Advertisement

Water deficit modulates growth, morphology, and the essential oil profile in Lippia alba L. (Verbenaceae) grown in vitro

Abstract

Lippia alba (Miller) N.E. Brown is an aromatic plant species of great economic importance due to the medicinal properties of its essential oils, which provide stress relief, respiratory and gastrointestinal disease control, and anti-inflammatory and natural sedative effects. The plant is also effective in biological control against various pathogens and in food preservation. Water deficit is the most critical abiotic factor limiting plant growth and morpho-physiological development, as well as production of secondary metabolism compounds. The objective of this work was to evaluate the effect of water deficit on growth, photosynthesis, essential oil profile, and the expression of genes related to the biosynthesis of these compounds in L. alba grown in vitro. Nodal segments were cultured on medium supplemented with 0, 1, 2, and 3% (w/v) polyethylene glycol for 45 days. Water stress had a negative effect on primary metabolism indicators, such as growth, leaf area, and photosynthetic rate; but a positive effect on amino acid and total protein content. Similarly, secondary metabolism exhibited an increase in linalool but a reduction in germacrene levels under water deficit. These findings provide a deeper understanding of how water deficit affects primary and secondary metabolism in L. alba, showing the potential of this medicinal species to adapt to soils with low water availability, while still being able to grow and synthesize essential oils.

Key message

Water deficit significantly alters the percentage of the essential oil components linalool and germacrene in Lippia alba plants grown in vitro.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Adams RP (1997) Identification of essential oil components by gas chromatography/mass spectroscopy. J Am Soc Mass Spectrom 6:671–672

  2. Allahverdiyev TI (2016) Impact of soil water deficit on some physiological parameters of durum and bread wheat genotypes. Agric For 62:131–144. https://doi.org/10.17707/AgricultForest.62.1.16

  3. Amin B, Hosseinzadeh H (2016) Black cumin (Nigella sativa) and its active constituent, thymoquinone: an overview on the analgesic and anti-inflammatory effects. Planta Med 82:8–16. https://doi.org/10.1055/s-0035-1557838

  4. Bahreininejad B, Razmjoo J, Mirza M (2014) Effect of water stress on productivity and essential oil content and composition of Thymus carmanicus. J Essent Oil-Bear Plants 17:717–725. https://doi.org/10.1080/0972060X.2014.901605

  5. Barkla BJ, Vera-Estrella R, Pantoja O (2013) Progress and challenges for abiotic stress proteomics of crop plants. Proteomics 13:1801–1815. https://doi.org/10.1002/pmic.201200401

  6. Batista DS, Castro KM, Silva AR, Teixeira ML, Sales TA, Soares LI, Cardoso MG, Santos MO, Viccini LF, Otoni WC (2016) Light quality affects in vitro growth and essential oil profile in Lippia alba (Verbenaceae). In Vitro Cell Dev Biol-Plant 52:276–282. https://doi.org/10.1007/s11627-016-9761-x

  7. Batista DS, Castro KM, Koehler AD, Porto BN, Silva AR, Souza VC, Teixeira ML, Cardoso MG, Santos MO, Viccini LF, Otoni WC (2017a) Elevated CO2 improves growth, modifies anatomy, and modulates essential oil qualitative production and gene expression in Lippia alba (Verbenaceae). Plant Cell Tissue Organ Cult 128:357–368. https://doi.org/10.1007/s11240-016-1115-1

  8. Batista DS, Dias LLC, Rêgo MMD, Saldanha CW, Otoni WC (2017b) Flask sealing on in vitro seed germination and morphogenesis of two types of ornamental pepper explants. Cienc Rural 47:1–6. https://doi.org/10.1590/0103-8478cr20150245

  9. Benelli G, Pavela R, Giordani C, Casettari L, Curzi G, Cappellacci L, Petrelli R, Maggi F (2018) Acute and sub-lethal toxicity of eight essential oils of commercial interest against the filariasis mosquito Culex quinquefasciatus and the housefly Musca domestica. Ind Crops Prod 112:668–680. https://doi.org/10.1016/j.indcrop.2017.12.062

