Plants are composed of complex organisms that include morphological, physiological and biochemical segments. A number of environmental factors such as, heavy metals, drought, salinity, heat, and cold cause stress towards plants and impact on their growth and yield values. Heavy metal contamination and drought are considered to be two significant environmental (abiotic) factors that are receiving increased attention due their effects on plants. Many plant species from previously non-drought prone areas now face drought as a new stress factor and must develop their avoidance mechanisms. Comparing drought-related tolerance strategies, plants have developed a number of strategies to fight against heavy metal pollution due to its wide coverage. These heavy metal tolerance strategies include detoxification, compartmentalization, and storage in cell vacuoles in plants. Few similarities have been found in the mechanisms of both drought and heavy metal strategies. The use of beneficial microbes is considered as one of the most promising methods to improve stress tolerance because plant-associated microbes decrease metal accumulation while enhancing nutrient supply and water under such stress. In this review, we summarize how drought and heavy metals contamination effect on plant growth, with particular focus on stress avoidance and tolerance mechanisms, as well as, the role of microbes to enhance stress tolerance. Recommendations including irrigation, fertilization and molecular techniques to increase the plant’s tolerance mechanisms against heavy metal and drought conditions are also discussed.
Introduction
Expeditious population growth, continuous industrialization and numerous anthropogenic activities are considered to be major factors responsible for the alternation of global biological, chemical, and physical environmental quality. Heavy metal, or metalloid, pollution has been considered to be one of the key anthropogenic activity effects. Heavy metal pollution has significantly increased since the initiation of global industrial revolution (Salt et al. 1995). Although some heavy metals like Zn (zinc), Cu (copper), Co (cobalt), Ni (nickel), Mo (molybdenum) and Mn (manganese) at low concentrations are essential for different metabolic and developmental pathways, elevated concentration above threshold levels in soils adversely affects plant physiology, metabolomics, and biochemical processes that lead to decreased growth, biomass, and yield (Thijs et al. 2017). In addition to restrained enzymatic function, toxic metals interfere with the uptake of essential nutrients and displace metals in biomolecules (e.g., As (arsenic) and Cd (cadmium) compete with Zn and P (phosphorus)) of plants (Mishra et al. 2017). To protect their physiological systems from heavy metal stress, plants have developed several defense mechanisms including reduction of heavy metal accumulation by sequestering metals inside vacuoles, altering pH in the rhizosphere, binding metallothionein, and stimulating different antioxidant enzymes (Clemens et al. 2002; Greger 2004; Raza et al. 2020).
Along with heavy metal pollution, climate change has a strong influence on the environment, humankind, and the plant kingdom. Even though some climate change effects have been shown to be beneficial for plant growth (increased atmospheric CO2 concentration increases plant growth), these would be nullified by other environmental alterations like elevated temperatures or irregularity in precipitation (Rajkumar et al. 2013). Decreased precipitation is considered to be a significant impact of climate change, triggering drought conditions globally. According to the US EPA (United States Environmental Protection Agency), droughts are defined by the prolonged disparity between precipitation and evaporation (EPA 2021). As such, drought alone may regulate several abiotic factors like; temperature, moisture content, and water availability in specific areas. Most plant species have certain adaptations to different abiotic factors, including cold, frost, drought, salinity, heat, etc. Droughts also play a significant role with regard to crop production; for example, corn production in year decreased by 12% when compared to the previous year in the US as a result of agricultural drought (Todaka et al. 2015).
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Abiotic stress is described as the alternation of environmental parameters that can impact a plant’s growth and production to a sub-optimum level (Cramer et al. 2011). Abiotic stresses include: extreme temperature, dehydration or water deficit conditions, increased salinity, low nutrition, radiation, and heavy metal contamination, and those also affect plant growth at different scales (Roy et al. 2021; Miryeganeh 2021). According to Tate and Gustard (2000) drought is described as the decrease in water availability during a specific period of time at a specific location. The terms “drought” and “water deficit condition” are used to refer to water limitations. Drought can more appropriately be explained as an environmental and agronomical situation, whereas water deficit explains the limitations of irrigation that trigger drought conditions (Ogbaga et al. 2020). Meanwhile, the terms “aridity” and “drought” are coupled with water precipitation. The word “aridity” is describing the kind of climate that is closely associated with increasing temperature and decreasing precipitation trends, whereas drought is the water shortage caused by below-normal precipitation for a certain period of time (Son and Bae 2015).
