Molecular mechanisms mediating post-submergence recovery in Arabidopsis thaliana

Abstract

Flooding events have increased significantly because of global climate change, in which rising water levels decrease oxygen levels for plants. Feeding the world is critical amidst severe crop loss from flooding combined with a growing population. Scientific research has mostly focused on how plants respond when flooded, but less studies focused on recovery after flooding. When flooding is over, plants must adapt to a new environment with high levels of sunlight and oxygen compared to under water. This causes reactive oxygen species (ROS) to form in the plant, which are very damaging molecules that hinder photosynthesis. Plants also cannot take up water through the roots, causing leaves to undergo senescence and desiccation stress. Two Arabidopsis thaliana ecotypes with different recovery rates were compared. Lp2-6 (naturally found in Lipovec, Czech Republic) was defined as a flooding tolerant plant that recovered faster, and Bay-0 as a flooding intolerant plant with slower recovery (found in Bayreuth, Germany). Lp2-6 had more green leaves and grew new leaves faster, resulting in more seed yield. A Ribosome-sequencing technique explained differences in recovery rates between Lp2-6 and Bay-0 on the molecular level. Lp2-6 and Bay-0 had contrasting gene expression for processes related to photosynthesis, light responses, antioxidant capacity, dehydration, and senescence. Hormones signaling these biological processes were also identified. ROS formed very quickly after the plant was removed from under water; ROS formation was highest in Bay-0 at 3 hours of recovery. Lp2-6 had lower ROS during recovery because of higher antioxidant levels. ROS was found to be produced in the form of hydrogen peroxide through the gene RESPIRATORY BURST OXIDASE HOMOLOGUE D (RbohD), which was highly induced in Bay-0. However, a minimal level of ROS signaling was required for recovery. Post-submergence recovery also induced dehydration and senescence, since leaves could not take up water from damaged roots. Bay-0 had more yellowing leaves and lower water content because stomata could not close. The plant hormone abscisic acid (ABA) which normally closes the stomata instead increased levels of the gene SENESCENCE ASSOCIATED GENE 113 (SAG113) which keeps the stomata open so more water is lost. Early senescence in Bay-0 was also because of higher ORE1/NAC DOMAIN CONTAINING PROTEIN 6 (NAC6) and CHLOROPLAST VESICULATION (CV) gene expression. Meanwhile in Lp2-6, induction of GATA, NITRATE-INDUCIBLE, CARBON-METABOLISM INVOLVED (GNC) and GNC-LIKE/CYTOKININ-RESPONSIVE GATA FACTOR 1 (GNL/CGA1) helped the stomata close and delayed senescence. Controlling ROS and stomatal aperture are therefore critical for improving recovery.