1. INTRODUCTION
The antioxidants participate as a prime substance in the plants [1]. The building of reactive oxygen species (ROS) in bulk amounts can trigger plant metabolism [1]. This situation arises in drought stress [1]. However, at the same time, the plants also produce compounds that stop the oxidation process and acquit themselves as a defence system to drop the level of free radicals such as O2-, OH-, and H2O2; the improvements of water content in tissue are done by major osmolytes such as proline, glycine, betaine, and sugars [2]. Drought stress produces a negative effect on the plants. It knocks the development of the plant, growth, and upgrade the richness of the soil [1]. Water stress activates the loss of water and decreases the water potential which will lead a reduction in turgidity of the cell. The production of abscisic acid (ABA) on the plants leads to reduction of loss of transpirational water by closing of stomata in water-deficient condition [2]. Intensity of drought will increase due to the long spell of drought. The osmotic adjustment leads to lower the root-shoot ratio, modification of cell wall. Apart from this, the activation of antioxidant system also occurs [3]. The plants when performed the photosynthesis hike the diffusion of gas barrier which can deplete the intercellular CO2 concentration. When the reduction of CO2 takes place, the activation of ribulose -1-5-biphosphate oxygenate undertake place. This leads the proffering of H2O2 (hydrogen peroxidase) in peroxisomes [4]. Mycorrhiza also plays a role in the sheltering the host plants in moisture stress.
It takes part in water absorption by extra radical mycelium, improvement of nutrient acquisition, defense system of plants. However, Arbuscular mycorrhiza fungi (AMF) plants also adapt the host plants morphologically and improve the structure of soil through the spread of hyphae. Furthermore, molecular changes in plants are also observed. The levels of ROS are dynamic during colonization of fungus. The generation of hydrogen peroxidase in mycorrhiza-contained cortical cell ensures the colonization of AM fungus in roots, but the production of H2O2 is transient and eliminates by building of super oxidase dismutase (SOD), CAT, and carotenoids. The study on Medicago truncatula, the accumulation of hydrogen peroxidase in arbuscular containing root of plants has observed but its roots were less branched. When hydrogen peroxide is scattered the hyphal wall of AMF branches, the fungus started senescence. The AMF inoculation raises the level of antioxidant in plants by 16% [5]. When sesame plants are come under drought stress, Funneliformis mosseae and Rhizophagus irregularis both increased the activity of ascorbate peroxidase (APX), phenylalanine ammonia-lyase (PAL). Apart from this, the content of total soluble sugar also high in plant [6]. In addition to this [7] in plant chicory, the level of antioxidant like SOD increases and reduced the accumulation of hydrogen peroxidase. Similarly in lettuce, symbiosis of AMF improved the concentration of carotenoids and anthocyanins in drought stress condition [8].
When there is more gathering of antioxidants enzymes, it alleviates the toxicity on lipids and DNA [9]. Therefore, AMF plants have more endurance than non-inoculated plants.
2. DROUGHT STRESS IN PLANTS
Drought stress is the momentous phase where diverse changes included the morphological, physiological, and biochemical responses are observed in the plants [Figure 1]. The stress in the plants leads the reduction of growth. It decreases the root length as well as shoots length [10,11]. It also reduces biomass in plants. Flowering as well as fruiting of plants is also affected. The physiological changes in plants are also observed such as the photosynthesis rate will decrease, the osmotic balance gets disrupted. Biochemically, the plants are also affected by the level of osmolytes like content of proline which can changes according to the condition. The defense system like antioxidants which shows changes in the concentration as compared to the normal plants which cannot face any stress condition [12,13].
 | Figure 1: Illustration of drought stress in plants. [Click here to view] |
2.1. Drought Tolerance: Insight Mechanism
The plants adapt itself in stress condition and cope up the effect of stress. Moisture stress changes the plant by physiologically and biochemically as well as morphologically. Drought avoidance is the mechanism by which plants can adapt in environment [14,15]. The deep and thick roots are the characteristics feature of the drought avoidance. The biomasses of roots as well as its length are increases which help the crop to avoid itself from drought [16]. Talking about drought tolerance in plants glaucousness also called waxy loom is the main characteristics for drought tolerance. These desirable traits help the plants to maintain the potential of water in tissues [17]. In wheat, this trait helps to increase the efficiency of water. This characteristic does not affect the harvest index of plants as well as total water use of plants. Glaucous leaves give more advantages to plants as compared to non-glaucous leaves. The glaucous leaves are cooler than normal leaves. The temperature of this waxy leaves is 0.7° cooler than non-waxy leaves. The other advantages of these leaves are that the rates of senescence of leaves are less which is higher in non-waxy leaves. The mechanism where plants lower the temperature by 0.5° the period of grain filling will increase up to 3 days or more. However, the yields in this condition are not increases. The stoma plays a crucial role for transpiration of plants [18]. The holes that are present in the surface of leaf became the main trail for entry of carbon dioxide. When the water stress occurs, the plant follows a mechanism of closure of stomata. This closing of stomata helps to decrease the water potential of leaf. This closure also lowers down the oxidative damage and assimilation of carbon. This feature increases the temperature of canopy [19]. Other traits like hairy leaves which decrease the leaf temperature of leaves and also the transpiration [20]. The hairiness of leaves decreases the water loss and increases the reflectance of light. Other characteristic like leaf pubescence helps the plants from heat. This is xeromorphic trait found when drought stress occurs. These types of mechanism which are establish in the plants assist the plants to prevail the moisture stress.
