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

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.

Group VII Ethylene Response Factors in Arabidopsis: Regulation and Physiological Roles

“…These proteins modulate the autophagy pathway and thereby enhance Arabidopsis tolerance to nutrient starvation (Qi et al, 2017). In fact, autophagy responses are also activated during hypoxia and contribute to plant submergence tolerance (Chen et al, 2015(Chen et al, , 2017a(Chen et al, and 2017b. This evidence suggests that an additional tier of regulation might connect the ERF-VIIs to submergence responses, through the SINAT factors.…”

Transcriptomes of eight Arabidopsis thaliana accessions reveal core conserved, genotype- and organ-specific responses to flooding stress

“…Arabidopsis mutants defective in autophagy are highly sensitive to submergence (Chen et al, 2015). Several of these genes involved in fatty acid and amino acid breakdown are crucial to maintain energy status and performance during stress conditions or in nonphotosynthetic developmental stages.…”

TRAF Family Proteins Regulate Autophagy Dynamics by Modulating AUTOPHAGY PROTEIN6 Stability in Arabidopsis

“…Given that autophagy contributes to the regulation of plant responses to both biotic (e.g., bacterial and fungal pathogens) and abiotic (e.g., hypoxia) stress in Arabidopsis (Lenz et al, 2011;Chen et al, 2015), we investigated whether the deletion of TRAF1a and TRAF1b would affect plant stress resistance. To this end, we inoculated wild-type, traf1a/b-1, traf1a/b-2, and traf1a/b-3 plants with the virulent bacteria Pseudomonas syringae pv tomato DC3000 and the necrotrophic fungi Botrytis cinerea, which are widely used to evaluate plant defense responses (Lenz et al, 2011;Xiao and Chye, 2011).…”

“…Loss of TRAF1a and TRAF1b Constitutively Increases Salicylic Acid Levels, Activates PR Gene Expression, and Enhances Cell Death and Hydrogen Peroxide Production Autophagy is a protective mechanism that is essential for the disposal of damaged organelles and for the maintenance of cellular reactive oxygen species (ROS) homeostasis in plants under stress conditions, a process likely controlled by the salicylic acid (SA) signaling pathway (Liu and Bassham, 2012;Chen et al, 2015). Given that SA, jasmonates (JAs), and ROS accumulate in Arabidopsis atg mutants (Yoshimoto et al, 2009), we examined the SA, JA, and ROS levels in the TRAF1a-and TRAF1b-knockout lines using liquid chromatographymass spectrometry.…”

“…In Arabidopsis thaliana, deletion of ATG genes causes hypersensitivity to nutrient deprivation, premature leaf senescence, shortened life span, alteration of the cellular metabolome, activated innate immunity, and impaired biotic and abiotic stress tolerance (Doelling et al, 2002;Hanaoka et al, 2002;Yoshimoto et al, 2004;Liu et al, 2005;Thompson et al, 2005;Xiong et al, 2005;Phillips et al, 2008;Chung et al, 2010;Minina et al, 2013;Li et al, 2014;Chen et al, 2015;Avin-Wittenberg et al, 2015).…”