Dynamics and thermal sensitivity of ribosomal RNA maturation paths in plants

Author(s):  
Thiruvenkadam Shanmugam ◽  
Deniz Streit ◽  
Frank Schroll ◽  
Jelena Kovacevic ◽  
Enrico Schleiff

Abstract Ribosome biogenesis is a constitutive fundamental process for cellular function. Its rate of production depends on the rate of maturation of precursor ribosomal RNA (pre-rRNA). The rRNA maturation paths are marked by four dominant rate-limiting intermediates with cell-type variation of the processivity rate. We have identified that high temperature stress in plants, while halting the existing pre-rRNA maturation schemes, also transiently triggers an atypical pathway for 35S pre-rRNA processing. This pathway leads to production of an aberrant precursor rRNA, reminiscent of yeast 24S, encompassing 18S and 5.8S rRNA that do not normally co-occur together at sub-unit levels; this response is elicited specifically by high and not low temperatures. We show this response to be conserved in two other model crop plant species (Rice and Tomato). This pathway persists even after returning to normal growth conditions for 1 hour and is reset between 1-6 hours after stress treatment, likely, due to resumption of normal 35S pre-rRNA synthesis and processing. The heat-induced ITS2 cleavage-derived precursors and stalled P-A2-like precursors were heterogeneous in nature with a fraction containing polymeric (A) tails. Furthermore, high temperature treatment and subsequent fractionation resulted in polysome and precursor rRNA depletion.

PLoS ONE ◽  
2020 ◽  
Vol 15 (12) ◽  
pp. e0244198
Author(s):  
Xiaoxiao Qin ◽  
Panpan Li ◽  
Shaowei Lu ◽  
Yanchuan Sun ◽  
Lifeng Meng ◽  
...  

High temperatures induce early bolting in lettuce (Lactuca sativa L.), which decreases both quality and production. However, knowledge of the molecular mechanism underlying high temperature promotes premature bolting is lacking. In this study, we compared lettuce during the bolting period induced by high temperatures (33/25 °C, day/night) to which raised under controlled temperatures (20/13 °C, day/night) using iTRAQ-based phosphoproteomic analysis. A total of 3,814 phosphorylation sites located on 1,766 phosphopeptides from 987 phosphoproteins were identified after high-temperature treatment,among which 217 phosphoproteins significantly changed their expression abundance (116 upregulated and 101 downregulated). Most phosphoproteins for which the abundance was altered were associated with the metabolic process, with the main molecular functions were catalytic activity and transporter activity. Regarding the functional pathway, starch and sucrose metabolism was the mainly enriched signaling pathways. Hence, high temperature influenced phosphoprotein activity, especially that associated with starch and sucrose metabolism. We suspected that the lettuce shorten its growth cycle and reduce vegetative growth owing to changes in the contents of starch and soluble sugar after high temperature stress, which then led to early bolting/flowering. These findings improve our understanding of the regulatory molecular mechanisms involved in lettuce bolting.


2007 ◽  
Vol 18 (2) ◽  
pp. 369-379 ◽  
Author(s):  
Frederic Pontvianne ◽  
Isabel Matía ◽  
Julien Douet ◽  
Sylvette Tourmente ◽  
Francisco J. Medina ◽  
...  

Nucleolin is one of the most abundant protein in the nucleolus and is a multifunctional protein involved in different steps of ribosome biogenesis. In contrast to animals and yeast, the genome of the model plant Arabidopsis thaliana encodes two nucleolin-like proteins, AtNUC-L1 and AtNUC-L2. However, only the AtNUC-L1 gene is ubiquitously expressed in normal growth conditions. Disruption of this AtNUC-L1 gene leads to severe plant growth and development defects. AtNUC-L1 is localized in the nucleolus, mainly in the dense fibrillar component. Absence of this protein in Atnuc-L1 plants induces nucleolar disorganization, nucleolus organizer region decondensation, and affects the accumulation levels of pre-rRNA precursors. Remarkably, in Atnuc-L1 plants the AtNUC-L2 gene is activated, suggesting that AtNUC-L2 might rescue, at least partially, the loss of AtNUC-L1. This work is the first description of a higher eukaryotic organism with a disrupted nucleolin-like gene and defines a new role for nucleolin in nucleolus structure and rDNA chromatin organization.


