Skip to main content
Beni-Suef University Journal of Basic and Applied Sciences
Download PDF

Mycorrhizal impact on Ocimum basilicum grown under drought stress

Beni-Suef University Journal of Basic and Applied Sciences volume 10, Article number: 72 (2021) Cite this article

Abstract

Background

Ocimum basilicum was grown under three levels of drought stress (100% Field capacity, 70% Field capacity, and 40% Field capacity). Half of the plants were inoculated with Arbuscular mycorrhiza and the other half was not inoculated. Arbuscular mycorrhizal fungi (AMF) were applied to improve plant growth and to alleviate drought stress on sweet basil.

Results

Drought Couse inhibition in the colonization of Arbuscular mycorrhiza, reduction in plant growth, decrease stomatal size increase stomatal density, a decline in soluble carbohydrates, accumulation of amino acids, proline, and glycine betaine, and reduction in some minerals such as P, K, and Na.

Conclusions

The effect of drought was alleviated by the application of inoculation with Arbuscular mycorrhiza.

Background

The world faces many global challenges like scarcity of water resources that enforced scientists to solve [1]. Many efforts must be done to cope with this environmental stress in both economic and environmentally sustainable ways [2]. Drought is defined as the deficiency of available soil moisture which may be sufficient to cause a reduction in growth, [3]. Plants require water for photosynthesis, nutrient uptake, and translocation transportation as well as cooling [4]. Drought stress is a major and serious threat to agriculture and crop production in arid and semiarid regions. Approximately, 70% of the global available water is used in agriculture to produce about 40% of the world's food [5]. Drought causes retardation in plant growth leading finally to a reduction in their yields. It disturbs plant metabolism causing inhibitions in total carbohydrates, total nitrogen contents, and total lipids [6, 7]. Several studied concerned with the negative effect of drought on plants, for example, it was observed a dramatic reduction in the grain yield of Zea mays plants grown under drought stress [8, 9].

Many trials were done to overcome the drought problem; it was reported that the application of organic fertilizers and biofertilizers reduced the drought stress effect and improve plant growth [10]. In this context, arbuscular mycorrhizal fungi (AMF) are used as biofertilizers to improve plant growth, production, and plant water status [11]. AMF are associated with the roots of over 80% of terrestrial plant species [12]. Broad bean plants grown under salinity stress show better growth when inoculated with mycorrhiza than non-inoculated plants, under stress or non-stress condition [13]. Inoculation with AMF succeeded in the alleviation of the negative effects of drought stress on tomato plants, and this alleviation was more pronounced in the moderated stress than severe stress [14]. AMF stimulated the growth and photosynthesis of sweet basil plants confirming the role of mycorrhizal symbiosis in plant defense against biotic and abiotic stress. They also noted that symbiosis leads to an improvement in the growth and yield regardless of the water status of the plant (stressed or none) [15]. The main advantage of mycorrhiza for host plants may be the extension of the penetration zone of the root fungus system which increases active uptake and transport of nutrients especially immobile minerals like P, Zn, and Cu [16].

Sweet basil (Ocimum basilicum L.) is a member of the family Lamiaceae, which is recorded as one of the most widespread species in the world. It is widely used in food and oral care products and its essential oil is also used as perfumery [17, 18]. The leaves and flowering of sweet basil have been used in traditional medicine for many ailments like headaches, coughs, and diarrhea and it is generally recognized as a safe rich source of phenolic antioxidant and flavonoid compounds [19]. It also possesses other various medicinal applications like antiseptic, carminative, antimicrobial, and antioxidative agents [20, 21].

This work aimed to study the interaction effect of AMF inoculation and drought stress, on the growth, yield, and biochemical parameters of sweet basil. Moreover, the possibility to use AMF to alleviate drought stress on sweet basil.

Methods

Seeds and Mycorrhiza propagules

Sweet basil (Ocimum basilicum) seeds were provided from Agricultural Research Center (ARC), Seds Station, Beni-Suef Governorate, Egypt, but the propaguled arbuscular mycorrhiza (Glomus versiform) was provided from Soil, Water and Environment Research Institute (SWERI), Agricultural Research Center (ARC), Giza, Egypt.

Soil

The used soil was a garden soil that was collected from the surface layer (0-30 cm depth) from arable fields at Somasta Center, Beni-Suef Governorate, Egypt. The soil pH was 7.83 with EC (dSm−1) 4.21, and its texture was silty clay (1:2.5). It contains 201, 12.88, and 0.37 mg/g soil as N, P, and CO3, respectively. The soil was air-dried and then was sieved through a 2-mm sieve. Sieved soil was autoclaved for sterilization and 3 kilograms of this prepared soil was dispensed into black plastic pots (40-cm diameter × 50-cm Height) to be ready for cultivation.

