The response of plants to drought and renewal (2024)

Abstract

Plants would be more vulnerable to water stress and subsequent rewatering or to a cyclical change of the water environment, which is more common under climate change conditions in the form of forecast scenarios. The effects of water stress on plants alone have been well documented in many reports. However, the combined responses to drought and rewatering and their mechanism are relatively poor. As we know, plant growth, photosynthesis and stomatal opening can be limited by water shortage, which would be regulated by physical and chemical signals. During severe drought, while peroxidation can be induced, relevant antioxidant metabolism would be involved to destroy the damage of reactive oxygen species. Upon rewatering, restoration of plant growth and photosynthesis would occur immediately through cultivation of new plant parts, reopening of stomata, and reduced peroxidation; the degree of recovery (conversely: pre-drought limitation) through reirrigation largely depends on the intensity, duration and nature of the pre-drought. Understanding how plants respond to episodic drought and irrigation pulses and the underlying mechanism is remarkably useful for implementing vegetation management practices under climate change.

Keyword:drought stress, peroxidation, photosynthesis, relative growth rate, pre-drought limitation, rewatering, signals, stomatal conductance

In the climate changing context, drought is and is becoming an acute problem that most limits plant growth and productivity of terrestrial ecosystems in many regions around the world, especially in arid and semi-arid areas.^1–3Based on the IPCC's Fourth Assessment Report, the average surface temperature on Earth will increase by 1.1 to 6.4°C by the end of this century.³It is indicated that warming above 3°C would eliminate a deeply captured carbon function of global terrestrial vegetation, shifting a net carbon source. Global warming is expected to escalate water shortages through increasing evaporation, increasing the frequency and intensity of droughts with an increase from 1% to 30% in the area of ​​extreme drought by 2100;³which would compensate for the beneficial effect of the increased CO₂concentration, further limiting the structure and function of the terrestrial ecosystem. The global climate models can predict rainfall regimes, including their distribution and amount, but the complex responses of terrestrial ecosystems to climate change can negatively affect the accuracy of the predictions.^1,4

The plant is thought to respond to water stress through dramatically complex mechanisms, from genetic molecular expression, biochemical metabolism through individual plant physiological processes to ecosystem levels.^2,5,6which can mainly include six aspects: (1) escaping drought through completion of plant life cycle before severe water shortage. E.g. earlier flowering in annual species before the onset of severe drought;⁷(2) avoiding drought by increasing the capacity to obtain water. E.g. developing or maintaining root systems, such as reduction of stomata and leaf surface;^8,9(3) drought tolerance, mainly via improving osmotic adaptability and increasing cell wall elasticity to maintain tissue turgidity;¹⁰(4) resistance to drought via alteration of the metabolic pathway to survive under severe stress (e.g., increased antioxidant metabolism);^11,12(5) giving up drought by removing part of an individual, e.g. shedding of older leaves under water stress;²(6) drought-sensitive biochemical-physiological traits for plant development under prolonged drought via genetic mutation and genetic modification.^13–15The processes may be simultaneously involved in multiple aspects of plant responses to drought stress and subsequent rewatering.

In the field context, there are always intermittent occurrences of drought and/or rewetting, especially under climate change conditions that portend more frequent droughts and floods.³The change in the water cycle can have a major impact on plant growth, photosynthesis and many important metabolic functions and thus on ecosystem productivity and agricultural performance.^5,16–18In fact, sporadic rainfall would become a critical problem to maintain the structural stability of the ecosystem and even survive in arid and semi-arid areas. For example, a small rain shower can trigger a rapid response in a desert ecosystem, kick-starting plant growth so the plants can survive.¹⁹Highlighting how plants and terrestrial ecosystems cope with anomalous variables in climate change is and always will be a crucial research question in the practical management of plant growth and vegetation productivity. Here we aim to provide a brief insight into how plants respond to drought and rewatering in terms of plant growth, gas exchange and important related physiological processes such as reactive oxygen species (ROS) metabolism. Finally, a regulatory flowchart is presented to attempt to explain the processes involved.

