Suffer from drought to withstand the cold.

The experimental approach in crop stress physiology has often focused on the effect of a single factor, that is, the measurement of the plant’s response to a single stress factor of variable intensity (Levitt, 1980). However, in natura, a combination of sublethal stresses is frequently observed, although their interaction is rarely taken into account. Furthermore, the increase in climate variability is likely to generate an increase in the incidence of various stress factors in plants, whereas little is known about the consequences of their potential interaction. Although some ecological studies have focused on this topic (e.g., winter drought; Charrier et al., 2017), it is still poorly addressed in the agronomic context (Yu et al., 2018).

In continental and mountainous environments, cold stress during nighttime is likely to coincide with drought stress when soil water capacity is relatively low. Some of the physiological processes affected by each stress factor are similar, for example, cellular exchanges through a decrease in membrane permeability (cold) or a decrease in water content and plasmolysis (drought). The accumulation of solutes in response to these two stresses is essential to maintain the osmotic potential and a protective solvation layer around macromolecules and cell structures. Plants have therefore developed similar molecular response pathways for these stresses (Nakashima et al., 2014), generally under the control of abscisic acid (ABA), involving Dehydration Responsive Elements containing C-repeat Binding Factors (Stockinger et al., 1997). The same pathways are thus activated in responses to cold and drought, regulating responses to osmotic stress (Yamaguchi-Shinozaki and Shinozaki, 1994). In this issue of Plant Physiology, Guo et al. (2021) investigated how drought and cold signaling pathways interact and lead to modulation of stress tolerance in maize.

Preliminary exposure to one stress factor may increase the resistance to the same or other stress factors, which is called a priming effect (Martinez-Medina et al., 2016). To test whether drought stress can act as a primer in plant cold tolerance, Guo et al. (2021) exposed the chilling-sensitive species Zea mays to cold stress with or without drought priming. They also tested the involvement of ABA-regulated pathways by mimicking drought exposure through exogenous ABA application. During the stress and after a recovery period, four experimental treatments were compared to a control (no stress; Figure 1): drought (7 d dehydration down to 20% soil water content), cold (4 d at 8°C/4°C day/night), drought-primed cold (7 d dehydration down to 20% soil water content and transfer to cold conditions at Day 4), ABA and cold treatments (ABA sprays for 3 d and transfer to cold at Day 4). The plants were transferred back to normal temperature and rehydrated for 48 h during a recovery phase.

Figure 1

Experimental plan and bulk responses of plants to drought and/or cold stress during stress and after recovery. (From supplemental figure S1.  Guo et al., 2021).

After stress and recovery, Guo et al. (2021) combined measurements of physiological, transcriptomic, metabolomics, and hormonal parameters with cell imaging, focusing on structural changes in chloroplasts. During stress, they observed significant changes in leaf water content, stomatal conductance, net assimilation, and chloroplast shape for all treatments. However, these features were recovered for all treatments except cold, indicating that they were not irreversible in the drought and drought-primed cold treatments. Furthermore, the plants exposed to these treatments all survived and the damage induced on Photosystem II was repaired. The patterns of transcriptomic, metabolomic, and hormonal responses to drought-primed cold treatment were more similar to those of drought treatment than those of cold treatment during stress and also after recovery. Drought-primed plants upregulated ABA and ABA-dependent transcripts of genes involved in the biosynthesis of raffinose, trehalose, and proline that acted as cold-protection molecules. The involvement of ABA-regulated pathways was confirmed, as the exogenous application of ABA as a priming factor induced a similar behavior as the drought-primed treatment.

Drought priming thus induces the production of protective solutes and provides higher resistance to other stress factors. The understanding of the physiological mechanisms of stress priming has been consolidated by the results obtained by Guo et al. (2021) and opens new research avenues for the improvement of plant tolerance to abiotic stress in order to guarantee future yields (Zhang et al., 2004). Ecophysiological studies will also benefit from these results as interacting abiotic factors limit the ranges of plant species at high latitude and elevation (Charrier et al., 2020). Stress priming may at times be detrimental, for example, in plants exposed to drought, an extended limitation of photosynthesis by stomatal closure would lead to a decrease in the level of nonstructural carbohydrates, resulting in a lower concentration of solutes and thus lower stress tolerance. It would now be useful to identify and assess physiological thresholds that induce stress priming to unravel the interaction, especially as we expect to see higher occurrence of combined stress factors with climate change.

Funding

This work has been carried out with the financial support of the Auvergne-Rhône-Alpes regional Council (Doux-Glace) and the Agence Nationale de la Recherche (Acoufollow ANR-20-CE91-0008).