Two experiments were done; first for calculating soil (FC) percentage to identify the water holding state of the used soil, while the second experiment was to estimate FC levels which will be applied to the main experiment.

Determination of field capacity (FC%)

Field capacity (FC%) was measured according to the method described by [22] with the formula:

$${\text{FC}}\,\left( \% \right) = \left[ {(a - b)/b} \right] \times 100,$$

where (a) is the weight of the wet soil, while (b) is the weight of the oven-dried soil. The obtained results showed that FC was equal to 31.25%.

Determination of maximum drought stress

To determine the maximum drought stress under which basil can be grown, seeds were germinated in serial FCs. In this experiment, 9-groups were irrigated with serial FCs (from 100% down to 20%), each group was of 5-replicates. After 5-weeks, the percentage of germination was calculated. It was observed that basil persisted growth down to FC 40%. According to these results, three FCs levels were selected; 100% (served as a control), 70% (as moderate water stress), and 40% (as severe water stress).

The main experiment

It was an open-field randomized pot experiment carried out in April 2019 within temperature range (26.76±4.32 °C, and 15.50±1.94 °C, maximum and minimum respectively), in the garden of the Department of Botany and Microbiology, Faculty of Science, Beni-Suef University. The experiment was divided into two main groups. The first group was inoculated by 10 gm of mycorrhiza (0.003% W/W) [23], while the second group was not inoculated. Each group was subdivided into 3 subgroups; the 1st subgroup was irrigated up to 100% FC, the 2nd subgroup was irrigated at 70% FC and the last subgroup was irrigated at 40% FC. Each subgroup consisted of 20 pots and each pot with 30 seeds. Five harvested were carried out at the seedling stage, vegetative stage, flowering stage, fruiting stage, and yield finally. Growth criteria of each harvest were recorded then plants were subjected to several different physiological and biochemical investigations.

Estimation of colonization percentage of arbuscular mycorrhizal fungi

After 30-days of inoculation, colonization percentage was estimated by staining the digested squashed root slices with 0.05% trypan blue stain [24].

Determination of stomatal criteria

Stomatal criteria included stomatal density (number per mm2), stomatal size (guard cell length and stomatal pore width), and stomatal spacing, by using optical micrometers (linear and square). For measuring these criteria, two well-expanded leaves of each plant were selected, and both of their lower surface (abaxial side) and the upper surface (adaxial side) were sticked by nail varnish technique [25].

Physiological and biochemical investigations

Soluble carbohydrate was determined by arsenomolybdate reagent [26]. Glycine-betaine (GB) estimation was done by cold KI/I2 reagent as the method described by [27]. Proline was determined 3% sulphosalicylic acid due to [28]. Extraction and determination of amino acids were carried out ninhydrin reagent [29]. Total soluble nitrogen in plant samples was measured by using Kjeldahl digestion method [30]. Determination of photosynthetic pigments (chlorophyll a, b, and carotenoids) was measure spectrophotometrically by [31]. Phosphorus (P) was estimated by using ammonium molybdate-sulphuric acid reagent [32]. The potassium and sodium content was extracted with 2% trichloroacetic acid (TCA) then elements were measured by flame photometry by using Venema automation b.v., Groningen, Holland "Venema", automatic laboratory system at sugar factory of Beni-Suef, Egypt.  All obtained results were subjected to different statistical analyses by using the SPSS program.

Statistical analyses

Kolmogorov-Smirnov and Levene’s tests were used to check the normality and homogeneity, respectively, of the data obtained from pot experiment. All data exhibited normality and homogeneity. They analyzed by using the independent sample T test, then one-way analysis of variance (ANOVA) was applied and the significant differences among values were analyzed with Duncan’s new multiple range tests at p ≤ 0.05 level of significance. To illustrate the effect of inoculation with mycorrhiza, drought and the interaction among the mentioned factors, two-way ANOVA analysis was conducted. Data were analyzed by using SPSS V20.

Results

The effect of drought on colonization percentage was negatively affecting as shown in Table 1. The reduction of colonization was at its maximum inhibition (72%) at 40% field capacity. This significant inhibition was obvious in all investigated parameters later.

Table 1 One-way ANOVA of the effects of drought on colonization % of Ocimum basilicum
Full size table

The response of the investigated growth criteria is tabulated in Tables 2 and 3. In all growth stages, all investigated parameters were significantly affected with treatment with mycorrhiza and drought, while the interaction between them was significantly varied. Particularly, drought stress inhibited root (length, fresh and dry weights), and shoot (length, fresh weight, and dry weight). For all parameters, the treatment with mycorrhiza alleviated the stress impact. The integration of all data showed that root length in all growth stages under the different FCs has significantly differed in both inoculated and non-inoculated plants. This pattern is similar in root fresh weight and root dry weight except in inoculated plants under 40% FC which gave a non-significant difference.

