Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding

Abstract

This review provides a comprehensive assessment of a previously unexplored topic: elucidating the role that plasma- and organelle-based membrane transporters play in plant-adaptive responses to flooding. We show that energy availability and metabolic shifts under hypoxia and anoxia are critical in regulating membrane-transport activity. We illustrate the high tissue and time dependence of this regulation, reveal the molecular identity of transporters involved and discuss the modes of their regulation. We show that both reduced oxygen availability and accumulation of transition metals in flooded roots result in a reduction in the cytosolic K(+) pool, ultimately determining the cell's fate and transition to programmed cell death (PCD). This process can be strongly affected by hypoxia-induced changes in the amino acid pool profile and, specifically, ϒ-amino butyric acid (GABA) accumulation. It is suggested that GABA plays an important regulatory role, allowing plants to proceed with H2 O2 signalling to activate a cascade of genes that mediate plant adaptation to flooding while at the same time, preventing the cell from entering a 'suicide program'. We conclude that progress in crop breeding for flooding tolerance can only be achieved by pyramiding the numerous physiological traits that confer efficient energy maintenance, cytosolic ion homeostasis, and reactive oxygen species (ROS) control and detoxification.

Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots

“…This cytosolic pH decrease is believed to represent the optimal conditions for metabolism under suboptimal oxygen supply (Ratcliffe 1997) and was postulated to act as an intracellular messenger to mediate the activation of the H + -ATPase (Reggiani et al 1992). Thus, finding QTLs associated with such cell acidosis and regulation of H + -ATPase may be a useful strategy for breeders, especially in the light of the crucial role of H + -ATPase in membrane potential maintenance and control over plant membrane transport activity (see Shabala et al 2014 for most recent review). Another important target may Sairam et al (2009) be hypoxia-induced shifts in cell metabolism and, specifically, interplay between carbohydrate concentrations, alcoholic fermentation, and GABA production (Jaeger et al 2009;Shabala 2011).…”

Regulation of Root Traits for Internal Aeration and Tolerance to Soil Waterlogging-Flooding Stress

“…This Update has focused on root aeration traits of aerenchyma, ROL barrier induction, and adventitious roots; here, we consider future research on these traits (for other traits, see Gibbs and Greenway, 2003;Greenway and Gibbs, 2003;Bailey-Serres and Voesenek, 2008;Colmer and Voesenek, 2009;Shabala et al, 2014).…”

“…This Update has focused on progress in understanding the signaling and genetic regulation of these root traits, but the need for additional physiological research on the responses of roots of various species to soil phytotoxins and root functioning in nutrient and water uptake from waterlogged soils also is emphasized (Shabala et al, 2014). The influence of a tight ROL barrier, as well as root morphology (including the role of lateral roots), on the acquisition of nutrients and water during soil waterlogging and upon subsequent drainage (including the recovery growth of roots) requires further study.…”

ROS as Key Players of Abiotic Stress Responses in Plants

“…In addition, expression of RBOHD was highly enhanced during water logging conditions in maize, suggesting that RBOHD-dependent production of H 2 O 2 play a key role in the formation of aerenchyma (Rajhi et al 2011). Furthermore, mitochondrial dysfunction and accumulation of metal ion was also shown to increase ROS production under flooding stress (Shabala et al 2014).…”