2018 ◽  
Author(s):  
Jinxin Li ◽  
Tingting Mao ◽  
Zhengting Lu ◽  
Mengxue Li ◽  
Zhengting Lu ◽  
...  

AbstractThe global warming has affected the growth, development and reproduction of insects. However, the molecular mechanism of high temperature stress-mediated metamorphosis regulation of lepidopteran insect has not been elucidated. In this study, the relationship between the insect developmental process and endogenous hormone level was investigated under high temperature (36 ° C) stress in Bombyx mori (B. mori). The results showed that the duration of 5th instar larvae were shortened by 28 ± 2 h, and the content of 20E was up-regulated significantly after 72 h of high temperature treatment, while the transcription levels of 20E response genes E93, Br-C, USP, E75 were up-regulated 1.35, 1.25, 1.28, and 1.27-fold, respectively. The high temperature treatment promoted the phosphorylation level of Akt and the downstream BmCncC/keap1 pathway was activated, the transcription levels of 20E synthesis-related genes cyp302a1, cyp306a1, cyp314a1 and cyp315a1 were up-regulated by 1.12, 1.51, 2.17 and 1.23-fold, respectively. After treatment with double stranded RNA of BmCncC (dsBmCncC) in BmN cells, the transcription levels of cyp302a1 and cyp306a1 were significantly decreased, whereas up-regulated by 2.15 and 1.31-fold, respectively, after treatment with CncC activator Curcumin. These results suggested that BmCncC/keap1-mediated P450 genes (cyp302a1, cyp306a1) expression resulted in the changes of endogenous hormone level, which played an important role in the regulation of metamorphosis under high temperature stress. Studies provide novel clues for understanding the CncC/keap1 pathway-mediated metamorphosis regulation mechanism in insects.Author SummaryMammalian nuclear transcription factor Nrf2 (NF-E2-related factor 2) plays an important role in the stress response of cells. CncC is a homolog of mammalian Nrf2 in insect, regulating the genes expression of insect antioxidant enzymes and cytochrome P450 detoxification enzyme. Evidence suggests that the CncC/Keap1 pathway also plays an important role in regulating insect development. Here, we investigated the regulatory mechanism between the CncC/Keap1 pathway and metabolism of silkworm hormones in Lepidoptera. We found that high temperature induction accelerated the development of silkworm, the ecdysone content and related metabolic genes in hemolymph were significantly up-regulated, the CncC/Keap1 pathway was activated, and the expression of BmCncC was significantly increased, indicating that the Cncc/Keap1 pathway plays an important role in this process. The expression of cyp302a1 and cyp306a1 was significantly decreased by RNA interference with BmCncC, which indicated that CncC in silkworm had a regulatory relationship with downstream 20E synthetic gene. In summary, the results indicate that the CncC/Keap1 pathway plays an important role in regulating hormone metabolism in silkworm, providing a basis for further study of the relationship between CncC/Keap1 pathway and development in insects.


2021 ◽  
Author(s):  
Zhaoran Wei ◽  
Qiaoling Yuan ◽  
Hai Lin ◽  
Xiaoxia Li ◽  
Chao Zhang ◽  
...  

Abstract Background: Rice plants suffer from the rising temperature which is becoming more and more prominent. Mining heat-resistant genes and applying them to rice breeding is a feasible and effective way to solve the problem.Result: Three main biomass traits, including shoot length, dry weight, and fresh weight, changed after abnormally high temperature treatment in the rice seedling stage of a recombinant inbred lines and germplasm population. Based on a comparison of the results of linkage analysis and genome-wide association analysis, two loci with lengths of 57 kb and 69 kb in qDW7 and qFW6, respectively, was associated with the rice response to abnormally high temperatures in the seedling stage. Meanwhile, based on integrated transcriptome analysis, some genes are considered as important candidate genes. Combining with known genes and analysis of homologous genes, it was found that there are eight genes in candidate intervals that need to be focused in subsequent research.Conclusions: The results indicated several relevant loci, which would help researchers to further discover beneficial heat-resistant genes that can be applied to rice heat-resistant breeding.


eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Yubing Liu ◽  
Wei Zou ◽  
Peiguo Yang ◽  
Li Wang ◽  
Yan Ma ◽  
...  

