Limits...
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

Deficiency of autophagy attenuates plant tolerance to ethanol stress. (A) Image of the wild-type (WT) and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) before treatment (CK) and after 6-d treatment with ethanol (EtOH) or water as a control (Water). Four-wk-old WT and atg mutants were sprayed with 100 mM ethanol or water for 6 d and photographs were taken at the end of treatment. (B) Relative chlorophyll contents and electrolyte leakage of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) at 6 d after spraying with water or 100 mM ethanol. The chlorophyll contents of wild-type samples treated with water were set to 100%, and the relative chlorophyll contents in the other samples were calculated accordingly. The ionic leakages (percentages) were calculated by comparison of leaked ionic strength to the corresponding total ionic strength. Data are average values ± SD (n = 3) of 3 biological replicates. For each replicate, >10 leaves were used for each genotype. Asterisks indicate significant differences from WT (**, P < 0.01 by the Student t test). (C) Phenotype of detached leaves from 4-wk-old WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) upon water or 100 mM ethanol immersion. Photos were taken at 0 and 6 d after detachment. (D) Images of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) germinated on MS medium containing without and with 50 mM ethanol for 2 wk.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4835207&req=5

f0004: Deficiency of autophagy attenuates plant tolerance to ethanol stress. (A) Image of the wild-type (WT) and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) before treatment (CK) and after 6-d treatment with ethanol (EtOH) or water as a control (Water). Four-wk-old WT and atg mutants were sprayed with 100 mM ethanol or water for 6 d and photographs were taken at the end of treatment. (B) Relative chlorophyll contents and electrolyte leakage of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) at 6 d after spraying with water or 100 mM ethanol. The chlorophyll contents of wild-type samples treated with water were set to 100%, and the relative chlorophyll contents in the other samples were calculated accordingly. The ionic leakages (percentages) were calculated by comparison of leaked ionic strength to the corresponding total ionic strength. Data are average values ± SD (n = 3) of 3 biological replicates. For each replicate, >10 leaves were used for each genotype. Asterisks indicate significant differences from WT (**, P < 0.01 by the Student t test). (C) Phenotype of detached leaves from 4-wk-old WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) upon water or 100 mM ethanol immersion. Photos were taken at 0 and 6 d after detachment. (D) Images of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) germinated on MS medium containing without and with 50 mM ethanol for 2 wk.

Mentions: Anaerobic respiration is the major cellular activity sustaining the plant's energy supply under submergence.2 However, anaerobic respiration produces toxic products such as ethanol, acetaldehyde, and lactate, which likely affect plant growth and survival. Our observations that the atg mutants exhibited hypersensitivity to submergence and accumulated high levels of ADH1 and PDC1 mRNAs, prompted us to consider the possible relationship of autophagy to fermentation-induced toxicity. To examine this, we first evaluated the response of wild-type Arabidopsis to fermentation products by treating plants with 100 mM ethanol, 220 mM (1%) acetaldehyde, or 11 mM (0.1%) lactate; we found that all 3 chemicals significantly induced cell death, as indicated by lesions on the leaves (Fig. 4A; Fig. S6). Among the treatments, 100 mM ethanol triggered yellowing and chlorosis, which could be easily visualized; therefore, we used ethanol treatments for further study. Before treatment or treated with water for 6 d, we observed no difference between the wild-type and atg mutants (Fig. 4A). However, all atg mutants showed severe yellowing in the whole leaves treated with 100 mM ethanol (Fig. 4A). By contrast, only the bottom leaves displayed chlorosis in the wild-type plants (Fig. 4A). Measurement of chlorophyll contents in the wild-type and atg mutants upon 0- and 6-day ethanol treatments suggested a significant decline of chlorophyll upon spraying with 100 mM ethanol in the atg mutants in comparison to the wild type (Fig. 4B). Consistent with this, upon ethanol treatment, atg mutants showed significantly higher ion leakage rates than the wild type (Fig. 4B). However, the wild-type and atg mutant plants treated with acetaldehyde or lactate showed no significant differences (Fig. S6).Figure 4.


