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Arbuscular mycorrhizal fungi improve growth, essential oil, secondary metabolism, and yield of tobacco (Nicotiana tabacum L.) under drought stress conditions

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Abstract

Drought is a major environmental threat limiting worldwide crop production. Drought stress affects the tobacco quality and yield; therefore, the current research studies were undertaken to investigate the effectiveness of arbuscular mycorrhizal fungi (AMF) under drought stress on morphological and biochemical attributes of tobacco (Nicotiana tabacum L. variety Yunyan 87). AMF-inoculated and AMF-non-inoculated plants were maintained in a greenhouse and irrigated with a half-strength Hoagland solution (100 mL pot−1) once a week. At harvesting, the plant height, number of leaves, fresh and dry weights, mycorrhizal colonization, and concentration of leaf photosynthetic pigments and photosynthetic rate were measured. Data were statistically analyzed by ANOVA and the principal component (PCA) analyses. The effect of root colonization significantly increased biomass production and essential oil accumulation. Results showed that drought at mild and severe stressed levels significantly affected tobacco growth by decreasing plant height, biomass, and a number of leaves. However, inoculation of AMF considerably increased plant height, fresh and dry weights, chlorophyll (a, b), total chlorophyll, and carotenoid content by 43.84, 40.87 and 49.76, 185.29, 325.60, 173.12, and 211.49%, respectively. Compared with non-inoculated plants, AMF inoculation significantly enhanced the essential oil yield and the uptake of nitrogen, phosphorus, and potassium with the increase of 257.36, 102.71, and 90.76, 62.32, and 84.51%, respectively, in mild drought + AMF-treated plants. Similarly, the antioxidant enzymatic activity, glomalin-related soil protein (GRSP), and accumulation of phenols and flavonoids and osmolytes content were also significantly improved in inoculated plants under drought stress. Additionally, AMF inoculation significantly upregulated the lipoxygenase (LOX) and phenylalanine ammonia-lyase (PAL) enzymes by 197 and 298.44% under drought conditions. These findings depicted that the symbiotic association of AMF improved the overall growth pattern and secondary metabolism in tobacco plants under severe drought stress conditions and may be used as an approaching source of important drugs in the field of pharmacology.

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Data Availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Abd-Allah EF, Hashem A, Alqarawi AA et al (2015) Enhancing growth performance and systemic acquired resistance of medicinal plant Sesbania sesban (L.) Merr using arbuscular mycorrhizal fungi under salt stress. Saudi J Biol Sci 22:274–283. https://doi.org/10.1016/j.sjbs.2015.03.004

    Article  CAS  Google Scholar 

  • Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry. Allured publishing corporation Carol Stream, IL

    Google Scholar 

  • Aebi H, (1984) Catalase in vitro. Methods in Enzymol, vol. 105. Academic Press, Cambridge, MA, USA, pp. 121–126. https://doi.org/10.1016/S0076-6879(84)05016-3

  • Ahanger MA, Agarwal RM, Tomar NS, Shrivastava M (2015) Potassium induces positive changes in nitrogen metabolism and antioxidant system of oat (Avena sativa L cultivar Kent). J Plant Interact 10:211–223. https://doi.org/10.1080/17429145.2015.1056260

    Article  Google Scholar 

  • Ahanger MA, Hashem A, Abd-Allah EF, Ahmad P (2014) Arbuscular mycorrhiza in crop improvement under environmental stress. Emerging technologies and management of crop stress tolerance. Elsevier, In, pp 69–95

    Google Scholar 

  • Ahanger MA, Tittal M, Mir RA, Agarwal R (2017a) Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 254:1953–1963. https://doi.org/10.1007/s00709-017-1086-z

    Article  CAS  Google Scholar 

  • Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017b) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23:731–744. https://doi.org/10.1007/s12298-017-0462-7

