Effect of salinity on DNA methylation and antioxidant phenolic compounds of wild watercress (Rorippa nasturtium aquaticum)

Authors

  • Marcela Verónica Gutiérrez-Velázquez Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0001-7587-320X
  • Norma Almaraz-Abarca Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0003-1603-4865
  • José Antonio Ávila-Reyes Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0001-9552-957X
  • Eli Amanda Delgado-Alvarado Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0003-3835-9572
  • Laura Silvia González-Valdez Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0002-2644-2435
  • Rene Torres-Ricario Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0002-2523-6699
  • Hugo Manuel Monreal-García Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional unidad Durango, Instituto Politécnico Nacional, Durango 34220, México https://orcid.org/0000-0001-9001-8930
  • Dante Yamid Rojas-Barboza Family and Consumer Science, New Mexico State University, Las Cruces 88003, United States https://orcid.org/0000-0002-4218-1925
  • Andrés Vasavilbazo-Saucedo Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, Mazatlán 82000, México https://orcid.org/0009-0006-1720-9654

DOI:

https://doi.org/10.14719/pst.2577

Keywords:

watercress, methylation, metabolites, stress, phenolics, antioxidant

Abstract

Epigenetic changes are involved in plant responses to stress. Cytosine methylation is one of the most important epigenetic changes, regulating gene expression. In this paper, the MSAP (methylation-sensitive amplification polymorphism) method was used to find out how the watercress (Rorippa nasturtium aquaticum) genome changed in response to 0, 60, 80, and 100 mM NaCl and how that affected phenylalanine ammonium lyase (PAL) activity, phenolic content, and antioxidant capacity. The results showed an inverse correlation between methylation levels and PAL activity and the contents of total phenolics and flavonoids, indicating salt stress-induced reprogramming of the methylation pattern of watercress, which has a negative effect on the synthesis of phenolics. The results revealed a significant decrease in phenolic contents and antioxidant activity under low and moderate salinity compared to control and an increase under strong salinity compared to moderate salinity. The findings of this study contribute to our understanding of the reprogramming of DNA methylation under salinity and its effect on watercress phenolic metabolism.

Downloads

Download data is not yet available.

References

Rejeb IB, Pastor V, Mauch-Mani B. Plant responses to simultaneous biotic and abiotic stress: Molecular mechanisms. Plants. 2014;3:458-75. https://doi.org/10.3390/plants3040458

You J, Chan Z. ROS regulation during abiotic stress responses in crop plants. Front Plant Sci. 2015;6:1092. https://doi.org/10.3389/fpls.2015.01092

Dumanovic J, Nepovimova E, Natic M, Kuca K, Jacevic V. The significance of reactive oxygen species and antioxidant defense system in plants: A concise overview. Front Plant Sci. 2020;11:552969. https://doi.org/10.3389/fpls.2020.552969

Hasanuzzaman M, Bhuyan MHMB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of a universal defense regulator. Antioxidants. 2020;9:681. https://doi.org/10.3390/antiox9080681

Sapna H, Ashwini N, Ramesh S, Nataraja K. Assessment of DNA methylation pattern under drought stress using methylation-sensitive randomly amplified polymorphism analysis in rice. Plant Genet Resour: Characterization and Utilization. 2020;18:222-30. https://doi:10.1017/S1479262120000234

Sicilia A, Scialò E, Puglisi I, Lo Piero AR. Anthocyanin biosynthesis and DNA methylation dynamics in sweet orange fruit [Citrus sinensis L.(Osbeck)] under cold stress. J Agric Food Chem. 2020;68:7024-31. https://doi:10.1021/acs.jafc.0c02360

Lee HM, Park JS, Shin YH, Park YD. Alterations in DNA methylation patterns in regenerated Chinese cabbage (Brassica rapa ssp. pekinensis) plants derived from tissue culture. Hortic Environ Biotechnol. 2021;62:605-18. https://doi:10.1007/s13580-020-00310-1

Gallusci P, Dai Z, Génard M, Gauffretau A, Leblanc-Fournier N, Richard-Molard C et al. Epigenetics for plant improvement: Current knowledge and modeling avenues. Trends Plant Sci. 2017;22(7):610-23. http://dx.doi.org/10.1016/j.tplants.2017.04.009

