G proteins as regulators in ethylene-mediated hypoxia signaling

Abstract

Waterlogging or flooding are frequently or constitutively encountered by many plant species. The resulting reduction in endogenous O2 concentration poses a severe threat. Numerous adaptations at the anatomical, morphological and metabolic level help plants to either escape low oxygen conditions or to endure them. Formation of aerenchyma or rapid shoot elongation are escape responses, as is the formation of adventitious roots. The metabolic shift from aerobic respiration to anaerobic fermentation contributes to a basal energy supply at low oxygen conditions. Ethylene plays a central role in hypoxic stress signaling, and G proteins have been recognized as crucial signal transducers in various hypoxic signaling pathways. The programmed death of parenchyma cells that results in hypoxia-induced aerenchyma formation is an ethylene response. In maize, aerenchyma are induced in the absence of ethylene when G proteins are constitutively activated. Similarly, ethylene induced death of epidermal cells that cover adventitious roots at the stem node of rice is strictly dependent on heterotrimeric G protein activity. Knock down of the unique Gα gene RGA1 in rice prevents epidermal cell death. Finally, in Arabidopsis, induction of alcohol dehydrogenase with resulting increased plant survival relies on the balanced activities of a small Rop G protein and its deactivating protein RopGAP4. Identifying the general mechanisms of G protein signaling in hypoxia adaptation of plants is one of the tasks ahead.

Figure 1

Model of G protein signaling in hypoxia adaptation. A role for G protein signaling in submergence signaling is described for Zea mays, Arabidopsis thaliana and Oryza sativa. The known signaling pathways are summarized in this model. Waterlogging or flooding result in reduced O₂ and enhanced ethylene levels. Ethylene promotes parenchymal cell death which results in the formation of aerenchyma. In maize, pharmacological studies implicated a crucial role for G protein signaling in parenchymal cell death. In rice, epidermal cell death precedes emergence of adventitious roots. Cell death is induced by ethylene and is mediated by H₂O₂. The heterotrimeric Gα subunit RGA1 acts downstream of ethylene and H₂O₂. Genetic downregulation of RGA1 results in repression of ethylene or H₂O₂ induced epidermal cell death. G protein signaling in aerenchyma formation in Arabidopsis has not yet been analyzed but is predicted in this model. In Arabidopsis, regulation of ethanolic fermentation is mediated by the activation of a RopGTPase which causes enhanced production of reactive oxygen species, which in turn promote ethanolic fermentation, and enhance low oxygen tolerance.