1111/jipb.12893
    Abstract (Browse 361)  |   Save

    Flowering time regulation is one of the most important processes in the whole life of flowering plants and FLOWERING LOCUS C (FLC ) is a central repressor of flowering time. However, whether metabolic acetate level affects flowering time is unknown. Here we report that ALDEHYDE DEHYDROGENASE ALDH3F1 plays essential roles in floral transition via FLC‐dependent pathway. In the aldh3f1‐1 mutant, the flowering time was significant earlier than Col‐0 and the FLC expression level was reduced. ALDH3F1 had aldehyde dehydrogenase activity to affect the acetate level in plants, and the amino acids of E214 and C252 are essential for its catalytic activity. Moreover, aldh3f1 mutation reduced acetate level and the total acetylation on histone H3. The H3K9Ac level on FLC locus was decreased in aldh3f1‐1 , which reduced FLC expression. Expression of ALDH3F1 could rescue the decreased H3K9Ac level on FLC, FLC expression and also the early‐flowering phenotype of aldh3f1‐1 , however ALDH3F1 E214A or ALDH3F1 C252A could not. Our findings demonstrate that ALDH3F1 participates in flowering time regulation through modulating the supply of acetate for acetyl‐CoA, which functions as histone acetylation donor to modulate H3K9Ac on FLC locus.

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    The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes
    Kai Tang, Lun Zhao, Yuying Ren, Shuhua Yang, Jian-Kang Zhu and Chunzhao Zhao
    J Integr Plant Biol 2020, 62 (3): 258-263.  
    doi: 10.1111/jipb.12918
    Abstract (Browse 409)  |   Save

    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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    Induction of priming by cold stress via inducible volatile cues in neighboring tea plants
    Mingyue Zhao, Lu Wang, Jingming Wang, Jieyang Jin, Na Zhang, Lei Lei, Ting Gao, Tingting Jing, Shangrui Zhang, Yi Wu, Bin Wu, Yunqing Hu, Xiaochun Wan, Wilfried Schwab and Chuankui Song
    J Integr Plant Biol 2020, 62 (10): 1461-1468.  
    doi: 10.1111/jipb.12937
    Abstract (Browse 399)  |   Save
    Plants have evolved sophisticated defense mechanisms to overcome their sessile nature. However, if and how volatiles from cold‐stressed plants can trigger interplant communication is still unknown. Here, we provide the first evidence for interplant communication via inducible volatiles in cold stress. The volatiles, including nerolidol, geraniol, linalool, and methyl salicylate, emitted from cold‐stressed tea plants play key role(s) in priming cold tolerance of their neighbors via a C‐repeat‐binding factors‐dependent pathway. The knowledge will help us to understand how plants respond to volatile cues in cold stress and agricultural ecosystems.
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    Immediate transcriptional responses of Arabidopsis leaves to heat shock
    Min Liu, Jiafu Zhu and Zhicheng Dong
    J Integr Plant Biol 2021, 63 (3): 468-483.  
    doi: 10.1111/jipb.12990
    Abstract (Browse 383)  |   Save
    Plants have evolved efficient mechanisms for adapting to temperature fluctuations, known as heat stress response and heat stress memory. Although the transcriptional regulatory network of plant heat stress response has been established, little is known about the genome‐wide transcriptional changes occurring within the first several minutes after heat shock. Here, we investigated the nascent RNA and mature messenger RNA (mRNA) from plant leaf tissues exposed to 5 min of heat shock treatment using global run‐on sequencing and RNA sequencing methods. Only a small group of genes were up‐ or downregulated at both the nascent RNA and mRNA levels. Primed plants that were already exposed to mild heat stress exhibited a more drastic alteration at multiple transcriptional steps than naïve plants that had not experienced heat stress. Upon heat shock, we also observed the following: (i) engaged RNA polymerase II accumulated downstream of transcription start sites; (ii) 5′ pausing release was a rate‐limiting step for the induction of some heat shock protein genes; (iii) numerous genes switched transcription modes; (iv) pervasive read‐through was induced at terminators; and (v) heat stress memory occurs at multiple steps of the transcription cycle, such as at Pol II recruitment, 5′ pausing, elongation, and termination.
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    Florigen trafficking integrates photoperiod and temperature signals in Arabidopsis
    Lu Liu, Yu Zhang and Hao Yu
    J Integr Plant Biol 2020, 62 (9): 1385-1398.  
    doi: 10.1111/jipb.13000
    Abstract (Browse 356)  |   Save

    The transition to flowering is the most dramatic phase change in flowering plants and is crucial for reproductive success. A complex regulatory network in plants has evolved to perceive and integrate the endogenous and environmental signals. These signals perceived, including day length and temperature, converge to regulate FLOWERING LOCUS T (FT), which encodes a mobile stimulus required for floral induction in Arabidopsis. Despite the discovery of modulation of FT messenger RNA (mRNA) expression by ambient temperature, whether the trafficking of FT protein is controlled in response to changes in growth temperature is so far unknown. Here, we show that FT transport from companion cells to sieve elements is controlled in a temperature‐dependent manner. This process is mediated by multiple C2 domain and transmembrane region proteins (MCTPs) and a soluble N‐ethylmaleimide‐sensitive factor protein attachment protein receptor (SNARE). Our findings suggest that ambient temperatures regulate both FT mRNA expression and FT protein trafficking to prevent precocious flowering at low temperatures and ensure plant reproductive success under favorable environmental conditions.

