Ethylene-mediated hypoxia tolerance in Arabidopsis thaliana

Abstract

Global warming has led to considerable changes in weather patterns over the past decades. Extreme climate events such as flooding, are expected to become even more frequent and severe in the future. Flooding being detrimental to major crop species, will have significant negative effects on global food production. Gas exchange rate is 104 times slower underwater than in the air. Consequently, plant growth underwater suffers from a lack of oxygen (O2) and carbon dioxide, which are essential for respiration and photosynthesis, respectively. The resulting reduction in photosynthesis and respiration lead to a carbohydrate and energy crisis ultimately affecting plant performance. Restricted gas diffusion underwater also results in rapid accumulation of the plant hormone ethylene in flooded plant tissues. Ethylene has been shown to be one of the key regulators of major flood adaptive responses. Unlike other flooding signals such as O2 and light availability that can be variable depending on other factors, ethylene accumulation under flooding conditions will always occur due to physical entrapment. Therefore, it is considered a consistent and reliable early flooding signal for plants. Previous studies have suggested that, when exposed to flooding stress, this early accumulation of ethylene prepares plants for subsequent O2 crisis. However, little is known about the molecular mechanisms underlying this improved hypoxia tolerance. This thesis aims to further investigate this ethylene-mediated hypoxia tolerance using the model plant Arabidopsis thaliana. The robust system developed in chapter 2 gave us the possibility to assess the mechanism by which ethylene improved hypoxia tolerance. Considering that this early ethylene signal is not only beneficial to seedlings (Arabidopsis Col-0, 4-, 5- and 7-day-old), but also adult plants Rumex palustris, the molecular mechanisms might be distinct due to potential developmental effects. However, this also further emphasized the crucial function of ethylene in early flooding signaling throughout the entire plant life cycle. Additionally, the system also allowed us to uncover the importance of the ethylene signal also in limiting damage upon re-aeration, which is a further challenge for plants after flood waters recede. The transcriptome analysis in this thesis, both the ethylene-mediated hypoxia and reoxygenation responses of 4-day-old Col-0 seedlings (Chapter 3) and the comparison between 4- and 7-day-old seedlings (Chapter 5), allowed us to unravel the molecular changes responsible for the survival differences. Among those biological processes identified, metabolic reprogramming of hormones biosynthesis and signaling, energy metabolism, redox homeostasis and epigenetic modifications were highlighted. Meanwhile, restricted ROS accumulation post-hypoxia resulted enhanced hypoxia survival in chapter 4, suggesting that ethylene-mediated hypoxia tolerance could be linked to the enhanced oxidative stress tolerance upon re-oxygenation. In summary, the findings in this thesis demonstrated the potential ability of plants to benefit from the early flooding signal ethylene in adaptation to hypoxia stress. We identified several ethylene specific responses, including hormones interaction, energy metabolism, redox balance maintenance and epigenetic modifications, which could be facilitating the increased hypoxia survival in Arabidopsis.