3. BIOCHEMICAL REACTION IN PLANTS UNDER DROUGHT STRESS
When plants are affected with drought, the various biochemical changes are occur. The plants result in accumulation of proline, solutes, free radicals, and hydrogen peroxides which result in the destruction of its cell metabolic functions [21,22]. The antioxidants include SOD and catalase (CAT) which also active in plants to protect from stress which makes various positive changes in crops [22]. The function of antioxidants not only the defense mechanism but also maintains redox balance during oxidative stress [23]. The moisture stress in plants causes the ROS production. This ROS cause the cell to destroy their machinery. ROS contains singlet oxygen, hydrogen peroxide, superoxide, and hydroxyl peroxide [24]. As hydrogen peroxide is the signal molecule which is produced during abiotic stress like drought. The removal of H2O2 is done by the ascorbic acid which is very useful for the protection of the plants. This ascorbic acid is useful for lower down the level of ROS in plants. The antioxidant mechanism is not much as simple because it requires the enzymes called as APX which is catalyzed to proceed the reaction used for elimination of H2O2 in cell. This APX known as APX mainly found in chloroplast, mitochondria. In oxidative stress, the molecules of hydrogen peroxide are produce. Hence, the plants face the drought conditions, the more content of hydrogen peroxide has been observed [25].
4. AMF-INOCULATED PLANTS IN DROUGHT STRESS
Mycorrhiza permits a mutual relationship between higher plants and the roots of fungi. Arbuscular mycorrhiza is also known AMF or Vesicular arbuscular mycorrhiza. There are many species of mycorrhiza which make the contribution [26]. The endomycorrhiza which is one of the type of AMF can penetrate in the cortical cell of plants and form structure. The structure is known as Arbuscular which is branch like structure and vesicles which is the storage organ [27]. The soil structures and stability are also improved by mycorrhiza. Apart from this, mycorrhiza can provide the plant nutrients like nitrogen and phosphorus to host plants. Mycorrhiza produces the antibodies and hormones which decrease the prevalence of disease and increases the production of plants [28]. The mycorrhiza gives protection against stress like drought and salt and it increases growth and productivity of the crops [29] [Figure 2]. From the point of morphological, physiological, and biochemical, the plants show better response as compared to normal plants [30]. Biochemically, the concentration of proline gets affected [31]. The antioxidants defense system is also affected by the mycorrhiza association. In rice plants, the mycorrhiza also shows better result in drought stress condition. The researches have shown that if plants are affected in drought stress, the morphologically physiologically [32] and biochemically [33] shows better result as compared to non-AMF plants in drought stress conditions. As different researches are conducted by scientists on the rice with several species of mycorrhiza, in one research where the scientist conduct a research with one species known as Glomus intraradices and observes the result at 70 days after transplanting (DAT) which seems to be positive. After 70 DAT, the AMF colonization increases. Similarly, the increment seen as the days passes. As the colonization increases, the effect of AMF in plants which are positive is also increases [34].
 | Figure 2: Mechanism of drought tolerance with Arbuscular mycorrhiza fungi in plants. [Click here to view] |
The rice with AMF has higher photosynthesis efficiency than without AMF plants. When the rice plants are imposed to drought stress, the photosynthetic activity has been affected. As the study suggested that when the plant in drought condition is more vulnerable to injury as compared to AMF plants. Growth system is affected and efficiency of CO2 in drought condition is also increasing in AMF plants. This damage causes the production of harmful chemicals in plant cell [35]. In this process, colonization by AMF makes the improvement in establishment of diverse network of hyphae and also secrete the glomalin. This secretion provides assistance in uptake of water and nutrient and therefore increases the structure of soil [36]. Various studies have been there which suggested that AMF itself develops drought adaptive strategies by extra radical hyphae. This impacted the plant mechanism which effects other rate of photosynthesis, hydraulic conductivity of root, and architecture of root [37].
The response of AMF composes the multifaceted mechanism of drought-responsive genes, along with activation of different metabolism pathways [38]. The amelioration of drought by AM symbioses which are engage in up and down-regulation of various biochemical and physiological pathways. The amendment of regulation of water by AMF has occurred in host plant by generation of hormonal signal and prompting of osmolytes. The enhancement of maize growth has been studied by the symbiosis of AMF. This was reported in drought-sensitive varieties in maize. This positive impact of symbiosis by AMF was correlated with better efficiency of photosystem II, stability of membrane, and lipid peroxidation [39-41].