Table 2 One-way ANOVA of growth criteria of Ocimum basilicum under drought and mycorrhiza
Full size table
Table 3 Two- way ANOVA of Growth criteria of Ocimum basilicum under Drought and mycorrhiza; Error, 36
Full size table

The response of the stomatal structure to the applied stress and mycorrhizal application was tabulated in Tables 4 and 5. In non-inoculated plants, under 100 FC and 40% FC, the length of guard cell (adaxial and abaxial) increased from growth stage to other, but under 70% FC there was no significant response. Stomatal guard cell length and stomatal pore width were decreased under drought stress especially in 40% of non-inoculated plants. Stomatal spacing decrease under drought stress, while stomatal density increases under stress especially in 40% of non-inoculated plants Inoculation under all FCs gave no significance.

Table 4 One-way ANOVA of Stomatal Criteria of Ocimum basilicum under Drought and mycorrhiza
Full size table
Table 5 Two-way ANOVA of stomatal criteria of Ocimum basilicum under Drought and mycorrhiza, Error 12
Full size table

Tables 6 and 7 showing the effect of drought and mycorrhiza on some soluble metabolites (soluble carbohydrate, total amino acids, glycine betaine, proline, and total nitrogenous fractions). The concentration of soluble carbohydrates inhibited due to drought stress especially under the higher level of drought (40% non-inoculated). The maximum retardation due to drought was 71.45% at the seedling stage. AM fungus application improves significantly soluble carbohydrates content in both control samples and plants subjected to a combination between drought and AM treatment.

Table 6 One-way ANOVA of some soluble metabolites of Ocimum basilicum under Drought and mycorrhiza
Full size table
Table 7 Two- way ANOVA of soluble metabolites of Ocimum basilicum under Drought and mycorrhiza; Error, 12
Full size table

Plants subjected to drought stress showed accumulations of total amino acids especially proline, glycine betaine. The vegetative stage showed maximum accumulation as it recorded 69.5%, 65.8%, and 11.8%, respectively. AM fungus application improved the concentration of proline, glycine betaine, and total free amino acids in control plant samples. Interaction between drought and AM decreased the accumulation of all three parameters, in relation to, the stressed non-treated samples.

Under normal growth conditions, total soluble nitrogen fractions recorded the most increment during the vegetative growth stage, while the lowest concentration was recorded in the fruiting stage. Drought caused an accumulation of total nitrogen soluble fractions and the degree of accumulation was concentration-dependent. The application of AM enhanced total soluble nitrogen metabolism which was reflected as an increment of their contents. AM also alleviated the drought inhibitory effect.

As shown in Tables 8 and 9, photosynthetic pigments (chlorophyll a, chlorophyll b, and Carotenoids) concentration recorded their maximum concentration in the vegetative growth stage, and application of AM upgraded these concentrations. On the other hand, drought stress induced a large decline in these photosynthetic pigments, at all FC levels. The highest decline percentage was recorded in vegetative growth stages and was positively dependent on the level of the applied stress. AM fungus application enhanced all estimated pigments under the different drought levels at all growth stages.

Table 8 One-way ANOVA of pigment fractions of Ocimum basilicum under Drought and mycorrhiza
Full size table
Table 9 Two-way ANOVA of pigment fractions of Ocimum basilicum under Drought and mycorrhiza; Error, 12
Full size table

Data of minerals fraction recorded in Tables 10 and 11 cleared that, K, Na, and P uptake and their concentration were elevated due to water deficit. AM application significantly helped plants to accumulate more minerals, which was more obvious in non-stressed plants, as well as, helped the stressed plant to overcome the bad drought stress. The pattern of accumulation of all minerals was to some extent parallel to each other.

Table 10 One-way ANOVA of elements of Ocimum basilicum under Drought and mycorrhiza
Full size table
Table 11 Two-way ANOVA of Elements of Ocimum basilicum under Drought and mycorrhiza; Error, 12
Full size table

Discussion

Drought reduces the growth of mycorrhiza and retards its colonization percentage. In this study, the obtained retardation was concomitant with many similar results obtained from Mays which suffered retardation of the colonization percentage [33] and similar retardation was observed in Leymus chinensis and Hemarthria altissima grasses [34]. The retardation in the percentage of colonization due to drought stress may be attributed to the consumption of a part of the energy to adjust the osmotic potential rather than being used for fungal growth [35]. The reduction of colonization may be also considered as a result due to an inhibition that occurred in hydrolyzing enzymes responsible for fungal growth and/or synthesizing enzymes especially those of protein synthases to keep amino acids free to raise cell osmotic potential [14, 15]. The inhibition of AM colonization may be a result of the inhibition that occurred in the growth of the host plant via strigolactones which are plant growth stimulating and enhancing proliferation of cell AM, as a shortage of strigolactones causes less proliferation and colonization retardation [36].

