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Authors: Tomás Urzúa Lehuedé, Victoria Berdion Gabarain, Tomas Moyano, Lucia Ferrero, Miguel Angel Ibeas, Hernan Salinas-Grenet, Gerardo Núñez-Lillo, Romina Acha, Jorge Perez, Florencia Perotti, Virginia Natali Miguel, Fiorella Paola Spies, Miguel A. Rosas, Michitaro Shibata, Diana R. Rodríguez-García, Adrian A. Moreno, Keiko Sugimoto, Karen Sanguinet, Claudio Meneses, Raquel L. Chan, Federico Ariel, Jose M. Alvarez and José M. Estevez.
bioRxiv (2024)
Abstract: "The root hair (RH) cells can elongate to several hundred times their initial size, and are an ideal model system for investigating cell size control. Their development is influenced by both endogenous and external signals, which are combined to form a integrative response. Surprisingly, a low temperature condition of 10°C causes an increased RH growth in Arabidopsis and in several monocots, even when the development of the rest of the root and aerial parts of the plant are halted. Previously, we demonstrated a strong correlation between the growth response and a significant decrease in nutrient availability in the medium under low temperature conditions. However, the molecular basis responsible for receiving and transmitting signals related to the availability of nutrients in the soil, and their relation to plant development, remain largely unknown. We decided to further investigate the intricate molecular processes behind the particular responsiveness of this root cell type at low temperature. In this study, we have discovered a gene regulatory network (GRN) controlling early transcriptome responses to low temperature. This GNR is commanded by specific transcription factors (FTs), namely ROOT HAIR DEFECTIVE 6-LIKE 4 (RSL4), a member of the homeodomain leucine zipper (HD-Zip I) group I 13 (AtHB13), the trihelix TF GT2-LIKE1 (GTL1), and a previously unidentified MYB-like TF (AT2G01060). Furthermore, we have identified four downstream RSL4 targets AtHB16, AtHB23, EARLY-RESPONSIVE TO DEHYDRATION 7 (ERD7) and ERD10 suggesting their participation in the regulation of RH development under these conditions. Functional analysis shows that such components of the RSL4-dependent transcriptional cascade influence the subsequent RH growth response to low temperature. These discoveries enhance our comprehension of how plants synchronize the RH growth in response to variations in temperature and nutrient availability at the cellular level."
Author: Leiyun Yang
The Plant Cell (2024)
Excerpts: "Simultaneously, low temperature stimulates plant immunity by activating salicylic acid (SA)-mediated signaling (Wu et al. 2019). However, the mechanism by which plants integrate cold signals and immune signaling remain elusive. To investigate this question, Shaoqin Li and colleagues (Li et al. 2024) studied the potential involvement of ICE1 in cold-induced immunity in Arabidopsis."
"To elucidate how ICE1 regulates cold-induced immunity, the authors conducted a yeast-two-hybrid screen and identified NON-EXPRESSER OF PR GENES 1 (NPR1), a master transcriptional co-activator of PATHOGENESIS-RELATED GENE 1 (PR1) in SA-activated immunity, as an ICE1 interactor.....Additionally, the authors found that ICE1 directly binds to the PR1 promoter for gene activation. These results illustrate that ICE1 interacts with NPR1 and is required for SA-mediated immunity by directly promoting PR1 expression."
"These results support the conclusion that ICE1 and TGA3 work synergistically to promote PR1 transcription. This study not only shed light on a new role of ICE1 in SA-mediated immunity at low temperature, but also revealed NPR1-TGA3/ICE1 as an important nexus integrating SA signaling and cold signals in plant immunity (see Figure)."
Authors: Ruiqing Li, Yue Song, Xueqiang Wang, Chenfan Zheng, Bo Liu, Huali Zhang, Jian Ke, Xuejing Wu, Liquan Wu, Ruifang Yang and Meng Jiang.
Journal of Integrative Plant Biology (2024)
Editor's view: OsNAC5 regulates cold-responsive genes (CORs) to promote cold tolerance in rice via the OsABI5-CORs transcription module, constituting an exquisite regulatory cascade to responses to changing temperature conditions, which provides new insights for using molecular design breeding to improve cold tolerance in rice.
Abstract: "Due to its tropical origins, rice (Oryza sativa) is susceptible to cold stress, which poses severe threats to production. OsNAC5, a NAC-type transcription factor, participates in the cold stress response of rice, but the detailed mechanisms remain poorly understood. Here, we demonstrate that OsNAC5 positively regulates cold tolerance at germination and in seedlings by directly activating the expression of ABSCISIC ACID INSENSITIVE 5 (OsABI5). Haplotype analysis indicated that single nucleotide polymorphisms in a NAC-binding site in the OsABI5 promoter are strongly associated with cold tolerance. OsNAC5 also enhanced OsABI5 stability, thus regulating the expression of cold-responsive (COR) genes, enabling fine-tuned control of OsABI5 action for rapid, precise plant responses to cold stress. DNA affinity purification sequencing coupled with transcriptome deep sequencing identified several OsABI5 target genes involved in COR expression, including DEHYDRATION-RESPONSIVE ELEMENT BINDING FACTOR 1A (OsDREB1A), OsMYB20, and PEROXIDASE 70 (OsPRX70). In vivo and in vitro analyses suggested that OsABI5 positively regulates COR gene transcription, with marked COR upregulation in OsNAC5-overexpressing lines and downregulation in osnac5 and/or osabi5 knockout mutants. This study extends our understanding of cold tolerance regulation via OsNAC5 through the OsABI5-CORs transcription module, which may be used to ameliorate cold tolerance in rice via advanced breeding."