  10. Bosabalidis AM, Kofidis G (2002) Comparative effects of drought stress on leaf anatomy of two olive cultivars. Plant Sci 163:375–379. https://doi.org/10.1016/S0168-9452(02)00135-8

  11. Cairns JE, Sanchez C, Vargas M, Ordoñez R, Araus JL (2012) Dissecting maize productivity: ideotypes associated with grain yield under drought stress and well-watered conditions. J Integr Plant Biol 54:1007–1020. https://doi.org/10.1111/j.1744-7909.2012.01156.x

  12. Castro KM, Batista DS, Fortini EA, Silva TD, Felipe SHS, Fernandes AM, Sousa RMJ, Nascimento LSQ, Campos VR, Grazul RM, Viccini LF, Otoni WC (2019) Photoperiod modulates growth, morphoanatomy, and linalool content in Lippia alba L. (Verbenaceae) cultured in vitro. Plant Cell Tissue Organ Cult 139:139–153. https://doi.org/10.1007/s11240-019-01672-w

  13. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125

  14. Chemat F, Maryline A-V, Xavier F (2013) Microwave-assisted extraction of essential oils and aromas. Microwave-assisted extraction for bioactive compounds. Springer, New York, pp 53–68. https://doi.org/10.1007/978-1-4614-4830-3_3

  15. Cornic G (2000) Drought stress inhibits photosynthesis by decreased stomatal aperture not by affecting ATP synthesis. Trends Plant Sci 5:187–188. https://doi.org/10.1016/S1360-1385(00)01625-3

  16. Costa AC, Rosa M, Megguer CA, Silva FG, Pereira FD, Otoni WC (2014) A reliable methodology for assessing the in vitro photosynthetic competence of two Brazilian savanna species: Hyptis marrubioides and Hancornia speciosa. Plant Cell Tissue Organ Cult 117:443–454. https://doi.org/10.1007/s11240-014-0455-y

  17. Cross JM, Von Korff M, Altmann T, Bartzetko L, Sulpice R, Gibon Y, Palacios N, Stitt M (2006) Variation of enzyme activities and metabolite levels in 24 Arabidopsis accessions growing in carbon-limited conditions. Plant Physiol 142:1574–1588. https://doi.org/10.1104/pp.106.086629

  18. Cruz CD (2016) Genes software-extended and integrated with the R, Matlab and Selegen. Acta Sci Agron 38:547–552. https://doi.org/10.4025/actasciagron.v38i4.32629

  19. Cruz EMDO, Pinto JAO, Fontes SS, Arrigoni-Blank MDF, Bacci L, Jesus HCRD, Santos DA, Alves PB, Blank AF (2014) Water deficit and seasonality study on essential oil constituents of Lippia gracilis Schauer germplasm. TSWJ 2014:1–9. https://doi.org/10.1155/2014/314626

  20. Du H, Wang N, Cui F, Li X, Xiao J, Xiong L (2010) Characterization of a β-carotene hydroxylase gene DSM2 conferring drought and oxidative stress resistance by increasing xanthophylls and ABA synthesis in rice. Plant Physiol 154:1304–1318. https://doi.org/10.1104/pp.110.163741

  21. Fernie AR, Roscher A, Ratcliffe RG, Kruger NJ (2001) Fructose 2,6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212:250–263. https://doi.org/10.1007/s004250000386

  22. Flexas J, Bota J, Loreto F, Cornic G, Sharkey TD (2004) Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol 6:269–279. https://doi.org/10.1055/s-2004-820867

  23. Ge T, Sui F, Bai L, Tong C, Sun N (2012) Effects of water stress on growth, biomass partitioning, and water-use efficiency in summer maize (Zea mays L.) throughout the growth cycle. Acta Physiol Plant 34:1043–1053. https://doi.org/10.1007/s11738-011-0901-y

