1 Introduction

Arable areas are being increased in recent decades, given the demand from the growing population. As a result, arable soils are being degraded by intensive agriculture and the application of fertilizers in excess, increasing the salt content in the soil and reducing the water availability (Lichtfouse 2013). To this fact, we must add the increase in temperature and the reduction of rainfall caused by climate change (Hatfield and Dold 2019), making drought and salinity stresses the most important causes of the biggest economic losses in agriculture. For that reason, both stresses have to be deeply studied and it is required to find solutions to face them and minimize the economic losses.

The roots of the plants are organs with a great adaptive capacity, being able to grow and carry out their development under different types of substrate, hydric and nutritional conditions and under adverse environmental conditions (Babé et al. 2012; Atkinson et al. 2014; Julkowska et al. 2014; Koevoets et al. 2016; Li et al. 2016c; Gray and Brady 2016). But the molecular routes by which roots are able to grow under such conditions are being elucidated at present.

The radical system of a majority of plants consists mainly of two parts. The main or primary root which is formed embryonically (Scheres et al. 1994), and lateral roots and adventitious roots which are included as secondary roots and are formed post-embryonically (Verstraeten et al. 2014; Bellini et al. 2014). There are also differences between monocot and dicot roots. For example, dicots present a tap root system with a well-developed main root from which lateral roots come out, whereas monocots have a fibrous root system, formed by the crown or adventitious roots (Coudert et al. 2013). All this root diversity has to be taken into account to study the role of a given root system (Olatunji et al. 2017).

Nevertheless, it is known that the roots of the plants, in addition to having a nutritional function, are responsible for keeping the plants anchored to the ground (Koevoets et al. 2016; Lynch 2018), developing a strategy of defence against underground pathogens (Ray et al. 2018; Elhady et al. 2018), establishing symbiotic relationships with beneficial microorganisms of the soil to improve their nutrition (Dodd and Ruiz-Lozano 2012; Santander et al. 2017), and even to explore the soil in search of water and nutrients when their availability is low (Li et al. 2016c).

The roots have been extensively studied throughout history, provided their internal structure and external anatomy are known (Fitter 1986; Lynch 2011, 2019; Fitters et al. 2017). All this information has made it possible to publicize the ability of plant adaptation to living in extreme climates. Accordingly, specialized plants of certain regions have developed strategies that allow them to live in extreme areas like aquatic environments and desert areas (Nobel 1984; Nie et al. 2015; Méndez-Alonzo et al. 2016).

In this chapter, we will expose the adaptations at the morphological and molecular levels of the plant roots grown under drought and salinity conditions. In order to identify genes that may be involved in the tolerance to both stresses and develop tolerant plants against such stresses, such genes will be highlighted.

2 Root Morphological Responses to Drought and Salt Stresses

The root system architecture (RSA) plays an important role in dealing with stresses like salinity and drought. For this, plants modify their root morphology to counteract the limited water availability and high salt content in the soil.

Some of these modifications are specific to each stress, while others are present in both osmotic stresses. However, there is much more information available about the changes presented by the roots subjected to drought than about the changes caused by salinity. In this section, the most important characteristics acquired by the roots in response to each of the stresses will be described.

2.1 Drought

Drought is a stress which is based on a reduction of water in the surface layers of the soil, caused either by high temperatures, high force winds or rain scarcity. Among the adaptations carried out by plant roots to cope with drought, these are the most important.

2.1.1 Root Angle

The normal root growth is due to gravitropism. This process, which is regulated by polar auxin transport (Aloni et al. 2006; Geisler et al. 2014), makes that plants develop their roots following a vertical growth. Under drought conditions, the roots maintain their vertical growth but increase the length of the root to get the soil water located in the deeper layer of soil (Alsina et al. 2011; Comas et al. 2013; Fenta et al. 2014; Koevoets et al. 2016). Nevertheless, this angle can be modified by plants to avoid low water availability areas, changing the direction of their main roots towards areas with high water potential. The root cap situated in the root extreme acts as a sensor to detect different water potentials. This phenome is known as hydrotropism and it has been described in several species like maize, cucumber, Arabidopsis and pea (Miyazawa et al. 2007; Takahashi et al. 2009; Cassab et al. 2013; Eapen et al. 2017; Nakajima et al. 2017; Tanaka-Takada et al. 2019).

2.1.2 Length and Branched Root

Drought induces growth of the main root and ramified roots to improve soil prospection to find water deposits, where branching roots are more efficient in taking up water (Osmont et al. 2007; Meister et al. 2014; Jaganathan et al. 2015; Salazar-Henao and Schmidt 2016). For instance, sugar beet plants produce root proliferation only when the water of superficial layers of the soil is reduced (Fitters et al. 2017). However, the number of lateral roots in barley and maize plants was reduced by drought (Babé et al. 2012).

Recently, a new process has been described and it is called hydropatterning. In it, the plants develop lateral roots on the main root in the function of the spatial disposition of water in the soil (Bao et al. 2014).

In addition, crown root number is a characteristic of some plants like maize and is the number of belowground nodal whorls and the number of roots per whorl (Saengwilai et al. 2014). Under drought conditions, a reduction of crown root number makes those plants develop deeper roots, improving the drought tolerance (Gao and Lynch 2016).

2.1.3 Root Diameter

The diameter of the root is an important factor involved in the soil penetration capacity of the root. It has been observed that thicker roots can reach deeper layer soil (Yu et al. 1995; Zheng et al. 2000). Concretely, two transgenic rice plants were more drought tolerant because of increase in the root diameter (Redillas et al. 2012; Lee et al. 2017).

2.1.4 Aerenchyma

The formation of aerenchyma has not only been related to aquatic plants and plants that grow in flooded soil, but it has also been observed in plants that grow under other stress conditions. The aerenchyma is an important adaptation because it improve the gas exchange. For instance, maize plants reduce the proportion of root cortical aerenchyma under drought stress conditions but it was developed in the root maturation zone (Díaz et al. 2018). On the other hand, transgenic rice plants were more tolerant against drought stress probably because their aerenchyma was increased (Redillas et al. 2012).

2.1.5 Apoplastic Barriers

It has been observed that plants grown under drought conditions showed the accumulation of suberin and lignin deposition. Specifically, plants of rice subjected to drought increased the suberization of the endodermis to hold water, making these plants more drought tolerant (Henry et al. 2012).

2.2 Salinity

Plants are subjected to salinity stress when the concentration of salts in the soil makes the soil water inaccessible for plants because of low water potentials. For that, plants have developed some root morphology changes to cope with it.