5. ACTIVITY OF ANTIOXIDANTS IN MOISTURE STRESS
Drought stress is emerging problem due to less water availability. When there is a stress-like condition, it occurs the ROS active in plants and its accumulation leads to the damaging to the cell. When this ROS is produced, the production of antioxidants takes place which results in a lower level of ROS in plants. The antioxidants such as SOD, hydrogen peroxidase, and CAT these all antioxidants reduced the level of harmful ROS and mitigate the damage which are caused by lipid peroxidation [Table 1]. Therefore, the antioxidants shield the structure of the cell membrane and also save from moisture stress [42]. Stress-responsive genes have a role in osmotic regulation and aquaporin’s which are manipulated in drought stress and intensify the tolerance of drought in plants [43,44]. An antioxidant like SOD is also called as a metal enzyme. This enzyme can eliminate the superoxide anion free radicals. As a result, the hydrogen peroxide is converted into the water by the activity of the CAT enzyme [45]. The plant in water-deficient conditions closes its stomata and reduces the loss of transpiration. When the ROS produced, the plants are also producing antioxidants which are very useful for plants in condition like drought stress [46].
Table 1: Antioxidants activity in various crops with response to AMF under water deficient conditions.
| Crops | Drought stress | Antioxidant activity | References |
|---|---|---|---|
| Wheat | At 50% field capacity | Reduction of Reactive oxygen species and improvement of CAT, SOD, Ascorbate peroxidase (APX), Glucocorticoid protein (GR) | [75] |
| Tobacco | At 30% field capacity | Mycorrhiza reduced the level of MDA (Malondialdehyde) and improved APX, CAT, SOD activities | [68] |
| Soybean | Drought stress was given at pod and seed development stage by skipping irrigation | AMF reduced the level of MDA and improved APX, CAT and SOD activities. Enhancement of P5CDH (?1Pyrroline-5-carboxylatedehydrogenase) | [76] |
| Sorghum | Skipping of irrigation was done to create moisture stress | AMF decrease the level of ROS and raise the level of CAT, POD (peroxidase) activity | [77] |
| White clover | At 55% field capacity | Mycorrhiza decreases the gathering of MDA and raise the level of CAT, SOD activities | [78] |
| Date palm | At 25% field capacity | AMF ameliorate the stability of membrane and high the content of CAT and SOD activities | [79] |
| Orange | At 55% field capacity | Reduction of MDA and improvement of CAT and SOD activities by AMF | [80] |
| Ryegrass | At 25% field capacity | AMF lower the assembling of MDA and improvement of CAT and SOD activities | [81] |
| French bean | Drought stress was inflict by retaining the irrigation for 5 days | Mycorrhiza boost the activities of CAT, SOD and GSH (Glutathione synthetase) | [82] |
| Tea | At 55% field capacity | AMF lower the level of MDA content | [83] |
AMF: Arbuscular mycorrhiza fungi, CAT: Catalase, SOD: Super oxidase dismutase.
The antioxidants such as CAT, SOD, and APX are generally produced. According to different species of plants the concentrations of enzymes are varies. Taking to the nature of CAT this enzyme is heme contains enzymes which are used to catalyze the H2O2 into oxygen and hydrogen in the ROS production. The CAT acts as a ROS scavenger and detoxifies the effect of ROS in plants. The research had done to check the activity of CAT on the crops such as wheat, beans tobacco, rice, and cotton. The rice in drought stress also produces the ROS and plant itself produced the CAT. The research had done by four varieties of rice Xiangnou no.1 and Zimano as drought-sensitive varieties and Xianghongxian no.2 and IR 50 as drought tolerant varieties. The result can change according to the types of cultivars. The concentration of CAT in rice sensitive variety was more as compared to rice tolerate variety [47].
The stress condition where AMF is colonized in plants, the production of antioxidant takes place. This enzymatic action acts as a defensive system which is mediated by AMF [48-51]. AMF plants steeply high the antioxidant content in plants by 16%. The study of sesame showed that the mycorrhiza species such as F. mosseae and R. irregularis increase the percentage of APX, polyphenol oxidase, CAT, PAL activities, and total soluble sugar content. The same study was observed by [7] who explain that the more activity of enzymes in chicory plants by the same species of mycorrhiza [8]. It was further observed that the more antioxidants in lettuce like carotenoids and anthocyanin cause more improvement in water-deficient conditions than well-watered conditions. The high content of antioxidant in mycorrhizal plants at the influence of moisture stress alleviate the toxicity effect on lipids, proteins and DNA and it causes high outcome in the functioning of plants under stress [9]. Despite of this fact, the mycorrhizal plants are more adaptive to tolerance than non-AMF plants. It also activates the secondary metabolites such as anthocyanins, flavonoids, and total phenol compounds in contrast to control plants which unveil to water deficit condition in the soil [52]. As per the report suggestion in Zea mays, the total phenol content was increased by Glomus versiforme in water-deficient condition which shows that the AMF mediating phenol acts as an active scavenger of ROS and this will protect the cellular structure of host plant [53]. Various study has shown that AMF plants increase the carotenoids level in Aloe barbadensis, Citrus aurantifola, and Ricinus communis in water less condition [54-56].When the changes in ROS occur by AMF, plants produce enzymatic and non-enzymatic antioxidant activities in drought stress condition.
