Morpho-Anatomical Adaptation against Salinity

*Smita Srivastava*

### **Abstract**

Plants tolerant of NaCl, implement several adjustments to acclimate to salt stress, such as biochemical, physiological, and morphological modifications. Besides, plants also adjust to saline circumstances by altering their anatomical structure of roots, leaves, and morphological modifications. The leaf and roots are among the essential plant organs and are involved in the transport of water and minerals used for photosynthesis. From a plant physiology perspective, water use efficiency in the quantity of CO2 fixed in photosynthesis compared to the leaf anatomy. In this review, we provide a comparative account of the morphology of the leaf and root under normal and salt stress circumstances. There is little information on the ultrastructure changes elicited in response to salt stress. The analysis expands our knowledge of how salt may impact the leaves and root anatomy.

**Keywords:** adaptive mechanisms, arbuscular mycorrhizal fungi, trichomes, stomata, mesophyll

#### **1. Introduction**

Salt stress is among the leading abiotic causes of modifications in many physiological, anatomical, and biochemical processes [1]. Anatomical and morphological changes in leaves under restricted moisture availability play a significant role in salt stress, and they are an indication of the level of tolerance. The epidermis is the external tissue of every plant organ and serves as the initial point of contact with its environment. It is essential to preserve physiologically appropriate circumstances in all plant and environment interactions for normal metabolism [2].

In salt-stressed plants, stem vascular cell thickness was much larger than control treatment; the salinity effect was concentration-dependent. Generally, plants grown in saline solution showed higher thickness in the cuticle, vascular tissues, and vessel than unstressed plants (**Figure 1B–C**). Furthermore, we observed that, in salt-stressed plants, the number of trichomes was increased from epidermal stem cells. In other words, an increase in salinity level led to more trichomes on the epidermal layer compare with control plants [3]. There are several reports on increased trichomes density under environmental stresses such as drought and salinity [4, 5]. An increase in trichome density may be a mechanism to increase tolerance to salt stress.

The importance of the cuticular layer in regulating a plant's water status and providing protection from environmental challenges has been recognized for a long time. The cuticular layer in plants restricts non-stomatal water loss and protects plants against damage from biotic and abiotic stress [6]. Due to their role

#### **Figure 1.**

*Salt stress effects on rice plant growth under control and at 200 mM NaCl treatment(A): rice leaf anatomy, Oriza sativa; (B–C): light microscopy (cross-section) in control; (C): light microscopy (cross-section) in 200 mM NaCl; cu = cuticle, ms: mesophyll cell, Bul: bulliform cells, cp: parenchyma cells, m: mesophyll, s: stomata, vb: vascular bundles, s: stomata stomata, lv: largr vascular bundle and red line indicates the thickness of parenchyma; and scale bar = 100 μm; (D): scanning electron microscopy of the adaxial surface in control rice leaves; and (E): under stress condition (200 mmol/l), showing epicuticular wax deposition.*

in controlling water loss, specialized epidermis structures have the potential to enhance the drought tolerance and WUE ("water use efficiency") of critical crops [7–10]. The cuticular wax on the leaves of the control (non-treated rice leaves) showed less than compared with the treated rice leaves (200 mmol/l NaCl), indicating adaptation against salinity to maintain photosynthesis to control water loss (**Figure 1D–E**).

Trichomes study has conventionally centered on specialized metabolic processes understanding in glandular trichomes [11–13]. Our data showed that in salinity tolerance, rice varieties have developed dense trichomes and increased in size with the help of a layer of air trapped in trichomes to reduce the rate of water transpiration as compared to susceptible varieties under differing concentrations of salt (40–160 mmol/l) [3].

The epidermis also includes stomata, which constitute epidermal pores that directly control the exchange of gases and also water status management. They may be found on a single surface (hypostomatic) and both leaf surfaces (amphistomatic) [14]. Stomata regulate water absorption through modifications in the stomatal opening, conductance, along with density. Shortly, plants alter their stomata closure to minimize water loss and a moderate absorption of CO2 for changing circumstances [15]. Our data indicated that tolerant cultivars of rice closed stomata at the highest concentration (160 mmol/l NaCl) of salt [3]. Plant leaves can rise in stomatal density and a decreased saline area indicating a change to saline stress [16, 17]. Thus, the equilibrium between the density of stomatal and site could lead to stomatal conductance control and evaporation water loss [18, 19], which establishes equilibrium in photosynthesis [20]. Similar behavior was found for other species like "*Leptochloafusca*" [21] *Imperata cylindrical* [22], and *Triticum aestivum* [23].