    Article  Google Scholar 

  • Ahmad H, Hayat S, Ali M, Liu T, Cheng Z (2018) The combination of arbuscular mycorrhizal fungi inoculation (Glomus versiforme) and 28-homobrassinolide spraying intervals improves growth by enhancing photosynthesis, nutrient absorption, and antioxidant system in cucumber (Cucumis sativus L.) under sali. Ecol Evol 8:5724–5740. https://doi.org/10.1002/ece3.4112

    Article  Google Scholar 

  • Ahmad P (2010) Growth and antioxidant responses in mustard (Brassica juncea L.) plants subjected to combined effect of gibberellic acid and salinity. Arch Agron Soil Sci 56:575–588. https://doi.org/10.1080/03650340903164231

    Article  CAS  Google Scholar 

  • Ahmad P, Ashraf M, Hakeem KR, Azooz MM, Rasool S, Chandna R, Akram NA (2014) Potassium starvation-induced oxidative stress and antioxidant defense responses in Brassica juncea. J Plant Interact 9:1–9

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Babenko LM, Shcherbatiuk MM, Skaterna TD, Kosakivska IV (2017) Lipoxygenases and their metabolites in formation of plant stress tolerance. Ukr Biochem J 89:5–21

    Google Scholar 

  • Bączek KB, Wiśniewska M, Przybył JL et al (2019) Arbuscular mycorrhizal fungi in chamomile (Matricaria recutita L.) organic cultivation. Ind Crops Prod 140. https://doi.org/10.1016/j.indcrop.2019.111562

  • Baghaie AH, Aghili F, Jafarinia R (2019) Soil-indigenous arbuscular mycorrhizal fungi and zeolite addition to soil synergistically increase grain yield and reduce cadmium uptake of bread wheat (through improved nitrogen and phosphorus nutrition and immobilization of Cd in roots). Environ Sci Pollut Res 26:30794–30807

    Article  CAS  Google Scholar 

  • Bahrami-Rad S, Hajiboland R (2017) Effect of potassium application in drought-stressed tobacco ( Nicotiana rustica L.) plants: comparison of root with foliar application. Ann Agric Sci S0570178317300222

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

  • Begum N, Ahanger MA, Zhang L (2020) AMF inoculation and phosphorus supplementation alleviates drought induced growth and photosynthetic decline in Nicotiana tabacum by up-regulating antioxidant metabolism and osmolyte accumulation. Environ Exp Bot 176:104088. https://doi.org/10.1016/j.envexpbot.2020.104088

    Article  CAS  Google Scholar 

  • Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019a) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1–15. https://doi.org/10.3389/fpls.2019.01068

    Article  Google Scholar 

  • Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M, Ahmed N, Zhang L (2019b) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.01068

  • Cervantes-Gámez RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza IE, Villalobos-López MÁ, Valdez-Ortíz Á, López-Meyer M (2016) Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-seq analysis. Plant Mol Biol Report 34:89–102

    Article  CAS  Google Scholar 

  • Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Schubert A, Gambino G, Balestrini R, Guerrieri E (2016) Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol 171:1009–1023. https://doi.org/10.1104/pp.16.00307

    Article  Google Scholar 

  • Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16:485–494

    Article  CAS  Google Scholar 

  • Luz S, Reis LA, Lemos O et al (2016) Effect of arbuscular mycorrhizal fungi on the essential oil composition and antioxidant activity of black pepper (Piper nigrum L.). Int J Appl Res Nat Prod 9:10–17

    Google Scholar 

  • da Trindade R, Almeida L, Xavier L et al (2019) 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, Switzerland) 8. https://doi.org/10.3390/plants8110442

  • Dalal VK, Tripathy BC (2012) Modulation of chlorophyll biosynthesis by water stress in rice seedlings during chloroplast biogenesis. Plant Cell Environ 35:1685–1703. https://doi.org/10.1111/j.1365-3040.2012.02520.x