The negative response of basil growth to drought was recognized in several studies [16, 37, 38]. The reduction that occurred in plant growth due to drought stress may be attributed to the inhibition that occurred in the cell division [39]. Drought also may inhibit the growth due to the inhibition that occurred in anabolic activity due to consumption of more energy to maintain cell water potential [14, 40]. The inhibition that occurred in photosynthesis may have participated in the general growth inhibition that occurred [41].

The enhancement impact obtained by AM on plant growth can be interpreted due to a direct improvement of water absorption from the soil into the roots, by the expanding surface of mycorrhizal roots which means more water uptake efficiency than more plant growth [42]. The improvement in water content due to AM inoculation can be also discussed as a result of fungal hyphae exploitation of water which finally caused more water content that enhanced more plant growth [16]. The improving effect of AM fungi on the estimated growth criteria may be also explained as a result of an anabolic acceleration of photosynthetic activity [14]. Such improvement can be also understood through the improvement of nutrient status which means more enzymatic activation as well as more raising of plant osmotic potential [38].

Stomata regulate and control water vapor fluxes through stomatal conductance and stomatal resistance via transpiration. The movement of the stomata is controlled by the guard cell which is harmonized by its turgor pressure. Turgor pressure of guard cell is affected by many regulatory factors including plant water status [43] which depends on and correlates with the degree of soil hydration [44]. The change of guard cell length is a mechanical mechanism of stomatal working to control its conductance, its resistance, and its pore width to overcome water shortage as a morphological adaptation [45]. Underwater shortage, stomata decrease their conductance and pore width [46] to hold more water content [47]. Stomatal density is another adaptive anatomical mechanism to acclimatize and resist drought to reduce the transpiration rate by increasing stomatal dimension [48] through specific gene system transcription [49]. In a recent study [50] it was shown that reduced soil water content significantly stimulated stomatal generation in maize, resulting in a significant increase in stomatal density but a decrease in stomatal size and aperture. In this research, it was also reported that stomatal density was significantly negatively correlated with both net photosynthetic rate and transpiration rate, but more strongly with the latter, so leaf instantaneous water use efficiency was correlated positively with stomatal density in Platanus acerifolia [51] and in Ziziphus jujuba which showed a negative correlation between stomatal density and stomatal length under different irrigation regimes [52].

The observed positive effect of mycorrhiza on stomata was estimated in maize [32], in walnut [23], and Leymus chinensis and Hemarthria altissima grasses [33]. This improvement may be attributed to an enhancement occurred in leaf water potential by the accumulation of osmoprotectant and solutes such as proline and total soluble sugars [53]. Also, AM accumulated phenolics which may improve leaf water potential [16]. The development of stomatal morphology may be accredited to increasing water and mineral uptake by fungal hyphae [54, 55]. The progress of stomatal structure and function may be ascribed finally to the excreted plant hormones by fungal cell especially abscisic acid (ABA) which regulate stomatal working [23].

Plants accumulate osmotically active soluble molecules as a major mechanism for increasing plant cell osmotic activity. In this study, Ocimum accumulated free amino acids (especially proline and glycine betaine) and total nitrogen soluble fractions. Amino acids and nitrogenous fractions may play a signaling role in plant tolerance besides their roles of osmotic adjustment, protection of cellular macromolecules, storage of nitrogen, maintenance of cellular pH, detoxification of the cells, and scavenging of free radicals [56]. Such accumulation may be due to activation that occurred in their biosynthesis and/or inhibition that occurred in their polymerization [57]. Accumulation of proline means an enhancement occurred in its anabolism and/or retardation occurred in oxidation, particularly, through those controlling enzymes; glutamate synthase, glutamate dehydrogenase, and glutamate decarboxylase [58]. Proline rises cellular osmolarity, regulates redox buffering and energy transfer to regulate redox potentials and a hydroxyl radical scavenger to alleviate oxidative stress, and programs cell death [33]. In parallel, glycine betaine acts as an osmoregulator, osmo-protector, and stomatal work controller [57, 59].

On the other hand, drought inhibited soluble carbohydrate fractions, and this may be attributed to stomatal closure, the reduction of chlorophyll concentration, and/or photosynthesis inhibition [60], and this obtained reduction may point to the trouble that occurred in their biosynthesis which is a gen dependent response [61].

