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Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana.

Chen L, Liao B, Qi H, Xie LJ, Huang L, Tan WJ, Zhai N, Yuan LB, Zhou Y, Yu LJ, Chen QF, Shu W, Xiao S - Autophagy (2015)

Bottom Line: Both submergence and ethanol treatments induce the accumulation of reactive oxygen species (ROS) in the rosettes of atg mutants more than in the wild type.Moreover, the production of ROS by the nicotinamide adenine dinucleotide phosphate (NADPH) oxidases is necessary for plant tolerance to submergence and ethanol, submergence-induced expression of ADH1 and PDC1, and activation of autophagy.The submergence- and ethanol-sensitive phenotypes in the atg mutants depend on a complete salicylic acid (SA) signaling pathway.

View Article: PubMed Central - PubMed

Affiliation: a State Key Laboratory of Biocontrol; Guangdong Provincial Key Laboratory of Plant Resources; Collaborative Innovation Center of Genetics and Development; School of Life Sciences; Sun Yat-sen University ; Guangzhou , China.

ABSTRACT
Autophagy involves massive degradation of intracellular components and functions as a conserved system that helps cells to adapt to adverse conditions. In mammals, hypoxia rapidly stimulates autophagy as a cell survival response. Here, we examine the function of autophagy in the regulation of the plant response to submergence, an abiotic stress that leads to hypoxia and anaerobic respiration in plant cells. In Arabidopsis thaliana, submergence induces the transcription of autophagy-related (ATG) genes and the formation of autophagosomes. Consistent with this, the autophagy-defective (atg) mutants are hypersensitive to submergence stress and treatment with ethanol, the end product of anaerobic respiration. Upon submergence, the atg mutants have increased levels of transcripts of anaerobic respiration genes (alcohol dehydrogenase 1, ADH1 and pyruvate decarboxylase 1, PDC1), but reduced levels of transcripts of other hypoxia- and ethylene-responsive genes. Both submergence and ethanol treatments induce the accumulation of reactive oxygen species (ROS) in the rosettes of atg mutants more than in the wild type. Moreover, the production of ROS by the nicotinamide adenine dinucleotide phosphate (NADPH) oxidases is necessary for plant tolerance to submergence and ethanol, submergence-induced expression of ADH1 and PDC1, and activation of autophagy. The submergence- and ethanol-sensitive phenotypes in the atg mutants depend on a complete salicylic acid (SA) signaling pathway. Together, our findings demonstrate that submergence-induced autophagy functions in the hypoxia response in Arabidopsis by modulating SA-mediated cellular homeostasis.

No MeSH data available.


Related in: MedlinePlus

Relative transcript levels of hypoxia-responsive genes (A) and ethylene-responsive genes (B) in the wild type (WT) and atg mutants (atg5-1 and atg7-3) upon submergence. Total RNA was isolated from 4-wk-old WT and atg mutants at 0, 3, 6, and 24 h after light submergence treatment. Transcript levels relative to WT at 0 h were normalized to that of ACT2. The experiments have been repeated 3 times with biological replicates and similar results were obtained. Data are average values ± SD (n = 3) of 3 technical replicates. Asterisks indicate significant differences from WT (*, P < 0.05; **, P < 0.01 by the Student t test).
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f0003: Relative transcript levels of hypoxia-responsive genes (A) and ethylene-responsive genes (B) in the wild type (WT) and atg mutants (atg5-1 and atg7-3) upon submergence. Total RNA was isolated from 4-wk-old WT and atg mutants at 0, 3, 6, and 24 h after light submergence treatment. Transcript levels relative to WT at 0 h were normalized to that of ACT2. The experiments have been repeated 3 times with biological replicates and similar results were obtained. Data are average values ± SD (n = 3) of 3 technical replicates. Asterisks indicate significant differences from WT (*, P < 0.05; **, P < 0.01 by the Student t test).

Mentions: To further examine the role of autophagy in submergence response, qRT-PCR was used to measure the expression of the hypoxia marker genes ADH1, pyruvate decarboxylase 1 (PDC1), and sucrose synthase 1 (SUS1) 41 in the wild type, atg5-1, and atg7-3 mutants at 0, 3, 6, and 24 h after submergence treatment. We also measured the expression of hemoglobin 1 (HB1), hypoxia-responsive unknown protein 43 (HUP43), and lob domain-containing protein 41 (LDB41), which have been suggested to be hypoxia-responsive genes.19 As shown in Figure 3A, the transcripts of ADH1, PDC1, LBD41, and HUP43 were upregulated in atg5-1 and atg7-3 mutants under normal conditions, while those of SUS1 and HB1 were unchanged in comparison to the wild type. Whereas all of these genes were induced by submergence in the wild type, they showed differential expression in the mutants (Fig. 3A). Specifically, the transcript levels of ADH1 and PDC1 in atg5-1 and atg7-3 mutants were significantly higher at the early stages (3 h and 6 h) after submergence treatment. In contrast, the transcript levels of SUS1, HB1, HUP43, and LBD41 were significantly lower in atg5-1 and atg7-3 mutants under submergence (Fig. 3A).Figure 3.