    Article  CAS  Google Scholar 

  • de Oliveira JSF, Xavier LP, Lins A, Andrade EHA, Maia JGS, de Mello AH, Setzer WN, Ramos AR, da Silva JKR (2019) Effects of inoculation by arbuscular mycorrhizal fungi on the composition of the essential oil, plant growth, and lipoxygenase activity of Piper aduncum L. AMB Express 9:29. https://doi.org/10.1186/s13568-019-0756-y

    Article  CAS  Google Scholar 

  • Dhindsa RS, Plumb-dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase content in a trusted digital archive. We use information technology and tools to increase production. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Doderer A, Kokkelink I, van der Veen S, Valk B, Schram A, Douma A (1992) Purification and characterization of two lipoxygenase isoenzymes from germinating barley. Biochim Biophys Acta 112:97–104

    Article  Google Scholar 

  • Ekblad A, Wallander H, Carlsson R, Huss-Danell K (1995) Fungal biomass in roots and extrametrical mycelium in relation to macronutrients and plant biomass of ectomycorrhizal Pinus sylvestris and Alnus incana. New Phytol 131:443–451

    Article  Google Scholar 

  • Ellman GL (1959) Tissue sulphydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  Google Scholar 

  • Fang S, Tao Y, Zhang Y, Kong F, Wang Y (2018) Effects of metalaxyl enantiomers stress on root activity and leaf antioxidant enzyme activities in tobacco seedlings. Chirality 30:469–474. https://doi.org/10.1002/chir.22810

    Article  CAS  Google Scholar 

  • Fokom R, Adamou S, Essono D, Ngwasiri DP, Eke P, Teugwa Mofor C, Tchoumbougnang F, Fekam BF, Amvam Zollo PH, Nwaga D, Sharma AK (2019) Growth, essential oil content, chemical composition and antioxidant properties of lemongrass as affected by harvest period and arbuscular mycorrhizal fungi in field conditions. Ind Crop Prod 138:111477. https://doi.org/10.1016/j.indcrop.2019.111477

    Article  CAS  Google Scholar 

  • Fong J, Schaffer FL, Kirk PL (1953) The ultramicrodetermination of glycogen in liver. A comparison of the anthrone and reducing - sugar methods 1 separation of glycogen. 319–326

  • Fouad MO, Essahibi A, Benhiba L, Qaddoury A (2014) Effectiveness of arbuscular mycorrhizal fungi in the protection of olive plants against oxidative stress induced by drought. Span J Agric Res 12:763–771. https://doi.org/10.5424/sjar/2014123-4815

    Article  Google Scholar 

  • Gang DR, Wang J, Dudareva N, Nam KH, Simon JE, Lewinsohn E, Pichersky E (2001) An investigation of the storage and biosynthesis of phenylpropenes in sweet basil. Plant Physiol 125:539–555

    Article  CAS  Google Scholar 

  • Garg N, Bharti A (2018) Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress. Mycorrhiza 28:727–746. https://doi.org/10.1007/s00572-018-0856-6

    Article  CAS  Google Scholar 

  • Gill SS, Singh LP, Tuteja N, Gill R (2012) Generation and scavenging of reactive oxygen species in plants under stress. Improve crop resistance to abiotic stress 1:49–70. https://doi.org/10.1002/9783527632930.ch3

    Article  CAS  Google Scholar 

  • Hanin M, Ebel C, Ngom M et al (2016) New insights on plant salt tolerance mechanisms and their potential use for breeding. Front Plant Sci 7:1787

    Article  Google Scholar 

  • Hao C, Xia Z, Fan R, et al (2016) 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 17:822

  • Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. https://doi.org/10.3390/ijms14059643

    Article  CAS  Google Scholar 

  • Hazzoumi Z, Moustakime Y, Hassan Elharchli E, 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. https://doi.org/10.1186/s40538-015-0035-3

    Article  CAS  Google Scholar 

  • Hassiotis CN, Orfanoudakis M (2018) The impact of Lavandula stoechas L. degradation on arbuscular mycorrhizal fungi, in a Mediterranean ecosystem. Appl Soil Ecol 126:182–188. https://doi.org/10.1016/j.apsoil.2018.02.025

