How the Nucleus and Mitochondria Communicate in Energy Production During Stress: Nuclear MtATP6, an Early-Stress Responsive Gene, Regulates the Mitochondrial F1F0-ATP Synthase Complex

Moghadam, Ali; Ebrahimie, Esmaeil; Taghavi, Seyed Mohsen; Niazi‎, Ali; Babgohari, Mahbobeh Zamani; Deihimi, Tahereh; Djavaheri, Mohammad; Ramezani, Alireza

doi:10.1007/s12033-012-9624-6

Cited by 27 publications

(14 citation statements)

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“…ABA is a very important hormone involved in signalling of various stresses such as salinity and drought [ 29 ]. The presence of ABRE and MYB motifs were also revealed in MtATP6 promoter as an abscisic acid-mediated signalling [ 30 ]. At salt conditions, It has been also shown that lack of AtHKT1;1 ( HKT isoform in Arabidopsis thaliana ) activation in mutated Arabidopsis thaliana leads to Na + accumulation in shoot and its decrease in root, in comparison to control plants [ 8 ].…”

Section: Resultsmentioning

confidence: 99%

In silico analysis of high affinity potassium transporter (HKT) isoforms in different plants

2014

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BackgroundHigh affinity potassium transporters (HKTs) are located in the plasma membrane of the vessels and have significant influence on salt tolerance in some plants. They exclude Na+ from the parenchyma cells to reduce Na+ concentration. Despite many studies, the underlying regulatory mechanisms and the exact functions of HKTs within different genomic backgrounds are relatively unknown. In this study, various bioinformatics techniques, including promoter analysis, identification of HKT-surrounding genes, and construction of gene networks, were applied to investigate the HKT regulatory mechanism.ResultsPromoter analysis showed that rice HKTs carry ABA response elements. Additionally, jasmonic acid response elements were detected on promoter region of TmHKT1;5. In silico synteny highlighted several unknown and new loci near rice, Arabidopsis thaliana and Physcomitrella patent HKTs, which may play a significant role in salt stress tolerance in concert with HKTs. Gene network prediction unravelled that crosstalk between jasmonate and ethylene reduces AtHKT1;1 expression. Furthermore, antiporter and transferase proteins were found in AtHKT1;1 gene network. Interestingly, regulatory elements on the promoter region of HKT in wild genotype (TmHKT1;5) were more frequent and variable than the ones in cultivated wheat (TaHKT1;5) which provides the possibility of rapid response and better understanding of environmental conditions for wild genotype.ConclusionDetecting ABA and jasmonic acid response elements on promoter regions of HKTs provide valuable clues on underlying regulatory mechanisms of HKTs. In silico synteny and pathway discovery indicated several candidates which act in concert with HKTs in stress condition. We highlighted different arrangement of regulatory elements on promoter region of wild wheat (TmHKT1;5) compared to bread wheat (TaHKT1;5) in this study.

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Section: Resultsmentioning

confidence: 99%

In silico analysis of high affinity potassium transporter (HKT) isoforms in different plants

2014

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“…However, BAT is a specialized tissue dedicated to thermogenesis regulation whose main characteristic is a dramatic increase in mitochondria number and UCP1 expression [50]. In other cell types, however, decreased ATP concentration may compromise cell metabolism [51]; therefore, cells somehow sense the cytoplasmic ATP concentration as a signal to change gene expression to quickly readjust the mitochondrial architecture and cell metabolism [18,52]. In this work, we show that the overexpression of UCP1 increases uncoupled respiration and decreases cellular ATP concentration.…”

Section: Discussionmentioning

confidence: 99%

Overexpression of UCP1 in tobacco induces mitochondrial biogenesis and amplifies a broad stress response