This will protect the organism from the damage which is caused by oxidative stress. It was observed that inoculation of AMF with Funneli formismossea made high hydrogen peroxide effluxes in plant root, it was found in the root meristem zone in orange under water shortage conditions. In addition, extra radical hyphae of mycorrhiza take part in the efflux of H2O2, it is due to hyphae of mycorrhiza consist of aquaporins, which are used to pass the hydrogen and hydrogen peroxidase [57]. However, colonization by mycorrhiza enhanced the net Ca2+ influxes which are found in the elongation zone of the root in trifoliate orange under the water stress. These influxes of Ca2+ act as a downstream component in the H2O2 signaling pathway. The invasion of calcium is generally related to root efflux of hydrogen peroxidase, which suggests that plant having AMF influx of Ca2+ cause less H2O2 production. In another study of [58], colonization by AMF concentrated more levels of calmodulin (CaM). This level of CaM may participate in the regulation of superoxide dismutase activity along with CaM binding protein as well as the activity of CAT. It was also shown that the activity of Cu/Zn –SOD and Mn–SOD which was increased by mycorrhiza in drought stress. On the other hand, it showed the opposite result in well moisture conditions. This study was concluded that the stress of water raises the activity of AM which can activate the over-expression of SOD isozymes, and lead a less concentration of ROS in the host plant. If the plants faces drought stress and the same plants are associated with mycorrhiza, the levels of SOD are higher in treated plants. The generation of superoxide also begins as the plants face drought stress. The crops such as lettuce, alfalfa, bean, coffee, maize, tobacco, and rice have undergone the change when plants face drought stress. The levels of SOD can change according to the nature of the variety of crops. The concentration increases when plants are inoculated with mycorrhiza and it was decreased in plants without the mycorrhiza. The research found that 93% content of SOD was increased in plants that had mycorrhiza [59].
The transcriptomic analysis also has done where the level of SOD concentration had increased. The high level of antioxidants will expand the photosynthetic activity in plants. This will alter the plant biomass as plants are associated with mycorrhiza [60].
5.1. APX Content in Mycorrhizal Plants
The ascorbate concentrations in plants are increasing when the plants are in drought stress but in rice plants, the result was the opposite as the study suggested. As the ascorbate is used to remove the hydrogen peroxide and it acts as an electron donor in the removal of hydrogen [61].
5.2. ABA in AMF Plants under Drought Stress
In drought stress, mycorrhiza plants prompt the biosynthesis of ABA and as a result, the levels of ABA in plants are increases. This causes the stomata to close to reduce the loss of water by transpiration [62,63]. In contrast to this, a decrease the level of ABA production, or a change in the signaling pathway of ABA has been noticed in the roots of Glycyrrhiza uralensis [64] when the roots are not under water-deficient conditions. It is evident that a low level of ABA indicates tolerance against moisture stress in mycorrhizal plants. This tolerant level upgrade the performance and metabolite function of the plant. Another non-enzyme is glutathione which is very important in the removal of ROS [65]. The antioxidant glutathione content is also high in plants that face drought stress [66].
5.3. Effect of H2O2 in Drought Stress with Mycorrhiza
The plants which are associated with mycorrhiza are less prone to oxidative damage and they also produced less amount of H2O2 [67]. The major finding suggested the difference in the level of hydrogen peroxide in plants with mycorrhiza and plants without mycorrhiza in drought stress conditions. In the plants which were having AMF, the concentration of hydrogen peroxides had decreased while in other plants, it has been increased.
5.4. Role of Phenols in Plants under the Influence of Mycorrhiza in Drought Stress
Phenols also act as major antioxidants in plants and perform a major role in the defense mechanism in drought stress. When the plants are subjected to drought stress with the association of AMF, the gathering of the phenolic compound increases. As a result, the tolerance of drought is improved and leads to strengthening antioxidant fortification [68]. Polyphenol compounds are the scavengers that attack on free radicals. It also safeguards the cell from damage and makes the cell to function properly. It was reported that plants that have an inoculation of AMF have more assemblage of 50–60% of phenolic compound. This lodgment of phenol makes the plant more tolerant to the stress of water. The phenols and flavonoids in AMF plants adapt to help the plants to adapt in drought stress and turn on the cellular signaling of the plant [69,70]. The enzyme PAL is there in plant and plays a major role in the metabolism of the plant. It also protects the plant from biotic and abiotic stress [71]. By the inoculation of AMF in plants, there is an improvement of PAL enzyme. The upregulation of PAL boosts the growth of plant and makes better protection in drought stress [72,73].
Furthermore, AMF is also high level of total glomalin-related soil protein (T-GRSP), easily extractable GRSP (EE-GRSP), and difficultly extractable globin protein (DE-GRSP) in moisture stress. This protein which has different carbohydrates, protein, and other aliphatic compound worked as a connector to bind the particles of the soil. The increment of T-GRSP, EE-GRSP and DE-GRSP in drought stress increases the chances of uptake of water and tolerance of plant in drought stress [74].