Authors: Huafeng Zhang, Yingping Pei, Feilong Zhu, Qiang He, Yunyun Zhou, Bohui Ma, Xiaoqing Chen, Jiangbai Guo, Abid Khan, Maira Jahangir, Lijun Ou and Rugang Chen.
The Plant Journal (2024)
Significance Statement: Abscisic acid (ABA) could be induced by cold stress, which can restrains the activity of PP2Cs to reduce the activity of CaSnRK2.4 kinase. CaSnRK2.4 can interact with and phosphorylate CaNAC035. CaNAC035 is induced by both cold and ABA treatments. Over expression of CaNAC035 resulted in enhanced cold stress tolerance, while knockdown of CaNAC035 significantly reduced resistance to cold stress. Additionally, CaNAC035 could bind to the promoters of CaNCED3 and CaAAO3, which led to the ABA accumulation.
Abstract: "Plant NAC transcription factors play a crucial role in enhancing cold stress tolerance, yet the precise molecular mechanisms underlying cold stress remain elusive. In this study, we identified and characterized CaNAC035, an NAC transcription factor isolated from pepper (Capsicum annuum) leaves. We observed that the expression of the CaNAC035 gene is induced by both cold and abscisic acid (ABA) treatments, and we elucidated its positive regulatory role in cold stress tolerance. Overexpression of CaNAC035 resulted in enhanced cold stress tolerance, while knockdown of CaNAC035 significantly reduced resistance to cold stress. Additionally, we discovered that CaSnRK2.4, a SnRK2 protein, plays an essential role in cold tolerance. In this study, we demonstrated that CaSnRK2.4 physically interacts with and phosphorylates CaNAC035 both in vitro and in vivo. Moreover, the expression of two ABA biosynthesis-related genes, CaAAO3 and CaNCED3, was significantly upregulated in the CaNAC035-overexpressing transgenic pepper lines. Yeast one-hybrid, Dual Luciferase, and electrophoretic mobility shift assays provided evidence that CaNAC035 binds to the promoter regions of both CaAAO3 and CaNCED3 in vivo and in vitro. Notably, treatment of transgenic pepper with 50 μm Fluridone (Flu) enhanced cold tolerance, while the exogenous application of ABA at a concentration of 10 μm noticeably reduced cold tolerance in the virus-induced gene silencing line. Overall, our findings highlight the involvement of CaNAC035 in the cold response of pepper and provide valuable insights into the molecular mechanisms underlying cold tolerance. These results offer promising prospects for molecular breeding strategies aimed at improving cold tolerance in pepper and other crops."
Authors: Jingye Fu, Wenzheng Pei, Linqian He, Ben Ma, Chen Tang, Li Zhu, Liping Wang, Yuanyuan Zhong, Gang Chen, Qi Wang and Qiang Wang.
PLoS Genetics (2023)
Abstract: "Rapid and uniform seed germination is required for modern cropping system. Thus, it is important to optimize germination performance through breeding strategies in maize, in which identification for key regulators is needed. Here, we characterized an AP2/ERF transcription factor, ZmEREB92, as a negative regulator of seed germination in maize. Enhanced germination in ereb92 mutants is contributed by elevated ethylene signaling and starch degradation. Consistently, an ethylene signaling gene ZmEIL7 and an α-amylase gene ZmAMYa2 are identified as direct targets repressed by ZmEREB92. OsERF74, the rice ortholog of ZmEREB92, shows conserved function in negatively regulating seed germination in rice. Importantly, this orthologous gene pair is likely experienced convergently selection during maize and rice domestication. Besides, mutation of ZmEREB92 and OsERF74 both lead to enhanced germination under cold condition, suggesting their regulation on seed germination might be coupled with temperature sensitivity. Collectively, our findings uncovered the ZmEREB92-mediated regulatory mechanism of seed germination in maize and provide breeding targets for maize and rice to optimize seed germination performance towards changing climates."
Authors: Shaoqin Li, Yongping Yang, Li He, Xiao Han, Yanru Hu and Yanjuan Jiang.
bioRxiv (2023)
Abstract: "Cold stress affects plant immune responses, and this process may involve the salicylic acid (SA) signaling pathway. However, the underlying mechanism by which low temperature signals coordinate with SA signaling to regulate plant immunity remains poorly characterized. Here, we found that low temperatures enhanced the disease resistance of Arabidopsis against Pseudomonas syringae pv. tomato (Pst) DC3000. This process required Inducer of CBF expression 1 (ICE1), the core transcription factor in cold-signal cascades. ICE1 physically interacted with Non-expresser of PR genes 1 (NPR1), the master regulator of the SA signaling pathway. Enrichment of ICE1 on the PR1 promoter and its ability to transcriptionally activate PR1 were enhanced by NPR1. Further analyses revealed that cold stress signals cooperate with SA signals to facilitate plant immunity against pathogen attack in an ICE1-dependent manner. Cold treatment promoted interactions of NPR1 and TGA3 with ICE1, and increased the ability of the ICE1-TGA3 complex to transcriptionally activate PR1. Together, our results characterize a previously unrecognized role of ICE1 as an indispensable regulatory node linking low temperature activated- and SA-regulated immunity. Discovery of a crucial role of ICE1 in coordinating multiple signals associated with immunity broadens our understanding of plant-pathogen interactions."