2.2.1 Root Angle

Plants, which are grown under salinity conditions, show a horizontal root growth, developing radical growth parallel to the soil. This effect is dependent on salt concentration. When the stress is moderate, the root growth follows a horizontal root growth, but when the plant is subjected to high salt concentrations the growth is vertical (gravitropism) (Shelef et al. 2010). In addition, similar to hydrotropism, the root plant can change the direction of their growth to avoid high salt concentrations in the soil. That process is called halotropism and it has been observed in plants like Arabidopsis, tomato and sorghum (Galvan-Ampudia et al. 2013). This movement is regulated by auxin distribution on the root which is a specific response to Na+ ions (Galvan-Ampudia et al. 2013; Pierik and Testerink 2014).

2.2.2 Length and Branched Roots

It has been described that main root growth and lateral root are inhibited by salinity in plants of rice, rye, and maize (Rodriguez et al. 1997; Rahman et al. 2001; Ogawa et al.2006; Julkowska et al. 2014). Arabidopsis and maize plants present a quiescent phase when they are subjected to high salinity (Rodriguez et al. 1997). In rye, the inhibition of root growth is due to a decrease in cell division and an increase in cell death (Ogawa et al. 2006). The quiescent phase in Arabidopsis is temporary, recovering the root growth properties after salinity stress relief (West 2004). Sebastian et al. (2016) postulate that crown roots act as a water availability sensor. This reduction has been seen in several plants like Setaria viridis (Sebastian et al. 2016) and maize (Gao and Lynch 2016). Li et al. (2019) observed that Solanum lycopersycum plants treated with salt had a reduction of total root length, surface area, volume and number of forks but these effects were offset with good soil aeration.

2.2.3 Root Diameter

Salinity increases the root diameter of the tip and middle segments compared to upper zones (Barzegargolchini et al. 2017).

2.2.4 Aerenchyma

Compared to drought, plants subjected to salinity show an increase in the percentage of aerenchyma in the root to improve the gas exchange, since in many cases, plants subjected to high concentrations of salt are usually flooded (Tong et al. 2014; Naz et al. 2018).

2.2.5 Apoplastic Barriers

In plants of Aeluropus littoralis has been observed an increase of endodermis cell wall thickness and lignification of protoxylem in undifferentiated root tips to improve the tolerance in early stages of salinity (Barzegargolchini et al. 2017).

A summary of this section is represented in Fig. 1.

Fig. 1
figure 1

Morphological changes that occur in plant roots caused by drought and salinity are shown schematically in this picture

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3 Root Water Uptake Under Drought and Salt Stresses

The plants adapt to the environment that is not only constantly changing through changes in the anatomy of the roots, but also making changes at the cellular and molecular level that favour the adaptation of the plant. In this section, we are going to focus on the molecular changes related to water uptake.

The direction of water flow inside plants follows the soil–plant–atmosphere continuum (SPAC). Water penetrates into the roots due to an osmotic or hydrostatic gradient which is known as radial transport (Doussan et al. 1998; Steudle and Peterson 1998; Knipfer and Fricke 2011). This transport is composed of the sum of three types of routes: apoplastic, symplastic and transcellular. In the apoplastic path, water circulates across the pores of the cell walls and intercellular spaces. In the symplastic path, water is moving by plasmodesmata which connect the cytoplasm of adjacent cells and in the transcellular path, water flows across the cellular membranes through aquaporins, which are intrinsic membrane proteins that act as water channels. The sum of symplastic and transcellular paths is known as cell-to-cell path because it is not possible to quantify them separately (Steudle and Peterson 1998). The three pathways act simultaneously. Nevertheless, the kind of plants and environmental conditions can favour one route more than the others like an adaptation strategy (Steudle 2000a). Under unstressed conditions the dominant route is the apoplastic one, nevertheless, there are some species in which the predominant route is other different (Steudle and Peterson 1998; Steudle 2000b).

Root hydraulic conductance (L) is a parameter which provides information on the predominant route that is used in water transport (depending on the method used) and the root water transport capacity (Calvo-Polanco et al. 2014; Sánchez-Romera et al. 2014). For example, under drought and salt stresses, plants reduce L and transpiration rate to avoid water loss (Aroca et al. 2006, 2008; Gao et al. 2010). In these cases, the apoplastic route is low, the percentage of water flowing from cell-to-cell path having increased (Steudle and Peterson 1998; Javot and Maurel 2002). Nevertheless, contradictory results have been observed. Concretely, poplar plants showed a reduction of L caused by drought, where the apoplastic path was predominant (Siemens and Zwiazek 2003, 2004).

The root water permeability can be modified due to several factors, such as suberin and lignin depositions, aquaporins and plant hormones. Suberin and lignin depositions, as was shown in the previous section, are a strategy to avoid the loss of water when the plants are subjected to osmotic stresses. It is known that these accumulations reduce water transport by the apoplastic pathway (Schreiber et al. 2005; Vandeleur et al. 2008; Ranathunge et al. 2011; Krishnamurthy et al. 2011) although some exceptions have also been found (Ranathunge and Schreiber 2011).

Aquaporins are water channels located in cell membranes. There are different types of aquaporins according to their amino acid sequence and predominant location: plasma membrane intrinsic proteins (PIP), tonoplast intrinsic proteins (TIP), nodulin-like intrinsic proteins (NIP), unrecognized intrinsic proteins (XIP) and small and basic intrinsic proteins (SIP) (Maurel 2007). But there is mobility of aquaporins between different organelles, so there is traffic of aquaporins between the membranes of different organelles, allowing plants to modify the permeability of membranes according to environmental conditions (Boursiac 2005; Boursiac et al. 2008b).

At the same time, aquaporins can be subdivided in different isoforms. Specifically, PIP2s aquaporins are known to have higher water transport capacity than PIP1s proteins. In addition, it is known that aquaporins need to be phosphorylated to be active, so the plant also controls their phosphorylation in order to adapt to external water conditions (Prak et al. 2008; Zhang et al. 2019).

Many studies have been carried out to investigate the changes in the expression and abundance of aquaporins under drought and salt conditions. Nevertheless, the results obtained did not display a clear pattern, since it depends on many factors such as the plant species, the severity of the stress and the growing conditions.