Plant-associated microbes also play a significant role as they facilitate different ecological processes within the soil that impact plant growth and defense mechanisms. A wide range of bacteria and fungi can confer adaptive advantages through various mechanisms to their host plant against a variety of stressors, such as drought or presence of heavy metals, salt, etc. thereby making the overall phytoremediation process considerably more efficient (Bashan et al. 2014; Bouskill et al. 2016). One of the major mechanisms of stress tolerance provided by bacteria includes the production of plant growth-promoting (PGP) substances such as 1‑aminocyclopropane-1-carboxylate (ACC), indole-3-acetic acid (IAA) and siderophores, as well as the transformation of mineral nutrients (Heidari and Golpayegani 2012; Barnawal et al. 2017). Thus, such microorganisms bestowed with abiotic stress resilience and PGP activities are crucial for successful phytoremediation processes. There are a substantial number of articles investigating heavy metal and metalloid accumulation in different crops and their health risk assessments following incorporation into the human food chain (Clemens et al. 2002; Greger 2004; Rascio and Navari-Izzo 2011; Sandhi et al. 2017, 2022). Therefore, the aim of this review is to provide a synopsis and discuss the role of heavy metals and drought stress, stress tolerance and avoidance mechanisms, and microbes-mediated tolerance due to stress activities in plants.
Methodology
This current review compiles information collected from different sources, including technical reports from reputed organizations and peer-reviewed published scientific articles available through scientific databases such as; google scholar, web of science, PubMed and ResearchGate. Different search words were used during the literature search in the above-mentioned databases such as; drought stress, global drought, aridity, Mediterranean, heavy metals, foliar uptake, stress, tolerance, avoidance, antioxidants, phytohormones, molecular mechanisms, gene expression, plant-microbe interactions, microbes-mediated tolerance, PGPR and phytoremediation. Most scientific articles included in this review were published between 2000 and 2021, but also included are a few research works published earlier. Those earlier articles were selected due to their particular scientific importance for this review article.
Global Drought Situation
There will be long-term effects of climate change as global temperatures rise worldwide. The Earth will be facing unprecedented levels of drought over the coming decades. Recent years, notably 2003, 2010, and 2018, have shown high deficiencies of precipitation that have caused large economic, social, and environmental costs and more damages are expected by the end of the 21st century (Spinoni et al. 2018; Bastos et al. 2020; Naumann et al. 2021b). In 2000, the global concern regarding water shortages and elongated periods of drought increased in Asia, Latin America, and the Caribbean, meanwhile major droughts affected much of the Middle East, south-eastern Europe, and central Asia to northern China (Sivakumar and Wilhite 2002). Among them, China and Pakistan have been severely affected by drought since the 1970s (Miyan 2015). Studies by Su et al. (2018) and Bachmair et al. (2016) reported that over 40 million hectares of agricultural production are affected yearly due to large-scale drought hazards. According to future climate change projections, drought vulnerability is anticipated to be higher by the end of 2040 (Haile et al. 2020). According to a recent study of 138 countries investigating drought, water drought variability, and drought vulnerability, 44 countries will face extremely high water-stress levels (He et al. 2021) (Fig. 1).
Fig. 1
Global water stress (categories based on low, low to medium, medium to high, high and extremely high categories, the percentage (%) placed in the map legend section) prediction in the year of 2040. (Armstrong 2022 (CC BY 3.0, https://creativecommons.org/licenses/by/3.0/))
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Climate diversity varies greatly in South Asia, for instance in Pakistan where the northeast region is covered by snow whereas the southwest is experiencing severe drought (Ullah et al. 2020). In Iran there are five well-defined geographic sections. Previous studies have shown that the western Iran has been suffering more from drought problems over the previous decades (1998–2017) and is predicted to experience prolonged severe drought in the future (Ghamghami and Irannejad 2019). In India, there is high metrological variation due to monsoonal rainfall where some regions get flooded and some regions lack severe rainfall, resulting in drought (Pal and Al-Tabbaa 2011). The total precipitation changes in timescale is one of the common parameters for the evaluation of drought situations and different mitigation strategies. For example, a very common useful scale is the Standardized Precipitation Index (SPI) and this is classified from SPI‑1 to SPI‑6 which describes agricultural droughts, and SPI‑7 to SPI-24 describes as hydrological droughts (Svoboda et al. 2012). Additionally, a scientometric-based study was conducted to evaluate drought situation, water issues, drought status, historical droughts, and their impact in Asia particularly in China, Pakistan, India and Iran (Wu et al. 2021).