Authors: Chong Ren, Peige Fan, Shaohua Li and Zhenchang Liang.
Plant Physiology (2023)
Abstract: "Grapevine (Vitis ssp.) is a deciduous perennial fruit crop, and the canes and buds of grapevine should withstand low temperatures (LTs) annually during winter. However, the widely cultivated Vitis vinifera is cold-sensitive and cannot survive the severe winter in regions with extremely LTs, such as viticulture regions in northern China. By contrast, a few wild Vitis species like V. amurensis and V. riparia exhibit excellent freezing tolerance. However, the mechanisms underlying grapevine cold tolerance remain largely unknown. In recent years, much progress has been made in elucidating the mechanisms, owing to the advances in sequencing and molecular biotechnology. Assembly of grapevine genomes together with resequencing and transcriptome data enable researchers to conduct genomic and transcriptomic analyses in various grapevine genotypes and populations to explore genetic variations involved in cold tolerance. In addition, a number of pivotal genes have been identified and functionally characterized. In this review, we summarize recent major advances in physiological and molecular analyses of cold tolerance in grapevine and put forward questions in this field. We also discuss the strategies for improving the tolerance of grapevine to cold stress. Understanding grapevine cold tolerance will facilitate the development of grapevines for adaption to global climate change.
Authors: Wenqing Yu, Peihua Ma, Jiping Sheng and Lin Shen.
Food Chemistry (2023)
Highlights: • SlERF2 helped to alleviate fruit quality deterioration during cold storage. • Mutations of SlERF2 altered ROS levels and antioxidant capacity of stored tomatoes. • SlERF2 contributed to activate ABA signaling during postharvest storage of tomatoes. • SlERF2 participated in the activation of CBF-dependent pathway in response to cold.
Abstract: "Ethylene production is essential for improving cold resistance of postharvest tomatoes. However, the role of ethylene signaling pathway in maintaining fruit quality during long-term cold storage remains poorly understood. Here, we demonstrated that a partial loss of function in ethylene signaling by mutation of Ethylene Response Factor 2 (SlERF2), worsened fruit quality during cold storage, as determined by visual characterization, and physiological analyses of membrane damage and reactive oxygen species metabolism. In addition, mutation of SlERF2 gene compromised cold-induced expression of genes in the C-repeat/dehydration-responsive binding factor (CBF) signaling pathway. Besides, the transcriptions of genes related to abscisic acid (ABA) biosynthesis and signaling were also altered by SlERF2 gene in response to cold storage. Therefore, it’s concluded that an ethylene signaling component, SlERF2 contributed to the regulations ABA biosynthesis and signaling pathway, as well as CBF cold signaling pathway, thus affecting the fruit quality during long-term cold storage of tomatoes."
Authors: Yuanlin Guan, Delight Hwarari, Harriet Mateko Korboe, Baseer Ahmad, Yiwei Cao, Ali Movahedi and Liming Yang.
Environmental and Experimental Botany (2023)
Abstract: "Plant geographical distribution, growth and development, and yield, are to a greater extend affected by the environmental factors, including cold stress. Low-temperature affects enzyme activity, membrane functionality, and cell dehydration, leading to cell metabolic instability or autophagy. Nonetheless, plants have evolved complex biochemical and molecular mechanisms to adapt to cold stress, regulated through transcriptional and translational modifications of genes. These complex mechanisms are principally divided into ABA-dependent and -independent pathways. Abscisic acid (ABA), as a crucial component in the pathways during the cold stress, regulates the expression of Cold-Responsive (COR) genes through several transcription factors such as the bZIP, HOS members, homo box, H4, and Zn finger factors. Particularly, in the ABA-independent pathway, the cold stress is regulated through the C-repeat binding factors (CBFs), and ABA activates the expression of the Inducer of CBF expression 1 (ICE1) through the Mitogen-Activated Protein Kinase (MAPK) signaling pathway. Consequently, upregulating the transcription and expression of CBF genes and COR genes downstream in a chain reaction, through binding to the C-repeat/Dehydration Responsive Element (CRT/DRE). In addition, the transcriptional and post-translational modifications (PTMs) modulate gene expressions in the signaling cascade at various levels of response leading to plant low temperature stress acclimation. This review paper discusses and summarizes the molecular mechanisms governing cold stress responses, addressing current researches and findings in light of the cold stress and their implications on plant genetic improvement."
Authors: Luyue Zhang, Jianing Song, Rui Lin, Mingjia Tang, Shujun Shao, Jingquan Yu and Yanhong Zhou.
