BPM-CUL3 E3 ligase modulates thermotolerance by facilitating negative regulatory domain-mediated degradation of DREB2A in Arabidopsis

DEHYDRATION-RESPONSIVE ELEMENT BINDING PROTEIN 2A (DREB2A) acts as a key transcription factor in both drought and heat stress tolerance in Arabidopsis and induces the expression of many drought- and heat stress-inducible genes. Although DREB2A expression itself is induced by stress, the posttranslational regulation of DREB2A, including protein stabilization, is required for its transcriptional activity. The deletion of a 30-aa central region of DREB2A known as the negative regulatory domain (NRD) transforms DREB2A into a stable and constitutively active form referred to as DREB2A CA. However, the molecular basis of this stabilization and activation has remained unknown for a decade. Here we identified BTB/POZ AND MATH DOMAIN proteins (BPMs), substrate adaptors of the Cullin3 (CUL3)-based E3 ligase, as DREB2A-interacting proteins. We observed that DREB2A and BPMs interact in the nuclei, and that the NRD of DREB2A is sufficient for its interaction with BPMs. BPM-knockdown plants exhibited increased DREB2A accumulation and induction of DREB2A target genes under heat and drought stress conditions. Genetic analysis indicated that the depletion of BPM expression conferred enhanced thermotolerance via DREB2A stabilization. Thus, the BPM-CUL3 E3 ligase is likely the long-sought factor responsible for NRD-dependent DREB2A degradation. Through the negative regulation of DREB2A stability, BPMs modulate the heat stress response and prevent an adverse effect of excess DREB2A on plant growth. Furthermore, we found the BPM recognition motif in various transcription factors, implying a general contribution of BPM-mediated proteolysis to divergent cellular responses via an accelerated turnover of transcription factors.

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A New Role for Sterol Regulatory Element Binding Protein 1 Transcription Factors in the Regulation of Muscle Mass and Muscle Cell Differentiation

Molecular and Cellular Biology ◽

10.1128/mcb.00690-09 ◽

2009 ◽

Vol 30 (5) ◽

pp. 1182-1198 ◽

Cited By ~ 54

Author(s):

Virginie Lecomte ◽

Emmanuelle Meugnier ◽

Vanessa Euthine ◽

Christine Durand ◽

Damien Freyssenet ◽

...

Keyword(s):

Transcription Factors ◽

Muscle Mass ◽

Target Genes ◽

Binding Protein ◽

Regulatory Element ◽

Element Binding Protein ◽

Sterol Regulatory Element ◽

Myogenic Program

ABSTRACT The role of the transcription factors sterol regulatory element binding protein 1a (SREBP-1a) and SREBP-1c in the regulation of cholesterol and fatty acid metabolism has been well studied; however, little is known about their specific function in muscle. In the present study, analysis of recent microarray data from muscle cells overexpressing SREBP1 suggested that they may play a role in the regulation of myogenesis. We then demonstrated that SREBP-1a and -1c inhibit myoblast-to-myotube differentiation and also induce in vivo and in vitro muscle atrophy. Furthermore, we have identified the transcriptional repressors BHLHB2 and BHLHB3 as mediators of these effects of SREBP-1a and -1c in muscle. Both repressors are SREBP-1 target genes, and they affect the expression of numerous genes involved in the myogenic program. Our findings identify a new role for SREBP-1 transcription factors in muscle, thus linking the control of muscle mass to metabolic pathways.

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Heat stress response and heat stress transcription factors

Journal of Biosciences ◽

10.1007/bf02936124 ◽

1998 ◽

Vol 23 (4) ◽

pp. 313-329 ◽

Cited By ~ 36

Author(s):

Klaus-Dieter Scharf ◽

Ingo Höhfeld ◽

Lutz Nover

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Stress Response ◽

Heat Stress Response ◽

Heat Stress Transcription Factors

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cAMP-Responsive Element Binding Protein: A Vital Link in Embryonic Hormonal Adaptation

Endocrinology ◽

10.1210/en.2012-2096 ◽

2013 ◽

Vol 154 (6) ◽

pp. 2208-2221 ◽

Cited By ~ 13

Author(s):

Maria Schindler ◽

Sünje Fischer ◽

René Thieme ◽

Bernd Fischer ◽

Anne Navarrete Santos

Keyword(s):