Plant growth and its distribution

Plant growth and biomass allocation are two most fundamental processes in the plant kingdom, which are remarkably influenced by environmental variables, including water change factor.^2,20Plant growth and vegetation production were clearly limited during the 2003 European drought with hot summers; a remarkable recovery seems visible after the wet year of 2004.^3,21The overcompensation of plant growth by rewatering after drought has also been confirmed by many experimental studies.^22–24For example, as plant individuals ofLeymus chinensishas been exposed to a short drought, leaf area was significantly stimulated by rewatering, which can always exceed the level of control bottoms under well-watered conditions.²⁴Men mePatagonsk steppe, when water was reapplied after the drought, vegetation density (as an indicator of ecosystem structure) was still not fully recovered, which would lead to annual net primary productivity gaps in the response to rewetting after the dry year,²⁵indicate that there could be so-called pre-drought mitigation (PDL). Our reports also showed that final biomass or leaf area in plants exposed to prolonged or severe drought may not reach the level of the control treatment, highlighting that whether plant growth fully recovers after rewatering may depend on the intensity before the drought. or expensive.^17,24This limitation of predrying after rewetting may contribute to meristem restriction in plant tissue.^25,26Our recent research shows that the number of tillers ofLeymus chinensiswas still lower compared to the control treated within 50 days after rewatering, but a full, even overcompensatory recovery occurred 70 days after rewatering, implying that the occurrence and development of tiller meristems is a crucial can play a role in the response to watering again after an experienced performance. -drought.¹⁷Plant growth ofKoeleria macranthahad a large response to water changes after a prolonged drought of 20 days with a lower relative water content (RWC) of 13%.²⁷However, the response to rewatering could not be observedThe media breezeplants. This might explain whyKoeleria macranthacan easily be found in calcareous grasslands where severe periods of drought often occurThe media breezedid not exist under the same extremely dry conditions,²⁷even bothThe media breezeInKoeleria macranthagrasses have a similar and high drought-tolerant trait, which was confirmed by the fact that the pollen RWC can maintain a similar level even if the soil moisture was reduced by less than 9%;²⁷It is suggested that the different responses of the two species to reirrigation may play a crucial role in their evolutionary processes under certain environmental pressures, possibly involving physiological plasticity to drought.¹⁵

Many researchers have proposed using carryover and/or memory effects to describe production's response to current environmental constraints from previous years as additional independent variables.^28,29For example, in a semiarid grassland in South Africa, Wiegand et al.²⁹found that 33–68% of unexplained variation is associated with a memory index that combines mean monthly temperature with a memory of past precipitation. The limitation of growth due to previous drought can be seen as a consequence of the memory behavior of plants under previous drought stress. In our work, PDL appeared to plant biomass under severe drought. However, no PDL of relative growth rate (RGR) was found; in contrast, stimulation occurred before the drought.¹⁷It is strongly suggested that prestress memory may play a central role in the growth of new parts rather than final production, which arises from reactivating the storage resources such as soil nutrition in addition to water recycling.

Plants can try to get water into the soil by improving the root system during soil drought. Many reports indicated that the increase in root-to-shoot biomass ratio under water stress confirms this conclusion.⁹However, during extreme soil drought, no increase in root-to-shoot ratio was observed, implying that there would be a threshold soil moisture response in response to plant biomass allocation to water stress.³⁰When the plant is exposed to extreme soil drought, its regulatory ability through an asymmetrical growth approach can also be abruptly lost.