Journal of Experimental Botany (2022)
Abstract: "Cold is a common abiotic environmental stress that seriously affects plant growth and development. MYB transcription factors are regulatory molecules that play important roles in various biological processes. We have previously demonstrated that SlMYB15 positively regulates cold tolerance in tomato. However, the underlying mechanism of SlMYB15-induced cold tolerance remains largely unexplored. Here, cold-induced SlMYB15 was found to be targeted by Solanum lycopersicum (sly)-miR156e-3p, which was decreased by cold stimulus in tomato. Tomato plants overexpressing sly-MIR156e-3p displayed significant enhancement in the susceptibility to cold stress, while silencing of sly-miR156e-3p by an artificial microRNA interference strategy caused tomato plants to be more tolerant to cold. Moreover, both overexpression of SlMYB15 and silencing of sly-miR156e-3p increased the accumulation of ABA, owing to that SlMYB15 can directly bind to the promoter regions of ABA biosynthesis and signalling genes, SlNCED1 and SlABF4, resulting in an enhanced cold tolerance. Further experiments showed that SlMYB15 and sly-miR156e-3p also coordinated the cold tolerance of tomato via reactive oxygen species (ROS) signalling pathway, as reflected by the increased expression of SlRBOH1, enhanced H2O2 and O2•－accumulation, amplified activity of antioxidant enzymes in SlMYB15-overexpressing and sly-miR156e-3p-silencing plants. Taken together, our results demonstrate that SlMYB15 targeted by sly-miR156e-3p confers higher survivability of cold stress of plants via ABA and ROS signals. This study will be valuable for breeding improved crop cultivars better equipped with cold resistance."
Authors: Yanglin Ding, Hao Yang, Shifeng Wu, Diyi Fu, Minze Li, Zhizhong Gong and Shuhua Yang.
Science Advances (2022)
Abstract: "Exposure to cold triggers a spike in cytosolic calcium (Ca2+) that often leads to transcriptional reprogramming in plants. However, how this Ca2+ signal is perceived and relayed to the downstream cold signaling pathway remains unknown. Here, we show that the CALCIUM-DEPENDENT PROTEIN KINASE 28 (CPK28) initiates a phosphorylation cascade to specify transcriptional reprogramming downstream of cold-induced Ca2+ signal. Plasma membrane (PM)–localized CPK28 is activated rapidly upon cold shock within 10 seconds in a Ca2+-dependent manner. CPK28 then phosphorylates and promotes the nuclear translocation of NIN-LIKE PROTEIN 7 (NLP7), a transcription factor that specifies the transcriptional reprogramming of cold-responsive gene sets in response to Ca2+, thereby positively regulating plant response to cold stress. This study elucidates a previously unidentified mechanism by which the CPK28-NLP7 regulatory module integrates cold-evoked Ca2+ signal and transcriptome and thus uncovers a key strategy for the rapid perception and transduction of cold signals from the PM to the nucleus."
Authors: Yufei Dong, Mingjia Tang, Zelan Huang, Jianing Song, Jin Xu, Golam Jalal Ahammed, Jingquan Yu and Yanhong Zhou.
The Plant Journal (2022)
Abstract: "Due to the high sensitivity to cold, the yield and quality of tomato (Solanum lycopersicum L.) are severely restricted by cold stress. The NAC transcription factor (TF) family has been characterized as an important player in plant growth, development, and stress response, but the role of NAC TFs in cold stress and their interaction with other post-transcriptional regulators such as microRNAs in cold tolerance remain elusive. Here, we demonstrated that SlNAM3, the predicted target of Sl-miR164a/b-5p, improved cold tolerance as evidenced by a higher maximum quantum efficiency of photosystem II (Fv/Fm), lower relative electrolyte leakage (REL) and less wilting in SlNAM3-overexpression plants than wild-type. Further genetic and molecular confirmation revealed that Sl-miR164a/b-5p functioned upstream of SlNAM3 by inhibiting the expression of the latter, thus playing a negative role in cold tolerance. Interestingly, this role is partially mediated by an ethylene-dependent pathway, as either Sl-miR164a/b-5p silencing or SlNAM3 overexpression improved cold tolerance in the transgenic lines by promoting ethylene production. Moreover, silencing the ethylene synthesis genes, SlACS1A, SlACS1B, SlACO1, and SlACO4, resulted in a significant decrease in cold tolerance. Further experiments demonstrated that NAM3 activates SlACS1A, SlACS1B, SlACO1, and SlACO4 transcription by directly binding to their promoters. Taken together, our study identified the miR164a-NAM3 module conferring cold tolerance in tomato plants via the direct regulation of SlACS1A, SlACS1B, SlACO1, and SlACO4 expression to induce ethylene synthesis."
Authors: Xipan Wang, Qiping Song, Yang Liu, Marian Brestic and Xinghong Yang.
Planta (2022)
Main conclusion: ICEs are key transcription factors in response to cold in plant, they also balance plant growth and stress tolerance. Thus, we systematize the information about ICEs published to date.
