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Overexpression of mitochondrial uncoupling protein 1 (UCP1) induces a hypoxic response in Nicotiana tabacum leaves.

ABSTRACT: Mitochondrial uncoupling protein 1 (UCP1) decreases reactive oxygen species production under stress conditions by uncoupling the electrochemical gradient from ATP synthesis. This study combined transcriptome profiling with experimentally induced hypoxia to mechanistically dissect the impact of Arabidopsis thaliana UCP1 (AtUCP1) overexpression in tobacco. Transcriptomic analysis of AtUCP1-overexpressing (P07) and wild-type (WT) plants was carried out using RNA sequencing. Metabolite and carbohydrate profiling of hypoxia-treated plants was performed using (1)H-nuclear magnetic resonance spectroscopy and high-performance anion-exchange chromatography with pulsed amperometric detection. The transcriptome of P07 plants revealed a broad induction of stress-responsive genes that were not strictly related to the mitochondrial antioxidant machinery, suggesting that overexpression of AtUCP1 imposes a strong stress response within the cell. In addition, transcripts that mapped into carbon fixation and energy expenditure pathways were broadly altered. It was found that metabolite markers of hypoxic adaptation, such as alanine and tricarboxylic acid intermediates, accumulated in P07 plants under control conditions at similar rates to WT plants under hypoxia. These findings indicate that constitutive overexpression of AtUCP1 induces a hypoxic response. The metabolites that accumulated in P07 plants are believed to be important in signalling for an improvement in carbon assimilation and induction of a hypoxic response. Under these conditions, mitochondrial ATP production is less necessary and fermentative glycolysis becomes critical to meet cell energy demands. In this scenario, the more flexible energy metabolism along with an intrinsically activated hypoxic response make these plants better adapted to face several biotic and abiotic stresses.

SUBMITTER: Barreto P

PROVIDER: S-EPMC4682437 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Overexpression of mitochondrial uncoupling protein 1 (UCP1) induces a hypoxic response in Nicotiana tabacum leaves.

Barreto Pedro P Okura Vagner V Pena Izabella A IA Maia Renato R Maia Ivan G IG Arruda Paulo P

Journal of experimental botany 20151022 1

Mitochondrial uncoupling protein 1 (UCP1) decreases reactive oxygen species production under stress conditions by uncoupling the electrochemical gradient from ATP synthesis. This study combined transcriptome profiling with experimentally induced hypoxia to mechanistically dissect the impact of Arabidopsis thaliana UCP1 (AtUCP1) overexpression in tobacco. Transcriptomic analysis of AtUCP1-overexpressing (P07) and wild-type (WT) plants was carried out using RNA sequencing. Metabolite and carbohydr ...[more]

PMID: 26494730

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Project description: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.

Project description:Crop molecular breeding primarily focuses on increasing the trait of plant yield. An elongator-associated protein, KTI12, is closely associated with plant biomass and yield. KTI12 is involved in developmental processes of most organs, including the leaf, root, flower, and seed, through regulating cell division and differentiation. Previous work has shown that in upland cotton (Gossypium hirsutum), GhKTI12 regulates plant height, flowering, and tolerance to salt and drought stress. However, little is known about the molecular regulation mechanism of GhKTI12 in plant developmental processes. In this study, we identified the main GhKTI12 (Gh_D02G144400) gene and transformed it into tobacco (Nicotonia tabacum cv NC89). From seven transgenic lines, we obtained three (OE5, OE6 and OE8) with high expression of GhKTI12; compared with wild type plants, these three lines exhibited larger plant size, later flowering, and higher seed yield. Microscopic observation revealed that the number of leaf epidermal cells and stem parenchyma cells was increased by ~55%. Biochemical analysis showed that chlorophyll content and starch accumulation were significantly increased in younger leaves at the top canopy of transgenic plants, which may contribute to improved photosynthetic rate and, in turn, increased seed yield. To understand the molecular mechanism of GhKTI12 in transgenic plants development, two lines (OE6 and OE8) with higher expression levels of GhKTI12 were used as representative plants to conduct RNA-seq analysis. Through transcriptome analysis of the plant's shoot apical meristematic tissue of these two lines, we identified 518 upregulated genes and 406 downregulated genes common to both overexpression lines. A large number of cellular component genes associated with cell division and differentiation, such as RD21, TET8, KTN80, AOX1, AOX2, CP1, and KIC, were found to be upregulated, and genes showing the most downregulation included MADS-box genes related to flowering time, such as MADS6, AP1, AP3, AGL8, AGL6, SEP1, and SEP2. Downregulation of these genes caused delayed flowering time and longer vegetative stage during development. Combined with the upregulation of the yield-related gene RD21, the GhKTI12 transgenic plants could produce a higher seed yield. We here show that the overexpression of GhKTI12 could positively improve key agronomic traits in tobacco by regulating cell proliferation, photosynthesis, and organ development, and suggest that homologs of GhKTI12 may also be important in the genetic improvement of other crop plants.

Dataset Information

Overexpression of mitochondrial uncoupling protein 1 (UCP1) induces a hypoxic response in Nicotiana tabacum leaves.

Publications

Overexpression of mitochondrial uncoupling protein 1 (UCP1) induces a hypoxic response in Nicotiana tabacum leaves.

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