Two buses together tell how plants sense that oxygen is running low

Waiting for ages for a bus to come along only for two to arrive at once is guaranteed to raise a frown, or worse. But, in this instance, two buses together are having a quite different effect. The buses concerned are two back-to-back ‘Letters’ that appeared on October 23 2011 in the journal Nature (Licausi et al. Nature doi:10.1038/nature10536 and Gibbs et al., Nature doi:10.1038/nature10534). Their appearance is bringing smiles rather than frowns to those who have long-wanted news of how plants sense that oxygen is running low and how they protect themselves against further oxygen loss. This is important since copious supplies of oxygen are needed by growing plants. However, oxygen supply is often threatened by over-wet soils and by deeper flooding or submergence especially of seedlings of our crop plants. Its not just water plants and semi-aquatic species such as rice that have evolved to cope with the problem. Land plants too possess adaptive mechanisms that cut-in when oxygen declines. These allow them to survive for a little longer if oxygen then dwindles further or disappears altogether. It has been know for years that exposing seedlings to partial oxygen shortage for a few hours improves their ability to survive a later period without oxygen. This training effect is linked to increased expression of certain genes, notably those coding for enzymes involved in anaerobic metabolism (e.g. alcohol dehydrogenase, pyruvate decarboxylase, sucrose synthase). But, how the plants sense the fall in oxygen and activate the appropriate genes has remained elusive until now. This is the question addressed by these two Letters to Nature.

Each group used the model plant Arabidopsis thaliana and each alighted on a sub-group of transcription factors called ethylene response factors (ERFs) as key mediating proteins sensing oxygen shortage. Don’t let the name mislead you. The plant hormone ethylene is neither necessarily involved in the production of sub-group members (ERF subgroupVII to be precise) nor in their activation of key adaptive genes such as alcohol dehydrogenase. Both papers also identify the regulation of ERF protein breakdown as the key oxygen-responsive process. The susceptibility of the protein breakdown mechanism to oxygen shortage is shown to depend on there being an appropriate N-terminal amino acid sequence. As oxygen concentrations fall, this terminal sequence is essential if the ERF is to be protected from the more usual degradation seen in fully aerobic cells. These N-terminal residues are found in proteins of other organisms too where they are already known to be substrates for the so-called N-end rule pathway that quickly degrades them. This pathway has an oxygen-requiring step that permits a process called ubiquitination. This, in turn, leads to breakdown within large protein bodies (proteosomes). Sensing low oxygen in plants thus amounts to blocking oxidation of a key ERF-type transcription factor at the N-terminal end. This, in turn, prolongs its cellular life sufficiently for it to activate adaptive genes needed for enhanced tolerance of oxygen loss. In addition to protecting from degradation when oxygen concentrations are low, there is a targeting of ERF to hypoxia-inducible genes in the nucleus.  Furthermore its not just enhanced post-translational stability and targeting that are involved. Transcription of the gene for the ERF known as RAP2.12 is also promoted when air (21 % oxygen) is replaced by 1 % oxygen.

Each of these two articles reinforces the other. The findings are rich in experimental detail and promise new molecular approaches to enhancing flooding tolerance in crop plants of the future. In an increasingly hungry and flood-prone world this can only be very good news.