Abstract: "Low temperature is an important factor affecting plant growth and development. Exposing to cold condition results in a suit of effects on plants including reduction of plant growth and reproduction, and decrease in crop yield and quality. Plants have evolved a series of strategies to deal with cold stress such as reprogramming of the expression of genes and transcription factors. ICEs (Inducer of CBF Expression), as transcription factors regulating CBFs (C-repeat binding factor), play key roles in balancing plant growth and stress tolerance. Studies on ICEs focused on the function of ICEs on cold tolerance, growth and development; post-translational modifications of ICEs and crosstalk between the ICEs and phytohormones. In this review, we focus on systematizing the information published to date. We summarized the main advances of the functions of ICEs on the cold tolerance, growth and development. And we also elaborated the regulation of ICEs protein stability including phosphorylation, ubiquitination and SUMOylation of ICE. Finally, we described the function of ICEs in the crosstalk among different phytohormone signaling pathway and cold stress. This review provides perspectives for ongoing research about cold tolerance, growth and development in plant."
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Authors: Tao Wang, Xuemin Ma, Ying Chen, Cuicui Wang, Zhenxiao Xia, Zixi Liu, Lihong Gao and Wenna Zhang.
Plant, Cell & Environment (2024)
Abstract: "Low temperature stress poses a significant challenge to the productivity of horticultural crops. The dynamic expression of cold-responsive genes plays a crucial role in plant cold tolerance. While NAC transcription factors have been extensively studied in plant growth and development, their involvement in regulating plant cold tolerance remains poorly understood. In this study, we focused on the identification and characterisation of SlNAC3 as the most rapid and robust responsive gene in tomato under low temperature conditions. Manipulating SlNAC3 through overexpression or silencing resulted in reduced or enhanced cold tolerance, respectively. Surprisingly, we discovered a negative correlation between the expression of CBF and cold tolerance in the SlNAC3 transgenic lines. These findings suggest that SlNAC3 regulates tomato cold tolerance likely through a CBF-independent pathway. Furthermore, we conducted additional investigations to identify the molecular mechanisms underlying SlNAC3-mediated cold tolerance in tomatoes. Our results revealed that SlNAC3 controls the transcription of ethylene biosynthetic genes, thereby bursting ethylene release in response to cold stress. Indeed, the silencing of these genes led to an augmentation in cold tolerance. This discovery provides valuable insights into the regulatory pathways involved in ethylene-mediated cold tolerance in tomatoes, offering potential strategies for developing innovative approaches to enhance cold stress resilience in this economically important crop species."
Authors: Shaoqin Li, Li He, Yongping Yang, Yixin Zhang, Xiao Han, Yanru Hu and Yanjuan Jiang.
The Plant Cell (2024)
One-sentence summary: The NPR1–TGA3–ICE1 regulatory module represents an important step in salicylic acid signaling during cold-activated resistance of plants to pathogen attack.
Abstract: "Cold stress affects plant immune responses, and this process may involve the salicylic acid (SA) signaling pathway. However, the underlying mechanism by which low-temperature signals coordinate with SA signaling to regulate plant immunity remains unclear. Here, we found that low temperatures enhanced the disease resistance of Arabidopsis thaliana against Pseudomonas syringae pv. tomato DC3000. This process required INDUCER OF CBF EXPRESSION 1 (ICE1), the core transcription factor in cold-signal cascades. ICE1 physically interacted with NONEXPRESSER OF PATHOGENESIS-RELATED GENES 1 (NPR1), the master regulator of the SA signaling pathway. Enrichment of ICE1 on the PATHOGENESIS-RELATED GENE 1 (PR1) promoter and its ability to transcriptionally activate PR1 were enhanced by NPR1. Further analyses revealed that cold stress signals cooperate with SA signals to facilitate plant immunity against pathogen attack in an ICE1-dependent manner. Cold treatment promoted interactions of NPR1 and TGACG-BINDING FACTOR 3 (TGA3) with ICE1 and increased the ability of the ICE1–TGA3 complex to transcriptionally activate PR1. Together, our results characterize a critical role of ICE1 as an indispensable regulatory node linking low-temperature-activated and SA-regulated immunity. Understanding this crucial role of ICE1 in coordinating multiple signals associated with immunity broadens our understanding of plant–pathogen interactions."
Authors: Chaoyi Hu, Mengqi Wang, Changan Zhu, Shaofang Wu, Jiajia Li, Jingquan Yu and Zhangjian Hu.
Plant, Cell & Environment (2024)
Summary Statement: This study demonstrated that the cold- and abscisic acid (ABA)-responsive transcription factor ETHYLENE RESPONSE FACTOR 15 positively regulates ABA-mediated cold tolerance in tomato plants by activating CBF1 and WRKY6 expression.
Abstract: "Cold stress is a major meteorological threat to crop growth and yield. Abscisic acid (ABA) plays important roles in plant cold tolerance by activating the expression of cold-responsive genes; however, the underlying transcriptional regulatory module remains unknown. Here, we demonstrated that the cold- and ABA-responsive transcription factor ETHYLENE RESPONSE FACTOR 15 (ERF15) positively regulates ABA-mediated cold tolerance in tomato. Exogenous ABA treatment significantly enhanced cold tolerance in wild-type tomato plants but failed to rescue erf15 mutants from cold stress. Transcriptome analysis showed that ERF15 was associated with the expression of cold-responsive transcription factors such as CBF1 and WRKY6. Further RT-qPCR assays confirmed that the ABA-induced increased in CBF1 and WRKY6 transcripts was suppressed in erf15 mutants when the plants were subjected to cold treatment. Moreover, yeast one-hybrid assays, dual-luciferase assays and electrophoretic mobility shift assays demonstrated that ERF15 activated the transcription of CBF1 and WRKY6 by binding their promoters. Silencing CBF1 or WRKY6 significantly decreased cold tolerance. Overall, our study identified the role of ERF15 in conferring ABA-mediated cold tolerance in tomato plants by activating CBF1 and WRKY6 expression. This study not only broadens our knowledge of the mechanism of ABA-mediated cold tolerance in plants but also highlights ERF15 as an ideal target gene for cold-tolerant crop breeding."