Salt tolerant plants exhibit leaves thickening [23–25] which may contribute to the maintenance of turgor and content of leaf water. Wankhade et al. [26] and Hameed et al. [17] identified an optimistic association between salt stress tolerance and epidermal cells' thickening. The epidermal thickness increases the water effectiveness of plants and offers more area in which NaCl is effective for the epidermis of the leaf [27]. It can also be important to increase the region of sclerenchyma with rising salinity since it provides organ rigidity and this may be an essential characteristic for salt resistance [16]. The area of the photosynthetic leaf, parenchyma

#### *Morpho-Anatomical Adaptation against Salinity DOI: http://dx.doi.org/10.5772/intechopen.101681*

tissues exhibited a progressive reduction in salinity which is likely to influence CO2 diffusion [18].

The most challenging issues to assess by traditional microscopy methods are rice mesophyll tissues as their cells are lesser and have a greater density of chloroplast [28, 29] comparison to other plants. Thus, precise mesophyll morphology evaluation is essential for assessing photosynthetic capability [30] and maintains the leaf structure against salinity via following ways;

1.*Salt exclusion*: It inhibits salts from entering the vascular scheme.


Significant modifications were detected in salt stress chloroplast in rice leaf contrast to tolerance variety. These include; (1) Modifications in the chloroplasts number & size, and starch level. (2) Disordered membranes of the chloroplast. (3) Variations in plastoglobuli numbers and sizes. (4) Loss of the disorganization and envelope of thylakoids and grana which directly affect the chlorophyll fluorescence and photosynthetic rate, and reduced the productivity of rice (12). Chloroplast is recognized as an organelle susceptible to environmental stress [31], and its pockets [32] are known to be present in salt. Even though earlier TEM investigations have shown alterations in the chloroplast ultrastructure to salt that influence photosynthetic [32], these structural variations are specifically noticeable in the thylakoids [28] that swell under salt stress [3–32]. Therefore, mesophyll conductance decrease was correlated with the olive leaf mesophyll thickening [33]. A substantial reduction in mesophyll cell size was also a notable leaf anatomical characteristic found in *A. gomboformis*. Comparatively, small cells were found to better withstand turgor pressure than massive ones and more efficiently help to maintain turgor [34]. Thus, the decline in cell size was relatively considered to sustain tissue turgescence in *A. gomboformis* as a leaf tolerance mechanism.

On the other side, improved porosity by raising the parenchyma intercellular space did not promote the propagation conductivity of stressed plants [35]. The existence of highly vacuolated epidermal cells with poor metabolic seemed to function as a dumping mechanism in preventing mesophyll cells from stress [36]. However, decreasing the diameter of the xylem tube contributed in decreased hydraulic and ionic conductance [37] and therefore reduced photosynthesis and plant development.

The influence of salinity on leaf ultrastructure changed with the plant tolerance to NaCl, as reported in two rice species, (*Oryza sativa* L.). The sensitive rice species ('Jaya') indicated variations in the chloroplast integrity compared to the tolerant species ('Kogut'). Specifically, the majority of chloroplasts of 'Jaya' exhibited indications of damage in reaction to elevated NaCl. In comparison, 'Korgut' tolerance chloroplasts variety did not exhibit any salinity impact. This response was associated with a 53% decrease in PN in Jaya, while no substantial variation in PN was found in 'Korgut' [3] (**Figure 2**). The impact of NaCl on the ultrastructure

#### **Figure 2.**

*(A) Transmission electron microscope images of salt-tolerant variety, (a) under control (without treatment) and (b) treated with 160mM Nacl, showing thylakoid system of chloroplasts remained unaffected in control as well as under treatment. However, salt-sensitive variety, transmission electron microscope images of leaf, (c) under control, Chloroplasts had a well-developed system of thylakoids, (d) Thylakoid were damaged with loss of grana stacking under treatment; (B) Gas Exchange measurements; (C) Light reaction of photosynthesis [3].*

of leaf chloroplast was investigated in two distinct pea varieties with numerous sensitivity concentrations to NaCl, one sensitive to salt ("cv. Challis") and another relatively [38].

Aranda-Romero et al. [39] investigated anatomical disturbances generated with chloride salts (NaCl, CaCl2, KCl) in both tolerant (*Cleopatra mandarin*) and sensitive (*Carrizo citrange*) citrus cultivars. Salts in *P*N were associated with alterations in leaf anatomy, like the decrease in the thickness of the leaf and decreased mesophyll cell area (**Figure 1B–C**), enhanced leaf succulence, and decreased intercellular air space, surface, and density of the tissue. The anatomical alterations related to *Arbutus unedo* leaves in semi-thin sections were found by Navarro et al. [40]. A relationship between control plants and saline plants revealed that the cell size was not significantly changed in the 1st layer of palisade cells. Hernández et al. [38] observed in the same research that the NaCl concentration of salt and salt-tolerant pea plants had a distinct impact. Moreover, *Argyranthemum coronopifolium*, as demonstrated by Morales et al. [41], is similarly susceptible to high levels of salt. These researchers discovered that the salt in these plants does not cause modifications in the chloroplast's number, while in palisade & mesophyll cells, chloroplasts have risen significantly owing to a rise in the quantity of starch in palisade parenchyma compared to mesophyll tissues. A smaller formation of sucrose and hexoses and high activity of phosphate – sucrose synthase may explain the development of starch in leaf-chloroplasts in saline condition, which may lead to the triosephosphate path towards the synthesis of starch or/and enzymes damage included in starch deterioration through modifications in the ionic chloroplast's composition [41, 42]. The variations in the sizes of a chloroplast, as well as starch accumulation among palisade and mesophyll, parenchyma was explained by various photosynthetic leaf rate values observed by Morales et al. [41].