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    The calcium‐dependent protein kinase ZmCDPK7 functions in heat‐stress tolerance in maize
    Yulong Zhao, Hanwei Du, Yankai Wang, Huali Wang, Shaoyu Yang, Chaohai Li, Ning Chen, Hao Yang, Yihao Zhang, Yulin Zhu, Luyao Yang and Xiuli Hu
    J Integr Plant Biol 2021, 63 (3): 510-527.  
    doi: 10.1111/jipb.13056
    Abstract (Browse 537)  |   Save
    Global warming poses a serious threat to crops. Calcium‐dependent protein kinases (CDPKs)/CPKs play vital roles in plant stress responses, but their exact roles in plant thermotolerance remains elusive. Here, we explored the roles of heat‐induced ZmCDPK7 in thermotolerance in maize. ZmCDPK7‐overexpressing maize plants displayed higher thermotolerance, photosynthetic rates, and antioxidant enzyme activity but lower H2O2 and malondialdehyde (MDA) contents than wild‐type plants under heat stress. ZmCDPK7‐knockdown plants displayed the opposite patterns. ZmCDPK7 is attached to the plasma membrane but can translocate to the cytosol under heat stress. ZmCDPK7 interacts with the small heat shock protein sHSP17.4, phosphorylates sHSP17.4 at Ser‐44 and the respiratory burst oxidase homolog RBOHB at Ser‐99, and upregulates their expression. Site‐directed mutagenesis of sHSP17.4 to generate a Ser‐44‐Ala substitution reduced ZmCDPK7's enhancement of catalase activity but enhanced ZmCDPK7's suppression of MDA accumulation in heat‐stressed maize protoplasts. sHSP17.4, ZmCDPK7, and RBOHB were less strongly upregulated in response to heat stress in the abscisic acid‐deficient mutant vp5 versus the wild type. Pretreatment with an RBOH inhibitor suppressed sHSP17.4 and ZmCDPK7 expression. Therefore, abscisic acid‐induced ZmCDPK7 functions both upstream and downstream of RBOH and participates in thermotolerance in maize by mediating the phosphorylation of sHSP17.4, which might be essential for its chaperone function.
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    Protein kinases in plant responses to drought, salt, and cold stress
    Xuexue Chen, Yanglin Ding, Yongqing Yang, Chunpeng Song, Baoshan Wang, Shuhua Yang, Yan Guo and Zhizhong Gong
    J Integr Plant Biol 2021, 63 (1): 53-78.  
    doi: 10.1111/jipb.13061
    Abstract (Browse 1177)  |   Save
    Protein kinases are major players in various signal transduction pathways. Understanding the molecular mechanisms behind plant responses to biotic and abiotic stresses has become critical for developing and breeding climate‐resilient crops. In this review, we summarize recent progress on understanding plant drought, salt, and cold stress responses, with a focus on signal perception and transduction by different protein kinases, especially sucrose nonfermenting1 (SNF1)‐related protein kinases (SnRKs), mitogen‐activated protein kinase (MAPK) cascades, calcium‐dependent protein kinases (CDPKs/CPKs), and receptor‐like kinases (RLKs). We also discuss future challenges in these research fields.
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    Reciprocal regulation between the negative regulator PP2CG1 phosphatase and the positive regulator OST1 kinase confers cold response in Arabidopsis
    Jian Lv, Jingyan Liu, Yuhang Ming, Yiting Shi, Chunpeng Song, Zhizhong Gong, Shuhua Yang and Yanglin Ding
    J Integr Plant Biol 2021, 63 (8): 1568-1587.  
    DOI: 10.1111/jipb.13100
    Abstract (Browse 583)  |   Save
    Protein phosphorylation and dephosphorylation have been reported to play important roles in plant cold responses. In addition, phospho-regulatory feedback is a conserved mechanism for biological processes and stress responses in animals and plants. However, it is less well known that a regulatory feedback loop is formed by the protein kinase and the protein phosphatase in plant responses to cold stress. Here, we report that OPEN STOMATA 1 (OST1) and PROTEIN PHOSPHATASE 2C G GROUP 1 (PP2CG1) reciprocally regulate the activity during the cold stress response. The interaction of PP2CG1 and OST1 is inhibited by cold stress, which results in the release of OST1 at the cytoplasm and nucleus from suppression by PP2CG1. Interestingly, cold-activated OST1 phosphorylates PP2CG1 to suppress its phosphatase activity, thereby amplifying cold signaling in plants. Mutations of PP2CG1 and its homolog PP2CG2 enhance freezing tolerance, whereas overexpression of PP2CG1 decreases freezing tolerance. Moreover, PP2CG1 negatively regulates protein levels of C-REPEAT BINDING FACTORs (CBFs) under cold stress. Our results uncover a phosphor/dephosphor-regulatory feedback loop mediated by PP2CG1 phosphatase and OST1 protein kinase in plant cold responses.
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    The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis
    Lin‐Lin Zhang, Wei Li, Ying‐Ying Tian, Seth Jon Davis and Jian‐Xiang Liu
    J Integr Plant Biol 2021, 63 (6): 1097-1103.  
    doi: 10.1111/jipb.13107
    Abstract (Browse 326)  |   Save
    Plants are capable of coordination of their growth and development with ambient temperatures. EARLY FLOWERING3 (ELF3), an essential component of the plant circadian clock, is also involved in ambient temperature sensing, as well as in inhibiting the expression and protein activity of the thermoresponsive regulator phytochrome interacting factor 4 (PIF4). The ELF3 activity is subjected to attenuation in response to warm temperature; however, how the protein level of ELF3 is regulated at warm temperature remains less understood. Here, we report that the E3 ligase XB3 ORTHOLOG 5 IN ARABIDOPSIS THALIANA, XBAT35, mediates ELF3 degradation. XBAT35 interacts with ELF3 and ubiquitinates ELF3. Loss-of-function mutation of XBAT35 increases the protein level of ELF3 and confers a short-hypocotyl phenotype under warm temperature conditions. Thus, our findings establish that XBAT35 mediates ELF3 degradation to lift the inhibition of ELF3 on PIF4 for promoting thermoresponsive hypocotyl growth in plants.
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    CDE4 encodes a pentatricopeptide repeat protein involved in chloroplast RNA splicing and affects chloroplast development under low-temperature conditions in rice
    Xinyong Liu, Xichun Zhang, Ruijie Cao, Guiai Jiao, Shikai Hu, Gaoneng Shao, Zhonghua Sheng, Lihong Xie, Shaoqing Tang, Xiangjin Wei and Peisong Hu
    J Integr Plant Biol 2021, 63 (10): 1724-1739.  
    doi: 10.1111/jipb.13147
    Abstract (Browse 298)  |   Save
    Pentatricopeptide repeat (PPR) proteins play important roles in the post-transcriptional modification of organellar RNAs in plants. However, the function of most PPR proteins remains unknown. Here, we characterized the rice (Oryza sativa L.) chlorophyll deficient 4 (cde4) mutant which exhibits an albino phenotype during early leaf development, with decreased chlorophyll contents and abnormal chloroplasts at low-temperature (20°C). Positional cloning revealed that CDE4 encodes a P-type PPR protein localized in chloroplasts. In the cde4 mutant, plastid-encoded polymerase (PEP)-dependent transcript levels were significantly reduced, but transcript levels of nuclear-encoded genes were increased compared to wild-type plants at 20°C. CDE4 directly binds to the transcripts of the chloroplast genes rpl2, ndhA, and ndhB. Intron splicing of these transcripts was defective in the cde4 mutant at 20°C, but was normal at 32°C. Moreover, CDE4 interacts with the guanylate kinase VIRESCENT 2 (V2); overexpression of V2 enhanced CDE4 protein stability, thereby rescuing the cde4 phenotype at 20°C. Our results suggest that CDE4 participates in plastid RNA splicing and plays an important role in rice chloroplast development under low-temperature conditions.
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    The direct targets of CBFs: In cold stress response and beyond
    Yue Song, Xiaoyan Zhang, Minze Li, Hao Yang, Diyi Fu, Jian Lv, Yanglin Ding, Zhizhong Gong, Yiting Shi and Shuhua Yang
    J Integr Plant Biol 2021, 63 (11): 1874-1887.  
    DOI: 10.1111/jipb.13161
    Abstract (Browse 522)  |   Save
    Cold acclimation in Arabidopsis thaliana triggers a significant transcriptional reprogramming altering the expression patterns of thousands of cold-responsive (COR) genes. Essential to this process is the C-repeat binding factor (CBF)-dependent pathway, involving the activity of AP2/ERF (APETALA2/ethylene-responsive factor)-type CBF transcription factors required for plant cold acclimation. In this study, we performed chromatin immunoprecipitation assays followed by deep sequencing (ChIP-seq) to determine the genome-wide binding sites of the CBF transcription factors. Cold-induced CBF proteins specifically bind to the conserved C-repeat (CRT)/dehydration-responsive elements (CRT/DRE; G/ACCGAC) of their target genes. A Gene Ontology enrichment analysis showed that 1,012 genes are targeted by all three CBFs. Combined with a transcriptional analysis of the cbf1,2,3 triple mutant, we define 146 CBF regulons as direct CBF targets. In addition, the CBF-target genes are significantly enriched in functions associated with hormone, light, and circadian rhythm signaling, suggesting that the CBFs act as key integrators of endogenous and external environmental cues. Our findings not only define the genome-wide binding patterns of the CBFs during the early cold response, but also provide insights into the role of the CBFs in regulating multiple biological processes of plants.
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