Compared with Asia, an enormous number of research investigations have been conducted by the percentage of a normal index (PNI) in order to understand hot spots and the climatic trend of meteorological drought all over Europe (Böhnisch et al. 2021; Vicente-Serrano et al. 2021). The PNI is a precipitation-based index to evaluate the metrological droughts throughout the world or in a particular subcontinent (Werick et al. 1994). A recent investigation has indicated that the most drought hotspots regions in Europe, in particular southern Europe, are expected to prolong more drying in near future (Böhnisch et al. 2021). The current long-term drought trends in Western Europe are dominated by internal variability and are subject to high natural variance (Bonaccorso et al. 2003; Santos et al. 2010; Hawkins and Sutton 2011; Vicente-Serrano et al. 2021). Zhao and Dai (2017) have reported that southern Europe shows drying trends and simulated forced signals which have similar effects on several regions around the globe. Another study (2019–2021) on La Plata Basin regarding the drought situation in the South American continent, has shown a significant climatological change that indicates a clear view about the drought expansion in southern Brazil, Uruguay, Paraguay and north-eastern part of Argentina (Naumann et al. 2021a).
Heavy Metals in the Drought-prone Areas
In recent decades, the climate change has been not only increased aridity, but also increased heavy metals problems which are associated with an unprecedented expansion of the utilization of several chemicals in industrial and agricultural production (Peñuelas et al. 2002; Sardans and Peñuelas 2005; Sensuła et al. 2021). The term heavy metals or metalloids can be explained as a group of metallic or chemical elements that have high atomic weight, numbers, and densities, can persist in the soil for long periods, and that may not be degradable by any physical or biological process (Suman et al. 2018). A recent study has shown that climate changes have strong impacts on pollution pathways occurring in Arctic ecosystems (Mcdonald et al. 2005). It has already been revealed that the drought can also have various indirect effects on plant growth and development and affects trace elements accumulation, and concentration in soil (Sardans et al. 2008). Recent studies regarding drought-prone regions, for example Mediterranean shrubland, different parts of China, Europe and Africa, showed that drought changes the dynamic concentration of elements in soil and accumulation in plants species (Sardans and Peñuelas 2005, 2007; Xia et al. 2015; Edokpayi et al. 2017; Skorbiłowicz et al. 2021). Importantly, drought affects the release of soluble trace elements into the soil solution via the lysis of bacterial cells and the destruction of soil aggregation in drying-rewetting events (Turner and Haygarth 2001). Generally, drought reduces the soil moisture and diffusion function which limits microbial activities and trace elements concentrations (Sardans et al. 2008). These fluctuations of trace element concentration in soil result in an increased high concentration of some trace elements and decreases plant growth and reproduction (Xiong 2006). According to the previous investigations by Xia et al. (2015) and Sardans et al. (2008), drought as well increases trace elements such as Al (aluminum), Cr (chromium), Cu, Zn, Ni, Co, Pb (lead) and As in plants and soil which become toxic at certain levels. Similarly, drought increases sulfur (S) concentrations and different chloride concentrations (Cl-, K+ and Na+) in Mediterranean forest regions (Sardans et al. 2008; Mahouachi et al. 2006). Tipping et al. (2003) has found that during drought periods, concentration of potentially toxic elements namely Al, Ni, Cu, Zn, Cd and Pb increased. Besides those, a similar study has also reported that under drought stress conditions Al and As concentrations strongly increased in soil (Stirling et al. 2020).
Heavy Metal Uptake in the Plants
A plant can be considered as a living pump, which can accumulate and concentrate a number of elements from their surrounding environment. All plants have the capability to uptake heavy metals that are essential for their both physiological and morphological growth and development such as Zn, Cu, Fe (iron), Mn (manganese), Mg (magnesium), Mo (molybdenum) (Salt et al. 1995). Besides these essential elements, plants also accumulate a number of toxic heavy metals in their body, which can cause adverse effects during their life cycle processes. Mainly, the lack of specificity of heavy metal accumulation and distribution in a plant’s body leads to this non-essential accumulation process (Clemens et al. 2002). It is well documented that rapid urbanization and global industrialization have a strong effect on heavy metal pollution throughout the world. So, it is not only industrialization alone, more importantly, anthropogenic activities such as mining, smelting, agricultural management and so on which are considered to be significant factors for heavy metal pollution in the environment. Different anthropogenic activities including the prolonged application of phosphatic fertilizer, sewage sludge use, industrial outlet water, and smelter dust are responsible for heavy metal pollution in the agricultural soil (Yadav 2010).