Transcription Factors ◽

Target Genes ◽

Binding Protein ◽

Cell Lineage ◽

Element Binding Protein ◽

A Cell ◽

Responsive Element ◽

Camp Responsive Element Binding

Abstract The transcription factor cAMP responsive element-binding protein (CREB) and activating transcription factors (ATFs) are downstream components of the insulin/IGF cascade, playing crucial roles in maintaining cell viability and embryo survival. One of the CREB target genes is adiponectin, which acts synergistically with insulin. We have studied the CREB-ATF-adiponectin network in rabbit preimplantation development in vivo and in vitro. From the blastocyst stage onwards, CREB and ATF1, ATF3, and ATF4 are present with increasing expression for CREB, ATF1, and ATF3 during gastrulation and with a dominant expression in the embryoblast (EB). In vitro stimulation with insulin and IGF-I reduced CREB and ATF1 transcripts by approximately 50%, whereas CREB phosphorylation was increased. Activation of CREB was accompanied by subsequent reduction in adiponectin and adiponectin receptor (adipoR)1 expression. Under in vivo conditions of diabetes type 1, maternal adiponectin levels were up-regulated in serum and endometrium. Embryonic CREB expression was altered in a cell lineage-specific pattern. Although in EB cells CREB localization did not change, it was translocated from the nucleus into the cytosol in trophoblast (TB) cells. In TB, adiponectin expression was increased (diabetic 427.8 ± 59.3 pg/mL vs normoinsulinaemic 143.9 ± 26.5 pg/mL), whereas it was no longer measureable in the EB. Analysis of embryonic adipoRs showed an increased expression of adipoR1 and no changes in adipoR2 transcription. We conclude that the transcription factors CREB and ATFs vitally participate in embryo-maternal cross talk before implantation in a cell lineage-specific manner. Embryonic CREB/ATFs act as insulin/IGF sensors. Lack of insulin is compensated by a CREB-mediated adiponectin expression, which may maintain glucose uptake in blastocysts grown in diabetic mothers.

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Unique miRNAs and their targets in tomato leaf responding to combined drought and heat stress

10.21203/rs.2.14408/v3 ◽

2020 ◽

Author(s):

Rong Zhou ◽

Xiaqing Yu ◽

Carl-Otto Ottosen ◽

Tingling Zhang ◽

Zhen Wu ◽

...

Keyword(s):

Heat Stress ◽

Dna Binding ◽

Solanum Lycopersicum ◽

Target Genes ◽

Crop Improvement ◽

Regulation Of Transcription ◽

Solanum Lycopersicum L ◽

Activity Sequence ◽

Small Rna Deep Sequencing ◽

Drought And Heat Stress

Abstract Background: Both drought and heat stress are serious global problems, leading to agricultural production loss. MicroRNAs (miRNAs) play important roles in plant species responding to individual drought and heat stress. However, the miRNAs and mRNAs in association with combined drought and heat in crops like tomato remains unclear. Results: We studied the crosstalk of miRNAs and their target genes in tomato plants grown under simultaneous drought and heat stress that frequently happen in field conditions. In total, 335 known miRNAs representing 55 miRNA families and 430 potential novel miRNAs were identified in Solanum lycopersicum L. using small RNA deep sequencing. Through expression analysis, miRNAs in association with drought, heat and the combination of these were investigated. In total, 61, 74 and 37 miRNAs were differentially regulated for combination (of both stresses) vs control, combination vs drought and combination vs heat, respectively. Target genes with different expression levels were found using degradome sequencing, which were mainly involved in transcription factor activity, sequence-specific DNA binding, transcription, regulation of transcription, nucleus, DNA binding etc . The quantitative real-time polymerase chain reaction (qRT-PCR) results confirmed the accuracy of sequencing. Conclusions: Our study serves as valuable knowledge on how crop adapted to combined drought and heat stress by regulating miRNAs and mRNAs, which provide information for crop improvement to deal with future climate changes. Keywords: Solanum lycopersicum L.; miRNAs; degradome; functional analysis; combined abiotic stress

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Transcriptomic and Metabolomic Analysis of the Heat-Stress Response of Populus tomentosa Carr.

Forests ◽

10.3390/f10050383 ◽

2019 ◽

Vol 10 (5) ◽

pp. 383 ◽

Cited By ~ 7

Author(s):

Shixiong Ren ◽

Kaibiao Ma ◽

Zhaogeng Lu ◽

Gang Chen ◽

Jiawen Cui ◽

...