In general, stress conditions tend to reduce the abundance and expression of aquaporins. However, specific aquaporins have been identified to confer stress tolerance (Perrone et al. 2012; Ma et al. 2019). For example, it has been seen that there are isoforms that are overexpressed in plants subjected to osmotic stress. Concretely, it has been observed that plants of soybean increase the expression of GmPIP2;9 aquaporin under drought conditions. Then, transgenic plants which overexpress that gen showed an increase of drought tolerance in comparison with wild-type plants (Lu et al. 2018). Similarly, overexpression of SlPIP2;1, SlPIP2;7 or SlPIP2;5 in transgenic Arabidopsis and tomato plants caused an increase of hydraulic conductivity in plants under unstressed and drought conditions, suggesting their important implication in enhancing plant water content and osmotic balance (Li et al. 2016b), whereas PIP1b overexpression in tobacco plants caused a rapid wilting under drought stress (Refael Aharon et al. 2003). Perrone et al. (2012) studied that the effect of VvPIP2;4 overexpression in grapevine roots and observed an enhance of gas exchange, shoot growth and L under unstressed conditions, but had a few effects over L under drought (Perrone et al. 2012).

In relation to salinity, it has been found that salt stress causes mobilization of aquaporins inside cells; concretely, PIPs were accumulated in intracellular membranes after salt application which caused a decrease of L (Boursiac et al. 2008a). Prak et al. (2008) noticed that PIPs lacked phosphorylation of Ser-283 under salt conditions, indicating that this phosphorylation also plays a role in regulating the aquaporin trafficking among membranes under salt treatment (Prak et al. 2008). Later, Calvo-Polanco et al. (2014) observed that bean plants treated with salt showed a recovery of L after 6 days of treatment. This increment of L was accompanied by a change in the location of PIPs aquaporins from cortex cells to the epidermis and in cells surrounding the xylem vessels (Calvo-Polanco et al. 2014).

Recent studies have shown the important role of aquaporins to cope with drought and salinity. For example, plants of maize grown under both (no simultaneously) stress conditions increased the expression of ZmPIP1;1 in root and leaves. Moreover, in transgenic Arabidopsis plants which overexpressed that aquaporin (ZmPIP1;1), enhanced drought and salt stress tolerance has been found because it reduce the oxidative damage in these plants (Zhou et al. 2018). Similarly, ScPIP1 overexpressed Arabidopsis plants grown under both stresses showed longer roots than wild-type plants because of decreased membrane damage and improved osmotic adjustment and decreased malonaldehyde (MDA) (stress indicator compound) and increased proline contents (osmoprotective compound) (Wang et al. 2019). Ectopic expression of SpPIP1 as well as the drought tolerance in Arabidopsis thaliana increase (Chen et al. 2018).

In the same way, PgTIP1 Arabidopsis and soybean transgenic plants were more tolerant against drought and salinity stresses because of increased expression of genes related with stress such as ascorbate peroxidase, catalase, SOS1 (a transporter of Na+), and synthesis of ABA and proline (An et al. 2017). However, Peng et al. (2007) discovered that PgTIP1 overexpression in Panax Ginseng increased drought tolerance when the plants were grown under 45 cm deep pots but decreased when they were grown in 10 cm deep pots (Peng et al. 2007) because transgenic plants depleted the water faster from the soil.

4 Implication of Plants Hormones in Root System Architecture

Phytohormones are compounds produced by plants and have a key function to overcome biotic and abiotic stresses. The best-known phytohormones are auxin, abscisic acid, jasmonic acid, ethylene, cytokinins, gibberellins and brassinosteroids. All these phytohormones have been thoroughly studied regarding different plant processes including their role in the face of drought and salinity, focusing on the root system.

4.1 Auxin (IAA)

Auxins are phytohormones involved in plant growth and the response to several stresses (Singh et al. 2017). It is produced mainly in young leaves and it is transported by the phloem to the roots. It intervenes in gravitropism and patterning, explained in the previous section. Root morphological adaptations are carried out by a gradient of the endogenous auxin concentration. Its ability to shape the roots according to the conditions of the rhizosphere makes this hormone important to cope with drought and salinity stresses. Specifically, rice plants overexpressing OsIAA6 gene, one AUX/IAA gene involved in auxin signal, were more drought tolerant (Jung et al. 2015). Similarly, potato and poplar plants increased the production of auxin under drought conditions. Although, this hormone has been much studied for its role in the development and growth of lateral roots and the main root; note that its ability to adapt the characteristics of the root according to the conditions of the rhizosphere makes this hormone vital to cope with saline stress and drought.

4.2 Abscisic Acid (ABA)

Abscisic acid is the most studied stress hormone. Its main function to defend the plant from stress is to delay the germination of the seeds under adverse conditions, regulate the closure of the stomata (which would affect the photosynthetic capacity of the plant and also prevent the loss of water), regulate the water uptake and its location in the plants (aquaporins and L are regulated under stress conditions by ABA), reduce the oxidative damage and finally modify the root system architecture features (Harris 2015; Barberon et al. 2016).

Similarly to IAA, endogenous ABA levels are altered in plants in response to the heterogeneous disposition of water in the soil (Puértolas et al. 2015). Therefore, ABA is involved in root local and systemic changes caused by environmental conditions. Under stress conditions, like drought, ABA synthesis is increased to maintain root development (Sharp et al. 1994; Spollen et al. 2000). It has been observed that ABA also regulates the lateral and primary root development (Bennett et al. 2013). Recently, Rosales et al. (2019) found that the effect of ABA on root morphology under drought conditions depends on the ABA internal concentrations. At mild drought stress conditions, ABA promotes root growth, but under more severe drought conditions ABA induces a reduction of root growth (Rosales et al. 2019). Under salt conditions, ABA induces changes in root architecture, carrying out a quiescence period and then, promoting root growth at the stage of recovery after a short period of salt stress (Zhao et al. 2014; Chen et al. 2017a). The study with ABA mutants defective in ABA synthesis showed that the hydrotropism process requires ABA signalling (Takahashi et al. 2002; Eapen et al. 2017) whereas the hydropatterning process is independent of ABA (Bao et al. 2014).

4.3 Brassinosteroids (BRs)

Brassinosteroids are a kind of phytohormones involved in plant growth and development and response against several stresses (Chen et al. 2017a). In particular, exogenous application of brassinosteroids increases waving frequency and torsion in Arabidopsis roots (Lanza et al. 2012). Several studies showed how brassinosteroids have a positive effect on drought tolerance (Kagale et al. 2007; Sahni et al. 2016). Nevertheless, a negative role of BR has also been observed under drought condition, where defective BR plants were more tolerant to drought (Northey et al. 2016; Ye et al. 2017).