Authors: Jingqiu Xia, Jiawen Liang, Mengmeng Yu, Rui Wang, Chen Sun, Huishan Song, Qinghua Xu, Jing Cang, Yuying Wang and Da Zhang.
Environmental and Experimental Botany (2024)
Highlights • TaMED25 is involved in JA signal pathway. • TaMED25 expression responded to low temperature stress in wheat. • Overexpression of TaMED25 gene enhances freeze resistance in Arabidopsis plants. • TaMED25 is localized in the nucleus. • TaMED25 interacts with TaJAZ7, TaMYC2 and TaICE41 proteins.
Abstract: "The MEDIATOR (MED) complex is a molecular bridge that regulates transcription by connecting transcription factors (TFs) and specific gene promoters. The MED subunit 25 (MED25) can interact with specific TFs in the phytohormone signaling pathways to regulate the transcription of downstream genes and affect various physiological processes in plants. Although MED25 plays an important role in adaptation to abiotic stresses, it is still unclear whether MED25 is involved in freezing tolerance in wheat. In this study, we found that the expression of TaMED25 was significantly increased under extremely low temperatures (–25 °C) in Dongnongdongmai1 (Dn1) plants, a variety of winter wheat with excellent cold-stress resistance,and hypothesized that TaMED25 may be a novel regulator of freezing tolerance in this wheat variety. To further characterize the function of TaMED25 in freezing tolerance, we cloned TaMED25 from Dn1 plants and overexpressed it in Arabidopsis thaliana. The results showed that the overexpression of TaMED25 improved freezing tolerance in Arabidopsis plants, with decreased relative conductivity, enhanced ability to effectively scavenge reactive oxygen species (ROS), and increased expression of cold-responsive genes. Furthermore, we proposed that TaMED25 mediates jasmonate-induced cold resistance in plants, possibly by interacting with TaJAZ7 and TaMYC2 of the jasmonate signaling pathway and TaICE41 of the ICE–CBF–COR pathway. Our findings reveal the functions of MED25 in plants and provide a scientific basis for an in-depth analysis of the transcriptional regulation mechanism of freezing tolerance in winter wheat."
Authors: Lihui Wang, Hui Chen, Guoyu Chen, Guangbao Luo, Xinyan Shen, Bo Ouyang and Zhilong Bie.
Plant Physiology (2023)
Abstract: "Tomato (Solanum lycopersicum) is a cold-sensitive crop but frequently experiences low-temperature stimuli. However, tomato responses to cold stress are still poorly understood. Our previous studies have shown that using wild tomato (S. habrochaites) as rootstock can significantly enhance the cold resistance of grafted seedlings, in which a high concentration of jasmonates (JAs) in scions exerts an important role, but the mechanism of JA accumulation remains unclear. Herein, we discovered that tomato SlWRKY50, a group II WRKY transcription factor that is cold-inducible, responds to cold stimuli and plays a key role in JA biosynthesis. SlWRKY50 directly bound to the promoter of tomato allene oxide synthase gene (SlAOS), and overexpressing SlWRKY50 improved tomato chilling resistance, which led to higher levels of Fv/Fm, antioxidative enzymes, SlAOS expression, and JA accumulation. SlWRKY50-silenced plants, however, exhibited an opposite trend. Moreover, DIECA (a JA biosynthesis inhibitor) foliar treatment drastically reduced the cold tolerance of SlWRKY50-OE plants to WT levels. Importantly, SlMYC2, the key regulator of the JA signaling pathway, can control SlWRKY50 expression. Overall, our research indicates that SlWRKY50 promotes cold tolerance by controlling JA biosynthesis and that JA signaling mediates SlWRKY50 expression via transcriptional activation by SlMYC2. Thus, this contributes to the genetic knowledge necessary for developing cold-resistant tomato varieties."
Authors: Xi Wang, Zhuoyang Li, Yiting Shi, Ziyan Liu, Xiaoyan Zhang, Zhizhong Gong and Shuhua Yang.
The EMBO Journal (2023)
Synopsis: Plants respond to extreme cold stress by synthesizing strigolactones; however, how this class of plant hormones promotes freezing tolerance is still poorly understood. Here, cold-induced strigolactones are shown to promote plant survival in sub-zero temperatures by enhancing expression of freezing tolerance regulators DREB1/CBF. Strigolactones positively regulate plant freezing tolerance via a CBF-dependent pathway. The E3 ligase MAX2 interacts with and ubiquitinates the transcription factor WRKY41, mediating its cold-induced degradation. WRKY41 represses the cold-induced expression of CBFs by directly binding to their promoters. SLs-mediated degradation of SMXLs also contributes to enhanced freezing tolerance by accumulating anthocyanin.