#### **2. Anatomy of roots**

The roots under salinity stress are essential to stress management studies since the root surfaces are initially exposed to environmental stress [43]. The root system *Morpho-Anatomical Adaptation against Salinity DOI: http://dx.doi.org/10.5772/intechopen.101681*

**Figure 3.**

*Effect of salinity on root anatomy (10x, magnification) of oryza sativa L.(A): anatomical structure of rice roots under control (without treatment); and (B):under salinity stress (200 mM NaCl). The different letter in the figures represents; a; epidermis, b; exodermis, c; sclerenchyma layers, d; mesodermis, e; endodermis, f; pericycle, g; pholem, h; metaxylem.*

anatomy correlates to root efficiency and permits plants to get nutrients and water, thus increasing the degree of replacement for lost plant water [44]. The anatomy system also prevents the salt build-up from roots, so that water from salty soils may continue [45]. Salt stress mainly controls root hair production and growth [46]. Root epidermal development demonstrates flexibility because external stimuli affect epidermal cells and root hair commencement [47]. The roots cross-section of rice species seedlings studied, in absence of stress, a greater roots thickness and wellorganized tissue were noted in rice but root thickness decreased in salt condition (**Figure 3**). Growth of the plasticity root epidermis suggests a role of root hairs in detecting environmental signals that plants adapt to stressful circumstances as a reaction to different environmental conditions [48]. Optimal root systems promote plant development and increase plant output, as roots interface plants with the earth [47]. A plant root system that is increasing thus seems better since it enables it to reach deeper soil layers and get water and nutrients [49]. Moreover, soil environmental variables (temperature fluctuations, salinity, mechanical impedance, lack of O2) may also have significant effects on the root morphology. Salt stress at a lower concentration induced plentiful root hairs, but progressively less root hair counts were calculated at increased salt levels [48]. Under the stress of salt, the root hair length and the root hair density were below 25 & 40% in comparison with untreated hydroponically cultivated wheat genotypes [36]. Two determinants of the total root surface area are total root duration and branching density – improved during moderate drought stress by comparison with "*Silene vulgaris* seedlings" [43]. Moreover, the morphology of certain plants indicates their salt sensitivity. Salinity inhibits the development of plants via osmotic & toxic effects and high sodium absorption levels because sodium raises soil tolerance, decreases root growth & root water flow by decreasing hydraulic conductivity [50]. The same behavior was also found in "*Euonymus japonica*" plants treated with a solution of NaCl and retrieved water comprising various levels of salt, which reduced the entire plant's root length, most particularly in thin ("Ø ≤ 0.5 mm") as well as average thickness ("0.5 < Ø≤2.0 mm") roots [51]. In other varieties of the plant (*Portulaca oleracea* &*Pinus banksiana*), Croser et al. [52] & Franco et al. [46] have reported a rise in root diameter as a result of salinity. The higher root density found in plants indicates better tolerance and perhaps greater reserved accumulation [45, 46] that might enhance plant resistance and accelerate the plant's establishment for farming and landscape objectives, particularly ornamental plants [53]. Root hydraulic conductivity can vary according to the salt concentration of irrigated water used in cultivated fields [54]. The root hydraulic behavior usually expresses the entire root dry weight, regardless of the root architectural function in