4.4 Jasmonic Acid (JA)

Jasmonic acid is another phytohormone widely studied for its defensive role against plant pathogens; however, there are also studies where it has been seen to reduce the negative effects of drought and salinity because it is involved in stomatal regulation, root development and oxidative damage reduction. However, most important is its role in regulating root abundance and aquaporin expression and L to cope with drought stress (Munemasa et al. 2007; Riemann et al. 2015; Sánchez-Romera et al. 2016).

4.5 Ethylene

Ethylene is a gaseous hormone involved in the process like fruit ripening, senescence and response to several stresses among others (Arraes et al. 2015). In particular, ethylene may contribute to reducing the root development under drought and salt stresses (Cao et al. 2007; Liu and Zhang 2017), reducing the cell proliferation at the root apical meristem (Street et al. 2015).

4.6 Hormones Interaction

There is a lot of information about the role of each hormone in the root development; however, there is little information that indicates how all hormones act simultaneously on the same process. It is known that hormones are molecules that regulate several physiological processes in plants by modifying their concentrations (hormone balance) or travelling through the plant. Plants use this hormonal balance as a strategy to regulate root growth and to cope with adverse conditions caused by periods of stress. The interaction between hormones has been widely studied at the level of aerial part, however, in the roots, there is much to discover (Kushwah et al. 2011; Ullah et al. 2018).

ABA and cytokinin (CK) (another phytohormone) interact by reducing the polar transport of auxin to carry out lateral root formation (Shkolnik-Inbar et al. 2013). Other studies observed that property concentration of CK and auxin are essential to root development. Similarly, it has been observed that JA inhibits the root length but is involved in lateral root development because JA can regulate the synthesis of IAA (Cai et al. 2014; Wasternack and Song 2017). With reference to JA, there is a study which observed that it regulates the root hydraulic properties in tomato plants and this effect was due to changes in calcium and ABA concentration in roots (Sánchez-Romera et al. 2014). On the other hand, ABA inhibits ethylene synthesis to promote the root growth under drought conditions (Ghassemian et al. 2000). In salinity, crosstalk between ABA and GA has been found’ negative feedback of these hormones regulates root development (Achard et al. 2008).

5 Role of Plant Nutrients in Root Architecture Under Drought and Salt Stresses

The nutritional status of plants is an important factor since plants with an optimal nutritional status can increase harvest and cope with stress conditions (Marschner et al. 1996; Amtmann and Armengaud 2009; George et al. 2011; Li et al. 2016c). Plants absorb the nutrients and water necessary to carry out their metabolic processes through their roots. The nutrients are divided into macronutrients and micronutrients, according to the concentrations required by the plant. Both high levels of nutrients in the soil and their scarcity cause serious physiological disorders in plants. In order to tolerate these concentrations, plants make morphological changes mainly in the roots although the whole plant is affected by them (Santos et al. 2017; dos Santos Araújo et al. 2018; Lynch 2018). The most common problem is the lack of nutrients in the soil due to intensive agriculture and weather effects. Scarce nutrient availability can be due to two factors: their abundance and mobility. In relation to the abundance, plants grown in soil poor of nutrients are smaller and more sensitive to stress conditions, which translate into economic losses (Gojon et al. 2009; Niu et al. 2013). In the case of mobility, it depends on the kind of nutrient and its form available in the soil. Nutrients can be mobile or immobile in the soil. This property is in part determined by the presence of water in the soil since the mobile elements are mainly dissolved in water. On the other hand, immobile elements are usually found on the soil surface and are retained into soil particles (Peret et al. 2014; Saengwilai et al. 2014; Dai et al. 2015).

Drought and salinity stresses, in addition to affecting the decomposition of soil organic matter, affect the mobility of nutrients. Therefore, root anatomy changes, made by plants in response to nutrient availability, are also related to water availability (Thorup-Kristensen and Kirkegaard 2016; Dathe et al. 2016).

In this section, we will be focusing on nitrogen and phosphorus due to their important role as a constituent of genetic material and cellular structures. Moreover, the implications of N and P in root development and stress tolerance have been deeply studied. Other nutrients such as potassium, calcium or boron will be briefly explained (see Table 1).

Table 1 Effects that the most important nutrients in plant nutrition have on the morphological characteristics of the root when they are subjected to abiotic stresses (nutrient deficiency, drought and salinity)
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5.1 Nitrogen (N)

Nitrogen is necessary for numerous physiological processes to be carried out in plants and that is because it is involved in the synthesis of molecules such as amino acids, proteins, coenzymes, nucleic acids and chlorophylls (Marschner et al. 1996; Amtmann and Armengaud 2009; Xu et al. 2012). N is found in the form of nitrate (NO3−) or ammonium (NH4+) in the soil, as a result of processes of mineralization of soil organic matter, and is absorbed by plants through specific transporters that are found in the roots (Dai et al. 2015; Lynch 2019). In agriculture, urea is used as nitrogen fertilizer. Nitrate is the main source of nitrogen for plants since being a soluble ion is easier to be absorbed by the roots. However, ammonium is more difficult to assimilate by plants because is an insoluble ion. Therefore, it has low mobility and is found in the most superficial layers of the soil (Lynch 2018, 2019).

5.1.1 Nitrogen Deficiency

Plants have the capacity of changing their root anatomy to enhance nutrient uptake. For example, plants of rice and maize grown in soil with low nitrogen concentration showed longer and deeper roots (Ke et al. 2008; Atkinson et al. 2014; Wang et al. 2015; Yu et al. 2015). In addition, several maize genotypes were compared to find the root characteristics which improved the nitrogen absorption. The results showed that genotypes with a deeper root and fewer crowns were the most efficient that uptake nitrogen (Saengwilai et al. 2014).

5.1.2 Nitrogen and Water Relations

As it was explained in the previous section, plants develop longer roots in order to reach water storage in the deepest layers of the soil. This root characteristic is directly related to the uptake of mobile ions like nitrate since mobile ions are dissolved in soil water. Then, the nitrate source may be also found in the deeper water reserves and the same root adaptations enhance the water and nutritional status. This connection between nitrate availability and water uptake has been observed in several kinds of plants like rice, maize, tomato and cucumber which increases the water absorption after N treatment (Gorska et al. 2008; Ishikawa-Sakurai et al. 2014). Aquaporins play an important role in nitrogen metabolism because they are involved in the uptake, mobilization and detoxification of N (Gerbeau et al. 1999; Liu et al. 2003; Loque et al. 2005). Several aquaporin subfamilies like PIP, NIP and TIP are able to transport N compounds (Gerbeau et al. 1999; Liu et al. 2003; Jahn et al. 2004; Bárzana et al. 2014).