The heavy metal accumulation in plants greatly depends on their bioavailability in their surrounding medium. Most previous investigations were focused on the concentration of heavy metals in the soil, water, and air, but the estimation of bioavailability gives more information, especially for risk assessment analysis (Soriano-Disla et al. 2010). However, the heavy metal bioavailability for plants depends on a number of factors of soil media such as; soil pH level, OM (organic matter) content, CEC (cation exchange capacity), soil moisture, soil clay content, redox potential, and the nature of sorbing soil surfaces (Greger 2004; McGrath et al. 1988; Verloo and Eeckhout 1990). Among these soil-related factors soil pH, CEC, clay content, and OM content contribute an important role in both heavy metal availability from the soil system and also the accumulation process in plant species (Greger 2004; Yu et al. 2013). Along with those, soil temperature also plays an important role in metal availability and accumulation in different plant species. Atmospheric temperature can affect the water availability of the soil and that could also change the OM mineralization, and thus the resulting availability of heavy metals in the soil system. The capability for accumulation of both nutrients and trace metals in plants decreases severely under drought conditions (Pascual et al. 2004). However, the temperature can affect a plant body in different ways, for example the extracellular concentration of metals increases with increased temperature, where the result is the alternation of the equilibrium between the cell wall exchange sites and the metals available in the surrounding solution (Yu et al. 2013).
The metal availability in aquatic systems are also affected by multiple factors. Metal availability or metal speciation in an aquatic system greatly depends on the number of factors in the aquatic ecosystem such as; OM content in the water, pH, redox potential, temperature, salinity, light intensity, valency state, ionic strength of the medium, hardness of the medium (de Paiva Magalhães et al. 2015; Greger 2004). Besides heavy metals, metalloids (ex; arsenic) speciation or oxidative states greatly depends on the pH and oxygenation level of the aquatic medium (Sandhi et al. 2018b; Zhao et al. 2010).
Alongside the bioavailability of heavy metals in the different environmental elements, the point of accumulation in plants also plays a vital role in heavy metal accumulation in their body. The point of accumulation of heavy metal plays also an important role as its changes for the different types of terrestrial or aquatic (including submerged, emergent floating and free-floating) plant species present in the environment (Fig. 2). Most heavy metals accumulate in plants through the root system. The plant root is considered the most important part of the plant body which is solely responsible for the uptake of heavy metals and nutrients (Li et al. 2009). Besides roots, the Arbuscular mycorrhizae (AM) in the root zone support different plants with essential nutrients from the soil through uptake by extraradical hyphae. The role of AM is considered heavy metal-specific, as it increases or has no effect on Zn, Pb, Ni, and Cu uptake but decreases Cd, Zn and Mn in the plant (Joner and Leyval 2001). However, few factors such as; root volume, root surface area, and root-specific length (SRL) in the root zone also play an important role in the accumulation of heavy metals in different plant species (Deng et al. 2020). Besides root organs, the aboveground parts, such as foliar parts, could also accumulate heavy metal from the air. The accumulation of heavy metals in the foliar surface is conducted by using the following parts such as stomata, cuticle cracks, lenticels, ectodesmata and aqueous pores (Fernández et al. 2013; Fernández and Brown 2013). The foliar accumulation occurs through ectodesmata, which is a kind of non-plasmatic channel and is placed in the cuticular membrane or outer epidermal cell wall. The accumulation of heavy metals in the foliar parts depends on a number of factors such as; foliar morphology, leaf surface, texture, chemical and physical characteristics of the absorbed heavy metals, plant habitus, exposure time, surrounding the environmental condition, and gas exchange capacity (Shahid et al. 2017). Conversely, to the uptake point in the terrestrial plants, many of the aquatic plant species can accumulate heavy metals with their whole-body part along with root organs, especially macrophyte species. Arsenic (metalloid) accumulation process is also relatively higher in those rootless plants compared to the terrestrial plant species due to the lack of barrier in between root-shoot metal transfer (Zhang et al. 2009). A macrophyte (Warnstorfia fluitans) has shown rapid accumulation of As from the water system and its thallus-like structure could play an adding factor in that process (Sandhi et al. 2018a).
