Effect of Waterlogging-Induced Autophagy on Programmed Cell Death in Arabidopsis Roots.

Bin Guan,Jiwei Li,Zhuqing Zhou,Xiangyi Deng,Chengyang Li,Dongcheng Liu,Ze Lin,Fangzhu Mei

doi:10.3389/fpls.2019.00468

Abstract

Autophagy, a highly conserved process in eukaryotes that involves vacuolar degradation of intracellular components and decomposition of damaged or toxic constituents, is induced by endogenous reactive oxygen species (ROS) accumulation, endoplasmic reticulum stress, and other factors. In plants, the role of autophagy in the induction of programmed cell death (PCD) is still unclear. Here, we show that ROS contribute to the regulation of PCD during waterlogging (which results in oxygen depletion) via autophagy. In wild-type roots, waterlogging induces the transcription of hypoxia-responsive genes and respiratory burst oxidase homolog (RBOH)-mediated ROS production. It also altered the transcription level of alternative oxidase1a and the activity level of antioxidant enzymes. Moreover, waterlogging increased the transcription levels of autophagy-related (ATG) genes and the number of autophagosomes. Autophagy first occurred in the root stele, and then autophagosomes appeared at other locations in the root. In rboh mutants, upregulation of autophagosomes was less pronounced than in the wild type upon waterlogging. However, the accumulation of ROS and the level of cell death in the roots of atg mutants were higher than those in the wild type after waterlogging. In conclusion, our results suggest that autophagy induced in Arabidopsis roots during waterlogging has an attenuating effect on PCD in the roots.

Highlights

Flooding, which results in soil waterlogging, and in many situations complete submergence, is a major issue for plant survival in many regions of the world
Accumulation of reactive oxygen species (ROS) Induced by Hypoxia Response of Waterlogged Arabidopsis thaliana To validate the system of waterlogging, we analyzed the relative expression of the hypoxia-responsive genes ADH1, PDC1, PDC2, SUS1, SUS4, lactate dehydrogenase (LDH), hemoglobin 1 (HB1), hypoxia-responsive unknown protein 43 (HUP43), and LOB domain-containing protein 41 (LBD41) (Hunt et al, 2002; Mustroph et al, 2010) in wild-type roots at 0, 4, 8, 12, and 24 h after waterlogging
The expression of the hypoxia-responsive genes ADH1, PDC1, SUS1, HB1, HUP43, and LBD41 started to increase within 4 h and peaked at 4 h (Supplementary Figure S1), and expression of PDC2, SUS4, and LDH peaked at 8 h under waterlogged conditions (Supplementary Figure S1)

Summary

Introduction

Flooding, which results in soil waterlogging, and in many situations complete submergence, is a major issue for plant survival in many regions of the world. The transition of plants from aerobic respiration to lactic acid fermentation increases the level of expression of the lactate dehydrogenase (LDH) gene (Kreuzwieser et al, 2009). The activities of enzymes required for alcohol fermentation, which include pyruvate decarboxylase (PDC) and alcohol dehydrogenase (ADH), are higher in waterlogged roots (Atkinson et al, 2008). A specific subfamily of transcription factors, Group VII ethylene response factors (ERF-VIIs), plays important roles in regulating the activation of fermentation-related genes (Bailey-Serres and Voesenek, 2008). ERF-VIIs are released and activate the expression of hypoxiaresponsive genes, including the fermentative genes PDC1 and ADH (Gasch et al, 2016)

Methods

Results

Conclusion