Concretely, plants showed an increase of aquaporin expressions after ammonium or nitrate application (Hacke et al. 2010; Ren et al. 2015; Ding et al. 2016), being higher with ammonium than nitrate (Guo et al. 2007a; Ding et al. 2016; Korhonen et al. 2018). Related to up-aquaporin expression after nitrogen treatment, it was also observed that a reduction of root aerenchyma and lignin accumulation explains the improvement of water absorption rate (Wang et al. 2001; Gaspar et al. 2003; Ishikawa-Sakurai et al. 2014; Ren et al. 2015). On the other hand, plants grown under low nitrogen levels showed an increase of aerenchyma formation, and a reduction of L values and root aquaporin gene expression (Ranathunge et al. 2016). Nevertheless, an increase of ZmTIP4;4 was found in maize roots and was related to urea mobilization across tonoplast, suggesting that ZmTIP4;4-regulated urea transport was essential for unloading vacuolar urea across the tonoplast under N starvation conditions (Gu et al. 2011). The use of nrt2.1 (the high-affinity NO3− transporter) mutant plants showed a diminution of NO3− content in roots and therefore, a reduction of L and PIP expression, suggesting a positive correlation between N and L (Li et al. 2016a).

Other studies suggest that nitrogen has a different effect on water relations which varies along the time. In short time, nitrogen application induce up expression of aquaporins whereas, after long time of nitrogen exposition, the plant act making modifications in root system architecture, increasing nitrate uptake (Wang et al. 2001; Remans et al. 2006; Walch-Liu et al. 2006).

Several TIPs and NIPs are involved in the N compounds transport across tonoplast (Gaspar et al. 2003; Soto et al. 2008; Gu et al. 2011; Bárzana et al. 2014; Zhang et al. 2016), either as a strategy to detoxify excess nitrogen (Wang et al. 2008), to release nitrogen reserve sources in situations of deficiency (Liu et al. 2003).

5.1.2.1 Drought

In relation to plants grown in nitrogen-poor soils, besides increasing the root length to improve its absorption, a reduction of enzymes and transporters related to nitrogen metabolism was observed when plants were subjected to drought conditions. For example, drought reduced the expression of some nitrate transporter but increased the expression of two ammonium transporters (AMT1; 2 and AMT4; 2) and two enzymes of nitrate reductase (NR and NRT 2; 5) in Malus prunifolia plants. Moreover, plants of Malus hupehensis increased NH4+/NO3− ratio in root and shoot as a strategy to cope with drought stress (Huang et al. 2018a, b). In relation to ammonium role in drought tolerance, it has been observed that ammonium treatment increased aquaporin expressions, improving the root water uptake under drought conditions (Ding et al. 2015a).

5.1.2.2 Salinity

There are a few studies related to the effect of N in plants subjected to salinity. Probably because N is only limited under reduced water conditions since nitrate is a mobile ion. Nevertheless, it has been seen that cotton plants treated with nitrate were more tolerant of salinity than plants treated with ammonium because they develop bigger roots and accumulated less Na+ (Dai et al. 2015).

5.2 Phosphorus (P)

Phosphorus is part of RNA and DNA and it is used as an energy storage molecule forming part of ATP and as a constituent of phospholipid membranes. It is an ion with low mobility and is located in the superficial layers of the soil because it comes from the degradation of organic matter (Lynch 2011; Shen et al. 2011).

5.2.1 Phosphorus Deficiency

In the case of Arabidopsis, rice and maize plants grown under P deficiency conditions, the root anatomy presents an increase of lateral root and hair root proliferation to increase the capacity of soil exploration, but the main root is reduced (Kirk and Van Du 1997; Bates and Lynch 2000; Williamson et al. 2001; Postma et al. 2014; Kawa et al. 2016). As well, plants of the Proteaceae family have developed special roots called proteoid or cluster roots. These roots are very branched, covered by a large number of long and densely clustered trichoblasts (Lamont 1972; Neumann et al. 2000).

5.2.2 Phosphorus and Water Relations

P is directly related to aquaporin activity because aquaporins are able to transport water when they are in the phosphorylated state. Therefore, P deprivation decreases the aquaporin activity and water uptake in roots (Carvajal et al. 1996; Wang et al. 2016).

5.2.2.1 Drought

With respect to plants grown under low phosphorus availability and drought, it has been observed that plants showed the same changes as for low phosphorus availability. Under water limitations, plants showed an increase of secondary root branching and a decrease of nodal thickness. Nevertheless, these changes managed to improve P uptake efficiency and increase the root:shoot ratio (De Bauw et al. 2019).

Molecular changes like an increase in the expression of phosphorus transporter genes, such as PHT1;7, PHT1;12 and PHT2;1, has been observed in the root of Malus domestica to face drought and starvation of P (Sun et al. 2017).

Other studies have been focused on improving the nutrient status to cope with drought. For example, plants of Matricaria chamomilla subjected to severe drought stress were treated with vermicompost and the results showed an increase of N, P and K uptake and it was related to enhancing drought tolerance (Salehi et al. 2016). In the same way, barley plants grown under severe drought stress increased H+/K+ ATPase activity and K+ uptake, this ion balance stimulated drought tolerance (Feng et al. 2015).

5.2.2.2 Salinity

On the other hand, under salinity conditions plants develop roots that grow parallel to the soil; therefore this root system may favour the absorption of nutrients that are immobile as is the case of phosphorus. Arabidopsis plants, subjected to double stress, salinity and P deprivation, showed an increase of density and length of lateral roots (Kawa et al. 2016). Experiments with maize plants treated with P were more tolerant to salt stress because enhanced P uptake and this resulted in a Na+ exclusion (Zhou et al. 2018).

5.3 Potassium (K)

K+ is a plant macronutrient which is known to be involved in processes like enzyme activation, osmotic adjustment, cell expansion, regulation of membrane electric potential and pH homeostasis (Hawkesford et al. 2011; Ragel et al. 2019).

5.3.1 Potassium and Water Relations

It has been observed a positive correlation between K+ and water uptake (Guo et al. 2007b). Therefore, AQP could play a role as turgor sensors to regulate K+ channel activities (Hill et al. 2004). K+ channel inhibitors reduced the expression of aquaporin and K+ channels in Arabidopsis roots, suggesting that K+ is involved in the hydraulic conductivity of plasma membranes (Sahr et al. 2005).

5.3.1.1 Drought

K+ starving and drought stress caused similar symptoms in plants (Liu et al. 2006). Several studies suggest that aquaporins and K+ channels can act like osmoregulators to improve tolerance to drought stress. Then K+ treatment could help to improve plant water status because AQP is activated to mobilized K+ ions under drought stress (Liu et al. 2006; Galmés et al. 2007).