Shahrajabian MH, Sun W, Cheng Q. DNA methylation as the most important content of epigenetics in traditional Chinese herbal medicine. J Med Plant Res. 2019;13:357-69. https://doi:10.5897/JMPR2019.6803

González-Benito ME, Ibáñez MÁ, Pirredda M, Mira S, Martín C. Application of the MSAP technique to evaluate epigenetic changes in plant conservation. Int J Mol Sci. 2020;21:7459. https://doi:10.3390/ijms21207459

Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PC. Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One. 2010;26:5(4):e10326. https://doi:10.1371/journal.pone.0010326

Kokhdan EP, Khodabandehloo H, Ghahremani H, Doustimotlagh AH. A narrative review on therapeutic potentials of watercress in human disorders. Evid Based Complement Alternat Med. 2021;7:5516450. https://doi:10.1155/2021/5516450

González-Elizondo M, López-Enríquez IL, González-Elizondo MS, Tena-Flores JA. Plantas medicinales del estado de durango y zonas aledañas. Instituto Politécnico Nacional–PROSIMA, México; 2004.

Timpano AJ, Zipper CE, Soucek DJ, Schoenholtz SH. Seasonal pattern of anthropogenic salinization in temperate forested headwater streams. Water Res. 2018;15:133:8-18. https://doi:10.1016/j.watres.2018.01.012

Ladwig R, Rock LA, Dugan HA. Impact of salinization on lake stratification and spring mixing. Limnol Oceanogr Lett. 2023;8:93-102. https://doi.org/10.1002/lol2.10215

Bartwal A, Mall R, Lohani P, Guru SK, Arora S. Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul. 2013;32:216-32. https://doi.org/10.1007/s00344-012-9272-x

Naikoo MI, Dar MI, Raghib F, Jaleel H, Ahmad B, Raina A et al. Role and regulation of plants phenolics in abiotic stress tolerance: An overview. In: Plant Signaling Molecules (Ed: Raina A). Academia. 2019;p. 157-68. doi: https://doi.org/10.1016/B978-0-12-816451-8.00009-5

Bharti P, Mahajan M, Vishwakarma AK, Bhardwaj J, Yadav SK. AtROS1 overexpression provides evidence for epigenetic regulation of genes encoding enzymes of flavonoid biosynthesis and antioxidant pathways during salt stress in transgenic tobacco. J Exp Bot. 2015;66:5959-69. https://doi:10.1093/jxb/erv304

Gutiérrez-Velázquez MV, Almaraz-Abarca N, Herrera-Arrieta Y, Ávila-Reyes JA, González-Valdez LS, Torres-Ricario R et al. Comparison of the phenolic contents and epigenetic and genetic variability of wild and cultivated watercress (Rorippa nasturtium var. aquaticum L.). Electron J Biotechnol. 2018;34:9-16. https://doi:10.1016/j.ejbt.2018.04.005

Skotti E, Anastasaki E, Kanellou G, Polissiou M, Tarantilis PA. Total phenolic content, antioxidant activity and toxicity of aqueous extracts from selected Greek medicinal and aromatic plants. Ind Crops Prod. 2014;53:46-54. https://doi:10.1016/j.indcrop.2013.12.013

Ordoñez AAL, Gomez JD, Vattuone MA, Isla MI. Antioxidant activities of Sechium edule (Jacq.) Swartz extracts. Food Chem. 2006;97:452-58. https://doi:10.1016/j.foodchem.2005.05.024

Anand T, Chandrasekaran A, Kuttalam S, Raguchander T, Prakasam V, Samiyappan R. Association of some plant defense enzyme activities with systemic resistance to early leaf blight and leaf spot induced in tomato plants by azoxystrobin and Pseudomonas fluorescens. J Plant Interact. 2007;2:233-44. https://doi:10.1080/17429140701708985