water absorption capacity. However, the number of fine roots that define the root and the area could vary significantly in any given relatively dry weight value, therefore influencing the degree of water absorption [55]. The detrimental impacts of abiotic stress may be reduced more by salt-tolerant rootstocks than by rootstocks sensitive to salt. Navarro et al. [54] reported lower fruit production and attribute in Carrizo grafting of the *Clemenules mandarins* ("salt-sensitive rootstock") in comparison with *Cleopatra* ("salt-tolerant rootstock"), both exposed to a solution of NaCl (30 mM). According to Penella et al. [56], the output of commercial pepper cultivars during salt irrigation was shown to be raised in salt-tolerant rootstocks. Nassar et al. [57] noted that the widths of vascular bundles and rice stems diameters reduced in NaCl. NaCl treatment in mung bean seedlings was noted by Khan et al. [58] to suppress the development of the vascular system. Gal et al. [59] found that shoot/root ratio was an essential indicator in predicting water consumption, water loss, and hydraulic conductivity in the C3 plants. The roots permeability to water is also measured by other root features, like the number of root hairs, root cortex width, xylem vessels number & diameter, and the suberin deposition in root endodermis and exodermis. This xylem structural modification may influence the capacity of water movement [60]. The xylem's capability to resist negativity depends on the specific environmental limitations [60]. Many studies show that every plant uses the same basic effectors and regulatory systems for salt tolerance and that the variation in glycophytic & halophytic species is quantitative rather than qualitative [61].

## **3. AMF ("arbuscular mycorrhizal fungi")**

The inoculation of roots AMF (that is considered an essential bio-ameliorators) for salt soils and facilitating host plants' strong growth under stressful circumstances through various complicated events of communication between the plants as well as the fungus, leading to enhancing photosynthetic activity and other features linked to gas exchanges [62] and enhanced absorption of water. Several investigations have shown that AMF's effectiveness imparts development and increase in salinity stress plants [63, 64]. AMF enhances plant nutrition by improving the availability and transport of different nutrients [65]; and also enhances soil quality by affecting its texture and structure, and therefore plant health [66, 67] and reduces Na and Cl uptake, resulting in a growth boost [68]. Good interactions between AMF-soil plants may allow reusing of recovered water, especially when roots develop in saline soil [69]. Mycorrhizal inoculation prominently increased photosynthetic rate with other gas interchange characteristics, the content of chlorophyll, and water usage effectiveness in "*Ocimumbasilicum* L." in saline circumstances [70]. AMF-inoculated plants with "*allium sativum*" exhibited increased development rates, such as the leaf area index, dry & fresh biomass in saline circumstances [71] Wang et al. [72] observed a substantial improvement in fresh & dry weights and N levels of Root & Shoot owing to inoculation with mycorrhizal in mild saline conditions.

## **4. Conclusion**

With a burgeoning population estimated to reach around 1.43 billion by 2030, India requires approximately 311 million tons of cereals and pulses to achieve food security. To meet the future food security target, it is expected to increase food grain production by 2 million tons per annum. To increase food grain production, there is a dire need to expand agricultural land and increase crop productivity. One

#### *Morpho-Anatomical Adaptation against Salinity DOI: http://dx.doi.org/10.5772/intechopen.101681*

of the possible solutions to address this problem is the genetic improvement of rice varieties in order to enhance their tolerance to salinity. In this review we have discussed morphology and anatomy review that indicates, high salinity is characterized by an increase in the leaf size, trichome and stomata size, and number, thickening of epidermis, area of vascular bundles, maintained thylakoid structure as adaptive characters for salinity stress; these characters are used as an indicator of the salinity of the soil. In addition, AMF is considered essential bio-ameliorators, which can enhance soil quality and maintain better productivity under salinity. Therefore, understanding different mechanisms enable crops to be sustained in hypersaline conditions; this may eventually contribute in improving rice yield on saline lands.

## **Author details**

Smita Srivastava Department of Botany, Goa University, Taleigao, Goa, India

\*Address all correspondence to: srivastavasmita13@gmail.com

© 2022 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

## **References**

[1] Silva BRS, Batista BL, Lobato AKS. Anatomical changes in stem and root of soybean plants submitted to salt stress. Plant Biology. 2021;**23**(1):57-65. DOI: 10.1111/plb.13176

[2] Glover BJ, Airoldi CA, Moyroud E. Epidermis: Outer cell layer of the plant. In: eLS. Chichester, UK: John Wiley & Sons, Ltd.; 2016. DOI: 10.1002/ 9780470015902.a0002072.pub3

[3] Srivastava S, Sharma PK. Morphophysiological and biochemical tolerance mechanisms in two varieties of Oryza sativato salinity. Russian Journal of Plant Physiology. 2022;**69**:37. DOI: 10.1134/S1021443722020194

[4] Abernethy GA, Fountain DW, McManus MT. Observations on the leaf anatomy of Festuca novae-zelandiae and biochemical responses to a water deficit. New Zealand Journal of Botany. 1998;**36**(1):113-123

[5] Aguirre-Medina JF, Gallegos JAA, del Ruiz Posadas L, Shibata JK, Lopez CT. Morphological differences on the leaf epidermis of common bean and their relationship to drought tolerance. Agricultura technical en mexico. 2002;**28**(1):53-64

[6] Riederer M, Schreiber L. Protecting against water loss: Analysis of the barrier properties of plant cuticles. Journal of Experimental Botany. 2001;**52**(363):2023-2032. DOI: 10.1093/ jexbot/52.363.2023