6. CONCLUSION
The AMF is also called VAM and is associated with various functions, but the review stated that the antioxidants engage an essential part in diminishing moisture stress. The antioxidants such as CAT and superoxide dismutase activity are shown high content with the inoculation of AMF in stress conditions in any type of crop. On the other hand, ascorbate acid content showed more positive results with the symbiosis of AMF in the stress condition. In stress conditions, hydrogen peroxides content is less accumulated in the plants which state that AMF brings positive changes. Therefore, it is concluded that the inoculation of AMF in plants which are effective in the changes such as biochemical and physiological. The plant with AMF protects the plants and produces positive changes which help the plants to cope the water stress and this change is remarkable in the production of more yield under the drought stress condition. The evidence and studies suggested that AMF can bring changes not only physiologically but also biochemically too. The antioxidants bring desirable changes because the antioxidants have the ability to cope up the stress. Further researches are going on to bring constructive result.
7. ACKNOWLEDGMENT
The authors would like to acknowledge the School of Agriculture, Lovely Professional University for their consistent support to write this review paper.
8. AUTHOR CONTRIBUTIONS
All authors made substantial contributions to conception and design, acquisition of data, or analysis and interpretation of data; took part in drafting the article or revising it critically for important intellectual content; agreed to submit to the current journal; gave final approval of the version to be published; and agree to be accountable for all aspects of the work.
9. FUNDING
There is no funding to report.
10. CONFLICTS OF INTEREST
The authors declare that there are no conflicts of interest.
11. ETHICAL APPROVALS
This study does not involve experiments on animals or human subjects.
12. DATA AVAILABILITY
The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.
13. PUBLISHER’S NOTE
This journal remains neutral with regard to jurisdictional claims in published institutional affiliation.
REFERENCES
1. Seleiman MF, Al-Suhaibani N, Ali N, Akmal M, Alotaibi M, Refay Y, et al. Drought stress impacts on plants and different approaches to alleviate its adverse effects. Plants (Basel) 2021;10:259. [CrossRef]
2. Wu QS, Xia RX, Zou YN. Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 2006;163:1101-10. [CrossRef]
3. Balasubramanian V, Ladha JK, Gupta RK, Naresh RK, Mehla RS, Singh B, et al. Technology options for rice in the rice-wheat system in South Asia. In:Improving the Productivity and Sustainability of Rice-wheat Systems:Issues and Impacts. Vol. 6. Madison, Wisconsin:American Society of Agronomy;2006. 115.
4. Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, et al. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 2016;171:1009-23. [CrossRef]
5. Lokhandwala A, Hoeksema JD. Priming by arbuscular mycorrhizal fungi of plant antioxidant enzyme production:A meta-analysis. Annu Plant Rev 2019;2:1069-84. [CrossRef]
6. Gholinezhad E, Darvishzadeh R, Moghaddam SS, Popovic-Djordjevic J. Effect of mycorrhizal inoculation in reducing water stress in sesame (Sesamum indicum L.):The assessment of agrobiochemical traits and enzymatic antioxidant activity. Agric Water Manag 2020;238:106234. [CrossRef]
7. Langeroodi AR, Osipitan OA, Radicetti E, Mancinelli R. To what extent arbuscular mycorrhiza can protect chicory (Cichorium intybus L.) against drought stress. Sci Hortic 2020;263:109109. [CrossRef]
8. Baslam M, Esteban R, Garcia-Plazaola JI, Goicoechea N. Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophyll and tocopherol in green and red leaf lettuces. Appl Microbiol Biotechnol 2013;97:3119-28. [CrossRef]
9. Acuna-Rodriguez IS, Newsham KK, Gundel PE, Torres-D?az C, Molina-Montenegro MA. Functional roles of microbial symbionts in plant cold tolerance. Ecol Lett 2020;23:1034-48. [CrossRef]
10. Hardie K. The effect of removal of extraradical hyphae on water uptake by vesicular arbuscular mycorrhizal plants. New Phytol 1985;101:677-84. [CrossRef]
11. Ruiz-Lozano JM, Gómez M, Azcón R. Influence of different Glomus species on the time-course of physiological plant responses of lettuce to progressive drought stress periods. Plant Sci 1995;110:37-44. [CrossRef]
12. Porcel R, Ruiz-Lozano JM. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 2004;55:1743-50. [CrossRef]
13. Ruíz-Sánchez M, Armada E, Muñoz Y, de Salamone IE, Aroca R, Ruíz-Lozano JM, et al. Azospirillum and arbuscular mycorrhizal colonization enhance rice growth and physiological traits under well-watered and drought conditions. J Plant Physiol 2011;168:1031-7. [CrossRef]
14. Turner NC, Wright G, Siddique KH. Adaptation of grain legumes (pulses) to water-limited environments. Adv Agron 2001;71:193-231. [CrossRef]
15. Kavar T, Maras M, Kidri?M, Šuštar-Vozli?J, Megli?V. Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol Breed 2008;21:159-72. [CrossRef]
16. Subbarao GV, Johansen C, Slinkard AE, Rao RC, Saxena NP, Chauhan YS, et al. Strategies for improving drought resistance in grain legumes. Crit Rev Plant Sci 1995;14:469-523. [CrossRef]
17. Ludlow MM, Muchow RC. A critical evaluation of traits for improving crop yields in water-limited environments. Adv Agron 1990;43:107-53. [CrossRef]
18. Shahinnia F, Le Roy J, Laborde B, Sznajder B, Kalambettu P, Mahjourimajd S, et al. Genetic association of stomatal traits and yield in wheat grown in low rainfall environments. BMC Plant Biol 2016;16:150. [CrossRef]
19. Yokota A, Kawasaki S, Iwano M, Nakamura C, Miyake C, Akashi K. Citrulline and DRIP-1 protein (ArgE homologue) in drought tolerance of wild watermelon. Ann Bot 2002;89:825-32. [CrossRef]
20. Sandquist DR, Ehleringer JR. Population and family level variation of brittlebush (Encelia farinosa, Asteraceae) pubescence:Its relation to drought and implications for selection in variable environments. Am J Bot 2003;90:1481-6. [CrossRef]
21. Matysik J, Alia B, Halu B, Mohanty P. Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants.Curr Sci 2002;82:525-32.