    Article  Google Scholar 

  • Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466. https://doi.org/10.4161/psb.21949

    Article  CAS  Google Scholar 

  • He Y, Cornelissen JHC, Zhong Z, et al (2017) How interacting fungal species and mineral nitrogen inputs affect transfer of nitrogen from litter via arbuscular mycorrhizal mycelium. Environ Sci Pollut Res

  • Hori M, Kondo H, Ariyoshi N, Yamada H, Hiratsuka A, Watabe T, Oguri K (1997) Changes in the hepatic glutathione peroxidase redox system produced by coplanar polychlorinated biphenyls in Ah-responsive and -less-responsive strains of mice: mechanism and implications for toxicity. Environ Toxicol Pharmacol 3:267–275. https://doi.org/10.1016/S1382-6689(97)00025-2

    Article  CAS  Google Scholar 

  • Hou Y, Meng K, Han Y et al (2015) The persimmon 9-lipoxygenase gene DkLOX3 plays positive roles in both promoting senescence and enhancing tolerance to abiotic stress. Front Plant Sci 6:1073

    Article  Google Scholar 

  • Hua J, Jiang Q, Bai J, Ding F, Lin X, Yin Y (2014) Interactions between arbuscular mycorrhizal fungi and fungivorous nematodes on the growth and arsenic uptake of tobacco in arsenic-contaminated soils. Appl Soil Ecol 84:176–184. https://doi.org/10.1016/j.apsoil.2014.07.004

    Article  Google Scholar 

  • Jain VK, Guruprasad KN (1989) Effect of chlorocholine chloride and gibberellic acid on the anthocyanin synthesis in radish seedlings. Physiol Plant 75:233–236. https://doi.org/10.1111/j.1399-3054.1989.tb06174.x

    Article  CAS  Google Scholar 

  • Karagiannidis N, Thomidis T, Lazari D, Panou-Filotheou E, Karagiannidou C (2011) Effect of three Greek arbuscular mycorrhizal fungi in improving the growth, nutrient concentration, and production of essential oils of oregano and mint plants. Sci Hortic (Amsterdam) 129:329–334

    Article  CAS  Google Scholar 

  • Khosravi H, Haydari E, Shekoohizadegan S, Zareie S (2017) Assessment the effect of drought on vegetation in desert area using Landsat data. Egypt J Remote Sens Sp Sci 20:S3–S12. https://doi.org/10.1016/j.ejrs.2016.11.007

    Article  Google Scholar 

  • Kist BB, (2018) Anuario Brasileiro Do Tabaco. 2018, p. 132.

  • Koide RT, Peoples MS (2013) Behavior of Bradford-reactive substances is consistent with predictions for glomalin. Appl Soil Ecol 63:8–14

    Article  Google Scholar 

  • Langeroodi ARS, Ghooshchi F, Dadgar T (2017) Alleviatory activities in mycorrhizal tobacco plants subjected to increasing chloride in irrigation water. Ital J Agron 12:8–16. https://doi.org/10.4081/ija.2016.792

    Article  Google Scholar 

  • León Morcillo RJ, Ocampo JA, García Garrido JM (2012) Plant 9-lox oxylipin metabolism in response to arbuscular mycorrhiza. Plant Signal Behav 7:1584–1588

    Article  CAS  Google Scholar 

  • Lim CW, Han S-W, Hwang IS, Kim DS, Hwang BK, Lee SC (2015) The pepper lipoxygenase CaLOX1 plays a role in osmotic, drought and high salinity stress response. Plant Cell Physiol 56:930–942

    Article  CAS  Google Scholar 

  • 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 53:250–258. https://doi.org/10.1007/s11099-015-0100-y

    Article  CAS  Google Scholar 

  • Mandal SM, Chakraborty D, Dey S (2010) Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal Behav 5:359–368. https://doi.org/10.4161/psb.5.4.10871

