When Air is in Short Supply – Shedding light on plant stress reactions when oxygen runs short

However, the elucidation of plant reactions to hypoxia confounded scientists. At the Leibniz Institute of Plant Biochemistry (IPB) in Halle (Germany) and at the University of Oxford (UK), experimental research provided the answers that closed the gaps in the existing hypotheses. Most importantly, the researchers explained the mechanism of the plant oxygen sensor and therefore the early stress reaction to hypoxia. In a paper published by Nature Communications, they share their results with us.

Even though plants produce oxygen during photosynthesis, at night and during special developmental stages, they depend on an external oxygen source to produce sufficient energy by way of their cellular respiration.

In case this oxygen is scarce, the plant throttles its metabolism by activating alternative metabolic pathways and uses these for the anaerobic degradation of nutrients. While these reactions provide less energy than the regular aerobic metabolism, the plant has still a chance to survive the time of oxygen scarcity. Switching to an anaerobic metabolism requires the activation of the necessary genes for anaerobic processes.

The protagonists of the stress reaction to hypoxia belong to the protein family of transcription factors. These factors move into the cell nucleus where they promote the transcription of genes associated with anaerobic metabolic activities. It is interesting to note that these transcription factors (the ethylene response factors [ERFs]) are always ready to initiate this stress response in an instant.

When the oxygen supply is at the regular level (normoxia) plants must actively prevent the ERFs from triggering the stress response. Experiments revealed on the molecular level that two enzymes rein in the ERFs in times of normoxia.

These enzymes accelerate the degradation of the transcription factors via the proteasome, one of the cell's removal and recycling system for proteins. Never before these details of the plant stress response to hypoxia were proven. The experiments performed by Dr. Nico Dissmeyer (IPB Halle) and Dr. Emily Flashman (University of Oxford) changed this.

According to the study, the first enzyme catalyzes the reaction, which adds two oxygen atoms to the first amino acid of the ERF protein. This first amino acid at the N-terminus (also known as amino terminus) of ERFs is cysteine. The Flashman lab proved that a plant cysteine oxidase (PCO) catalyzes this oxidation and that this oxidation occurs in a single step. So far, this PCO is the first discovered plant cysteine dioxygenase.

The oxidation of the cysteine to cysteine sulfinic acid tags the ERF protein for the attack by the second enzyme. The lab headed by Nico Dissmeyer identified the second enzyme as arginine transferase. The arginine transferase recognizes the cysteine sulfinic acid residue as its substrate and adds one arginine molecule to the N-terminus of the ERF protein.

Proteins with arginine at their N-terminus often have a extremely short life span because their N-terminus marks them for degradation. The proteasome related enzymes recognize the arginine at the end of the ERFs and initiate the degradation of ERFs via the proteasome. In times of regular oxygen supply, ERFs are degraded before they reach the cell nucleus and before they can activate the stress response genes.

In the event flooding cuts down the oxygen supply for the plant, there will not be enough oxygen for the ERF oxidation by the first enzyme. The ERF transcription factors will not be oxidized and therefore not degraded. The stable transcription factors can now move to the cell nucleus and activate the hypoxia-related genes. Therefore, the ERF transcription factors as well as the plant cysteine dioxygenases play an important role as oxygen sensor in this control loop.

Evolution could be the reason for the fact that in times of regular oxygen pressure, the plant must actively suppress the stress response to hypoxia. 460 million years ago, when plants slowly emerged from water and started living on dry land, frequent flooding was probably the way of life. Under these circumstances, it was advantageous for the survival of plants to react quickly to flooding and the stress of hypoxia.

Today, climate change brings the threat of flooding back into our focus. Therefore, the knowledge of the plant stress response to hypoxia is tremendously important. Stabilizing the ERF transcription factors or the targeted inactivation of PCOs may assist in cultivating new crop plants, which are able to withstand flooding longer and more efficiently.

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