5.3.1.2 Salinity

García-Martí et al. (2019) observed that plants treated with an increase in K+ and Ca2+ concentrations in the irrigation solution (higher than recommended values) and subjected to salt and heat stresses improved their biomass production and reduced their oxidative damage than plants watered with Hoagland solution, suggesting the importance of plant nutrition to cope with combined stress situations (García-Martí et al. 2019).

5.4 Calcium (Ca)

Calcium is an essential element involved in the growth and development of plants. Calcium is important in the formation of the cell wall and membrane stability, but its main function is as the second messenger in many plant physiological processes, such as response of plants to abiotic stresses.

5.4.1 Calcium Deficiency

Although calcium deficiency in the soil, is not common, the symptoms are observed often in developing tissue-like young leaves and fruits because calcium shows low mobilization via phloem from old tissues to young ones (White and Broadley 2003; Thor 2019). The studies related to calcium role in roots are few. Nevertheless, it has been observed that Arabidopsis plants subjected to calcium deprivation treatment presented an increase of root fresh weight and a superficial and highly branched root system. The main root was drastically reduced after 100 µM calcium application and moderately reduced after 500 µM calcium. Nevertheless, although the main root was inhibited, the density of first-order lateral root was increased (Gruber et al. 2013).

5.4.2 Drought and Salinity

Calcium application improves drought tolerance in plants of sugar beet as well as increases the plant biomass and sugar root concentration. Salt stress inhibits the aquaporin activity; this fact was related to a reduction of cytosolic calcium in pepper plants (Martínez-Ballesta et al. 2008). In the same way, calcium treatment improves water transport which could be due to aquaporin activity (Carvajal et al. 1996, 2000; Cabañero et al. 2006).

In brief, these results suggest that calcium could act like an aquaporin regulator to respond to environmental stimuli (Steudle and Henzler 1995; Johansson et al. 1998; Vera-Estrella et al. 2004; Luu and Maurel 2005).

5.5 Boron (B)

Boron (B) is one of the essential micronutrients. Although the necessary concentration of B is low, this function is critical to carry out the growth and development of plants. Its function is focused on the structure and function of the plant cell wall (Shireen et al. 2018).

5.5.1 B Deficiency and Toxicity

Boron deficiency is a large-scale problem, leading to losses in the quality and yield of many crops at a global level. B deprivation causes a speed inhibition of primary and lateral root elongation (Kobayashi et al. 2017; Wu et al. 2017; Riaz et al. 2018). This effect is due to alteration of cell division, cell wall component and cell elongation in the root elongation zone (De Cnodder et al. 2000; González-Fontes et al. 2016).

5.5.2 Boron and Water Relations

Aquaporins are able to transport some ions like B and distribute it to all plant tissues (Dordas et al. 2000; Fitzpatrick and Reid 2009). Specifically, AtNIP5;1 is an aquaporin involved in a boric acid transport; its expression is upregulated under B deficiency conditions. Its function is essential for adequate B transport into the roots. Knockout Arabidopsis plants for nip5;1 showed inhibition of root and shoot growth under B deficiency (Takano et al. 2006; Kato et al. 2009). Other aquaporins, like AtNIP6;1 in Arabidopsis and OsNIP3;1 in rice plants, are implicated in uptake and distribution of B in the plant (Hanaoka and Fujiwara 2007; Tanaka et al. 2008).

In barley, it has been observed that a down regulation of HvNIP2;1 expression to induce B toxicity tolerance, reduces the B uptake and accumulation inside the plant (Schnurbusch et al. 2010). Similarly, overexpression of AtTIP5;1 in Arabidopsis plants in the tonoplast membrane was found to store B inside the vacuole and reduce the B toxicity (Pang et al. 2010). Other PIPs aquaporins were also involved in B transport in rice plants to reduce B toxicity (Kumar et al. 2014; Mosa et al. 2016).

6 Root Molecular Responses to Drought and Salt Stresses

This section has been focused on collecting a series of genes which are directly or indirectly involved in the regulation of root system architecture (RSA). Several publications have shown that these genes could play an important role in facing the drought and salinity stresses at the root level. A summary is showed in Table 2.

Table 2 Summary of genes involved in changes that occur in root morphology to improve tolerance to drought and salinity
Full size table

6.1 DEEPER ROOTING 1 (DRO1)

DEEPER ROOTING 1 (DRO1) is a gene which is implicated in the regulation of length and angle of the root (Uga et al. 2011, 2013). Uga et al. (2013) realized an experiment where one tolerant and another sensitive rice species were compared. Tolerant plants which have a full-length copy of DRO1 showed deeper root and the grain production was not affected by stress conditions. On the other hand, sensitive plants, which have a truncated copy of the gene, showed superficial roots and lower weight gain and production. Later, it was observed that sensitive plants had not a functional allele of DRO1, DRO2 and DRO3 as well were identified. In addition, DRO3 is involved in RSA only when DRO1 is functional in the plant, suggesting that DRO3 is involved in the DRO1 regulation (Uga et al. 2015). Other studies showed that overexpression of AtDRO1 in Arabidopsis plants decreased the angle of lateral root and narrower lateral roots, and overexpression of PpeDRO1 in Prunus domestica increased the length root with respect to control plants (Guseman et al. 2017).

The implication of this gene on drought tolerance has been accepted, whereas no information about its role against salinity stress has been found. This gene could be proposed to be effective to improve salt tolerance.

6.2 ENHANCED DROUGHT TOLERANCE1/HOMEODOMAIN GLABROUS11 (AtEDT1/HDG11)

ENHANCED DROUGHT TOLERANCE1/HOMEODOMAIN GLABROUS11 (AtEDT1/HDG11) is a gene involved in the encoding of transcription factors of homeodomain‐leucine zipper (HD‐ZIP) (Schrick et al. 2004). Specifically, AtEDT1/HDG11 genes perform on the encoding of cell wall proteins involved in root cell elongation and controlling the extended root system, which is related to drought tolerance (Xu et al. 2014).

Yu et al. (2016) observed that AtHDG11-overexpressing plants of cotton (Gossypium hirsutum) and poplar (Populus tomentosa Carr.) were more tolerant of salt and drought conditions. In the case of transgenic cotton plants, they were more tolerant against salt and drought stresses because they improved the RSA. These plants produced longer roots and increased root dry biomass. In the same way, transgenic poplar had also a bigger developed root system with longer primary root and more lateral roots. For this reason, they were more resistant than wild-type plants under drought and salt conditions. Moreover, these plants showed better water status and less damage (Yu et al. 2016).