22. Nair AS, Abraham TK, Jaya DS. Studies on the changes in lipid peroxidation and antioxidants in drought stress induced cowpea (Vigna unguiculata L.) varieties. J Environ Biol 2008;29:689-91.
23. Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 2002;7:405-10. [CrossRef]
24. Desikan R, Hancock JT, Neill SJ. Oxidative stress signaling. In:Hirt H, Shinozaki K, editors. Plant Responses to Abiotic Stress. Berlin, Heidelberg:Springer Verlag;2003. 121-48. [CrossRef]
25. Araus JL, Slafer GA, Reynolds MP, Royo C. Plant breeding and drought in C3 cereals:What should we breed for?Ann Bot 2002;89:925-40. [CrossRef]
26. Brady NC, Weil RR. The Nature and Properties of Soil. 12th ed. New York:Mac Pub Com;2009. 625-40.
27. Smith SE, Read DJ. Mycorrhizal Symbiosis. Cambridge:Academic Press;2008.
28. Bahadur A, Batool A, Nasir F, Jiang S, Mingsen Q, Zhang Q, et al. Mechanistic insights into arbuscular mycorrhizal fungi-mediated drought stress tolerance in plants. Int J Mol Sci 2019;20:4199. [CrossRef]
29. Rapparini F, Peñuelas J. Mycorrhizal fungi to alleviate drought stress on plant growth. In:Use of Microbes for the Alleviation of Soil Stresses. New York:Springer;2014. 21-42. [CrossRef]
30. Gong M, Tang M, Chen H, Zhang Q, Feng X. Effects of two Glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. New For 2012;44:399-408. [CrossRef]
31. Kala S, Godara AK. Effect of moisture stress on leaf total proteins, proline and free amino acid content in commercial cultivars of Ziziphus mauritiana. J Sci Res 2011;55:65-9.
32. AugéRM, Stodola AJ, Tims JE, Saxton AM. Moisture retention properties of a mycorrhizal soil. Plant Soil 2001;230:87-97. [CrossRef]
33. Beltrano J, Ronco MG. Improved tolerance of wheat plants (Triticum aestivum L.) to drought stress and rewatering by the arbuscular mycorrhizal fungus Glomus claroideum:Effect on growth and cell membrane stability. Braz J Plant Physiol 2008;20:29-37. [CrossRef]
34. Vallino M, Greppi D, Novero M, Bonfante P, Lupotto E. Rice root colonisation by mycorrhizal and endophytic fungi in aerobic soil. Ann Appl Biol 2009;154:195-204. [CrossRef]
35. Maheshwari R, Dubey RS. Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 2009;59:37-49. [CrossRef]
36. Pagano MC. Drought stress and mycorrhizal plant. In:Miransari M, editor. Use of Microbes for the Alleviation of Soil Stresses. New York, USA;Springer;2014. 97-110. [CrossRef]
37. Lee BR, Muneer S, Avice JC, Jung WJ, Kim TH. Mycorrhizal colonization and P-supplement effects on N uptake and N assimilation in perennial ryegrass under well-watered and drought-stressed conditions. Mycorrhiza 2012;22:525-34. [CrossRef]
38. Gholamhoseini M, Ghalavand A, Dolatabadian A, Jamshidi E, Khodaei-Joghan A. Effects of arbuscular mycorrhizal inoculation on growth, yield, nutrient uptake and irrigation water productivity of sunflowers grown under drought stress. Agric Water Manag 2013;117:106-14. [CrossRef]
39. Grondin A, Mauleon R, Vadez V, Henry A. Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.). Plant Cell Environ 2016;39:347-65. [CrossRef]
40. Hu Y, Xie W, Chen B. Arbuscular mycorrhiza improved drought tolerance of maize seedlings by altering photosystem II efficiency and the levels of key metabolites. Chem Biol Technol Agric 2020;7:20. [CrossRef]
41. Yooyongwech S, Samphumphuang T, Tisarum R, Theerawitaya C, Cha-um S. Arbuscular mycorrhizal fungi (AMF) improved water deficit tolerance in two different sweet potato genotypes involves osmotic adjustments via soluble sugar and free proline. Sci Hortic 2016;198:107-17. [CrossRef]
42. Reddy AR, Chaitanya KV, Vivekanandan M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 2004;16:1189-202. [CrossRef]
43. Shukla PS, Shotton K, Norman E, Neily W, Critchley AT, Prithviraj B. Seaweed extract improve drought tolerance of soybean by regulating stress-response genes. AoB Plants 2018;10:plx051. [CrossRef]
44. He F, Sheng M, Tang M. Effects of Rhizophagus irregularis on photosynthesis and antioxidative enzymatic system in Robinia pseudoacacia L. under drought stress. Front Plant Sci 2017;8:183. [CrossRef]
