Sensing and signalling in response to oxygen deprivation in plants and other organisms

Abstract

Aims and scope: All aerobic organisms require molecular di-oxygen (O2) for efficient production of ATP though oxidative phosphorylation. Cellular depletion of oxygen results in rapid molecular and physiological acclimation. The purpose of this review is to consider the processes of low oxygen sensing and response in diverse organisms, with special consideration of plant cells.

Conclusions: The sensing of oxygen deprivation in bacteria, fungi, metazoa and plants involves multiple sensors and signal transduction pathways. Cellular responses result in a reprogramming of gene expression and metabolic processes that enhance transient survival and can enable long-term tolerance to sub-optimal oxygen levels. The mechanism of sensing can involve molecules that directly bind or react with oxygen (direct sensing), or recognition of altered cellular homeostasis (indirect sensing). The growing knowledge of the activation of genes in response to oxygen deprivation has provided additional information on the response and acclimation processes. Conservation of calcium fluxes and reactive oxygen species as second messengers in signal transduction pathways in metazoa and plants may reflect the elemental importance of rapid sensing of cellular restriction in oxygen by aerobic organisms.

Fig. 1.

Sensing of oxygen deprivation through direct and indirect mechanisms. Oxygen deprivation can result in rapid changes in cell physiology, transient changes in gene transcription or long-term alterations in physiology and development. These adaptive responses are promoted by rapid alteration in the accumulation, location or activity of transcription factors or activation of signal transduction pathways. The sensing of oxygen deprivation involves molecules which bind or consume oxygen or that are altered by oxidation state. Indirect sensing occurs as a result of a change in cellular homeostasis, possibly driven by flux in cytosolic calcium levels, adenylate charge, ratio of reduced to oxidized glutathione and carbohydrate availability. Diversity in responses may result from cross-talk between one or more sensing and signalling pathways.

Fig. 2.

Sensing and signalling in response to oxygen deprivation in plant cells. Depression of cellular oxygen concentration leads to changes in the cellular milieu that promote altered gene expression, metabolism and development. To date, there is no known mechanism of direct oxygen sensing in plant cells. Indirect sensing may be regulated by the changes in cytosolic pH, local and temporal fluxes in calcium concentration, reduction in adenylate charge or production of ROS, including NO and H₂O₂. The accumulation of the active form of the ROP GTPase, ROP-GTP, stimulates the induction of ADH expression and ethanolic fermentation, at least in Arabidopsis. The increase in cytosolic calcium, released from the mitochondria and influx from the apoplast, contributes to this gene regulation. Paradoxically, the activation of ROP signalling is associated with increased levels of H₂O₂; genotypes that are unable to regulate ROP signalling negatively are sensitive to oxygen deprivation despite strong induction of ADH gene expression. ROP GTPase signalling is attenuated by a ROPGAP, which promotes hydrolysis of GTP that is bound to ROP. This negative regulation limits ROS production and most probably conserves carbohydrates. H₂O₂ is a signalling molecule in plant cells as well as a damaging agent; antioxidants and antioxidant enzymes ameliorate its accumulation. NO is also a signalling molecule; its levels may be regulated by increases in haemoglobin in response to oxygen deprivation. The growth regulators ethylene, gibberellin, auxin and ABA control developmental adaptations including aerenchyma formation, cell, stem and petiole elongation, petiole hyponasty and adventitious root formation. There is evidence of cross-talk between the response pathways.