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Metabolic Pathways ◽

Inositol Phosphate ◽

Photosynthetic Electron Transport ◽

Tca Cycle ◽

Populus Tomentosa ◽

Light Harvesting Complexes ◽

Heat Stress Response ◽

Populus Tomentosa Carr

Plants have evolved mechanisms of stress tolerance responses to heat stress. However, little is known about metabolic responses to heat stress in trees. In this study, we exposed Populus tomentosa Carr. to control (25 °C) and heat stress (45 °C) treatments and analyzed the metabolic and transcriptomic effects. Heat stress increased the cellular concentration of H2O2 and the activities of antioxidant enzymes. The levels of proline, raffinose, and melibiose were increased by heat stress, whereas those of pyruvate, fumarate, and myo-inositol were decreased. The expression levels of most genes (PSB27, PSB28, LHCA5, PETB, and PETC) related to the light-harvesting complexes and photosynthetic electron transport system were downregulated by heat stress. Association analysis between key genes and altered metabolites indicated that glycolysis was enhanced, whereas the tricarboxylic acid (TCA) cycle was suppressed. The inositol phosphate; galactose; valine, leucine, and isoleucine; and arginine and proline metabolic pathways were significantly affected by heat stress. In addition, several transcription factors, including HSFA2, HSFA3, HSFA9, HSF4, MYB27, MYB4R1, and bZIP60 were upregulated, whereas WRKY13 and WRKY50 were downregulated by heat stress. Interestingly, under heat stress, the expression of DREB1, DREB2, DREB2E, and DREB5 was dramatically upregulated at 12 h. Our results suggest that proline, raffinose, melibiose, and several genes (e.g., PSB27, LHCA5, and PETB) and transcription factors (e.g., HSFAs and DREBs) are involved in the response to heat stress in P. tomentosa.

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Heat stress response in plants: a complex game with chaperones and more than twenty heat stress transcription factors

Journal of Biosciences ◽

10.1007/bf02712120 ◽

2004 ◽

Vol 29 (4) ◽

pp. 471-487 ◽

Cited By ~ 312

Author(s):

Sanjeev Kumar Baniwal ◽

Kapil Bharti ◽

Kwan Yu Chan ◽

Markus Fauth ◽

Arnab Ganguli ◽

...

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Stress Response ◽

Heat Stress Response ◽

Heat Stress Transcription Factors

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A Heat Stress Responsive NAC Transcription Factor Heterodimer Plays Key Roles in Rice Grain Filling

Journal of Experimental Botany ◽

10.1093/jxb/erab027 ◽

2021 ◽

Author(s):

Ye Ren ◽

Zhouquan Huang ◽

Hao Jiang ◽

Zhuo Wang ◽

Fengsheng Wu ◽

...

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Stress Responses ◽

Transcriptional Regulatory Network ◽

Grain Filling ◽

Rice Grain ◽

Knock Out ◽

Heat Stress Response ◽

Monosaccharide Transporter ◽

Stimulus Response

Abstract High temperature often leads to the failure of grain filling in rice (Oryza sativa) to cause yield loss, while the mechanism is not well elucidated yet. Here, we report that two seed-specific NAM/ATAF/CUC domain transcription factors, ONAC127 and ONAC129, are responsive to heat stress and involved in the grain filling process of rice. ONAC127 and ONAC129 are dominantly expressed in the pericarp and can form a heterodimer during rice grain filling. CRISPR/Cas9 induced mutants and overexpression lines were then generated to investigate the functions of these two transcription factors. Interestingly, both knock-out and overexpression plants showed incomplete grain filling and shrunken grains, which became more severe under heat stress. Transcriptome analysis revealed that ONAC127 and ONAC129 mainly regulate stimulus response and nutrient transport. ChIP-seq analysis identified that the direct targets of ONAC127 and ONAC129 in developing rice seeds include monosaccharide transporter OsMST6, sugar transporter OsSWEET4, calmodulin-like protein OsMSR2 and AP2/ERF factor OsEATB. These results suggest that ONAC127 and ONAC129 may regulate grain filling through affecting sugar transportation and abiotic stress responses. Overall, this study demonstrates a transcriptional regulatory network involving ONAC127 and ONAC129 and coordinating multiple pathways to modulate seed development and heat stress response at rice reproductive stage.

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Identification and Characterization of Heat-Responsive miRNAs and their Regulatory Network in Maize

10.21203/rs.3.rs-44831/v1 ◽

2020 ◽

Author(s):

Yang Zhao ◽

Qiye Wei ◽

Tianci Chen ◽

Lijuan Xu ◽

Jing Liu ◽

...