Fig. 2
Heavy metal uptake points for terrestrial, emergent and submerged plant species. The red arrows indicate the uptake points of heavy metal in the plants. The black dots represent heavy metal molecules in soil and aquatic media (illustration modified from Sandhi 2017)
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Plant Tolerance and Avoidance Mechanisms
Drought has been considered as the most important abiotic factor for its effect on the regular growth rate in plants by altering activities in morphological, physiological, biochemical and molecular changes (Farhangi-Abriz and Ghassemi-Golezani 2019). This stress decreases cell water potential and turgor in the plant body and that has a strong effect on solute concentration in the cell and plant growth mechanisms (Todaka et al. 2015). Drought also influences the above-ground parts of plants, where drought decreases shoot water potential, stomatal conductance and root-surface phosphatase activity (Sardans et al. 2008). With regard to the effect of drought conditions towards heavy metal accumulation in the plant, parts have not yet been investigated thoroughly. Drought conditions could severely damage the capacity of trace elements and nutrient uptake in the plant parts. A study has found that drought could significantly reduce Cd uptake in matured peanuts (Arachis hypogaea L.) in the matured plants when compared with seedling stage conditions (Xia et al. 2015). Drought stress not only affects the heavy metal accumulation in plants, but it could also influence the heavy metal content in the soil system. A study has found that loamy soil retains heavy metal content well, whereas the evaporation process could transfer the heavy metals upward in the sandy soil in an arid region (Lima et al. 2014). A study in the Mediterranean region has found that Cd availability increased in the soil during rewetted conditions after drought and Cd concentration in the root was increased in several evergreen tree species (Sardans and Peñuelas 2007). Besides terrestrial ecosystems, drought has also had an effect on the aquatic system as drought initiates the decline of water volume levels in the perennial water resources (Bond et al. 2008). A study has detected that drought also warms the climate faster than the average weather condition, particularly southern and northeastern United States (Chiang et al. 2018). Even drought has an impact on both temperature rise and water resources, but the effect of drought on heavy metal and metalloid accumulation in aquatic plant species has not been investigated much. A recent study has found that high temperature does not have significant effect on As accumulation in a macrophyte species in a controlled climate condition (W. fluitans) (Sandhi et al. 2018b).
Drought
Plants are sessile organisms and cannot physically move unlike animals when they are exposed to adverse environmental conditions. Therefore, they have developed sophisticated signaling pathways and defensive systems to not be instantly damaged to death. Such mechanisms could occur at physiological, biochemical, molecular, tissue, organs and whole plant levels. Similar to heavy metal stress, drought stress tolerance is also divided into two schemes in the plants such as stress tolerance and avoidance (Fang and Xiong 2015). Plant drought-tolerance is particularly defined as the ability to grow, reproduce and yield by maintaining morphological, phenological, physiological, biochemical, and molecular responses (Islam et al. 2015; Sequera-Mutiozabal et al. 2016). The main scheme of drought avoidance consists of specific mechanisms such as stomatal closure for transpiration, maintaining water uptake root to shoot, the extensive root structure of roots that ultimately assist plants to drought avoidance to contribute to final yield (Fig. 3) (Turner et al. 2001; Kavar et al. 2008; Farooq et al. 2009). Another strategy is a waxy cuticle on leaves that assists to maintain water potential and the reduction of leaf temperature (Richards et al. 1986). Similarly, plants also improve phenotypic flexibility for example; reduction of the number of leaves and area in order to cut down the water budget at the cost of yield losses to respond to the drought stress (Schuppler et al. 1998).