  24. Ghotbi-Ravandi AA, Shahbazi M, Shariati M, Mulo P (2014) Effects of mild and severe drought stress on photosynthetic efficiency in tolerant and susceptible barley (Hordeum vulgare L.) genotypes. J Agron Crop Sci 200:403–415. https://doi.org/10.1111/jac.12062

  25. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Ann Rev Plant Biol 51:463–499. https://doi.org/10.1146/annurev.arplant.51.1.463

  26. Jaleel CA, Manivannan P, Lakshmanan GMA, Gomathinayagam M, Panneerselvam R (2008) Alterations in morphological parameters and photosynthetic pigment responses of Catharanthus roseus under soil water deficits. Colloid Surf B 61:298–303. https://doi.org/10.1016/j.colsurfb.2007.09.008

  27. Kumar A, Nayak AK, Pani DR, Das BS (2017) Physiological and morphological responses of four different rice cultivars to soil water potential based deficit irrigation management strategies. Field Crops Res 205:78–94. https://doi.org/10.1016/j.fcr.2017.01.026

  28. Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294. https://doi.org/10.1046/j.0016-8025.2001.00814.x

  29. Li J, Cang Z, Jiao F, Bai X, Zhang D, Zhai R (2017) Influence of drought stress on photosynthetic characteristics and protective enzymes of potato at seedling stage. J Saudi Soc Agric Sci 16:82–88. https://doi.org/10.1016/j.jssas.2015.03.001

  30. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

  31. Lorenzi H, Matos FJA (2008) Plantas Medicinais no Brasil—Nativas e Exóticas. Instituto Plantarum de Estudos da Flora, Nova Odessa, p 512

  32. Loreto F, Centritto M, Chartzoulakis K (2003) Photosynthetic limitations in olive cultivars with different sensitivity to salt stress. Plant Cell Environ 26:595–601. https://doi.org/10.1046/j.1365-3040.2003.00994.x

  33. Maatallah S, Nasri N, Hajlaoui H, Albouchi A, Elaissi A (2016) Evaluation changing of essential oil of laurel (Laurus nobilis L.) under water deficit stress conditions. Ind Crops Prod 91:170–178. https://doi.org/10.1016/j.indcrop.2016.07.001

  34. Mahmoud AA, Gendy ASH, Said-Al Ahl HAH, Grulova D, Astatkie T, Abdelrazik TM (2018) Impacts of harvest time and water stress on the growth and essential oil components of horehound (Marrubium vulgare). Sci Hortic 232:139–144. https://doi.org/10.1016/j.scienta.2018.01.004

  35. Mandoulakani BA, Eyvazpour E, Ghadimzadeh M (2017) The effect of drought stress on the expression of key genes involved in the biosynthesis of phenylpropanoids and essential oil components in basil (Ocimum basilicum L.). Phytochemistry 139:1–7. https://doi.org/10.1016/j.phytochem.2017.03.006

  36. Merwad ARM, Desoky ESM, Rady MM (2018) Response of water deficit-stressed Vigna unguiculata performances to silicon, proline or methionine foliar application. Sci Hortic 228:132–144. https://doi.org/10.1016/j.scienta.2017.10.008

  37. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009

  38. Molnar I, Dulai S, Csernak A, Pronay J, Molnar-Lang M (2005) Photosynthetic responces to drought stress in different Aegilops species. Acta Biol Szeged 49:141–142

  39. Morshedloo MR, Craker LE, Salami A, Nazeri V, Sang H, Maggi F (2017) Effect of prolonged water stress on essential oil content, compositions and gene expression patterns of mono-and sesquiterpene synthesis in two oregano (Origanum vulgare L.) subspecies. Plant Physiol Biochem 111:119–128. https://doi.org/10.1016/j.plaphy.2016.11.023