[7] Bleeker PM, Mirabella R, Diergaarde PJ, VanDoorn A, Tissier A, Kant MR, et al. Improved herbivore resistance in cultivated tomato with the sesquiterpene biosynthetic pathway from a wild relative. Proceedings of the National Academy of Sciences of the United States of America. 2012;**109**(49):20124-20129. DOI: 10.1073/pnas.1208756109

[8] Antunes WC, Provart NJ, Williams TCR, Loureiro ME. Changes in stomatal function and water use efficiency in potato plants with altered sucrolytic activity. Plant, Cell and Environment. 2012;**35**(4):747-759. DOI: 10.1111/j.1365-3040.2011.02448.x

[9] Tian D, Tooker J, Peiffer M, Chung SH, Felton GW. Role of trichomes in defense against herbivores: Comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum Lycopersicum). Planta. 2012;**236**(4):1053-1066. DOI: 10.1007/s00425-012-1651-9

[10] Galmés J, Ochogavía JM, Gago J, Roldán EJ, Cifre J, Conesa MÀ. Leaf responses to drought stress in mediterranean accessions of solanum lycopersicum: Anatomical adaptations in relation to gas exchange parameters. Plant, Cell and Environment. 2013;**36**(5):920- 935. DOI: 10.1111/pce.12022

[11] Franks PJ, Doheny-Adams WT, Britton-Harper ZJ, Gray JE. Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytologist. 2015;**207**(1):188-195. DOI: 10.1111/nph.13347

[12] Schleiff U, Muscolo A. Fresh look at plant salt tolerance as affected by dynamics at the soil/root-interface using Leek and Rape as model crops. European Journal of Plant Science and Biotechnology. 2011;**5**:27-32

[13] Spyropoulou EA, Haring MA, Schuurink RC. RNA sequencing on Solanum lycopersicum trichomes identifies transcription factors that activate terpene synthase promoters. BMC Genomics. 2014;**15**:402. DOI: 10.1186/1471-2164-15-402

[14] Kang JH, McRoberts J, Shi F, Moreno JE, Jones AD, Howe GA. The flavonoid biosynthetic enzyme chalcone *Morpho-Anatomical Adaptation against Salinity DOI: http://dx.doi.org/10.5772/intechopen.101681*

isomerase modulates terpenoid production in glandular trichomes of tomato. Plant Physiology. 2014;**164**(3):1161-1174. DOI: 10.1104/ pp.113.233395

[15] Richardson F, Brodribb TJ, Jordan GJ. Amphistomatic leaf surfaces independently regulate gas exchange in response to variations in evaporative demand. Tree Physiology. 2017;**37**(7):869-878. DOI: 10.1093/ treephys/tpx073

[16] McElwain JC, Yiotis C, Lawson T. Using modern plant trait relationships between observed and theoretical maximum stomatal conductance and vein density to examine patterns of plant macroevolution. New Phytologist. 2016;**209**(1):94-103. DOI: 10.1111/ nph.13579

[17] Hameed M, Ashraf M, Naz N, Qurainy FA. Anatomical adaptations of Cynodondactylon (L.) Pers. from the Salt Range, Pakistan to salinity stress. I. Root and stem anatomy. Pakistan Journal of Botany. 2010;**42**:279-289

[18] Aasamaa K, Söber A, Rahi M. Leaf anatomical characteristics associated with shoot hydraulic conductance, stomatal conductance and stomatal sensitivity to changes of leaf water status in temperate deciduous trees. Functional Plant Biology. 2001;**28**(8):765-774. DOI: 10.1071/PP00157

[19] Zhang H, Wang X, Wang S. A study on stomatal traits of Platanus acerifolia under urban stress. Journal of Fudan Journal of Fudan. 2004;**43**:651-656

[20] Bosabalidis AM, Kofidis G. Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Science. 2002;**163**(2):375-379. DOI: 10.1016/S0168-9452(02)00135-8

[21] Degl'Innocenti E, Hafsi C, Guidi L, &Navari-Izzo, F. The effect of salinity

on photosynthetic activity in potassiumdeficient barley species. Journal of Plant Physiology. 2009;**166**(18):1968-1981. DOI: 10.1016/j. jplph.2009.06.013

[22] Ola HAE, Reham EF, Eisa SS, Habib SA. Morphoanatomical changes in salt stressed kallar grass (Leptochloafusca L. Kunth). Research Journal of Agriculture and Biological Sciences. 2012;**8**:158-166

[23] Ali I, Abbas SQ, Hameed M, Naz N, Zafar S, Kanwal S. Leaf anatomical adaptations in some exotic species of Eucalyptus L.'Hér. (Myrtaceae). Pakistan Journal of Botany. 2009;**41**: 2717-2727