Fig. 3
A schematic diagram shows the major stress mechanisms (in below ground and above ground parts) adapted and applied by the plant species due to the drought and heavy metal contamination in their surrounding environment
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Osmoprotection or osmotic adjustment, antioxidant and scavenging defense and alternation in metabolic pathway mechanisms are the most important physiological and biochemical approaches for drought tolerance to prolong vegetative stages and final yields (Mai-Kodomi et al. 1999; Raza et al. 2020). In drought stress conditions, plants produce more ROS (reactive oxygen species) which may cause severe damage in cell organelles, thus to overcome those plants accumulate more solutes like sugar, proline, different enzyme activation catalase (CAT), peroxidase (POD), ascorbate (ASC), superoxide dismutase (SOD) and some non-enzymatic substances such as reduced glutathione (GSH) (Islam et al. 2015; Ullah et al. 2017). Additionally, phytohormones such as jasmonic acid (JA), abscisic acid (ABA), auxin (Aux), gibberellins (GAs), ethylene (Eth), salicylic acid (SA) and cytokines (CKs) are key contributors to regulate plant growth and development under stress conditions (Ullah et al. 2018). Among the phytohormones, ABA usually presents abundantly in water stress conditions and can independently activate the genes involved in drought stress tolerance (Yang et al. 2011; Aguado et al. 2014). Likewise, exogenous ABA treatment was also found to improve plant abiotic stress tolerance by a range of physiological and biochemical changes (Akther et al. 2020). Mounting evidence suggest that ABA activates various signaling pathways of transcription factors (TFs) or kinases response, and transcriptional changes in antioxidant enzyme activity and plant metabolism towards abiotic stress adaptation (Chaves and Oliveira 2004; Liu et al. 2014; Islam et al. 2020). In addition, in the plants’ response to drought stress, at least four classes of TFs regulons can be identified as, (1) the NAC (NAM, ATAF and CUC) and ZF-HD (zinc-finger homeodomain) regulon; (2) the CBF/DREB regulon; (3) the AREB/ABF (ABA-responsive element-binding protein/ABA-binding factor) regulon; and (4) the MYC (myelocytomatosis oncogene)/MYB (myeloblastosis oncogene) regulon (Saibo et al. 2009). Throughout the regulons, the first two regulons are ABA independent and the last two are ABA dependent. In plants, up to 10% TFs are classified into WRKY, bZIP, DREB, AREB, NAC and MYB gene families while 6% only in Arabidopsis playing role drought stress by the ABA-dependent or independent pathway (Rayko et al. 2010; Jin et al. 2014).
The signaling pathway of drought tolerance and resistance, includes; perception of signals by cell membrane receptors (hormones, Ca2+) > transduction (Ca2+-dependent sensors and relay proteins) > transcriptional regulations by different TFs (Liu et al. 2014). Thus, the drought stress tolerance in a number of plant species depends on various chemical signals and the activation of the gene array that leads to the synthesis of proteins and metabolites which confer drought stress tolerance (Fang and Xiong 2015).
Heavy Metals
A number of tolerance/defense mechanisms start in the both physiological and molecular levels inside the plant body after the accumulation of heavy metals in the plants. Plant tolerance’s to particular heavy metals is regulated by a series of inter-related networks of molecular and physiological mechanisms (Shahid et al. 2017). There are two basic functional strategies in the plant body for different kinds of heavy metal uptake management, including metal exclusion (avoidance) and metal accumulation (tolerance) (PP and Puthur 2021). Depending on the heavy metal accumulation, the plant species have been classified into three different groups such as excludator metal accumulator, and hyperaccumulator (Greger 2004). Metal excluder-type plant species cause strong resistance towards heavy metal accumulation and reduce the translocation from the surrounding medium to them. The accumulator-type plant species give attention to tolerance mechanisms and concentrate accumulated heavy metal inside their body. On the contrary, hyperaccumulator plant species could absorb exceedingly higher amounts (10–1000 folds higher than non-hyperaccumulating plant species) (Greger 2004; PP and Puthur 2021; Rascio and Navari-Izzo 2011). The first line of defense against heavy metal accumulation in the plant parts occurred in their root zone. The detoxification of heavy metals in the root parts could proceed either in external or internal parts. Plants detoxify heavy metals outside of their root by converting it into a metal-oxalate complex and continue uptake, whereas complexation of metals as part of detoxification could also be executed inside of plant root (Fig. 3) (Ma and Hiradate 2000; PP