The alleviating impact of mycorrhiza may be attributed to the more water absorbed by fungal hyphae [62]. The improvement of these soluble fractions due to mycorrhizal symbiosis may be ascribed to the activation occurred in their anabolic activity due to more mycorrhizal absorbed minerals acting as specific enzyme activator [63]. Mycorrhiza also secretes some hormones like ABA which regulate stomatal working which means more photosynthetic products acting as a precursor of these osmolytes [64]. Mycorrhiza also supplies plant roots with necessary N, K, P, and especially Mg elements and more anabolized molecules used in the biosynthesis of such osmoregulatory and osmo-protecting molecules [65].

Retardation in photosynthetic pigments due to drought stress is a commonly observed phenomenon. In the current study, this retardation is coincident with decrement occurred insoluble carbohydrate. The inhibition of photosynthetic pigment may be attributed to the general anabolic inhibition due to drought stress [14]. The inhibition of Mg concentration may be a direct factor of chlorophyll inhibition [66].

On the other hand, the assuaging impact of mycorrhiza may be accredited on the improvement of plant water status helped stomata for more opening and efficiency [67]. More absorbed Mg, by mycorrhizal hyphae, may participate in more chlorophyll biosynthesis [65]. Water use efficiency may explain such improvement as it influences the balance between carbon gain in photosynthesis and water loss via transpiration [68].

Accumulation of minerals is a known response mechanism against drought stress to raise cell osmotic potential which consumes more energy leading to deprivation of cells from more anabolic reactions [13]. Besides the participation of osmotic potential raising, some of these minerals are engaged to activate some osmoregulating and osmoprotectant molecules [64]. The improvement of mineral uptake due to AM treatment may be attributed to the absorbing capacity of fungal hyphae especially the P element [12].

Conversely, Mycorrhiza improved mineral uptake and this improvement can be denoted to hyphae uptake itself [69] and/or more root uptake by the saved energy instead of its consumption for raising cell osmotic potential [62].

Conclusions

Generally, the application of arbuscular mycorrhiza improved the growth of basil (Ocimum basilicum) grown either under normal conditions or under drought stress, and this result can advise by using this application to improve the growth and quality of this plant under normal or drought stress conditions.

Availability of data and materials

Not applicable.

Abbreviations

AM:

Arbuscular mycorrhiza

AMF:

Arbuscular mycorrhizal fungi

EC:

Electrical conductivity

FC:

Field capacity

GB:

Glycine-betaine

References

  1. Kim TW, Jehanzaib M (2020) Drought risk analysis, forecasting and assessment under climate change. Water 12(7):1862. https://doi.org/10.3390/w12071862

    Article  Google Scholar 

  2. Human Development Report 2006. http://hdr.undp.org/en/content/human-development-report-2006. Accessed 19 Jan 2021

  3. Rauf S (2008) Breeding sunflower (Helianthus annuus L.) for drought tolerance. Commun Biometry Crop Sci 3(1):29–44

  4. Farooq M, Wahid A, Kobayashi N, Fujita DB, Basra SM (2009) Plant drought stress: effects, mechanisms and management. J Sustain Agric 153–88.

  5. Somerville C, Briscoe J (2001) Genetic engineering and water. Science 292(5525):2217

    CAS  Article  Google Scholar 

  6. Hamed BA, Khodary SE (2002) Changes in grain metabolic contents and growth parameters of some wheat varieties in response to drought stress. Bull Fac Sci Assiut Univ 31(1-D):219–225

  7. Hamed BA (2009) Effect of Incorporation of date palm seeds with soil on the growth of parsley plant growing under drought stress. Lipids 3:4

    Google Scholar 

  8. Konuşkan Ö, Gözübenli H, Atış İ, Atak M (2017) Effects of salinity stress on emergence and seedling growth parameters of some maize genotypes (Zea mays L.). TURJAF 5(12):1668–1672

  9. Bose S, Fakir OA, Alam MK, Hossain AZ, Hossain A, Mymensingh B, Rashid MH (2018) Effects of salinity on seedling growth of four maize (Zea Mays L.) cultivars under hydroponics. J Agric Sci 6(1):56–69

  10. Khadem SA, Galavi M, Ramrodi M, Mousavi SR, Rousta MJ, Rezvani-Moghadam P (2010) Effect of animal manure and superabsorbent polymer on corn leaf relative water content, cell membrane stability and leaf chlorophyll content under dry condition. Aust J Crop Sci 4(8):642

    Google Scholar 

  11. Kheirizadeh Arough Y, Seyed Sharifi R, Seyed Sharifi R (2016) Bio fertilizers and zinc effects on some physiological parameters of triticale under water-limitation condition. J Plant Interact 11(1):167–177

    Article  Google Scholar 

  12. Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 62:227–250

    CAS  Article  Google Scholar 

  13. Hamed BA, Mousa, ASM (2008) Effect of arbuscular mycorrhiza inoculation on the yield quality of salinity stressed broad bean (Vicia faba L.) treated with rhizobia or potassium nitrate. J Biol Pharm Sci 6(1):11–21