    Article  CAS  Google Scholar 

  • Meena M, Divyanshu K, Kumar S, Swapnil P, Zehra A, Shukla V, Yadav M, Upadhyay RS (2019) Regulation of L-proline biosynthesis, signal transduction, transport, accumulation and its vital role in plants during variable environmental conditions. Heliyon 5(e0):29–52. https://doi.org/10.1016/j.heliyon.2019.e02952

    Article  Google Scholar 

  • Miransari M, Abrishamchi A, Khoshbakht K, Niknam V (2014) Plant hormones as signals in arbuscular mycorrhizal symbiosis. Crit Rev Biotechnol 34:123–133

    Article  CAS  Google Scholar 

  • Mirzaee M, Moieni A, Ghanati F (2013) Effects of drought stress on the lipid peroxidation and antioxidant enzyme activities in two canola (Brassica napus L.) cultivars. J Agric Sci Technol 15:593–602

    CAS  Google Scholar 

  • Mohasseli V, Sadeghi S (2019) Exogenously applied sodium nitroprusside improves physiological attributes and essential oil yield of two drought susceptible and resistant specie of thymus under reduced irrigation. Ind Crop Prod 130:130–136. https://doi.org/10.1016/j.indcrop.2018.12.058

    Article  CAS  Google Scholar 

  • Mookherjee BD, Wilson RA (1990) Tobacco constituents―their importance in flavor and fragrance chemistry. Perfum flavorist 15:27–49

    CAS  Google Scholar 

  • Moradtalab N, Hajiboland R, Aliasgharzad N, Hartmann TE, Neumann G (2019) Silicon and the association with an arbuscular-mycorrhizal fungus (Rhizophagus clarus) mitigate the adverse effects of drought stress on strawberry. Agronomy 9:1–22. https://doi.org/10.3390/agronomy9010041

    Article  CAS  Google Scholar 

  • Mukherjee SP, Choudhuri MA (1983) Implications of water stress-induced changes in the levels of endogenous ascorbic acid and hydrogen peroxide in Vigna seedlings. Plant Physiol 58:166–170

    Article  CAS  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in Spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232

    Article  CAS  Google Scholar 

  • Nell M, Vötsch M, Vierheilig H, Steinkellner S, Zitterl-Eglseer K, Franz C, Novak J (2009) Effect of phosphorus uptake on growth and secondary metabolites of garden sage (Salvia officinalis L.). J Sci Food Agric 89:1090–1096. https://doi.org/10.1002/jsfa.3561

    Article  CAS  Google Scholar 

  • Nell M, Wawrosch C, Steinkellner S, Vierheilig H, Kopp B, Lössl A, Franz C, Novak J, Zitterl-Eglseer K (2010) Root colonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Med 76:393–398

    Article  CAS  Google Scholar 

  • NIST (2011) National institute of standard and technology (2011) NIST standard reference database number 69. http://webbook.nist.gov/. Accessed 25 Nov 2018

  • Olsen SR, Cole CV, Watandbe F, Dean L (1954) Estimation of available phosphorus in soil by extraction with sodium bicarbonate. J Chem Inf Model 53(9):1689–1699

    Google Scholar 

  • Osakabe Y, Nishikubo N, Osakabe K (2007) Phenylalanine ammonia-lyase in woody plants: a key switch of carbon accumulation in biomass. Jpn J Plant Sci 1:103–108

    Google Scholar 

  • Pereira A (2016) Plant abiotic stress challenges from the changing environment. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.01123

  • Peedin GF (2011) Tobacco cultivation. In: Myers ML (ed) Specialty Crops International Labor Organization

    Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–IN18. https://doi.org/10.1016/s0007-1536(70)80110-3

    Article  Google Scholar 

  • Poltronieri P, (2016) Tobacco seed oil for biofuels, biotransformation of agricultural waste and by-products: the food, feed, fibre, fuel (4F) economy. Elsevier Inc. https://doi.org/10.1016/B978-0-12-803622-8.00006-9.