  40. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x

  41. Naeem M, Naeem MS, Ahmad R, Ihsan MZ, Ashraf MY, Hussain Y, Fahad S (2018) Foliar calcium spray confers drought stress tolerance in maize via modulation of plant growth, water relations, proline content and hydrogen peroxide activity. Arch Agron Soil Sci 64:116–131. https://doi.org/10.1080/03650340.2017.1327713

  42. Oliveira PC, Leite MN (2017) Amazonian medicinal herbs: physiology of stress. J Med Plants 5:255–264

  43. Otoni CG, Espitia PJ, Avena-Bustillos RJ, McHugh TH (2016) Trends in antimicrobial food packaging systems: Emitting sachets and absorbent pads. Food Res Int 83:60–73. https://doi.org/10.1016/j.foodres.2016.02.018

  44. Ozkur O, Ozdemir F, Bor M, Turkan I (2009) Physiochemical and antioxidant responses of the perennial xerophyte Capparis ovate Desf. to drought. Environ Exp Bot 66:487–492. https://doi.org/10.1016/j.envexpbot.2009.04.003

  45. Pascual ME, Slowing K, Carretero E, Sánches Mata D, Villar A (2001) Lippia: traditional uses, chemistry and pharmacology: a review. J Ethnopharm 76:201–214. https://doi.org/10.1016/S0378-8741(01)00234-3

  46. Pavela R, Govindarajan M (2017) The essential oil from Zanthoxylum monophyllum a potential mosquito larvicide with low toxicity to the non-target fish Gambusia affinis. J Pest Sci 90:369–378. https://doi.org/10.1007/s10340-016-0763-6

  47. Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin-mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water-stress. Plant Biotechnol J 9:747–758. https://doi.org/10.1111/j.1467-7652.2010.00584.x

  48. Peng Y, Li Y (2014) Combined effects of two kinds of essential oils on physical, mechanical and structural properties of chitosan films. Food Hydrocoll 36:287–293. https://doi.org/10.1016/j.foodhyd.2013.10.013

  49. Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, Anjum NA (2017) Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: phytohormones, mineral nutrients and transgenics. Plant Physiol Biochem 115:126–140. https://doi.org/10.1016/j.plaphy.2017.03.018

  50. Pérez-Clemente RM, Gómez-Cadenas A (2012) In vitro tissue culture, a tool for the study and breeding of plants subjected to abiotic stress conditions. In: Recent advances in plant in vitro culture. IntechOpen. https://doi.org/10.5772/50671

  51. Pérez Zamora CM, Torres CA, Nuñez MB (2018) Antimicrobial activity and chemical composition of essential oils from Verbenaceae species growing in South America. Molecules 23:544. https://doi.org/10.3390/molecules23030544

  52. Petropoulos SA, Daferera D, Polissiou MG, Passam HC (2008) The effect of water deficit stress on the growth, yield and composition of essential oils of parsley. Sci Hortic 115:393–397. https://doi.org/10.1016/j.scienta.2007.10.008

  53. Pola CC, Medeiros EA, Pereira OL, Souza VG, Otoni CG, Camilloto GP, Soares NF (2016) Cellulose acetate active films incorporated with oregano (Origanum vulgare) essential oil and organophilic montmorillonite clay control the growth of phytopathogenic fungi. Food Pack Shelf Life 9:69–78. https://doi.org/10.1016/j.fpsl.2016.07.001

  54. Raut JS, Karuppayil SM (2014) A status review on the medicinal properties of essential oils. Ind Crops Prod 62:250–264. https://doi.org/10.1016/j.indcrop.2014.05.055

  55. Saljoughian S, Shahin R, Alaa El-Din AB, Ralf G, Alireza O, Nooshin N, Amin MK (2018) The effects of food essential oils on cardiovascular diseases: a review. Crit Rev Food Sci Nutr 58:1688–1705. https://doi.org/10.1080/10408398.2017.1279121