  14. Hamed BA, Mousa ASM (2008) Interaction effect between arbuscular mycorrhiza and tripotassium phosphate fertilizer on tomato (Lycopersicum esculentum L.) growing under drought condition. J Biol Pharm Sci 6(1):22–32

  15. Hazzoumi Z, Moustakime Y, Joutei KA (2015) Effect of arbuscular mycorrhizal fungi (AMF) and water stress on growth, phenolic compounds, glandular hairs, and yield of essential oil in basil (Ocimum gratissimum L.). Chem Biol Technol Agric 2(10):1–11

  16. Zolfaghari M, Nazeri V, Sefidkon F, Rejali F (2013) Effect of arbuscular mycorrhizal fungi on plant growth and essential oil content and composition of Ocimum basilicum L. Iran J Plant Physiol 3(2):643–650

    Google Scholar 

  17. Bauer K, Garbe D, Surburg H (1997) Common fragrance and flavor materials, 3rd edn. Wiley-VCH, Weinheim, p 171

    Book  Google Scholar 

  18. Marwat SK, Khan MS, Ghulam S, Anwar N, Mustafa G, Usman K (2011) Phytochemical constituents and pharmacological activities of sweet Basil-Ocimum basilicum L. (Lamiaceae). Asian J Chem 23(9):3773

  19. Kathirvel P, Ravi S (2012) Chemical composition of the essential oil from basil (Ocimum basilicum Linn.) and its in vitro cytotoxicity against HeLa and HEp-2 human cancer cell lines and NIH 3T3 mouse embryonic fibroblasts. Nat Prod Res 26(12):1112–1118

  20. Mansoorkhani AR, Shahriari Z, Mohaselli V, Osfoori M, Shahriari AG (2012) Effect of graded levels of NPK on herb, oil yield and oil composition of basil (Ocimum basilicum L.). Glob J Res Med Plants Indig Med 1(7):258.

  21. Lee SJ, Umano K, Shibamoto T, Lee KG (2005) Identification of volatile components in basil (Ocimum basilicum L.) and thyme leaves (Thymus vulgaris L.) and their antioxidant properties. Food Chem 91(1):131–137

  22. Kapur P, Govil SR (2000) Experimental plant ecology. CBS, Publisher and Distributors, Darya ganj, New Delhi, India

  23. Behrooz A, Vahdati K, Rejali F, Lotfi M, Sarikhani S, Leslie C (2019) Arbuscular mycorrhiza and plant growth-promoting bacteria alleviate drought stress in walnut. HortScience 54(6):1087–1092

    CAS  Article  Google Scholar 

  24. Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d'un système radiculaire. Recherche de méthode d'estimation ayant une signification fonctionnelle. In: Physiological and genetical aspects of mycorrhizae: proceedings of the 1st european symposium on mycorrhizae, Dijon, INRA, Paris, 1–5 July 1985:217–221

  25. Van Duren M, Morpurgo R, Dolezel J, Afza R (1996) Induction and verification of autotetraploids in diploid banana (Musa acuminata) by in vitro techniques. Euphytica 88(1):25–34

    Article  Google Scholar 

  26. Said A, Naguib MI, Ramzy MA (1964) Sucrose determination as a means of estimation of the draw back tax on exported Halawa Tehinia. Bull Fac Sci Cairo Univ 39:207–216

    Google Scholar 

  27. Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant Soil 70(2):303–307

    CAS  Article  Google Scholar 

  28. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    CAS  Article  Google Scholar 

  29. Lee YP, Takahashi T (1966) An improved colorimetric determination of amino acids with the use of ninhydrin. Anal Biochem 14(1):71–77

    CAS  Article  Google Scholar 

  30. Jackson ML (1958) Soil chemical analysis, vol 498. Prentice Hall, Englewood Cliffs, pp 183–204

  31. Metzner H, Rau M, Senger H (1956) Untersuchungen zur synchronisierbark eit einzeiner pigmenten angel Mutanten von Chlorella. (studies on synchronization of some pigment-deficient Chlorella mutants). Planta 65:186

  32. Clark M, Switzer R.(1977) In Experimental biochemistry, 2nd edn. Free Man Company, San Francisco

  33. Zhu X, Song F, Liu S (2011) Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system. J Food Agric Environ 9(2):583–587

    Google Scholar 

  34. Li J, Meng B, Chai H, Yang X, Song W, Li S, Lu A, Zhang T, Sun W (2019) Arbuscular mycorrhizal fungi alleviate drought stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) grasses via altering antioxidant enzyme activities and photosynthesis. Front Plant Sci 10:499