et al. 2014

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BackgroundUncoupling protein one (UCP1) is a mitochondrial inner membrane protein capable of uncoupling the electrochemical gradient from adenosine-5′-triphosphate (ATP) synthesis, dissipating energy as heat. UCP1 plays a central role in nonshivering thermogenesis in the brown adipose tissue (BAT) of hibernating animals and small rodents. A UCP1 ortholog also occurs in plants, and aside from its role in uncoupling respiration from ATP synthesis, thereby wasting energy, it plays a beneficial role in the plant response to several abiotic stresses, possibly by decreasing the production of reactive oxygen species (ROS) and regulating cellular redox homeostasis. However, the molecular mechanisms by which UCP1 is associated with stress tolerance remain unknown.ResultsHere, we report that the overexpression of UCP1 increases mitochondrial biogenesis, increases the uncoupled respiration of isolated mitochondria, and decreases cellular ATP concentration. We observed that the overexpression of UCP1 alters mitochondrial bioenergetics and modulates mitochondrial-nuclear communication, inducing the upregulation of hundreds of nuclear- and mitochondrial-encoded mitochondrial proteins. Electron microscopy analysis showed that these metabolic changes were associated with alterations in mitochondrial number, area and morphology. Surprisingly, UCP1 overexpression also induces the upregulation of hundreds of stress-responsive genes, including some involved in the antioxidant defense system, such as superoxide dismutase (SOD), glutathione peroxidase (GPX) and glutathione-S-transferase (GST). As a consequence of the increased UCP1 activity and increased expression of oxidative stress-responsive genes, the UCP1-overexpressing plants showed reduced ROS accumulation. These beneficial metabolic effects may be responsible for the better performance of UCP1-overexpressing lines in low pH, high salt, high osmolarity, low temperature, and oxidative stress conditions.ConclusionsOverexpression of UCP1 in the mitochondrial inner membrane induced increased uncoupling respiration, decreased ROS accumulation under abiotic stresses, and diminished cellular ATP content. These events may have triggered the expression of mitochondrial and stress-responsive genes in a coordinated manner. Because these metabolic alterations did not impair plant growth and development, UCP1 overexpression can potentially be used to create crops better adapted to abiotic stress conditions.

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“…MtATP6 is a nuclear gene which encodes a 6-kDa subunit of the mitochondrial F 1 F 0 -ATP synthase complex and expression of this gene is upregulated during salt stress in Arabidopsis (ZHANG et al 2008), wheat (MOGHADAM et al 2013, and rice (ZHANG et al 2006). In wheat, both salt tolerant cultivated and wild species have higher and more prolonged expression of MtATP6 during stress than salt sensitive cultivars (MOGHADAM et al 2013). MtATP6 from the biodiesel crop Jatropha curcas was independently identified as conferring salt tolerance using a heterologous screening system in yeast (ESWARAN et al 2010).…”

Section: Regulation Of Energy Production As a Stress Tolerance Measurementioning

confidence: 99%

The role of mitochondria in plant development and stress tolerance

Liberatore

Dukowic-Schulze

Miller

et al. 2016

Free Radical Biology and Medicine

119

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Eukaryotic cells require orchestrated communication between nuclear and organellar genomes, perturbations in which are linked to stress response and disease in both animals and plants. In addition to mitochondria, which are found across eukaryotes, plant cells contain a second organelle, the plastid. Signaling both among the organelles (cytoplasmic) and between the cytoplasm and the nucleus (i.e. nuclear-cytoplasmic interactions (NCI)) is essential for proper cellular function. A deeper understanding of NCI and its impact on development, stress response, and long-term health is needed in both animal and plant systems. Here we focus on the role of plant mitochondria in development and stress response. We compare and contrast features of plant and animal mitochondrial genomes (mtDNA), particularly highlighting the large and highly dynamic nature of plant mtDNA. Plant-based tools are powerful, yet underutilized, resources for enhancing our fundamental understanding of NCI. These tools also have great potential for improving crop production. Across taxa, mitochondria are most abundant in cells that have high energy or nutrient demands as well as at key developmental time points. Although plant mitochondria act as integrators of signals involved in both development and stress response pathways, little is known about plant mtDNA diversity and its impact on these processes. In humans, there are strong correlations between particular mitotypes (and mtDNA mutations) and developmental differences (or disease). We propose that future work in plants should focus on defining mitotypes more carefully and investigating their functional implications as well as improving techniques to facilitate this research.

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How the Nucleus and Mitochondria Communicate in Energy Production During Stress: Nuclear MtATP6, an Early-Stress Responsive Gene, Regulates the Mitochondrial F1F0-ATP Synthase Complex

Cited by 27 publications

References 50 publications

In silico analysis of high affinity potassium transporter (HKT) isoforms in different plants

In silico analysis of high affinity potassium transporter (HKT) isoforms in different plants

Overexpression of UCP1 in tobacco induces mitochondrial biogenesis and amplifies a broad stress response

The role of mitochondria in plant development and stress tolerance

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