[24] Akram M, Akhtar S, Javed IUH, Wahid A, Rasul E. Anatomical attributes of different wheat (Triticum aestivum) accessions/varities to NaCl salinity. International Journal of Agriculture and Biology. 2002;**4**:166-168

[25] Nawaz T, Hameed M, Ashraf M, Ahmad MSA, Batool R, Fatima S. Anatomical and physiological adaptations in aquatic ecotypes of Cyperus alopecuroidesRottb. under saline and waterlogged conditions. Aquatic Botany. 2014;**116**:60-68. DOI: 10.1016/j.aquabot.2014.01.001

[26] Wankhade SD, Cornejo MJ, Mateu-Andrés I, Sanz A. Morphophysiological variations in response to NaCl stress during vegetative and reproductive development of rice. Acta Physiologiae Plantarum. 2013;**35**(2):323- 333. DOI: 10.1007/s11738-012-1075-y

[27] Shabala S, Hariadi Y, Jacobsen SE. Genotypic difference in salinity tolerance in quinoa is determined by differential control of xylem Na+ loading and stomatal density. Journal of Plant Physiology. 2013;**170**(10):906-914. DOI: 10.1016/j.jplph.2013.01.014

[28] Oi T, Enomoto S, Nakao T, Arai S, Yamane K, Taniguchi M. Three-dimensional intracellular structure of a whole rice mesophyll cell observed with FIB-SEM. Annals of Botany. 2017;**120**(1):21-28. DOI: 10.1093/aob/mcx036

[29] Sage TL, Sage RF. The functional anatomy of rice leaves: Implications for refixation of photorespiratory CO2 and efforts to engineer C4 photosynthesis into rice. Plant and Cell Physiology. 2009;**50**(4):756-772. DOI: 10.1093/ pcp/pcp033

[30] Burundukova OL, Zhuravlev YN, Solopov NV, P'yankov VI. A method for calculating the volume and surface area in rice mesophyll cells. Russian Journal of Plant Physiology. 2003;**50**(1):133-139. DOI: 10.1023/A:1021961123504

[31] Omoto E, Kawasaki M, Taniguchi M, Miyake H. Salinity induces granal development in bundle sheath chloroplasts of NADP-malic enzyme type C4 plants. Plant Production Science. 2009;**12**(2):199-207. DOI: 10.1626/pps.12.199

[32] Yamane K, Oi T, Enomoto S, Nakao T, Arai S, Miyake H, et al. Three-dimensional ultrastructure of chloroplast pockets formed under salinity stress. Plant, Cell and Environment. 2018;**41**(3):563-575. DOI: 10.1111/pce.13115

[33] Loreto F, Centritto M, Chartzoulakis K. Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant, Cell and Environment. 2003;**26**(4):595-601. DOI: 10.1046/j.1365-3040.2003.00994.x

[34] Boughalleb F, Abdellaoui R, Hadded Z, Neffati M. Anatomical adaptations of the desert species Stipa lagascae against drought stress. Biologia. 2015;**70**(8):1042-1052. DOI: 10.1515/ biolog-2015-0125

[35] Boughalleb F, Denden M, Tiba BB. Anatomical changes induced by

increasing NaCl salinity in three fodder shrubs, Nitraria retusa, Atriplex halimus and Medicago arborea. Acta Physiologiae Plantarum. 2009;**31**(5):947-960. DOI: 10.1007/ s11738-009-0310-7

[36] Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Annals of Botany. 2003;**91**(5):503-527. DOI: 10.1093/ aob/mcg058

[37] Van Ieperen W, Van Meeteren U, Van Gelder H. Fluid ionic composition influences hydraulic conductance of xylem conduits. Journal of Experimental Botany. 2000;**51**(345): 769-776. DOI: 10.1093/jexbot/51. 345.769

[38] Hernández JA, Olmos E, Corpas FJ, Sevilla F, del Río LA. Salt-induced oxidative stress in chloroplast of pea plants. Plant Science. 1995;**105**(2): 151-167. DOI: 10.1016/0168-9452 (94)04047-8

[39] Romero-Aranda R, Moya JL, Tadeo FR, Legaz F, Primo-Millo E, Talon M. Physiologicalandanatomical disturbances induced by chloride salts in sensitive and tolerant citrus: Beneficial and detrimental effects of cations. Plant, Cell and Environment. 1998;**21**(12):1243-1253. DOI: 10.1046/j.1365-3040.1998.00349.x

[40] Navarro A, Bañón S, Olmos E, Sánchez-Blanco MJ. Effects of sodium chloride on water potential components, hydraulic conductivity, gas exchange and leaf ultrastructure of arbutus unedo plants. Plant Science. 2007;**172**(3):473- 480. DOI: 10.1016/j. plantsci.2006.10.006