    Article  Google Scholar 

  35. Figueiredo MV, Burity HA, Martinez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L.) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40(1):182–188

  36. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4(7):e226

  37. Aradooei S, Zakerin AR, Aboutalebi A (2013) Effect of different levels of irrigation period and foliar application of methanol on essence of sweet basil (Ocimum basilicum L.). Ann Biol Res 4(6):220–223

  38. Aslani Z, Hassani A, Rasouli-Sadaghiani M, Esmailpour B, Rohi Z (2014) Effects of arbuscular mycorrhizal (AM) fungi on essential oil content and nutrients uptake in basil under drought stress. J Med Plants Product 3(2):147–153

    Google Scholar 

  39. Shaw B, Thomas TH, Cooke DT (2002) Responses of sugar beet (Beta vulgaris L.) to drought and nutrient deficiency stress. Plant Growth Regul 37(1):77–83

  40. Ashraf M, Iram A (2005) Drought stress induced changes in some organic substances in nodules and other plant parts of two potential legumes differing in salt tolerance. Flora 200:535–546

    Article  Google Scholar 

  41. Hamed BA, Atteya AM (2013) Metabolic changes associated with the growth of coriander (Coriandrum sativum L.) grown under drought stress and sprayed with SAHARA nutritive solution. In: Egyptian journal international conference, Helwan University, Egypt 17–18 April 2013, pp 123–134

  42. Pebriansyah A (2012) Effect of drought stress and addition of arbuscula mycorrhizal fungi (AMF) on growth and productivity of tropical grasses (Chloris gayana, Paspalum dilatatum, and Paspalum notatum). Pastura 2(1):41–48

    Google Scholar 

  43. Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB (2008) Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. Plant Cell 20(4):1134–1151

    CAS  Article  Google Scholar 

  44. Hoshika Y, Omasa K, Paoletti E (2013) Both ozone exposure and soil water stress are able to induce stomatal sluggishness. Environ Exp Bot 88:19–23

    CAS  Article  Google Scholar 

  45. Xu Z, Zhou G (2008) Responses of leaf stomatal density to water status and its relationship with photosynthesis in a grass. J Exp Bot 59(12):3317–3325

    CAS  Article  Google Scholar 

  46. Spence RD, Wu H, Sharpe PJ, Clark KG (1986) Water stress effects on guard cell anatomy and the mechanical advantage of the epidermal cells. Plant Cell Environ 9(3):197–202

    Google Scholar 

  47. Parkash V, Singh S (2020) A review on potential plant-based water stress indicators for vegetable crops. Sustainability 12(10):3945

    CAS  Article  Google Scholar 

  48. Arve LE, Torre S, Olsen JE, Tanino KK (2011) Stomatal responses to drought stress and air humidity. In Abiotic stress in plants-Mechanisms and adaptations. IntechOpen, pp 267–280. https://doi.org/10.5772/24661

  49. Fracasso A, Vallino M, Staropoli A, Vinale F, Amaducci S, Carra A (2020) Increased water use efficiency in miR396-downregulated tomato plants. Plant Sci J:110729.

  50. Zhao W, Sun Y, Kjelgren R, Liu X (2015) Response of stomatal density and bound gas exchange in leaves of maize to soil water deficit. Acta Physiol Plant 37(1):1704

    Article  Google Scholar 

  51. Zhang H, Wang XR, Wang SB (2004) A study on stomatal traits of Platanus acerifolia under urban stress. J Fudan Univ 43:651–656

    Google Scholar 

  52. Shuguang Wang FD, Daizhen Sun YC, Xue Yan RJ (2018) QTL analysis for stomatal density and size in wheat spike organ. Emir J Food Agric 173–179.

  53. Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55(403):1743–1750

    CAS  Article  Google Scholar 

  54. Zeng Y, Guo LP, Chen BD, Hao ZP, Wang JY, Huang LQ, Yang G, Cui XM, Yang L, Wu ZX, Chen ML, Zhang Y (2013) Arbuscular mycorrhizal symbiosis and active ingredients of medicinal plants: current research status and prospectives. Mycorrhiza 23(4):253–265

    CAS  Article  Google Scholar 

  55. Wu QS, Zou YN (2017) Arbuscular mycorrhizal fungi and tolerance of drought stress in plants. In: Wu QS Arbuscular mycorrhizas and stress tolerance of plants. Springer, Singapore, pp 25–41

  56. Othman MOM (2012) Alleviation of drought stress on Vigna radiate L. by using glycine betaine, proline or their Mixture. Dissertation, Botany and Microbiology Department, Faculty of Science, Beni-Suef University, Egypt

  57. Hamed BE, AbdElgawad H (2018) Differential effects of some ascorbates on Phaseolus vulgaris L. in response to salinity stress. Egypt J Bot 58(1):23–36