Autophagy contributes to regulation of the hypoxia response during submergence in Arabidopsis thaliana.

Chen L, Liao B, Qi H, Xie LJ, Huang L, Tan WJ, Zhai N, Yuan LB, Zhou Y, Yu LJ, Chen QF, Shu W, Xiao S - Autophagy (2015)

Relative transcript levels of hypoxia-responsive genes (A) and ethylene-responsive genes (B) in the wild type (WT) and atg mutants (atg5-1 and atg7-3) upon submergence. Total RNA was isolated from 4-wk-old WT and atg mutants at 0, 3, 6, and 24 h after light submergence treatment. Transcript levels relative to WT at 0 h were normalized to that of ACT2. The experiments have been repeated 3 times with biological replicates and similar results were obtained. Data are average values ± SD (n = 3) of 3 technical replicates. Asterisks indicate significant differences from WT (*, P < 0.05; **, P < 0.01 by the Student t test).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835207&req=5

f0003: Relative transcript levels of hypoxia-responsive genes (A) and ethylene-responsive genes (B) in the wild type (WT) and atg mutants (atg5-1 and atg7-3) upon submergence. Total RNA was isolated from 4-wk-old WT and atg mutants at 0, 3, 6, and 24 h after light submergence treatment. Transcript levels relative to WT at 0 h were normalized to that of ACT2. The experiments have been repeated 3 times with biological replicates and similar results were obtained. Data are average values ± SD (n = 3) of 3 technical replicates. Asterisks indicate significant differences from WT (*, P < 0.05; **, P < 0.01 by the Student t test).
Mentions: To further examine the role of autophagy in submergence response, qRT-PCR was used to measure the expression of the hypoxia marker genes ADH1, pyruvate decarboxylase 1 (PDC1), and sucrose synthase 1 (SUS1) 41 in the wild type, atg5-1, and atg7-3 mutants at 0, 3, 6, and 24 h after submergence treatment. We also measured the expression of hemoglobin 1 (HB1), hypoxia-responsive unknown protein 43 (HUP43), and lob domain-containing protein 41 (LDB41), which have been suggested to be hypoxia-responsive genes.19 As shown in Figure 3A, the transcripts of ADH1, PDC1, LBD41, and HUP43 were upregulated in atg5-1 and atg7-3 mutants under normal conditions, while those of SUS1 and HB1 were unchanged in comparison to the wild type. Whereas all of these genes were induced by submergence in the wild type, they showed differential expression in the mutants (Fig. 3A). Specifically, the transcript levels of ADH1 and PDC1 in atg5-1 and atg7-3 mutants were significantly higher at the early stages (3 h and 6 h) after submergence treatment. In contrast, the transcript levels of SUS1, HB1, HUP43, and LBD41 were significantly lower in atg5-1 and atg7-3 mutants under submergence (Fig. 3A).Figure 3.

Bottom Line: Both submergence and ethanol treatments induce the accumulation of reactive oxygen species (ROS) in the rosettes of atg mutants more than in the wild type.Moreover, the production of ROS by the nicotinamide adenine dinucleotide phosphate (NADPH) oxidases is necessary for plant tolerance to submergence and ethanol, submergence-induced expression of ADH1 and PDC1, and activation of autophagy.The submergence- and ethanol-sensitive phenotypes in the atg mutants depend on a complete salicylic acid (SA) signaling pathway.

View Article: PubMed Central - PubMed

Affiliation: a State Key Laboratory of Biocontrol; Guangdong Provincial Key Laboratory of Plant Resources; Collaborative Innovation Center of Genetics and Development; School of Life Sciences; Sun Yat-sen University ; Guangzhou , China.

ABSTRACT
Autophagy involves massive degradation of intracellular components and functions as a conserved system that helps cells to adapt to adverse conditions. In mammals, hypoxia rapidly stimulates autophagy as a cell survival response. Here, we examine the function of autophagy in the regulation of the plant response to submergence, an abiotic stress that leads to hypoxia and anaerobic respiration in plant cells. In Arabidopsis thaliana, submergence induces the transcription of autophagy-related (ATG) genes and the formation of autophagosomes. Consistent with this, the autophagy-defective (atg) mutants are hypersensitive to submergence stress and treatment with ethanol, the end product of anaerobic respiration. Upon submergence, the atg mutants have increased levels of transcripts of anaerobic respiration genes (alcohol dehydrogenase 1, ADH1 and pyruvate decarboxylase 1, PDC1), but reduced levels of transcripts of other hypoxia- and ethylene-responsive genes. Both submergence and ethanol treatments induce the accumulation of reactive oxygen species (ROS) in the rosettes of atg mutants more than in the wild type. Moreover, the production of ROS by the nicotinamide adenine dinucleotide phosphate (NADPH) oxidases is necessary for plant tolerance to submergence and ethanol, submergence-induced expression of ADH1 and PDC1, and activation of autophagy. The submergence- and ethanol-sensitive phenotypes in the atg mutants depend on a complete salicylic acid (SA) signaling pathway. Together, our findings demonstrate that submergence-induced autophagy functions in the hypoxia response in Arabidopsis by modulating SA-mediated cellular homeostasis.

No MeSH data available.


Related in: MedlinePlus