[41] Morales MA, Sánchez-Blanco MJ, Olmos E, Torrecillas A, Alarcón JJ. Changes in the growth, leaf water relations and cell ultraestructure in argyranthemum coronopifolium plants under saline conditions. Journal of Plant *Morpho-Anatomical Adaptation against Salinity DOI: http://dx.doi.org/10.5772/intechopen.101681*

Physiology. 1998;**153**(1-2):174-180. DOI: 10.1016/S0176-1617(98)80062-X

[42] Balibrea ME, Dell'Amico J, Bolarín MC, Pérez-Alfocea F. Carbon partitioning and sucrose metabolism in tomato plants growing under salinity. Physiologia Plantarum. 2000;**110**(4):503-511. DOI: 10.1111/j.1399-3054.2000.1100412.x

[43] Szabó-Nagy A, Galiba G, Erdei L. Induction of soluble phosphatases under ionic and non-ionic osmotic stresses in wheat. Journal of Plant Physiology. 1992;**140**(5):629-633. DOI: 10.1016/ S0176-1617(11)80800-X

[44] Khan MH, Panda SK. Alterations in root lipid peroxidation and antioxidative responses in two rice cultivars under NaCl-salinity stress. Acta Physiologiae Plantarum. 2007;**30**(1):81-89. DOI: 10.1007/s11738-007-0093-7

[45] Franco JA, Bañón S, Vicente MJ, Miralles J, Martínez-Sánchez JJ. Root development in horticultural plants grown under abiotic stress conditions–a review. Journal of Horticultural Science and Biotechnology. 2011;**86**(6):543-556. DOI: 10.1080/14620316.2011.11512802

[46] Munns R, Passioura JB, Colmer TD, Byrt CS. Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytologist. 2020;**225**(3):1091- 1096. DOI: 10.1111/nph.15862

[47] Dwivedi SL, Stoddard FL, Ortiz R. Genomic-based root plasticity to enhance abiotic stress adaptation and edible yield in grain crops. Plant Science. 2020;**295**:110365. DOI: 10.1016/j.plantsci.2019.110365

[48] Vamerali T, Saccomani M, Bona S, Mosca G, Guarise M, Ganis A. A comparison of root characteristics in relation to nutrient and water stress in two maize hybrids. Plant and Soil. 2003;**255**(1):157-167. DOI: 10.1023/A:1026123129575

[49] Smith DM, Inman-Bamber NG, Thorburn PJ. Growth and function of the sugarcane root system. Field Crops Research. 2005;**92**(2-3):169-183. DOI: 10.1016/j.fcr.2005.01.017

[50] López-Berenguer C, García-Viguera C, Carvajal M. Are root hydraulic conductivity responses to salinity controlled by aquaporins in broccoli plants? Plant and Soil. 2006;**279**(1):13-23

[51] Gómez-Bellot MJ, Álvarez S, Castillo M, Bañón S, Ortuño MF, Sánchez-Blanco MJ. Water relations, nutrient content and developmental responses of Euonymus plants irrigated with water of different degrees of salinity and quality. Journal of Plant Research. 2013;**126**(4):567-576. DOI: 10.1007/s10265-012-0545-z

[52] Croser C, Renault S, Franklin J, Zwiazek J. The effect of salinity on the emergence and seedling growth of piceamariana, picea glauca, and pinus banksiana. Environmental Pollution. 2001;**115**(1):9-16. DOI: 10.1016/ s0269-7491(01)00097-5

[53] Sánchez-Blanco MJ, Ortuño MF, Bañon S, Álvarez S. Deficit irrigation as a strategy to control growth in ornamental plants and enhance their ability to adapt to drought conditions. The Journal of Horticultural Science and Biotechnology. 2019;**94**(2):137-150

[54] Navarro JM, Gómez-Gómez A, Pérez-Pérez JG, Botía P. Effect of saline conditions on the maturation process of clementine Clemenules fruits on two different rootstocks. Spanish Journal of Agricultural Research. 2010;**8**(S2):21-29. DOI: 10.5424/sjar/201008S2-1344

[55] Wu HI, Sharpe PJ, Walker J, Penridge LK. Ecological field theory: A spatial analysis of resource interference among plants. Ecological Modelling. 1985;**29**(1-4):215-243

[56] Penella C, Nebauer SG, Quiñones A, San Bautista A, López-Galarza S, Calatayud A. Some rootstocks improve pepper tolerance to mild salinity through ionic regulation. Plant Science. 2015;**230**:12-22. DOI: 10.1016/j. plantsci.2014.10.007

[57] Nassar RMA, Kamel HA, Ghoniem AE, Alarcón JJ, Sekara A, Ulrichs C, et al. Physiological and anatomical mechanisms in wheat to cope with salt stress induced by seawater. Plants. 2020;**9**(2):237. DOI: 10.3390/plants9020237