Ribosome degradation through the autophagy-lysosome pathway is crucial for cell survival during nutrient starvation, but whether it occurs under normal growth conditions and contributes to animal physiology remains unaddressed. In this study, we identified RNST-2, a C. elegans T2 family endoribonuclease, as the key enzyme that degrades ribosomal RNA in lysosomes. We found that loss of rnst-2 causes accumulation of rRNA and ribosomal proteins in enlarged lysosomes and both phenotypes are suppressed by blocking autophagy, which indicates that RNST-2 mediates autophagic degradation of ribosomal RNA in lysosomes. rnst-2(lf) mutants are defective in embryonic and larval development and are short-lived. Remarkably, simultaneous loss of RNST-2 and de novo synthesis of pyrimidine nucleotides leads to complete embryonic lethality, which is suppressed by supplements of uridine or cytidine. Our study reveals an essential role of autophagy-dependent degradation of ribosomal RNA in maintaining nucleotide homeostasis during animal development.


2019 ◽  
Vol 20 (11) ◽  
pp. 2718 ◽  
Author(s):  
Manuela Piazzi ◽  
Alberto Bavelloni ◽  
Angela Gallo ◽  
Irene Faenza ◽  
William L. Blalock

Energetically speaking, ribosome biogenesis is by far the most costly process of the cell and, therefore, must be highly regulated in order to avoid unnecessary energy expenditure. Not only must ribosomal RNA (rRNA) synthesis, ribosomal protein (RP) transcription, translation, and nuclear import, as well as ribosome assembly, be tightly controlled, these events must be coordinated with other cellular events, such as cell division and differentiation. In addition, ribosome biogenesis must respond rapidly to environmental cues mediated by internal and cell surface receptors, or stress (oxidative stress, DNA damage, amino acid depletion, etc.). This review examines some of the well-studied pathways known to control ribosome biogenesis (PI3K-AKT-mTOR, RB-p53, MYC) and how they may interact with some of the less well studied pathways (eIF2α kinase and RNA editing/splicing) in higher eukaryotes to regulate ribosome biogenesis, assembly, and protein translation in a dynamic manner.


2020 ◽  
Vol 48 (11) ◽  
pp. 5891-5906 ◽  
Author(s):  
Cristina Sorino ◽  
Valeria Catena ◽  
Tiziana Bruno ◽  
Francesca De Nicola ◽  
Stefano Scalera ◽  
...  

Abstract Originally identified as an RNA polymerase II interactor, Che-1/AATF (Che-1) has now been recognized as a multifunctional protein involved in cell-cycle regulation and cancer progression, as well as apoptosis inhibition and response to stress. This protein displays a peculiar nucleolar localization and it has recently been implicated in pre-rRNA processing and ribosome biogenesis. Here, we report the identification of a novel function of Che-1 in the regulation of ribosomal RNA (rRNA) synthesis, in both cancer and normal cells. We demonstrate that Che-1 interacts with RNA polymerase I and nucleolar upstream binding factor (UBF) and promotes RNA polymerase I-dependent transcription. Furthermore, this protein binds to the rRNA gene (rDNA) promoter and modulates its epigenetic state by contrasting the recruitment of HDAC1. Che-1 downregulation affects RNA polymerase I and UBF recruitment on rDNA and leads to reducing rDNA promoter activity and 47S pre-rRNA production. Interestingly, Che-1 depletion induces abnormal nucleolar morphology associated with re-distribution of nucleolar proteins. Finally, we show that upon DNA damage Che-1 re-localizes from rDNA to TP53 gene promoter to induce cell-cycle arrest. This previously uncharacterized function of Che-1 confirms the important role of this protein in the regulation of ribosome biogenesis, cellular proliferation and response to stress.