Medina-Medrano JR, Almaraz-Abarca N, González-Elizondo MS, Uribe-Soto JN, González-Valdez LS, Herrera-Arrieta Y. Phenolic constituents and antioxidant properties of five wild species of Physalis (Solanaceae). Bot Stud. 2015;56:24-37. https://doi:10.1186/s40529-015-0101-y

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med. 1999;6(9-10):1231-37. https://doi:10.1016/s0891-5849(98)00315-3

Chavan RR, Bhinge SD, Bhutkar MA, Randive DS, Wadkar GH, Todkar SS et al. Characterization, antioxidant, antimicrobial and cytotoxic activities of green synthesized silver and iron nanoparticles using alcoholic Blumea eriantha DC plant extract. Mater Today Commun. 2020;24:101320. https://doi.org/10.1016/j.mtcomm.2020.101320

Bhau BS, Gogoi G, Baruah D, Ahmed R, Hazarika G, Borah B et al. Development of an effective and efficient DNA isolation method for Cinnamomum species. Food Chem. 2015;188:264-70. https://doi:10.1016/j.foodchem.2015.05.004

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2021. https://www.R-project.org/

Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ. Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci. 2008;174:61-70. https://doi:10.1016/j.plantsci.2007.09.012

Yuan G, Wang X, Guo R, Wang Q. Effect of salt stress on phenolic compounds, glucosinolates, myrosinase and antioxidant activity in radish sprouts. Food Chem. 2010;121:1014-19. https://doi:10.1016/j.foodchem.2010.01.040

Valifard M, Mohsenzadeh S, Kholdebarin B, Rowshan V. Effects of salt stress on volatile compounds, total phenolic content and antioxidant activities of Salvia mirzayanii. S Afr J Bot. 2014;93:92-97. https://doi:10.1016/j.sajb.2014.04.002

Zhou Y, Tang N, Huang L, Zhao Y, Tang X, Wang K. Effects of salt stress on plant growth, antioxidant capacity, glandular trichome density and volatile exudates of Schizonepeta tenuifolia Briq. Int J Mol Sci. 2018;19:252. https://doi:10.3390/ijms19010252

Telesinski A, Nowak J, Smolik B, Dubowska A, Skrzypiec N. Effect of soil salinity on activity of antioxidant enzymes and content of ascorbic acid and phenols in bean (Phaseolus vulgaris L.) plants. J Elem. 2008;13:401-09.

Falcinelli B, Benincasa P, Calzuola I, Gigliarelli L, Lutts S, Marsili V. Phenolic content and antioxidant activity in raw and denatured aqueous extracts from sprouts and wheatgrass of einkorn and emmer obtained under salinity. Molecules. 2017;2:22(12):2132. https://doi:10.3390/molecules22122132

Monreal-García HM, Almaraz-Abarca N, Ávila-Reyes JA, Torres-Ricario R, González-Elizondo MS, Herrera-Arrieta Y. Phytochemical variation among populations of Fouquieria splendens Engelm. (Fouquieriaceae). Bot Sci. 2019;97(3):398-412. https://doi.org/10.17129/botsci.2191

Tuteja N, Gill SS, Tuteja R. Plant responses to abiotic stresses: Shedding light on salt, drought, cold and heavy metal stress. In: Tuteja N, Gill SS, Tuteja R, editors. Omics and Plant Abiotic Stress Tolerance. e-book, Bentham Science Publishers; 2011. p.39–61. https://doi:10.2174/97816080505811110101

Aymen S, Morena G, Vincenzo L, Laura P, Lorenza B, Abderrazak S et al. Salt tolerance of the halophyte Limonium delicatulum is more associated with antioxidant enzyme activities than phenolic compounds. Funct Plant Biol. 2016;43:607-19. https://doi:10.1071/FP15284

Hernández-Pacheco CE, Almaraz-Abarca N, Rojas-López M, Torres-Ricario R, Ávila-Reyes JA, González-Valdez LS et al. Salinity generates varying chemical and biochemical responses in Physalis ixocarpa (Solanaceae) during different times of exposure. Electron JBiotech. 2022;59:25-35. https://doi.org/10.1016/j.ejbt.2022.06.002