[58] Khan MN, Siddiqui MH, Mukherjee S, Alamri S, Al-Amri AA, Alsubaie QD, et al. Calcium–hydrogen sulfide crosstalk during K+-deficient NaCl stress operates through regulation of Na+/H+ antiport and antioxidative defense system in mung bean roots. Plant Physiology and Biochemistry. 2021;**159**:211-225. DOI: 10.1016/j. plaphy.2020.11.055

[59] Gal A, Hendel E, Peleg Z, Schwartz N, Sade N. Measuring the hydraulic conductivity of grass root systems. Current Protocols in Plant Biology. 2020;**5**(2):e20110. DOI: 10.1002/cppb.20110

[60] Brodribb TJ. Xylem hydraulic physiology: The functional backbone of terrestrial plant productivity. Plant Science. 2009;**177**(4):245-251. DOI: 10.1016/j.plantsci.2009.06.001

[61] Flowers TJ, Troke PF, Yeo AR. The mechanism of salt tolerance in halophytes. Annual Review of Plant Physiology. 1977;**28**(1):89-121. DOI: 10.1146/annurev.pp.28.060177.000513

[62] Birhane E, Sterck FJ, Fetene M, Bongers F, Kuyper TW. Arbuscular mycorrhizal fungi enhance photosynthesis, water use efficiency, and growth of frankincense seedlings under pulsed water availability conditions. Oecologia. 2012;**169**(4):895- 904. DOI: 10.1007/s00442-012-2258-3

[63] Talaat NB, Shawky BT. Protective effects of arbuscular mycorrhizal fungi on wheat (*Triticum aestivum* L.) plants exposed to salinity. Environmental and Experimental Botany. 2014;**98**:20-31. DOI: 10.1016/j.envexpbot.2013.10.005

[64] Abdel Latef AA, Miransari M. The role of arbuscular mycorrhizal fungi in alleviation of salt stress. In: Use of Microbes for the Alleviation of Soil Stresses. Vol. 23. New York: Springer; 2014. DOI: 10.1007/978-1-4939- 0721-2\_2

[65] Rouphael Y, Franken P, Schneider C, Schwarz D, Giovannetti M, Agnolucci M, et al. Arbuscular mycorrhizal fungi act as bio-stimulants in horticultural crops. Scientia Horticulturae. 2015;**196**:91-108. DOI: 10.1016/j.scienta.2015.09.002

[66] Zou YN, Srivastava AK, Wu QS. Glomalin: A potential soil conditioner for perennial fruits. International Journal of Agriculture and Biology. 2016;**18**(2):293-297. DOI: 10.17957/ IJAB/15.0085

[67] Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ. Are mycorrhizal fungi our sustainable saviours considerations for achieving food security. Journal of Ecology. 2017;**105**(4):921-929. DOI: 10.1111/1365-2745.12788

[68] Evelin H, Giri B, Kapoor R. Contribution of *Glomusintraradices* inoculation to nutrient acquisition and mitigation of ionic imbalance in NaClstressed *Trigonella foenum-Graecum*. Mycorrhiza. 2012;**22**(3):203-217. DOI: 10.1007/s00572-011-0392-0

## [69] Calvo-Polanco M,

Sánchez-Romera B, Aroca R, Asins MJ, Declerck S, Dodd IC, et al. Exploring the use of recombinant inbred lines in combination with beneficial microbial inoculants (AM fungus and PGPR) to improve drought stress tolerance in tomato. Environmental and

*Morpho-Anatomical Adaptation against Salinity DOI: http://dx.doi.org/10.5772/intechopen.101681*

Experimental Botany. 2016;**131**:47-57. DOI: 10.1016/j.envexpbot.2016.06.015

[70] Elhindi KM, El-Din AS, Elgorban AM. The impact of arbuscular mycorrhizal fungi in mitigating saltinduced adverse effects in sweet basil (*Ocimumbasilicum* L.). Saudi Journal of Biological Sciences. 2017;**24**(1):170-179. DOI: 10.1016/j.sjbs.2016.02.010

[71] Borde M, Dudhane M, Jite PK. AM fungi influences the photosynthetic activity, growth and antioxidant enzymes in *Allium sativum* L. under salinity condition. Notulae Scientia Biologicae. 2010;**2**(4):64-71. DOI: 10.15835/nsb245434

[72] Wang Y, Wang M, Li Y, Wu A, Huang J. Effects of arbuscular mycorrhizal fungi on growth and nitrogen uptake of Chrysanthemum morifolium under salt stress. PLoS One. 2018;**13**(4):e0196408. DOI: 10.1371/ journal.pone.0196408

## **Chapter 12**