ROS and peroxidation

Under environmental stress such as drought, rapid accumulation of ROS, including singlet oxygen (O₂⁻), superoxide (^•O₂), hydroxyl (OH⁻¹) and hydrogen peroxide (H₂O₂) can occur, which can lead to a negative impact on antioxidant metabolism and consequently damage due to cell peroxidation.^31–33In general, ROS increases during the pre-drought period can be reversed after water replenishment.^34,35There was a sharp decline in H₂O₂with a better recovery of the net photosynthesis rate (IN_net) and net transpiration rate when Prunus plants were rewatered after a prolonged drought stress of 70 days, reaching a severe water stress level of −4 MPa leaf water potential.³⁴When a T plant received a drought treatment for 20 days, leaf RWC decreased to a severe drought status of 41-53%, H₂O₂the content increased significantly and then decreased dramatically upon rewetting.³⁵H₂O₂bluegrass leaf content increased 67% with a low RWC of 68% under drought conditions, but could not return to control levels until 1 day after rewatering.³³However, in the roots, both drought and rewatering led to notable H₂O₂accumulation,³³indicating that the reaction mechanism would be different in different plant parts. As is known, antioxidant enzymes such as superoxide dismutase (SOD) may play a central role in antioxidant metabolism in plants exposed to environmental stresses, including drought, possibly by regulating their gene expression and/or activities.^32,36Although the SOD activities in the bluegrass leaves did not change obviously under moderate drought and after rewatering, the gene expressions of FeSOD and Cu/ZnSOD were remarkably down-regulated by drought, but can return to the control level after groundwater recharge.³³However, in alfalfa nodules, FeSOD and CuZnSODc were upregulated by moderate drought, while the upregulation was observed only in CuZnSODp after rewatering relative to the control level, but the expression of MnSOD for each of the treatments was kept relatively constant, implying that the responses may vary depending on the species and tissue.³⁶ROS and their regulated metabolism may depend on species, cultivars/varieties, tissue, stress intensity and duration.^34,35

Field grown evergreen plantsPhillyrea angustifolia(Oleaceae) plants, even if the leaves had a low RWC of 50% after 48 days of drought treatment, the malondialdehyde (MDA) content did not change significantly, but the photoprotector zeaxanthin and the antioxidant α-tocopherol accumulated more 200% compared to always good Watered plants and leaf reflectance also showed a corresponding change, indicating a higher capacity of photo- and antioxidant protection of this species through the involvement of the xanthophyll cycle and the promotion of antioxidants.^12,37In benthic grasses, Bian and Jiang³³reported that moderate drought and recovery have only a marginal effect on lipid peroxidation in bluegrass leaves. However, it was clearly caused by prolonged drought, as the RWC of the plant's leaves dropped to a severe dehydration level of less than 40%;³⁸and when T plants were exposed to severe water deficit, MDA accumulated significantly, which could be dramatically reversed by re-wetting,³⁹indicates that whether lipid peroxidation occurs or is restored depends strongly on the intensity/duration of drought,^33,38and species/cultivars.^35,39In our study, cell ion leakage, an indicator of damage to cell integration, was dramatically reduced by rewatering after a relatively long period of drought (30 days), although this did not reach normal levels in well-watered plants; moreover, this phenomenon only occurred in young leaves ofLeymus chinensis,²⁴implies that the new parts of the plants can have a high metabolic recovery capacity when rewatering after a lack of water before watering.

Photosynthesis and stomatal behavior

Many studies have reported drought limitation of photosynthesis.²of which a few articles addressed the photosynthetic responses to the water deficit in the cycle. As reported, a full recovery of the net photosynthetic rate (IN_net) have been observed because drought stress is eliminated after rewatering.^5,17After refreshing for example 15 days,Black peopleL. leafIN_netcan fully recover to the level recorded after a water deficit in the plants that have been rewatered to the soil moisture level per leafIN_netdecreased to almost zero at the lowest soil moisture (fraction of available groundwater, FASW 25%) at 35 days after the start of the drought treatment.⁴⁰In our latest report¹⁷severe and extreme drought caused a light-saturated net photosynthetic rate (IN_sad) to significant reductions of 22% and 75%, respectively, compared to the abundant moisture treatment as a control. However, rewatering almost completely eliminated the difference between drought-treated and control plants, indicating full recovery. ThatIN_netand stomatal conduction (G_S) in the drought-stricken summerPhillyrea angustifoliaplants was reduced by approximately 90% with a low leaf RWC of 50%, but the maximum efficiency of photosystem II (PSII) photochemistry (F_v/F_M) were not affected under the same drought conditions,¹²indicating that the downregulation of photosynthesis may mainly arise from stomatal restriction for this species. Based on recent research by Izanloo et al.⁵For different wheat cultivars, PSII activities showed different change trends when subjected to a cyclical drought regime that even reached the withering point of soil moisture, resulting in a drastic decrease inF_v/F_M(from 0.82 to 0.65) was found in Kukri plants, with no significant change for the other two cultivars compared to a well-watered treatment. Plants downLonicera japonicaThumb. with tetraploid chromosome have higher drought resistance under water shortage and faster recovery after renewal in terms of gas exchange and chlorophyll fluorescence compared to those with diploid chromosome,³⁹shows the different responses of different genetic types. In our experiment there was a clear decrease in numberF_v/F_MvanLeymus chinensisleaves under severe soil drought, while complete recovery was observed after water recharge. This indicated that, compared to these gas exchange parameters, the functional activity of PSII photochemistry may contribute to both higher drought tolerance and recovery capacity, which may not be independent of species and/or cultivars.