and Puthur 2021). The production of root exudates could alter the pH level in the plant rhizosphere and restrict heavy metal accumulation in the apoplastic region (Ghori et al. 2019). It has also been found that root exudate secretion is also very specific for plant varieties. For example, few resistant varieties of wheat could more efficiently secret root exudates (malic acid) compared with their susceptible varieties towards Al toxicity (Huang et al. 1996). As part of metal detoxification strategies, root exudates could also repeatedly bind heavy metal ions or attach in the cell wall to reduce their mobility inside the plant body (Ghori et al. 2019). The cell vacuole inside the plant cell has an important role in non-essential metal tolerance inside the plant body. In the case of heavy metal sequestration into the cell vacuole, where metal/H+ antiporters and proton pumps play a significant role especially two transporters such as (1) vacuolar ATPase (V-ATPase) and (2) the vacuolar pyrophosphatase (V-PPase) (Khoudi 2021). The production of ROS has considered as one of the most common activities initiated due to heavy metal stress in the plant body (Ghori et al. 2019; Jalmi et al. 2018). To fight against ROS stress inside the plant body, the plant also operates with a number of chemicals and enzymes and act like antioxidants (Mittler 2002; Srivastava et al. 2011). In order to reduce heavy metal stress and as a part of the detoxification mechanisms, the plant initiated several strategies such as the formation of a complex of organic molecules to decrease the heavy metal availability. A number of organic molecules such as malate, citrate, low molecular weight protein; metallothionein (MT), low molecular weight peptides, phytochelatins (PCs) and glutathione (GSH) could assist to form a complex structure with accumulated heavy metals inside plant body (Filiz et al. 2019). The PCs are polymers of glutathione (GSH) with repeating units of γ‑glu-cys attached to a glycine residue ((γ-glu-cys)n-gly; N = 2–11) and maintain an inactive formation until the plant species have been exposed to specific heavy metals such as Ag, Cu, As, Hg, and Cd in their surrounding medium (Peterson and Oliver 2006).
Heavy metal accumulation and detoxification processes in the hyperaccumulator plant species shows exceptional strategies such as they store most of their accumulated heavy metals in their aerial parts especially in the leaves (major organ for photosynthesis process and energy production) and the detoxification process occurs in mainly in the epidermis trichomes and cuticles (less photosynthetic activities) in plants (Rascio and Navari-Izzo 2011). However, a few succulent plant (halophyte) species have been reported to tolerate heavy metals in their succulent parts, though succulent plant species are also common plant species in arid conditions (Li et al. 2019).
Role of Microbes in Alleviation of Heavy Metal and Drought Stress in Plants
As crops developments and yield are highly restricted in the semi-arid or arid region as well due to metal stress, thus it is important to understand the effects of drought and heavy metals on other environmental phenomena for example, soil aggregation in order to learn how plant growth can be improved under these adverse conditions (Bouskill et al. 2016). Drought and heavy metal stresses have been detected with almost similar effects on plant growth, by decreasing photosynthetic pigments contents, blocking gas exchange factors and production of ROS, resulting in oxidative stress (Mishra et al. 2017). However, microorganisms have been already well-known to have plenty of potential for bioremediation of soil pollutants, improvement of plant defense responses to drought, and enhance agricultural crops productivity with low input. Additionally, microorganisms can remove several heavy metals such as Cd, Pb, Zn, Cu, As, Al from rhizospheric soil through biosorption of metal ions by their functional anionic groups (Mishra et al. 2017). In arid or semiarid areas different microorganisms produce exopolysaccharide (EPS) and biosurfactants that helps to maintain soil structure and fertility even in adverse conditions by different metal contaminants (Ayangbenro and Babalola 2017). As the nature of EPS is known to be hygroscopic, therefore its helps to maintain high water concentration of soil under drought conditions, nutrients uptake in roots, and thus protect from drought (Alami et al. 2000; Bashan et al. 2014; Sandhya and Ali 2015; Lesk et al. 2016). In Table 1, different classes of microorganisms remove heavy metal contamination and secure water availability under drought stress through the production of EPS and they also increase 1‑aminocyclopropane-1-carboxylate (ACC), different phytohormone regulation, antioxidant production and volatile organic compounds (Sandhya and Ali 2015; Yadav et al. 2020).