Farhadi N, Ghassemi-Golezani K. Physiological changes of Mentha pulegium in response to exogenous salicylic acid under salinity. Sci Hortic. 2020;267(1-8):109325. https://doi:10.1016/j.scienta.2020.109325

Gao S, Ouyang C, Wang S, Xu Y, Tang L, Chen F. Effects of salt stress on growth, antioxidant enzyme and phenylalanine ammonia-lyase activities in Jatropha curcas L. seedlings. Plant Soil Environ. 2008;54:374-81. https://doi:doi.org/10.17221/410-PSE

Gholizadeh A, Kohnehrouz BB. Activation of phenylalanine ammonia lyase as a key component of the antioxidative system of salt-challenged maize leaves. Brazilian J Plant Physiol. 2010;22:217-23. https://doi:10.1590/S1677-04202010000400001

Bahramikia S, Yazdanparast R. Antioxidant efficacy of Nasturtium officinale extracts using various in vitro assay systems. J Acupunct Meridian Stud. 2010;3:283-90. https://doi:10.1016/S2005-2901(10)60049-0

Rebey IB, Bourgou S, Rahali FZ, Msaada K, Ksouri R, Marzouk B. Relation between salt tolerance and biochemical changes in cumin (Cuminum cyminum L.) seeds. J Food Drug Anal. 2017;25:391-402. https://doi:10.1016/j.jfda.2016.10.001

Djenidi H, Khennouf S, Bouaziz A. Antioxidant activity and phenolic content of commonly consumed fruits and vegetables in Algeria. Prog Nutr. 2020;22:224-35. https://doi:10.23751/pn.v22i1.7701

Xu X, Li T, Li Y, Wang H. Variation of DNA cytosine methylation patterns among parent lines and reciprocal hybrids in hot pepper. Chem Eng Trans. 2015;46:1345-50. https://doi:10.3303/CET1546225

Tiwari JK, Saurabh S, Chandel P, Singh BP, Bhardwaj V. Analysis of genetic and epigenetic variation in in vitro propagated potato somatic hybrid by AFLP and MSAP marker. Electron J Biotech. 2013;16:6. https://doi:10.2225/vol16-issue6-fulltext-9

Sun M, Yang Z, Liu L, Duan L. DNA methylation in plant responses and adaption to abiotic stresses. Int J Mol Sci. 2022;23:6910. https://doi:10.3390/ijms23136910

Shan X, Wang X, Yang G, Wu Y, Su S, Li S, Liu H, Yuan Y. Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylation-sensitive amplified polymorphisms. J Plant Biol. 2013;56:32-38. https://doi:10.1007/s12374-012-0251-3

Akhter Z, Bi Z, Ali K, Sun C, Fiaz S, Haider FU, Bai J. In response to abiotic stress, DNA methylation confers epigenetic changes in plants. Plants. 2021;10:1096. https://doi:10.3390/plants10061096

Shi W, Hu X, Chen X, Ou X, Yang J, Geng Y. Increased population epigenetic diversity of the clonal invasive species Alternanthera philoxeroides in response to salinity stress. Genes Genet Syst. 2018;93:259-69. https://doi:10.1266/ggs.18-00039

Shahrajabian MH, Sun W, Cheng Q. DNA methylation as the most important content of epigenetics in traditional Chinese herbal medicine. J Med Plants Res. 2019;13:357-69. https://doi:10.5897/JMPR2019.6803

Published

20-10-2023 — Updated on 02-01-2024

Versions

How to Cite

1.
Gutiérrez-Velázquez MV, Almaraz-Abarca N, Ávila-Reyes JA, Delgado-Alvarado EA, González-Valdez LS, Torres-Ricario R, Monreal-García HM, Rojas-Barboza DY, Vasavilbazo-Saucedo A. Effect of salinity on DNA methylation and antioxidant phenolic compounds of wild watercress (Rorippa nasturtium aquaticum). Plant Sci. Today [Internet]. 2024 Jan. 2 [cited 2024 Nov. 21];11(1):196-205. Available from: https://horizonepublishing.com/journals/index.php/PST/article/view/2577

Issue

Section

Research Articles

Most read articles by the same author(s)

Similar Articles

You may also start an advanced similarity search for this article.