Abstract: "Cold stress is a major abiotic stress that adversely affects plant growth and crop productivity. The C-REPEAT BINDING FACTOR/DRE BINDING FACTOR 1 (CBF/DREB1) transcriptional regulatory cascade plays a key role in regulating cold acclimation and freezing tolerance in Arabidopsis (Arabidopsis thaliana). Here, we show that max (more axillary growth) mutants deficient in strigolactone biosynthesis and signaling display hypersensitivity to freezing stress. Exogenous application of GR245DS, a strigolactone analog, enhances freezing tolerance in wild-type plants and strigolactone-deficient mutants and promotes the cold-induced expression of CBF genes. Biochemical analysis showed that the transcription factor WRKY41 serves as a substrate for the F-box E3 ligase MAX2. WRKY41 directly binds to the W-box in the promoters of CBF genes and represses their expression, negatively regulating cold acclimation and freezing tolerance. MAX2 ubiquitinates WRKY41, thus marking it for cold-induced degradation and thereby alleviating the repression of CBF expression. In addition, SL-mediated degradation of SMXLs also contributes to enhanced plant freezing tolerance by promoting anthocyanin biosynthesis. Taken together, our study reveals the molecular mechanism underlying strigolactones promote the cold stress response in Arabidopsis."
Authors: Junping He, Lu Yao, Lorenzo Pecoraro, Changxiao Liu, Juan Wang, Luqi Huang and Wenyuan Gao.
Critical Reviews in Biotechnology (2023)
Abstract: "Plants make different defense mechanisms in response to different environmental stresses. One common way is to produce secondary metabolites. Temperature is the main environmental factor that regulates plant secondary metabolites, especially flavonoids and terpenoids. Stress caused by temperature decreasing to 4–10 °C is conducive to the accumulation of flavonoids and terpenoids. However, the accumulation mechanism under cold stress still lacks a systematic explanation. In this review, we summarize three aspects of cold stress promoting the accumulation of flavonoids and terpenoids in plants, that is, by affecting (1) the content of endogenous plant hormones, especially jasmonic acid and abscisic acid; (2) the expression level and activity of important transcription factors, such as bHLH and MYB families. This aspect also includes post-translational modification of transcription factors caused by cold stress; (3) key enzyme genes expression and activity in the biosynthesis pathway, in addition, the rate-limiting enzyme and glycosyltransferases genes are responsive to cold stress. The systematic understanding of cold stress regulates flavonoids, and terpenoids will contribute to the future research of genetic engineering breeding, metabolism regulation, glycosyltransferases mining, and plant synthetic biology."
Authors: Jianyan Huang, Xiaobo Zhao, Marco Bürger, Joanne Chory and Xinchao Wang.
Trends in Plant Science (2023)
Highlights: As a major environmental factor impacting the seasonal growth and geographical distribution of plants, temperature change significantly affects crop quality and productivity. Ethylene is a gaseous hormone with an important role in plant growth, development, and multiple stress responses, including heat and cold. Temperature stress affects ethylene biosynthesis and signaling pathways, with APETALA2/ETHYLENE RESPONSIVE FACTOR (AP2/ERF) transcription factors being the main node of ethylene-mediated temperature stress response. Crosstalk among different phytohormones also alters and regulates the expression of temperature stress-responsive genes.
Abstract: "Temperature influences the seasonal growth and geographical distribution of plants. Heat or cold stress occur when temperatures exceed or fall below the physiological optimum ranges, resulting in detrimental and irreversible damage to plant growth, development, and yield. Ethylene is a gaseous phytohormone with an important role in plant development and multiple stress responses. Recent studies have shown that, in many plant species, both heat and cold stress affect ethylene biosynthesis and signaling pathways. In this review, we summarize recent advances in understanding the role of ethylene in plant temperature stress responses and its crosstalk with other phytohormones. We also discuss potential strategies and knowledge gaps that need to be adopted and filled to develop temperature stress-tolerant crops by optimizing ethylene response."
Authors: Fei Ding, Chuang Wang, Ning Xu and Meiling Wang.
Environmental and Experimental Botany (2022)
Highlights: • Transcription of SlERF.B8 was markedly induced by JA and cold stress. • Silencing of SlERF.B8 decreases JA accumulation and attenuates cold tolerance. • SlERF.B8 activates the transcription of JA biosynthesis genes. • JA signaling activates the transcription of SlERF.B8. • JA and ET synergistically regulate tomato cold tolerance.
Abstract: "Cold stress inhibits growth, decreases yields and impairs fruit quality in tomato (Solanum lycopersicum). Previous studies have shown that cold stress leads to increased JA accumulation, however, how jasmonate biosynthesis is regulated upon cold stress remains largely unknown. Here, we report an ethylene response factor SlERF.B8 that acts as a crucial regulator of JA biosynthesis in tomato under cold stress. Transcription of SlERF.B8 was markedly enhanced by JA and cold stress, and silencing of SlERF.B8 led to decreased JA accumulation and attenuated cold tolerance in tomato. ChIP-qPCR and dual-luciferase assays showed that SlERF.B8 functions as a transcriptional activator of JA biosynthesis genes, including LOXD, AOC and OPR3. Furthermore, MYC2, a critical mediator of JA signaling, activates the transcription of SlERF.B8, thus forming a positive feedback loop, which amplifies the output of JA signaling. Taken together, our data favor that SlERF.B8 is a key regulator of JA biosynthesis and cold tolerance in tomato plants."