45. Kapoor R, Evelin H, Mathur P, Giri B. Arbuscular mycorrhiza:Approaches for abiotic stress tolerance in crop plants for sustainable agriculture. In:Tuteja N, Gill SS, editors. Plant Acclimation to Environmental Stress. New York:Springer Science +Business Media;2013. 359-401. [CrossRef]
46. Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH. Drought and oxidative load in the leaves of C3 plants:A predominant role for photorespiration. Ann Bot 2002;89:841-50. [CrossRef]
47. Guo Z, Ou W, Lu S, Zhong Q. Differential responses of antioxidative system to chilling and drought in four rice cultivars differing in sensitivity. Plant Physiol Biochem 2006;44:828-36. [CrossRef]
48. Millar NS, Bennett AE. Stressed out symbiotes:Hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 2016;182:625-41. [CrossRef]
49. Lenoir I, Fontaine J, Sahraoui AL. Arbuscular mycorrhizal fungal responses to abiotic stresses:A review. Phytochemistry 2016;123:4-15. [CrossRef]
50. Wu QS, Zou YN, Abd-Allah EF. Mycorrhizal association and ROS in plants. In:Ahmad P, editor. Oxidative Damage to Plants. Amsterdam:Elsevier Inc.;2014. 453-75. [CrossRef]
51. Wu QS, Zou YN. Arbuscular mycorrhizal fungi and tolerance of drought stress in plants. In:Arbuscular Mycorrhizas and Stress Tolerance of Plants. Singapore:Springer;2017. 25-42. [CrossRef]
52. Pirasteh-Anosheh H, Saed-Moucheshi A, Pakniyat H, Pessarakli M. Stomatal responses to drought stress. In:Water Stress and Crop Plants:A Sustainable Approach. Vol. 1. UK, Oxford:Wiley Blackwell;2016. [CrossRef]
53. Begum N, Ahanger MA, Su YY, Lei YF, Mustafa NS, Ahmad P, et al. Improved drought tolerance by AMF inoculation in maize (Zea mays) involves physiological and biochemical implications. Plants (Basel) 2019;8:579. [CrossRef]
54. Zhang T, Hu Y, Zhang K, Tian C, Guo J. Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind Crops Prod 2018b;117:13-9. [CrossRef]
55. Bagheri V, Shamshiri MH, Alaei H, Salehi H. The role of inoculum identity for growth, photosynthesis, and chlorophyll fluorescence of zinnia plants by arbuscular mycorrhizal fungi under varying water regimes. Photosynthetica 2019;57:409-19. [CrossRef]
56. Khajeeyan R, Salehi A, Dehnavi MM, Farajee H, Kohanmoo MA. Physiological and yield responses of Aloe vera plant to biofertilizers under different irrigation regimes. Agric Water Manag 2019;225:105768. [CrossRef]
57. Zou YN, Huang YM, Wu QS, He XH. Mycorrhiza-induced lower oxidative burst is related with higher antioxidant enzyme activities, net H2O2 effluxes, and Ca2+ influxes in trifoliate orange roots under drought stress. Mycorrhiza 2015a;25:143-52. [CrossRef]
58. Huang YM, Srivastava AK, Zou YN, Ni QD, Han Y, Wu QS. Mycorrhizal-induced calmodulin mediated changes in antioxidant enzymes and growth response of drought-stressed trifoliate orange. Front Microbiol 2014;5:682. [CrossRef]
59. Alguacil MM, Hernandez JA, Caravaca F, Portillo B, Roldan A. Antioxidant enzyme activities in shoots from three mycorrhizal shrub species afforested in a degraded semi?arid soil. Physiol Plant 2003;118:562-70. [CrossRef]
60. Rodell M, Velicogna I, Famiglietti JS. Satellite-based estimates of groundwater depletion in India. Nature 2009;460:999-1002. [CrossRef]
61. Azcón R, Barea JM. Mycorrhizo sphere interactions for legume improvement. In:Microbes for Legume Improvement. Vienna:Springer;2010. 237-71. [CrossRef]
62. Nejad KZ, Ghasemi M, Shamili M, Damizadeh GR. Effect of mycorrhiza and vermicompost on drought tolerance of lime seedlings (Citrus aurantifolia cv. Mexican lime). Int J Fruit Sci 2019;20:646-57. [CrossRef]
63. Pozo MJ, Lopez-Raez JA, Azcon-Aguilar C, Garcia-Garrido JM. Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 2015;205:1431-6. [CrossRef]
64. Xie W, Hao Z, Zhou X, Jiang X, Xu L, Wu S, et al. Arbuscular mycorrhiza facilitates the accumulation of glycyrrhizin and liquiritin in Glycyrrhiza uralensis under drought stress. Mycorrhiza 2018;28:285-300. [CrossRef]