On the other hand, overexpression of AtEDT1 enhances the elongation of roots in Salvia miltiorrhiza (Liu et al. 2017) and AtEDT1-overexpression in alfalfa (Medicago sativa L.) plants also improved the root system, showing an increase of root length, root weight and root diameters with respect to wild-type plants. It should be noted that these plants were more tolerant to drought, so this gene is of great importance to make plants more resistant (Fan et al. 2017).

These improvements against drought and salt conditions have also been observed in several kinds of (AtEDT1/HDG11) transgenic plants like rice, tobacco, sweet potato, wheat, poplar and cotton (Yu et al. 2013, 2016; Zhu et al. 2016; Chen et al. 2017b; Tariq et al. 2017; Guo et al. 2019). Therefore, these genes could be a good tool to make drought- and salt-tolerant plants.

6.3 14-3-3 Genes

The 14-3-3 proteins are phosphopeptide-binding proteins (Campo et al. 2012). They are characterized because they interact with proteins of phosphoserine/threonine motifs to regulate signal transduction due to their properties, such as their ability to move between different subcellular localizations, stability and affinity to interact with other proteins (Paul et al. 2012; Tan et al. 2016). Specifically, these genes codify proteins which are involved in the regulation of other target proteins related with signalling, transcription activation and defence against stress (Robert et al. 2002; Jaganathan et al. 2015; Cao et al. 2016; Liu et al. 2016).

For example, it has been observed that tobacco plants decreased the expression of T14-3-3 mRNA under salt conditions (Chen et al. 1994; Zhang et al. 2018). However contradictory results have been found in relation to drought. On the one hand, GsGF14 overexpression in Arabidopsis thaliana had a negative effect on drought tolerance and plant growth because the plants showed deficits in root hair formation and development and changes in stomata size, and thereby reduced the water intake capacity. Moreover, knockout mutant Arabidopsis (AtGF14) improved drought tolerance and seed germination rate (Sun et al. 2014). Then, it could be explained as an decrease in the expression of this gene or their protein could improve the tolerance against the salt and drought stresses (Tan et al. 2016; Guo et al. 2018). However, opposite results have been obtained because the At14-3-3λ overexpression in maize plants enhanced their drought tolerance, modifying stomatal size and root system architecture (Yan et al. 2004; Campo et al. 2012; He et al. 2015). In addition, wheat plants increase the expression of 14-3-3 gene when they were grown under polyethylene glycol 6000, NaCl, H2O2 and abscisic acid treatments. Therefore, this gene also confers tolerance to drought and salt stresses. Transgenic tobaccos showed an increase of length root, relative water content, survival rate, photosynthetic rate and water use efficiency than wild-type plants under drought and salt stress conditions. These results suggest that this gene enhanced the drought and salt tolerance and that it is regulated by ABA signalling (Zhang et al. 2018).

6.4 Non-specific Phospholipase C5

Non-specific phospholipase C5 (NPC5) and its derived lipid mediator diacylglycerol (DAG) have been involved in salt stress tolerance. Concretely, an increase of lateral root development was observed under salt stress in Arabidopsis thaliana. In knockout mutant npc5-1, lateral roots were decreased under mild NaCl stress, whereas overexpression of NPC5 increased it. The increase of lateral root by NPC5 was independent of auxin, being regulated by stress (Peters et al. 2014). On the other hand, no studies in relation to drought tolerance by NPC5 have been observed.

6.5 NAC Family Transcription Factors

NAC is the result of the abbreviations of NAM (no apical meristem), ATAF1-2 (Arabidopsis transcription activation factor) and CUC2 (cup-shaped cotyledon) (Aida et al. 1997). NAC-type transcription factor gene AtNAC2 has been identified in Arabidopsis thaliana, mainly expressed in roots. It has been observed that its expression is induced under salinity conditions, increasing abscisic acid (ABA), 1-Aminocyclopropane-1-carboxylic acid (ACC ethylene precursor) and naphthaleneacetic acid (NAA is a synthetic plant hormone in the auxin family) content also. Overexpression of AtNAC2 in transgenic Arabidopsis plants resulted in the promotion of lateral root development. These results suggest that AtNAC2 may be a transcription factor induced by environmental and endogenous conditions to regulate plant lateral root development (He et al. 2005).

Root-specific (RCc3) and constitutive (GOS2) promoters were used to create two lines of transgenic plants (RCc3:OsNAC9 and GOS2:OsNAC9) which overexpressed OsNAC9. The two lines showed an enlarged stele and aerenchyma. Concretely, RCc3:OsNAC9 roots had a greater extent aerenchyma than those of GOS2:OsNAC9 and non-transgenic roots. Therefore, this phenotype could be used to enhance drought resistance (Redillas et al. 2012).

6.6 Sucrose Non-fermenting1-Related Protein Kinase 2

Sucrose non-fermenting1-related protein kinase 2 (SnRK2) is involved in abiotic stress signalling. Overexpression of TaSnRK2.8 in transgenic Arabidopsis improved drought and salt tolerance. These plants showed longer primary roots, higher relative water content, strengthened cell membrane stability, lower osmotic potential, increased chlorophyll content and enhanced PSII activity. Moreover, TaSnRK2.8 overexpressed plants increased the transcript level of ABA biosynthesis, ABA signalling and stress-responsive genes under control and stressed conditions (Zhang et al. 2010).

6.7 WRKY Transcription Factor

WRKY transcription factor (WRKY46) is expressed along lateral root primordia during early lateral root development but this expression is restricted to the stele of the mature LR. Under osmotic and salt stress conditions, lack of WRKY46 (wrky46 mutants) decreased lateral root formation, whereas overexpression of WRKY46 improved it. Auxin application restores LR development in defective plants (Ding et al. 2015b).

6.8 TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALLING F-BOX PROTEIN

Auxin joins TIR1/AFB receptor proteins to regulate the gene expressions. Two auxin receptors have been found in Arabidopsis mutant plants to induce more stress tolerance, tir1 afb2 being more resistant against salinity because of enhanced germination rate and root development and decreased oxidative damage (Iglesias et al. 2010). Subsequently, the same authors observed that miR393, which form part of miR393-TIR1/AFB2/AFB3 regulatory module, is involved in suppression lateral root development during salt stress (Iglesias et al. 2014). Other studies showed how overexpression of a miR393-resistant TIR1 gene improved salt stress tolerance, increasing the germination rate and proline and anthocyanin content, reducing water loss and inhibition of root length and delaying senescence (Chen et al. 2015). Other studies observed that TIR1 mutant plants of Arabidopsis did not modify their root angle when the plants were under water deficit conditions, therefore the auxin is essential to suggesting redirected root growth angles downward under drought stress (Rellán-Álvarez et al. 2015).