  • Popova V, Ivanova T, Nikolova V et al (2017) Biologically active and volatile compounds in leaves and extracts of Nicotiana alata Link & otto from Bulgaria. J Pharm Sci Res 9:2045–2051

    CAS  Google Scholar 

  • Popova V, Ivanova T, Prokopov T, et al (2019) Carotenoid-related volatile compounds of tobacco (Nicotiana tabacum L.) essential oils. Molecules 24:3446

  • Porcar-Castell A, Tyystjärvi E, Atherton J, van der Tol C, Flexas J, Pfündel EE, Moreno J, Frankenberg C, Berry JA (2014) Linking chlorophyll a fluorescence to photosynthesis for remote sensing applications: mechanisms and challenges. J Exp Bot 65:4065–4095. https://doi.org/10.1093/jxb/eru191

    Article  CAS  Google Scholar 

  • Purin S, Rillig MC (2007) The arbuscular mycorrhizal fungal protein glomalin: limitations, progress, and a new hypothesis for its function. Pedobiologia (Jena) 51:123–130

    Article  CAS  Google Scholar 

  • Rapparini F, Llusià J, Peñuelas J (2007) Effect of arbuscular mycorrhizal (AM) colonization on terpene emission and content of Artemisia annua L. Plant Biol 9:e20–e32

    Google Scholar 

  • Rillig MC, Wright SF, Nichols KA, Schmidt WF, Torn MS (2001) Large contribution of arbuscular mycorrhizal fungi to soil carbon pools in tropical forest soils. Plant Soil 233:167–177

    Article  CAS  Google Scholar 

  • Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151. https://doi.org/10.1104/pp.006858

    Article  CAS  Google Scholar 

  • Road O, Division AP (1990) How to quantify Amf colonization on Root. New Phytol 115:495–495

    Google Scholar 

  • Rojas-Andrade R, Cerda-García-Rojas C, Frías-Hernández J, Dendooven L, Olalde-Portugal V, Ramos-Valdivia A (2003) Changes in the concentration of trigonelline in a semi-arid leguminous plant (Prosopis laevigata) induced by an arbuscular mycorrhizal fungus during the presymbiotic phase. Mycorrhiza 13:49–52

    Article  CAS  Google Scholar 

  • Rubin RL, van Groenigen KJ, Hungate BA (2017) Plant growth promoting rhizobacteria are more effective under drought: a meta-analysis. Plant Soil 416:309–323. https://doi.org/10.1007/s11104-017-3199-8

    Article  CAS  Google Scholar 

  • Ruiz-Rodriguez A, Bronze M-R, Da Ponte MN (2008) Supercritical fluid extraction of tobacco leaves: a preliminary study on the extraction of solanesol. J Supercrit Fluids 45:171–176

    Article  CAS  Google Scholar 

  • Sadasivam S, Manickam A (2004) Biochemical methods, 2nd edn. New Age International Limited Publishers, New Delhi, India

    Google Scholar 

  • Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546. https://doi.org/10.1002/elps.201300568

    Article  CAS  Google Scholar 

  • Singleton VL, Rossi JA, Jr J (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

  • Steinkellner S, Lendzemo V, Langer I, Schweiger P, Khaosaad T, Toussaint JP, Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions. Molecules 12:1290–1306

    Article  CAS  Google Scholar 

  • Steyermark A, (1961) Quantitative organic microanalysis. p. 665. Academic Press, London.