  56. Seki M, Umezawa T, Urano K, Shinozaki K (2007) Regulatory metabolic networks in drought stress responses. Curr Opin Plant Biol 10:296–302. https://doi.org/10.1016/j.pbi.2007.04.014

  57. Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222. https://doi.org/10.1046/j.1365-3040.2002.00798.x

  58. Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578. https://doi.org/10.3390/ijms160613561

  59. Szczepanski S, Lipski A (2014) Essential oils show specific inhibiting effects on bacterial biofilm formation. Food Control 36:224–229. https://doi.org/10.1016/j.foodcont.2013.08.023

  60. Vieira RF, Silva DB, Salimena FRG (2016) Lippia alba—Erva-cidreira. In: Vieira RF, Camillo J, Coradin L (eds) Espécies nativas da flora brasileira de valor econômico atual ou potencial—Plantas para o futuro: Região Centro-Oeste. MMA, Brasília, pp 383–394

  61. Welburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313. https://doi.org/10.1016/S0176-1617(11)81192-2

  62. Wilkinson S, Davies WJ (2010) Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ 33:510–525. https://doi.org/10.1111/j.1365-3040.2009.02052.x

  63. Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ (2012) Plant hormone interactions: innovative targets for crop breeding and management. J Exp Bot 63:3499–3509. https://doi.org/10.1093/jxb/ers148

  64. Wu F, Bao W, Li F, Wu N (2008) Effects of drought stress and N supply on the growth, biomass partitioning and water-use efficiency of Sophora davidii seedlings. Environ Exp Bot 63:248–255. https://doi.org/10.1016/j.envexpbot.2007.11.002

  65. Xie H, Yang DH, Yao H, Bai GE, Zhang YH, Xiao BG (2016) iTRAQ-based quantitative proteomic analysis reveals proteomic changes in leaves of cultivated tobacco (Nicotiana tabacum) in response to drought stress. Biochem Biophys Res Commun 469:768–775. https://doi.org/10.1016/j.bbrc.2015.11.133

  66. Xuemei J, Dong B, Shiran B, Talbot MJ, Edlington JE, Trijntje H, Rosemary GW, Frank G, Dolferus R (2011) Control of ABA catabolism and ABA homeostasis is important for reproductive stage stress tolerance in cereals. Plant Physiol 156:647–662. https://doi.org/10.1104/pp.111.176164

  67. Yadav RK, Sangwan RS, Sabir F, Srivastava AK, Sangwan NS (2014) Effect of prolonged water stress on specialized secondary metabolites, peltate glandular trichomes, and pathway gene expression in Artemisia annua L. Plant Physiol Biochem 74:70–83. https://doi.org/10.1016/j.plaphy.2013.10.023

Download references

Acknowledgements

We thank Dr. Fátima Salimena (Department of Botany, UFJF) for identifying the Lippia alba accessions. The authors also thank the Brazilian sponsoring agencies, CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais) and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Ensino Superior), for financial support. We would like to thank Editage (www.editage.com) for English language editing.

Author information

KMC and DSB conceived and designed the experiments; KMC raised the in vitro plants; TDS, EAF, SHSF, AMF, and RMJS performed the morphoanatomical and physiological analyses; KMC, LSQN, VRC, and RMG performed the chemical analyses; KMC, DSB, LFV, RMG, and WCO contributed to the design and interpretation of the research and to the writing of the paper. All authors have read and approved the manuscript.

Correspondence to Wagner Campos Otoni.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

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

Communicated by Ali R. Alan.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Castro, K.M., Batista, D.S., Silva, T.D. et al. Water deficit modulates growth, morphology, and the essential oil profile in Lippia alba L. (Verbenaceae) grown in vitro. Plant Cell Tiss Organ Cult (2020). https://doi.org/10.1007/s11240-020-01766-w

Download citation

Keywords

  • Abiotic stress
  • Germacrene
  • Linalool
  • Polyethylene glycol