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)

Deficiency of autophagy attenuates plant tolerance to ethanol stress. (A) Image of the wild-type (WT) and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) before treatment (CK) and after 6-d treatment with ethanol (EtOH) or water as a control (Water). Four-wk-old WT and atg mutants were sprayed with 100 mM ethanol or water for 6 d and photographs were taken at the end of treatment. (B) Relative chlorophyll contents and electrolyte leakage of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) at 6 d after spraying with water or 100 mM ethanol. The chlorophyll contents of wild-type samples treated with water were set to 100%, and the relative chlorophyll contents in the other samples were calculated accordingly. The ionic leakages (percentages) were calculated by comparison of leaked ionic strength to the corresponding total ionic strength. Data are average values ± SD (n = 3) of 3 biological replicates. For each replicate, >10 leaves were used for each genotype. Asterisks indicate significant differences from WT (**, P < 0.01 by the Student t test). (C) Phenotype of detached leaves from 4-wk-old WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) upon water or 100 mM ethanol immersion. Photos were taken at 0 and 6 d after detachment. (D) Images of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) germinated on MS medium containing without and with 50 mM ethanol for 2 wk.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f0004: Deficiency of autophagy attenuates plant tolerance to ethanol stress. (A) Image of the wild-type (WT) and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) before treatment (CK) and after 6-d treatment with ethanol (EtOH) or water as a control (Water). Four-wk-old WT and atg mutants were sprayed with 100 mM ethanol or water for 6 d and photographs were taken at the end of treatment. (B) Relative chlorophyll contents and electrolyte leakage of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) at 6 d after spraying with water or 100 mM ethanol. The chlorophyll contents of wild-type samples treated with water were set to 100%, and the relative chlorophyll contents in the other samples were calculated accordingly. The ionic leakages (percentages) were calculated by comparison of leaked ionic strength to the corresponding total ionic strength. Data are average values ± SD (n = 3) of 3 biological replicates. For each replicate, >10 leaves were used for each genotype. Asterisks indicate significant differences from WT (**, P < 0.01 by the Student t test). (C) Phenotype of detached leaves from 4-wk-old WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) upon water or 100 mM ethanol immersion. Photos were taken at 0 and 6 d after detachment. (D) Images of WT and atg mutants (atg2-1, atg5-1, atg7-3, and atg10-1) germinated on MS medium containing without and with 50 mM ethanol for 2 wk.
Mentions: Anaerobic respiration is the major cellular activity sustaining the plant's energy supply under submergence.2 However, anaerobic respiration produces toxic products such as ethanol, acetaldehyde, and lactate, which likely affect plant growth and survival. Our observations that the atg mutants exhibited hypersensitivity to submergence and accumulated high levels of ADH1 and PDC1 mRNAs, prompted us to consider the possible relationship of autophagy to fermentation-induced toxicity. To examine this, we first evaluated the response of wild-type Arabidopsis to fermentation products by treating plants with 100 mM ethanol, 220 mM (1%) acetaldehyde, or 11 mM (0.1%) lactate; we found that all 3 chemicals significantly induced cell death, as indicated by lesions on the leaves (Fig. 4A; Fig. S6). Among the treatments, 100 mM ethanol triggered yellowing and chlorosis, which could be easily visualized; therefore, we used ethanol treatments for further study. Before treatment or treated with water for 6 d, we observed no difference between the wild-type and atg mutants (Fig. 4A). However, all atg mutants showed severe yellowing in the whole leaves treated with 100 mM ethanol (Fig. 4A). By contrast, only the bottom leaves displayed chlorosis in the wild-type plants (Fig. 4A). Measurement of chlorophyll contents in the wild-type and atg mutants upon 0- and 6-day ethanol treatments suggested a significant decline of chlorophyll upon spraying with 100 mM ethanol in the atg mutants in comparison to the wild type (Fig. 4B). Consistent with this, upon ethanol treatment, atg mutants showed significantly higher ion leakage rates than the wild type (Fig. 4B). However, the wild-type and atg mutant plants treated with acetaldehyde or lactate showed no significant differences (Fig. S6).Figure 4.

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