Abstract
The molecular mechanisms controlling underwater elongation are based extensively on studies on internode elongation in the monocot rice (Oryza sativa) and petiole elongation in Rumex rosette species. Here, we characterize underwater growth in the dicot Nasturtium officinale (watercress), a wild species of the Brassicaceae family, in which submergence enhances stem elongation and suppresses petiole growth. We used a genome-wide transcriptome analysis to identify the molecular mechanisms underlying the observed antithetical growth responses. Though submergence caused a substantial reconfiguration of the petiole and stem transcriptome, only little qualitative differences were observed between both tissues. A core submergence response included hormonal regulation and metabolic readjustment for energy conservation, whereas tissue-specific responses were associated with defense, photosynthesis, and cell wall polysaccharides. Transcriptomic and physiological characterization suggested that the established ethylene, abscisic acid (ABA), and GA growth regulatory module for underwater elongation could not fully explain underwater growth in watercress. Petiole growth suppression is likely attributed to a cell cycle arrest. Underwater stem elongation is driven by an early decline in ABA and is not primarily mediated by ethylene or GA. An enhanced stem elongation observed in the night period was not linked to hypoxia and suggests an involvement of circadian regulation.
Highlights
The frequency and severity of extreme weather events, such as floods and droughts, have increased globally in recent decades due to climate change (Hirabayashi et al, 2008, 2013; Alfieri et al, 2018)
Our results indicate that the molecular processes regulating underwater growth in watercress deviate from the established ethylene–abscisic acid (ABA)–GA regulatory growth module
Submergence triggers stem elongation and petiole growth suppression in watercress Watercress responded to complete submergence under short-day conditions with increased stem internode elongation (Fig. 1a), accelerated leaf senescence, and delayed leaf formation compared with air-grown plants (Fig. S1a,b)
Summary
The frequency and severity of extreme weather events, such as floods and droughts, have increased globally in recent decades due to climate change (Hirabayashi et al, 2008, 2013; Alfieri et al, 2018). Flooding is a compound stress, during which the plant is confronted with reduced light levels due to turbid floodwaters (Vervuren et al, 2003) and a shortage in O2 and CO2, as a combined result of replacing air-filled (soil) spaces with water and restricted gas diffusion in water (Jackson, 1985). When O2 becomes limited (hypoxia), mitochondrial respiration is compromised due to the loss of a functional electron transport chain, resulting in an energy crisis. Whereas roots experience hypoxia more often, even under well-drained conditions (van Veen et al, 2016), shoots only suffer from hypoxia during the night when completely submerged unless floodwaters are turbid and severely reduce access to light (Mommer et al, 2007; Vashisht et al, 2011; van Veen et al, 2013). Underwater photosynthesis can provide some of the required O2 for respiration, but this process is restricted by low light and a slow CO2 entry into the leaves (Mommer & Visser, 2005; Pedersen et al, 2013)
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