Authors: Jiaqi Tang, Xiaojie Tian, Enyang Mei, Mingliang He, Junwen Gao, Jun Yu, Min Xu, Jiali Liu, Lu Song, Xiufeng Li, Zhenyu Wang, Qingjie Guan, Zhigang Zhao, Chunming Wang and Qingyun Bu.
The Plant Cell (2022)
Abstract: "Cold tolerance at the booting stage (CTB) is a major factor limiting rice (Oryza sativa L.) productivity and geographical distribution. A few cold-tolerance genes have been identified, but they either need to be overexpressed to result in CTB or cause yield penalties, limiting their utility for breeding. Here, we characterize the function of the cold-induced transcription factor WRKY53 in rice. The wrky53 mutant displays increased CTB, as determined by higher seed setting. Low temperature is associated with lower gibberellin (GA) contents in anthers in the wild type but not in the wrky53 mutant, which accumulates slightly more GA in its anthers. WRKY53 directly binds to the promoters of GA biosynthesis genes and transcriptionally represses them in anthers. In addition, we uncover a possible mechanism by which GA regulates male fertility: SLENDER RICE1 (SLR1) interacts with and sequesters two critical transcription factors for tapetum development, UNDEVELOPED TAPETUM1 (UDT1) and TAPETUM DEGENERATION RETARDATION (TDR), and GA alleviates the sequestration by SLR1, thus allowing UDT1 and TDR to activate transcription. Finally, knocking out WRKY53 in diverse varieties increases cold tolerance without a yield penalty, leading to a higher yield in rice subjected to cold stress. Together, these findings provide a target for improving CTB in rice."
Authors: Divya Mishra.
Plant Physiology (2022)
Excerpts: "In the present issue of Plant Physiology, Sun et al. (2022) unveil the roles of OsmiR1320 and its target Ethylene Response Factors, OsERF096 in regulating cold stress responses through the modulation of jasmonate (JA)-mediated signaling. The authors discovered that OsmiR1320 was significantly downregulated by cold stress. Interestingly, overexpression of the miR1320 gene in rice resulted in enhanced seedling growth compared to wild type (WT) during cold stress. Knockdown of miR1320 expression (miR1320-KD) led to growth inhibition, suggesting that miR1320 is critical for response to cold stress."
"Previous studies have shown that jasmonate serves as a positive signal for the Inducer of CBF expression 1/ DRE binding factor1 (ICE-CBF/DREB1) pathway to regulate cold tolerance (Hu et al., 2013). Because the expression of OsDREB1s and JA content in OsERF096 transgenic lines were altered, the authors proceeded to analyze the roles of jasmonate signaling in OsERF096- mediated cold stress response. Interestingly, methyl jasmonate treatments rescued the cold sensitive phenotypes of OsERF096-OE transgenic lines, suggesting that JA signaling functions downstream of OsERF096. In a nutshell, OsERF096 represses JA-mediated responses and hence makes the plant more susceptible to cold stress (Figure 1). The tight regulation between OsmiR1320 and OsERF096 may be utilized in generating genetically engineered crops with enhanced tolerance to cold stress."
Authors: Mingzhe Sun, Yang Shen, Yue Chen, Yan Wang, Xiaoxi Cai, Junkai Yang, Bowei Jia, Weifeng Dong, Xi Che and Xiaoli Sun.
Plant Physiology (2022)
Abstract: MicroRNAs play key roles in abiotic stress response. Rice (Oryza sativa L.) miR1320 is a species-specific miRNA that contributes to miR168-regulated immunity. However, it is still unknown whether miR1320 is involved in rice response to abiotic stress. In this study, we illustrated that the miR1320 precursor generated two mature miR1320s, miR1320-3p and miR1320-5p, and they both displayed decreased expression under cold stress. Genetic evidence showed that miR1320 overexpression resulted in increased cold tolerance, while miR1320 knockdown reduced cold tolerance. Furthermore, an AP2/ERF (APETALA2/ethylene-responsive factor) transcription factor OsERF096 was identified as a target of miR1320 via 5′-RACE and dual luciferase assays. OsERF096 expression was altered by miR1320 overexpression and knockdown and exhibited an opposite pattern to that of miR1320 in different tissues and under cold stress. Consistently, OsERF096 negatively regulated cold stress tolerance. Furthermore, we suggested that OsERF096 could bind to the GCC and DRE cis-elements and act as a transcriptional activator in the nucleus. Based on RNA-seq and targeted metabolomics assays, we found that OsERF096 modified hormone content and signaling pathways. Finally, phenotypic and RT-qPCR assays showed that MeJA application recovered the cold-sensitive phenotype and JA-activated expression of three DREB (Dehydration Responsive Element Binding) genes in the OsERF096-OE line. Taken together, our results strongly suggest that the miR1320-OsERF096 module regulates cold tolerance by repressing the JA-mediated cold signaling pathway."
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