65. Meyer AJ. The integration of glutathione homeostasis and redox signaling. J Plant Physiol 2008;165:1390-403. [CrossRef]
66. Kranner I. Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytol 2002;154:451-60. [CrossRef]
67. Bienert GP, Møller AL, Kristiansen KA, Schulz A Møller IM, Schjoerring JK, et al. Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes. J Biol Chem 2007;282:1183-92. [CrossRef]
68. Begum N, Akhtar K, Ahanger MA, Iqbal M, Wang P, Mustafa NS, et al. Arbuscular mycorrhizal fungi improve growth, essential oil, secondary metabolism, and yield of tobacco (Nicotiana tabacum L.) under drought stress conditions. Environ Sci Pollut Res Int 2021;28:“45276-95. [CrossRef]
69. Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, et al. Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 2007;12:1290-306. [CrossRef]
70. Mandal SM, Chakraborty D, Dey S. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 2010;5:359-68. [CrossRef]
71. Quiroga G, Erice G, Aroca R, Chaumont F, Ruiz-Lozano JM. Enhanced drought stress tolerance by the arbuscular mycorrhizal symbiosis in a drought-sensitive maize cultivar is related to a broader and differential regulation of host plant aquaporins than in a drought-tolerant cultivar. Front Plant Sci 2017;8:1056. [CrossRef]
72. Hao C, Xia Z, Fan R, Tan L, Hu L, Wu B, et al. De novo transcriptome sequencing of black pepper (Piper nigrum L.) and an analysis of genes involved in phenylpropanoid metabolism in response to Phytophthora capsici. BMC Genomics 2016;17:822. [CrossRef]
73. De Trindade R, Almeida L, Xavier L, Lins AL, Andrade EH, Maia JG, et al. Arbuscular mycorrhizal fungi colonization promotes changes in the volatile compounds and enzymatic activity of lipoxygenase and phenylalanine ammonia lyase in Piper nigrum L.'Bragantina'. Plants (Basel) 2019;8:442. [CrossRef]
74. Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS. Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 2001;233:167-77. [CrossRef]
75. Tereucán G, Ruiz A, Nahuelcura J, Oyarzún P, Santander C, Winterhalter P, et al. Shifts in biochemical and physiological responses by the inoculation of arbuscular mycorrhizal fungi in Triticum aestivum growing under drought conditions. J Sci Food Agric 2022;102:1927-38. [CrossRef]
76. Sheteiwy MS, Ali DF, Xiong YC, Brestic M, Skalicky M, Hamoud YA, et al. Physiological and biochemical responses of soybean plants inoculated with Arbuscular mycorrhizal fungi and Bradyrhizobium under drought stress. BMC Plant Biol 2021;21:195. [CrossRef]
77. Kamali S, Mehraban A. Effects of Nitroxin and arbuscular mycorrhizal fungi on the agro-physiological traits and grain yield of sorghum (Sorghum bicolor L.) under drought stress conditions. PLoS One 2020a;15:e0243824. [CrossRef]
78. Liang SM, Jiang DJ, Xie MM, Zou YN, Wu QS, Ku?a K. Physiological responses of mycorrhizal symbiosis to drought stress in white clover. Not Bot Horti Agrobot Cluj Napoca 2021;49:12209. [CrossRef]
79. Harkousse O, Slimani A, Jadrane I, Aitboulahsen M, Mazri MA, Zouahri A, et al. Role of local biofertilizer in enhancing the oxidative stress defence systems of date palm seedling (Phoenix dactylifera) against abiotic stress. Appl Environ Soil Sci 2021;2021:6628544. [CrossRef]
80. He Y, Fang J, Xu W, Shi P. Substantial increase of compound droughts and heatwaves in wheat growing seasons worldwide. Int J Climatol 2022;42:5038-54. [CrossRef]
81. Yang Q, Zhao Z, Bai Z, Hou H, Yuan Y, Guo A, et al. Effects of mycorrhizae and water conditions on perennial ryegrass growth in rare earth tailings. RSC Adv 2019;9:10881-8. [CrossRef]
82. Prabha C, Sharadamma N, Nagesh BR. Arbuscular mycorrhizal influence on oxidative stress in French bean (Phaseolus vulgaris) under drought conditions. GSC Biol Pharm Sci 2019;7:21-9. [CrossRef]
83. Liu CY, Wang YJ, Wu QS, Yang TY, Ku?a K. Arbuscular mycorrhizal fungi improve the antioxidant capacity of tea (Camellia sinensis) seedlings under drought stress. Not Bot Horti Agrobot Cluj Napoca 2020;48:1993-2005. [CrossRef]