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046. https://doi.org/10.3852/16-042

    Article  CAS  Google Scholar 

  • Tarraf W, Ruta C, De Cillis F et al (2015) Effects of mycorrhiza on growth and essential oil production in selected aromatic plants. Ital J Agron 10:160–162. https://doi.org/10.4081/ija.2015.633

    Article  Google Scholar 

  • Tarraf W, Ruta C, Tagarelli A, de Cillis F, de Mastro G (2017) Influence of arbuscular mycorrhizae on plant growth, essential oil production and phosphorus uptake of Salvia officinalis L. Ind Crop Prod 102:144–153. https://doi.org/10.1016/j.indcrop.2017.03.010

    Article  CAS  Google Scholar 

  • Urcoviche RC, Gazim ZC, Dragunski DC, Barcellos FG, Alberton O (2015) Plant growth and essential oil content of Mentha crispa inoculated with arbuscular mycorrhizal fungi under different levels of phosphorus. Ind Crop Prod 67:103–107

    Article  CAS  Google Scholar 

  • Vaganan MM, Ravi I, Nandakumar A et al (2014) Phenylpropanoid enzymes, phenolic polymers and metabolites as chemical defenses to infection of Pratylenchus coffeae in roots of resistant and susceptible bananas (Musa spp.). Indian J Exp Biol 52(3):252–260

    CAS  Google Scholar 

  • Vierheilig H, Gagnon H, Strack D, Maier W (2000) Accumulation of cyclohexenone derivatives in barley, wheat and maize roots in response to inoculation with different arbuscular mycorrhizal fungi. Mycorrhiza 9:291–293

    Article  CAS  Google Scholar 

  • Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56:435–447. https://doi.org/10.1093/jxb/eri060

    Article  CAS  Google Scholar 

  • Weatherley PE (1949) Studies in the water relations of the field measurement of water deficits in leaves. New Phytol 49:81–86

    Article  Google Scholar 

  • Weisany W, Sohrabi Y, Siosemardeh A, Ghassemi-Golezani K (2017) Funneliformis mosseae fungi changed essential oil composition in Trigonella foenum graecum L., Coriandrum sativum L. and Nigella sativa L. J Essent Oil Res 29:276–287. https://doi.org/10.1080/10412905.2016.1216469

    Article  CAS  Google Scholar 

  • Wright SF, Anderson RL (2000) Aggregate stability and glomalin in alternative crop rotations for the Central Great Plains. Biol Fertil Soils 31:249–253

    Article  CAS  Google Scholar 

  • Wu Q-S, Xia R-X, Zou Y-N (2008) Improved soil structure and citrus growth after inoculation with three arbuscular mycorrhizal fungi under drought stress. Eur J Soil Biol 44:122–128

    Article  Google Scholar 

  • Yao MK, Desilets H, Charles MT et al (2003) Effect of mycorrhization on the accumulation of rishitin and solavetivone in potato plantlets challenged with Rhizoctonia solani. Mycorrhiza 13:333–336

    Article  CAS  Google Scholar 

  • Ye L, Zhao X, Bao E, Cao K, Zou Z (2019) Effects of arbuscular mycorrhizal fungi on watermelon growth, elemental uptake, antioxidant, and photosystem ii activities and stress-response gene expressions under salinity-alkalinity stresses. Front Plant Sci 10:1–12. https://doi.org/10.3389/fpls.2019.00863

    Article  Google Scholar 

  • Yooyongwech S, Phaukinsang N, Cha-um S, Supaibulwatana K (2013) Arbuscular mycorrhiza improved growth performance in Macadamia tetraphylla L. grown under water deficit stress involves soluble sugar and proline accumulation. Plant Growth Regul 69:285–293. https://doi.org/10.1007/s10725-012-9771-6

    Article  CAS  Google Scholar 

  • Yuan S, Li M, Fang Z, Liu Y, Shi W, Pan B, Wu K, Shi J, Shen B, Shen Q (2016) Biological control of tobacco bacterial wilt using Trichoderma harzianum amended bioorganic fertilizer and the arbuscular mycorrhizal fungi Glomus mosseae. Biol Control 92:164–171. https://doi.org/10.1016/j.biocontrol.2015.10.013