  58. Verslues PE, Sharma S (2010) Proline metabolism and its implications for plant-environment interaction. Arabidopsis Book Am Soc Plant Biol 8:e0140. https://doi.org/10.1199/tab.0140

    Article  Google Scholar 

  59. Giri J (2011) Glycinebetaine and abiotic stress tolerance in plants. Plant Signal Behav 6(11):1746–1751

    CAS  Article  Google Scholar 

  60. Neto D, Carvalho LM, Cruz C, Martins-Loucao MA (2006) How do mycorrhizas affect C and N relationships in flooded Aster tripolium plants? Plant Soil 279(1):51–63

    CAS  Article  Google Scholar 

  61. Abu-Ghalia H, El-Khalal S (2001) Interaction between mycorrhizal fungi and Jasmonic acid and their effects upon the growth, and metabolic activities of lupine plants grown under saline conditions. Egypt J Bot 41:201–226

    Google Scholar 

  62. Rasouli-Sadaghiani M, Hassani A, Barin M, Danesh YR, Sefidkon F (2010) Effects of AM fungi on growth, essential oil production and nutrients uptake in basil. J Med Plant Res 4(21):2222–2228

    CAS  Google Scholar 

  63. Kyriazopoulos AP, Orfanoudakis M, Abraham EM, PARISSI ZM, Serafidou N (2014) Effects of arbuscular mycorrhiza fungi on growth characteristics of Dactylis glomerata L. under drought stress conditions. Not Bot Horti Agrobo 42(1):132–137

  64. Liu T, Sheng M, Wang CY, Chen H, Li Z, Tang M (2015) Impact of arbuscular mycorrhizal fungi on the growth, water status, and photosynthesis of hybrid poplar under drought stress and recovery. Photosynthetica 53(2):250–258

    CAS  Article  Google Scholar 

  65. Nazeri NK, Lambers H, Tibbett M, Ryan MH (2014) Moderating mycorrhizas: arbuscular mycorrhizas modify rhizosphere chemistry and maintain plant phosphorus status within narrow boundaries. Plant Cell Environ 37(4):911–921

    CAS  Article  Google Scholar 

  66. Zhao Y, Han Q, Ding C, Huang Y, Liao J, Chen T, Yuan M (2020) Effect of low temperature on chlorophyll biosynthesis and chloroplast biogenesis of rice seedlings during greening. Int J Mol Sci 21(4):1390

    CAS  Article  Google Scholar 

  67. Pinior A, Grunewaldt-Stöcker G, von Alten H, Strasser RJ (2005) Mycorrhizal impact on drought stress tolerance of rose plants probed by chlorophyll a fluorescence, proline content and visual scoring. Mycorrhiza 15(8):596–605

    CAS  Article  Google Scholar 

  68. Pirasteh-Anosheh H, Saed-Moucheshi A, Pakniyat H, Pessarakli M (2016) Stomatal responses to drought stress. In: Ahmad P (ed) Water stress and crop plants, Ed1, Vol 1. Wiley Online Library, pp 24–40. https://doi.org/10.1002/9781119054450.ch3

  69. Mohammad MJ, Malkawi HI, Shibli R (2003) Effects of arbuscular mycorrhizal fungi and phosphorus fertilization on growth and nutrient uptake of barley grown on soils with different levels of salts. J Plant Nutr 26(1):125–137

    CAS  Article  Google Scholar 

Download references

Acknowledgements

Not applicable.

Funding

Not applicable.

Author information

Affiliations

  1. Department of Botany and Microbiology, Faculty of Science, Beni-Suef University, Beni Suef, 62521, Egypt

    Shaimaa E. Abd-Elghany, Attaya A. Moustafa, Nasr H. Gomaa & Badr-eldin A. Hamed

  2. Biology Department, College of Science, Jouf University, Sakaka, Saudi Arabia

    Nasr H. Gomaa

Authors
  1. Shaimaa E. Abd-Elghany
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Attaya A. Moustafa
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nasr H. Gomaa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Badr-eldin A. Hamed
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NH and AM have drafted the review. SE and NH prepared different tables and figures required for the manuscript. BA provided guidance during the development of the idea and wrote and revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Shaimaa E. Abd-Elghany.

Ethics declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Abd-Elghany, S.E., Moustafa, A.A., Gomaa, N.H. et al. Mycorrhizal impact on Ocimum basilicum grown under drought stress. Beni-Suef Univ J Basic Appl Sci 10, 72 (2021). https://doi.org/10.1186/s43088-021-00166-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s43088-021-00166-z

Keywords

  • Stomata
  • Osmoregulating
  • Proline
  • Glycine betaine
  • Amino acids
  • Chlorophyll
  • Minerals