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Soil flooding creates low-oxygen environments in root zones and thus severely affects plant growth and productivity. Plants adapt to low-oxygen environments by a suite of orchestrated metabolic and anatomical alterations. Of these, formation of aerenchyma and development of adventitious roots are considered very critical to enable plant performance in waterlogged soils. Both traits have been firmly associated with stress-induced increases in ethylene levels in root tissues that operate upstream of signalling pathways. Recently, we used a bioinformatic approach to demonstrate that several Ca2+ and K+-permeable channels from KCO, AKT, and TPC families could also operate in low oxygen sensing in Arabidopsis. Here we argue that low-oxygen-induced changes to cellular ion homeostasis and operation of membrane transporters may be critical for cell fate determination and formation of the lysigenous aerenchyma in plant roots and shaping the root architecture and adventitious root development in grasses. We summarize the existing evidence for a causal link between tissue-specific changes in oxygen concentration, intracellular Ca2+ and K+homeostasis, and reactive oxygen species levels, and their role in conferring those two major traits enabling plant adaptation to a low-oxygen environment. We conclude that, for efficient operation, plants may rely on several complementary signalling pathway mechanisms that operate in concert and 'fine-tune' each other. A better understanding of this interaction may create additional and previously unexplored opportunities to crop breeders to improve cereal crop yield losses to soil flooding.
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