Keyword(s):

Heat Stress ◽

Regulatory Network ◽

High Throughput Sequencing ◽

Target Genes ◽

Regulatory Mechanisms ◽

Heat Stress Response ◽

Yield And Quality ◽

And Control ◽

Identification And Characterization

Abstract Background: MicroRNAs (miRNAs) are a class of small non-coding RNAs, which have been demonstrated to play essential roles in plant growth and development, and in responses to abiotic stress. Heat stress is one of the most serious stresses that affecting crop yield and quality, however, the related regulatory mechanisms of miRNAs remains poorly understanding in maize. Results: In this study, a total of 340 miRNAs, including 215 known and 125 novel members, were identified from maize seedlings under heat stress (MH) and control conditions (MC) using high-throughput sequencing approach. The 215 known miRNAs can be further divided into 40 different families, and 21-nt miRNAs were found to be most abundant among the known miRNAs. Thirty-five miRNAs, including 26 known and 9 novel members, were significantly different expressed between MC and MH libraries. Furthermore, 174 target genes were predicted to be cleaved by 115 miRNAs using degradome sequencing. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses were performed for these targets to explore the biological function and pathways involved. Based on the relationships of miRNAs, target genes and the enriched results, a regulatory network was constructed for the miRNAs and their respective target genes, and 16 significantly differently expressed miRNAs (DEMs) were involved in the network. Conclusions: The results revealed novel insights into the roles of miRNAs in heat stress response and provided a useful foundation for understanding the regulatory mechanisms of heat-responsive miRNAs in maize.

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SET-9 and SET-26 are H3K4me3 readers and play critical roles in germline development and longevity

eLife ◽

10.7554/elife.34970 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 6

Author(s):

Wenke Wang ◽

Amaresh Chaturbedi ◽

Minghui Wang ◽

Serim An ◽

Satheeja Santhi Velayudhan ◽

...

Keyword(s):

Heat Stress ◽

Stress Response ◽

Binding Sites ◽

Target Genes ◽

Germline Development ◽

Heat Stress Response ◽

C Elegans ◽

Redundant Functions

C. elegans SET-9 and SET-26 are highly homologous paralogs that share redundant functions in germline development, but SET-26 alone plays a key role in longevity and heat stress response. Whereas SET-26 is broadly expressed, SET-9 is only detectable in the germline, which likely accounts for their different biological roles. SET-9 and SET-26 bind to H3K4me3 with adjacent acetylation marks in vitro and in vivo. In the soma, SET-26 acts through DAF-16 to modulate longevity. In the germline, SET-9 and SET-26 restrict H3K4me3 domains around SET-9 and SET-26 binding sites, and regulate the expression of specific target genes, with critical consequence on germline development. SET-9 and SET-26 are highly conserved and our findings provide new insights into the functions of these H3K4me3 readers in germline development and longevity.

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Transcriptional Basis for Differential Thermosensitivity of Seedlings of Various Tomato Genotypes

Genes ◽

10.3390/genes11060655 ◽

2020 ◽

Vol 11 (6) ◽

pp. 655

Author(s):

Yangjie Hu ◽

Sotirios Fragkostefanakis ◽

Enrico Schleiff ◽

Stefan Simm

Keyword(s):

Transcription Factors ◽

Heat Stress ◽

Stress Response ◽

Elevated Temperatures ◽

Heat Stress Response ◽

Atp Production ◽

Different Temperatures ◽

Related Plant ◽

Shock Proteins ◽

Tomato Genotypes

Transcriptional reprograming after the exposure of plants to elevated temperatures is a hallmark of stress response which is required for the manifestation of thermotolerance. Central transcription factors regulate the stress survival and recovery mechanisms and many of the core responses controlled by these factors are well described. In turn, pathways and specific genes contributing to variations in the thermotolerance capacity even among closely related plant genotypes are not well defined. A seedling-based assay was developed to directly compare the growth and transcriptome response to heat stress in four tomato genotypes with contrasting thermotolerance. The conserved and the genotype-specific alterations of mRNA abundance in response to heat stress were monitored after exposure to three different temperatures. The transcripts of the majority of genes behave similarly in all genotypes, including the majority of heat stress transcription factors and heat shock proteins, but also genes involved in photosynthesis and mitochondrial ATP production. In turn, genes involved in hormone and RNA-based regulation, such as auxin- and ethylene-related genes, or transcription factors like HsfA6b, show a differential regulation that associates with the thermotolerance pattern. Our results provide an inventory of genes likely involved in core and genotype-dependent heat stress response mechanisms with putative role in thermotolerance in tomato seedlings.

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