Stomatal regulation plays a key role in gas exchange between the vegetation-atmosphere interface. Ninety percent plant loss occurs through the stomatal opening of the transpiration tanks.⁴¹On the other hand, stomatal limitation will be recognized as an important factor for photosynthetic reduction when available water becomes scarce, while non-stomatal limitation such as decrease in Rubisco activity, CO₂The availability in the chloroplast and the efficiency of PSII photochemistry gradually increase with water stress intensity and persistence duration.^17,42,43However, stomatal conduction will not always occurIN_netin some cases,⁴⁴which can still be debated. Interestingly, the report by Flexas et al.⁴²that Rubisco's activity is directly and closely linked to the declineG_Sand mesophyll conductance induced by abscisic acid (ABA) instead of leaf RWC, indicating that some signals, such as ABA, mediate between stomatal behavior and CO₂fixation in mesophyll cells may play a sensing role in regulating the relationship between photosynthesis and stomatal movement. As reported, full recovery always occurred in both photosynthetic function and stomatal opening when rewatered after an episodic drought.⁵even a bigger oneG_Sin pre-drought treated plants this appeared after rewatering, compared to control plants that had no pre-drought experience, indicating overcompensation in gas exchange.⁴⁵Dog meLeymus chinensissheet,G_Shad only partial recovery after rewatering, but did not reach the level of the well-watered treatment,⁴⁶similar in hybrid Richter-110 (Vine berlandierix, Vine rupestris) planter.^47,48Flexas et al.⁴⁸further indicated that the relative contribution of stomatal (SL) and mesophyll conductance (MCL) limitations rather than biochemical limitations would be responsible for the reduced photosynthesis under water stress and the slow recovery after rewatering, and that the former would largely inhibit the photosynthetic recovery after rewatering can limit. The relative contributions of different limiting components during drought and after rewatering may need to be elucidated in future experiments with different species.

Moreover, unequivocally based on a recent report by Huang et al.⁴⁹H₂O₂could also be a regulator of stomatal behavior in optimizing water use efficiency (WUE), as a drought and salt tolerance (DST) protein has been confirmed to be involved in the process by mediating H₂O₂Products. There is evidence that loss of function during DST may lead to a decrease in stomatal opening and its density, thereby increasing WUE and improving the tolerance of rice plants to water deficits.⁴⁹In fact, H₂O₂produced by photorespiration may act on the redox states in leaves of antioxidant pools, implying the possibility of photorespiratory H₂O₂as a signaling role during drought.⁵⁰It is suggested that stomatal movement and photosynthesis may be related to ROS metabolism, which signals cascade and photorespiration.^50,51that need to be explored together in the future.