Table 1
Role of the microbiome in drought and heavy metal stress tolerance in plants
Crops
Microbe inoculation
Abiotic stress
Tolerance strategy
Reference
Bean (Phaseolus vulgaris)
Rhizobium sp. strain YAS34
Severe drought for 25 days
Increased root nodulation, nitrogen uptake and ABA content in shoots
Miscellaneous past studies have shown that different strains of Rhizobium, Pseudomonas mendocina increase stabilization, soil fertility under drought stress conditions (Kohler et al. 2009; Yadav et al. 2020; Shintu and Jayaram 2015). Similarly, Rhizobium KYGT207 strain produces EPS which is rich in glucose, galactose and mannuronic acid that increases root-adhering soil significantly (Konnova et al. 2001). Furthermore, EPS producing cyanobacteria provide direct contact between the toxic metals and plants cells whole EPS- and ACC producing Bacillus gibsonii PM11 and Bacillus xiamenensis PM14 promote plant growth under heavy metal contamination (Jittawuttipoka et al. 2013; Zainab et al. 2020). In addition to that, EPS-producing Bacillus anthracis PM21strain enhanced seed germination, biomass productions and increased different antioxidant activities in several plant species under drought stress conditions (Ali et al. 2021). Nevertheless, plant growth-promoting (PGP) microbes and EPS productions have a significant role in alleviation/bioremediation of heavy metal and drought stress tolerance (Mosa et al. 2016; Thijs et al. 2017). Although various microbes have been shown promising results to relieve the adverse effects of drought and heavy metals, still the development and commercialization of specific abiotic stress tolerant microbes-based biofertilizers are still more conceptual than the reality. In this regard, Gholiloo et al. (2019) have recommended the utilization of Azotobacter and Azospirillum based biofertilizers.
Conclusion and Future Outlook
Water resources play the most vital role for plant’s growth, development and physiological mechanisms which include; stomatal closure, root: shoot ratio inclination, leaf area decline, and osmotic adjustment process (Kaya et al. 2006). It has already been noted that water deficit conditions are the major problem that needs to be solved in order to maintain the growth of the plant species especially in the arid region. Most arid regions are now employing different crop cultivation methods by using several advanced irrigation techniques to minimize the global food demand. Meanwhile, an alteration phase (from livestock to crop production system) is practiced in semi-arid and arid regions (Murali et al. 2020). Most of the investigations in the arid climatic zone previously focused on reducing drought conditions and plant production compared to investigating the effect of heavy metal content and their accumulation pattern in the plants. One of the major environmental catastrophes occurred in South Asia due to extensive use of groundwater-based irrigation systems for high-yielding agronomic crop varieties, with the consequence of As loading in the cereal crops (Sandhi et al. 2017). Arsenic-rich foodstuffs are already becoming a global concern due to their health threat.
In spite of this, the primary crop management practice should be irrigation management, especially in the arid region. A recent study has found that the application of deficit irrigation could be an option for crop cultivation in the arid region (Mandal et al. 2020). On the other hand, re-watering could be a concern in the arid region for increasing heavy metal solubility, since previous studies have shown that the re-watering process can enhance Cd solubility (Sardans and Peñuelas 2007). Therefore, apart from optimization of irrigation, the advanced molecular techniques such as genetic modification approach, molecular markers or QTLs (quantitative trait locus) based DNA markers techniques application in the arid region could be effective solutions for the reduction of heavy metal content in crops grown there.
Another strategy that could be applied would be to use Si (silicon) fertilization, as Si is one of the effective elements to fight against different kinds of biotic-abiotic stresses and reduce the accumulation of several heavy metals (e.g.; Cd, As) in the plant species (Greger et al. 2015; Meharg and Meharg 2015). It has also found that Si-induced drought stress alleviation in maize (Zea mays) additionally improved growth and production (Kaya et al. 2006). Along these examples, it’s also necessary to select crop varieties that have developed avoidance of heavy metals from their growth medium. In case of high heavy metal contamination, it could be possible to introduce some short rotation bioenergy crop species (e.g.; Salix spp.) and use them for removal of heavy metals in a sustainable way and later use in bioenergy production (Sandhi and Greger 2012). Additionally, utilization of plant-microbe interaction is a relatively advanced modern approach under climate change scenarios for food production. In the future, more research is necessary to develop an efficient microbial formulation for the advancement of the plant under drought and heavy metals stress that will reduce the use of chemical fertilizers and ultimately organic farming practices.
Acknowledgements
The authors are thankful to Professor Stefano Amaducci, Department of Sustainable Crop Production, Università Cattolica del Sacro Cuore, Italy for his revision and suggestions. The authors are also thankful to Anders Johnson, Department of Biology and Environmental Science, Linnaeus University, Kalmar, Sweden, for editing English grammar of this article.
Conflict of interest
M. Islam and A. Sandhi declare that they have no competing interests.
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