Molecular mechanisms mediating contrasting flooding survival strategies in two Rumex species

Abstract

Flooding is a major recurring event for many ecosystems and is important in shaping vegetation composition. It negatively affects plant survival because in water gas diffusion is approximately 10,000 times slower than in air. This has major repercussions for photosynthesis that requires carbon dioxide and for respiring tissues that need oxygen. Many crop plants suffer severely from flooding events. To improve survival of complete submergence, some plant species can retard growth and energy consuming processes, whilst others show a rapid upward elongation of the shoot tissue that allows for reinstating of aerial contact. Those species that elongate underwater can now use interconnected aerial spaces within the plant that allow for rapid aerial diffusion of gases. These species have escaped the negative impact of flooding by snorkeling for air. Understanding the underlying mechanisms of these contrasting survival strategies in species from flood-prone environments will provide novel insights into how plants have adapted to complete submergence, whilst simultaneously exploring tolerance mechanisms that could potentially be transferable to crop species. In an unbiased approach, two Rumex species with contrasting survival strategies were investigated, Rumex acetosa (growth retardation) and Rumex palustris (escape). With modern DNA sequencing technology specific metabolic alterations mediating growth retardation were discovered in R. acetosa. On the other hand, in R. palustris, escaping the floodwaters was found to utilize the same molecular machinery that plants use to grow towards the light, but when submerged was activated by the gaseous hormone ethylene, which accumulates in flooded organs, rather than light cues. An additional finding was the improvement of low oxygen tolerance by ethylene, only in the more frequently flooded R. palustris. Overall we thus identified several novel mechanisms with which plants could improve their tolerance to adverse flood events.