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.

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