Signals and other biochemical process

Drought sensing signals and their roles, including physical and chemical types, are already well documented.^2,52Among them, a stress hormone, usually ABA, is highlighted, which is recognized as an important signal for sensing drought, from root to shoot.^2,41although this is not the case with all species.⁵²ABA produced in the root would be transported to the shoot, which regulates stomatal behavior.^53,54ABA may exist as an apoplastic component in the stem xylem, originating from the root via the apoplastic pathway, which may play a coupling signaling role between shoot and roots.⁵³IGlycine maxL. Merr. plants, a decrease inG_Sand an increase in xylem [ABA] may occur simultaneously before leaf turgor undergoes a significant change, suggesting that apparently root-derived ABA would regulate stomatal behavior under moderate drought.⁵⁵It is also suggested that the accumulation of ABA in leaves, induced by physical or other chemical signals from the roots, will directly regulate stomatal movement.^2,54,55There is some evidence that high ABA levels can be eliminated if the plant is rewatered to optimal water conditions.⁴¹perhaps leading to reopening of the stomata. Wheat plants with low ABA content, together with high osmotic adjustment, will achieve rapid and complete recovery of functional processes such as growth rate, photosynthesis andG_Sof drought-stressed mitigation after rewatering depending on different genotypes.⁵However, there is evidence that some physical cues, such as hydraulic pressure from roots, can cause leaf leaf closure when groundwater is in short supply.^52,55,56In some species, no ABA increase was also observed when the plants were subjected to rapid desiccation.⁵⁷An ABA application for leaves ofCraterostigma plantagineumdoes not increase drought tolerance.⁵⁸Whether and how the stomatal opening is controlled by ABA is therefore still up for debate.

Recent research has shown that the cytokinins (CKs) may have a regulatory effect in response to water stress in transgenic tobacco plants, with an increase in catalase in peroxisomes and CO₂compensation point, indicating that cytokinin-mediated occurrence of photorespiration may play a beneficial role in protecting photosynthetic processes under severely limited water conditions.⁵¹The water channel as an initial hydrostatic signal is also a crucial component for plants to absorb water from the soil and transport it to shoots and shoots that undergo an extensive biological process.^53,59Thus, under severe drought stress, damage to tissue cells may negatively impact biochemical activities, including the water channel, and as a result, the flexible response of plants to water change may be limited.⁶In another recent observation, isoprene emissions also partially recovered afterwardsIN_netfull recovery after rewatering in plants that experienced 35 days of pre-drought, suggesting that protein levels or substrate supply limited by renewed drought may play an important role in isoprene biochemical processes.⁴⁰It is noted that the limitations of predrying and recovery by subsequent rewatering can influence biochemical metabolism and signaling cascade.

Conclusions

The response of plants to water changing conditions involves many aspects, from the genetic molecular level, biochemical and physiological processes, through the whole individual to the community level. For example, when the plant is exposed to moderate drought, a stomatal opening can be reduced by sensing physical or chemical signals such as hydraulic pressure and ABA. A decrease in stomatal conductance can limit net photosynthetic rates and water transpiration under progressive water stress, leading to increased WUE because transpiration is inhibited more than photosynthesis. If drought intensity were to become severe or even extreme, photochemical efficiency and Rubisco activity would be limited, which could decreaseIN_netto zero; at the same time, other adverse biochemical-physiological metabolisms, including peroxidation, may be exacerbated, collectively reducing plant growth rates. Photosynthesis and plant growth can be stimulated immediately after applying the irrigation pulse. However, the degree and magnitude of stimulation by renewal may depend on the intensity and duration before drought (severe stress can irreversibly damage the tissue apparatus) and species/varieties from which compensatory/complete/partial recovery may occur (figure 1). Furthermore, plants could acclimatize to episodic drought or water pulses by abandoning older parts and regenerating younger parts and by promoting biomass redistribution to the roots. Highlighting the complex processes of responses to changes in the water cycle is of great ecological importance because both drying and warming trends exist in terrestrial ecosystems at global and regional scales, especially in many arid and semi-arid areas in terms of climate change prediction. The underlying mechanisms of the molecular and integrative responses to episodic drought will be further elucidated.

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Figure 1

Simplified representation of some response pathways in plants exposed to drought and subsequent rewatering. Note: From the soil, stomatal conductance and net photosynthetic rate are reduced when plants were exposed to varying degrees of drought stress involving signals such as ABA; photosynthetic equipment can be damaged during severe/extreme drought, e.g. lead to a decrease in the photochemical efficiency of PSII and an increase in peroxidation. The growth rate of plants would gradually decrease if there was a shortage of water. After replacing the water, gas exchange can take place and plant growth can recover, the extent of which obviously depends on the intensity of the drought stress.

Recognitions

Dit werk werd ondersteund door de National Key Basic Research Specific Foundation (2006CB400502), de National Natural Science Foundation of China (40625015) en de Japan Society for the Promotion of Science (P07622).

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References