6.9 ABSCISIC ACID INSENSITIVE4

ABA is a plant hormone involved in stress defence. ABSCISIC ACID INSENSITIVE4 (ABI4) gene which is expressed in the root stele is also implicated in RSA (Shkolnik-Inbar and Bar-Zvi 2010; Shkolnik-Inbar et al. 2013; Rowe et al. 2016). In relation to salinity, Arabidopsis mutants affected in ABI 4 gene showed tolerance to salinity because they stored lower levels of sodium ions. That was due to an increase in the expression of HKT1;1 gene (transporter of Na+). Moreover, these plants showed an increment proline content which reduced the oxidative damage. Therefore, ABI4-overexpression plants were sensitive to salinity, suggesting the important role of ABI4 in the root formation regulation (Shkolnik-Inbar et al. 2013).

6.10 FASCICLIN-LIKE ARABINOGALACTAN PROTEIN 4

FASCICLIN-LIKE ARABINOGALACTAN PROTEIN 4 (At-FLA4) gene is required in the root development of plants subjected to salt conditions. Seifert et al. (2014) observed that the ABA application suppressed the At-FLA4 function in Arabidopsis plants grown under salt stress. They proposed that the At-FLA4 gene is involved in cell wall biosynthesis and root growth but its role is dependent on ABA signalling (Seifert et al. 2014).

6.11 Rho-Like GTPases

Rho-family GTPases are plant-specific molecular switches that are involved in the regulation of processes like cytoskeletal reorganization and vesicular trafficking (Nagawa et al. 2010). Rho-like GTPases from plants (ROPs) are related to plant survival to cope with abiotic stresses. Seventeen novel ROP proteins had been identified and characterized from Musa acuminata (MaROPs). Six genes of them were highly expressed in response to cold, salt and drought stress conditions in two genotypes with similar behaviour against these abiotic stresses, MaROP5g being more expressed under salinity conditions. Subsequently, transgenic Arabidopsis thaliana plants overexpressing MaROP5g grown under salt stress showed longer primary roots and more survival rate than wild-type A. thaliana. Therefore, ROPs genes might be taken into account as a gene involved in tolerance to saline stress (Miao et al. 2018).

6.12 Calcineurin B-Like Proteins (CBLs)

Calcineurin B-like proteins (CBLs) are calcium sensors that can interact with a family of protein kinases, known as CBL-interacting protein kinases (CIPKs). Expression analysis in Arabidopsis pants showed that CIPK23 genes are expressed in roots and leaves (Cheong et al. 2007). Transgenic plants, which overexpressed TaCIPK23 gene in wheat and Arabidopsis plants grown under drought conditions, improved survival and germination rate, root system architecture, accumulation of osmolytes and reduced water loss rate (Cui et al. 2018).

6.13 Root Hair Defective-3 (MaRHD3)

Wong et al. (2018) observed that transgenic Arabidopsis plants expressing root hair defective-3 (MaRHD3) were more tolerant to drought stress. The MaRHD3 plants increased biomass accumulation, relative water content, chlorophyll content and abundance of root hairs and branching roots than control plants (Wong et al. 2018).

6.14 RCAR/PYR1/PYL

RCAR/PYR1/PYL is ABA-binding receptor involved in the ABA signalling pathway. Transgenic plants in which RCAR11–RCAR14 overexpressed improved ABA sensitivity, root length and drought resistance (Li et al. 2018).

In a study carried out with cotton (Gossypium hirsutum), 27 predicted PYL proteins were described. Expression determinations showed that nine of GhPYL genes were down-regulated, whereas three of them increased their expression when the plants were subjected to drought stress. Overexpression of GhPYL10/12/26 in Arabidopsis made that transgenic plants bigger and more drought tolerant than wild-type plants, increasing the length of primary roots under unstressed conditions and mannitol stress. These results proposed that PYL genes may be essential in plant response to deal with drought/osmotic stresses (Chen et al. 2017a).

7 Perspectives

Environmental problems such as soil degradation by intensive agriculture, deforestation and an increase in greenhouse gases in the atmosphere are causing plants to develop new strategies that allow them to survive a stressful situation. In addition, if it is considered that the world population is rising, it is necessary that plants of great economic interest (tomato, beans, corn, wheat and rice) would be able to adapt to such unfavourable conditions without greatly affecting their economic production. Throughout this chapter, we have presented information about adaptations that plants suffer in nature to cope with such stresses but we have also talked about genes involved in the regulation of these changes. Given the information collected so far, we propose new ideas to give light to the unknown remaining mechanisms.

In addition, there are many studies carried out to study the effect of drought on plant roots, but little is known about the effect of salinity despite the fact that sometimes both stresses complement each other. Therefore, studies related to salinity should be increased, especially related to the absorption of nutrients and the overexpression of aquaporins. There are some topics which may shed new light on the root role. For example, to study the changes which roots undergo by contrasting a root of dicotyledons and monocotyledons plants, since both roots are embryologically different. Although there are studies where these roots are analyzed separately, it is necessary to include experiments where a comparison of these both kinds of roots will be grown under the same conditions of humidity, soil characteristics and nutrients, because all these factors affect drastically the root development.

On the other hand, I believe that the role of root exudates in the soil is an unexplored target. It could be interesting to study the changes in the composition of exudates against conditions of salinity and drought since they can influence the morphology of the root and therefore plant survival.

In relation to monocotyledons and dicotyledons differences and root exudates, to continue with the use of technologies such as quantitative trait loci (QTL), amplified fragment length polymorphism (AFLP) or clustered regularly interspaced short palindromic repeats (CRISPR) to identify new genes of interest involved in the tolerance of plants to saline stress and drought. Subsequently, these genes will be used to create transgenic plants of economic interest which will show these strategies, will be more resistant and will reduce crop losses.

Finally, many studies that focused on hormones signalling may be carried out to clarify the role of hormones, their receptors, intermediary products and interaction with other signal molecules that occur in the root system, since in truth all of them work together to achieve the desired result by the plant. The ideal would be to understand how a stress-tolerant plant can do so in terms of hormonal balance, root morphology, ability to regulate and store water in its tissues, reduction of oxidative damage and nutrient availability, and thus understand the communication that occurs between the root and aerial part of the plant.