2020 ◽  
Vol 21 (18) ◽  
pp. 6808
Author(s):  
Yuepeng Song ◽  
Panfei Chen ◽  
Peng Liu ◽  
Chenhao Bu ◽  
Deqiang Zhang

High-temperature stress is a threat to plant development and survival. Long noncoding RNAs (lncRNAs) participate in plant stress responses, but their functions in the complex stress response network remain unknown. Poplar contributes to terrestrial ecological stability. In this study, we identified 204 high-temperature-responsive lncRNAs in an abiotic stress-tolerant poplar (Populus simonii) species using strand-specific RNA sequencing (ssRNA-seq). Mimicking overexpressed and repressed candidate lncRNAs in poplar was used to illuminate their regulation pattern on targets using nano sheet mediation. These lncRNAs were predicted to target 185 genes, of which 100 were cis genes and 119 were trans genes. Gene Ontology enrichment analysis showed that anatomical structure morphogenesis and response to stress and signaling were significantly enriched. Among heat-responsive LncRNAs, TCONS_00202587 binds to upstream sequences via its secondary structure and interferes with target gene transcription. TCONS_00260893 enhances calcium influx in response to high-temperature treatment by interfering with a specific variant/isoform of the target gene. Heterogeneous expression of these two lncRNA targets promoted photosynthetic protection and recovery, inhibited membrane peroxidation, and suppressed DNA damage in Arabidopsis under heat stress. These results showed that lncRNAs can regulate their target genes by acting as potential RNA scaffolds or through the RNA interference pathway.


2020 ◽  
Author(s):  
Zhaoran Wei ◽  
Qiaoling Yuan ◽  
Hai Lin ◽  
Xiaoxia Li ◽  
Chao Zhang ◽  
...  

Abstract Background: With the increase of global temperature, the problem of rice yield decline caused by the rising temperature is becoming more and more prominent, which urgently needs to be solved . Mining heat-resistant genes and applying them to rice breeding is a feasible and effective way to solve the problem. Result: Three main biomass traits, including shoot length, dry weight, and fresh weight, changed after abnormally high temperature treatment in the seedling stage of a recombinant inbred line and natural groups. Based on a comparison of the results of linkage analysis and genome-wide association analysis, the presence of two sections with lengths of 57 kb and 69 kb in qDW7 and q F W6 , respectively, was associated with the rice response to abnormally high temperatures in the seedling stage. Meanwhile, based on integrated transcriptome analysis, some genes are considered as candidate genes for subsequent research and analysis. Combining with reports of known genes and analysis of homologous genes, it was found that there are 8 genes in candidate genes that need to be focused in subsequent research. Conclusions: The results indicated several relevant beneficial loci reacted to heat stress in rice seedling stage, which would help researchers to further discover excellent heat-resistant genes that can be applied to rice heat-resistant breeding.


2020 ◽  
Vol 47 (3) ◽  
pp. 248-254
Author(s):  
Usamah Jaisyurahman ◽  
Desta Wirnas ◽  
Trikoesoemaningtyas ◽  
Dan Heni Purnamawati

Global warming becomes a pressure in food production sustainability because it affected crop growth and development. The purpose of this study was to obtain information on the effect of high-temperature stress on the growth and development phase of rice and to evaluate the genotype for tolerance to high-temperature stress. Two environment conditions were used in the field and greenhouse of IPB Cikabayan experimental field, IPB University from August 2016 until February 2017. The study used varieties of IPB 4S, IPB 6R, Mekongga, and Situ Patenggang. High-temperature treatment was done by transferring the rice plants to the greenhouse at 50 days after transplanting. Observations were made on the generative phase in two different environmental conditions. The results showed that the total tillers number, filled grain number per panicle, unfilled grain number per panicle, total grain number per panicle, grain filling rate, percentage of filled grain and filled grain weight per plant had different responses among rice genotypes due to high-temperature stress. High-temperature decreased pollen fertility in all genotypes, which classified IPB 4S as a sensitive genotype and Mekongga as a tolerant genotype. This information could be useful for development and improving rice variety to anticipate high-temperature stress. Keywords: Climate change, fertility, pollen, stress tolerance index


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