    Article  Google Scholar 

  • Zhang J, Zhang J, Wang M, Wu S, Wang H, Niazi NK, Man YB, Christie P, Shan S, Wong MH (2019a) Effect of tobacco stem-derived biochar on soil metal immobilization and the cultivation of tobacco plant. J Soils Sediments 19:2313–2321

    Article  CAS  Google Scholar 

  • Zhang X, Gao H, Zhang L, Liu D, Ye X (2012) Extraction of essential oil from discarded tobacco leaves by solvent extraction and steam distillation, and identification of its chemical composition. Ind Crop Prod 39:162–169. https://doi.org/10.1016/j.indcrop.2012.02.029

    Article  CAS  Google Scholar 

  • Zhang Z, Zhang J, Xu G, Zhou L, Li Y (2019b) Arbuscular mycorrhizal fungi improve the growth and drought tolerance of Zenia insignis seedlings under drought stress. New For 50:593–604. https://doi.org/10.1007/s11056-018-9681-1

    Article  Google Scholar 

  • Zheng S-J, van Dijk JP, Bruinsma M, Dicke M (2007) Sensitivity and speed of induced defense of cabbage (Brassica oleracea L.): dynamics of BoLOX expression patterns during insect and pathogen attack. Mol Plant-Microbe Interact 20:1332–1345

    Article  CAS  Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  CAS  Google Scholar 

  • Zhu S, Lu X, Xing J, Zhang S, Kong H, Xu G, Wu C (2005) Comparison of comprehensive two-dimensional gas chromatography/time-of- flight mass spectrometry and gas chromatography-mass spectrometry for the analysis of tobacco essential oils. Anal Chim Acta 545:224–231. https://doi.org/10.1016/j.aca.2005.04.070

    Article  CAS  Google Scholar 

  • 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.

  • Zubek S, Błaszkowski J, Seidler-Łożykowska K, Bąba W, Mleczko P (2013) Arbuscular mycorrhizal fungi abundance, species richness and composition under the monocultures of five medicinal plants. Acta Sci Pol-Hortoru 12:127–141

    Google Scholar 

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Acknowledgement

The present research experiment was financed by the National Key Research and Development Program of China (No. 2017YFE0114000) and the Sci-Tec project of the Shaanxi Branch of China National Tobacco Corporation (No. KJ-2020-02). The authors are highly grateful to the Northwest A&F University, Yangling, Shaanxi, P.R. China, for providing the necessary facilities.

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Authors and Affiliations

  1. College of Life Sciences, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Naheeda Begum, Muhammad Abass Ahanger & Lixin Zhang

  2. National Center for Soybean Improvement, Key Laboratory of Biology and Genetics and Breeding for Soybean, Ministry of Agriculture, State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, 210095, China

    Naheeda Begum

  3. Institute of Nuclear Agricultural Sciences, Key Laboratory of Nuclear Agricultural Sciences of Ministry of Agriculture and Zhejiang Province, Zhejiang University, Hangzhou, 310058, China

    Kashif Akhtar

  4. Department of Agricultural Chemistry, University of Agriculture, Peshawar, Peshawar, Pakistan

    Mudassar Iqbal

  5. Shaanxi Tobacco Scientific Institution, Xi’an, 71000, China

    Pingping Wang

  6. Pomology Department, National Research Centre, Cairo, Egypt

    Nabil S. Mustafa

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  1. Naheeda Begum
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  2. Kashif Akhtar
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  3. Muhammad Abass Ahanger
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  4. Mudassar Iqbal
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  5. Pingping Wang
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  6. Nabil S. Mustafa
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  7. Lixin Zhang
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Contributions

The study was designed by NB and MAA. The experiments were performed and analyzed by NB. NB wrote the manuscript. NB, MAA, KA, and MI, PW, and NSM revised the manuscript. LZ supervised the work.

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Correspondence to Lixin Zhang.

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Begum, N., Akhtar, K., Ahanger, M.A. 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 28, 45276–45295 (2021). https://doi.org/10.1007/s11356-021-13755-3

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