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Seasonal Changes in the Antioxidative Defence System of a Liverwort Dumortiera hirsuta

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Abstract

Liverworts are influenced by several ecological factors, such as photoperiod, temperature, precipitation, and nutrient availability. These factors vary in different seasons of the Indian calendar year, divisible into pre-monsoon (March–May), monsoon (June–August), post-monsoon (September–November), and fruiting (December–February) seasons. Seasonality causes disturbance in cellular homeostasis, which may trigger ROS formation. To restore the threshold level of ROS, liverworts must be equipped with complex antioxidant defence machinery. Thus, in this study, we analysed the effect of seasonal changes on oxidative stress markers [malondialdehyde (MDA) and total peroxide (H2O2 content)], total protein and pigment contents, and enzymatic and non-enzymatic antioxidants activities/contents in a liverwort, Dumortiera hirsuta, during its four distinct growing seasons. During the fruiting season, the results revealed the highest level of MDA and H2O2 with the lowest level during the pre-monsoon/monsoon seasons. The protein and pigment contents were maximal during the monsoon season and minimal during the fruiting season. With the exception of few [ascorbate peroxidase (APX) and ascorbic acid (ASC)], enzymatic [superoxide dismutase (SOD), catalase (CAT), and glutathione reductase (GR)] and non-enzymatic antioxidants (total thiol, proline, and carotenoids) activities/contents were correspondingly high during the fruiting season and low during the pre-monsoon/monsoon seasons, indicating their defensive role in neutralizing/suppressing the increased ROS during the fruiting season when the temperature was very low and the nutrient availability was less. These results therefore suggest that the antioxidative defence machinery plays a potential role in the adaptation of D. hirsuta against oxidative stress, naturally imposed by seasonal climatic changes.

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References

  • Aebi H (1984) Catalase in Vitro Meth Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Alam A (2012) Some Indian bryophytes known for their biologically active compounds. Int J Appl Biol Pharm 3:239–246

    Google Scholar 

  • Alam A, Tripathi A, Vats S, Behera KK, Sharma V (2011) In vitro antifungal efficacies of aqueous extract of Dumortiera hirsuta (Swaegr.) Nees against sporulation and growth of postharvest phytopathogenic fungi. Arch Bryol 103:1–9

    Google Scholar 

  • Anderson JV, Chevone BI, Hess JL (1992) Seasonal variation in the antioxidant system of eastern white pine needles: evidence for thermal dependence. Plant Physiol 98:501–508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angelcheva L, Mishra Y, Antii H, Kjellsen TD, Funk C, Strimbeck RG, Schröder WP (2014) Metabolomic analysis of extreme freezing tolerance in Siberian spruce (Picea obovata). New Phytol 204:545–555

    Article  CAS  PubMed  Google Scholar 

  • Aoussar N, Rhallabi N, Mhand RA, Manzali R, Bouksaim M, Douira A, Mellouki F (2020) Seasonal variation of antioxidant activity and phenolic content of Pseudevernia furfuracea, Evernia prunastri and Ramalina farinacea from Morocco. J Saudi Soc 19:1–6

    Google Scholar 

  • Asakawa Y (1984) Phytochemistry of Hepaticae: isolation of biologically active aromatic compounds and terpenoids. Ver Latinoam Quim 14:109–115

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Beckett RP, Minibayeva FV, Lüthje S, Böttger M (2004) Reactive oxygen species metabolism in desiccation-stressed thalli of the liverwort Dumortiera hirsuta. Physiol Plant 122:3–10

    Article  CAS  Google Scholar 

  • Bowman JL, Kohchi T, Yamato KT, Jenkins J et al (2017) Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:287–304

    Article  CAS  PubMed  Google Scholar 

  • Bradford M (1976) A rapid and sensitive method for the quantification of microgram of protein utilizing the principle of protein dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Chen Y, Zhang M, Chen T, Zhang Y, An L (2006) The relationship between seasonal changes in anti-oxidative system and freezing tolerance in the leaves of evergreen woody plants of Sabina. S Afr J Bot 72:272–279

    Article  Google Scholar 

  • de Kok LJ, Oosterhuis FA (1983) Effects of frost-hardening and salinity on glutathione and sulfhydryl levels and on glutathione reductase activity in spinach leaves. Physiol Plant 58:47–51

    Article  Google Scholar 

  • Dilks TJK, Proctor MCF (1976) Seasonal variation in desiccation tolerance in some British bryophytes. J Bryol 9:239–247

    Article  Google Scholar 

  • Feller U (2016) Drought stress and carbon assimilation in a warming climate: reversible and irreversible impacts. J Plant Physiol 203:84–94

    Article  CAS  PubMed  Google Scholar 

  • Forrest LL, Allen NS, Gudiño JA, Korpelainen H, Long DG (2011) Molecular and morphological evidence for distinct species in Dumortiera (Dumortieraceae). Bryologist 114:102–115

    Article  Google Scholar 

  • Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

    Article  CAS  Google Scholar 

  • Ghorbanli M, Amirkian TT, Niyakan M (2012) Seasonal changes in antioxidant activity, flavonoid, anthocyanin and phenolic compounds in Flavoparmelia caperata (L.) Hale and Physcia dubia (Hoffm.) Lettau from Babol forest sites in north of Iran. J Plant Physiol 2:461–469

    Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I Occurrence in higher plants. Plant Physiol 59:309–314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooijmaijers C (2008) Membrane integrity, oxidative damage and chlorophyll fluorescence during dehydration of the thalloid liverwort Monoclea forsteri Hook. J Bryol 30:217–222

    Article  Google Scholar 

  • Juurlink BH (1997) Response of glial cells to ischemia: roles of reactive oxygen species and glutathione. Neurosci Biobehav Rev 21:151–166

    Article  CAS  PubMed  Google Scholar 

  • Kapila S, Devi K, Rao A, Mahajan A (2014) Seasonal variations in carbohydrate, protein, free amino acids and enzyme activities in three species of Marchantiaceae. Lindbergia 37:85–89

    Article  Google Scholar 

  • Kaur S, Srivastava A, Kumar S, Srivastava V, Ahluwalia AS, Mishra Y (2019) Biochemical and proteomic analysis reveals oxidative stress tolerance strategies of Scenedesmus abundans against allelochemicals released by Microcystis aeruginosa. Algal Res 41:101525

    Article  Google Scholar 

  • Keller T, Schwager H (1977) Air pollution and ascorbic acid. Eur J Plant Pathol 7:338–350

    CAS  Google Scholar 

  • Körner C (2016) Plant adaptation to cold climates. F1000 Res 5:2769

    Article  Google Scholar 

  • Kumar SN, Singh CP (1996) Chlorophyll content in maize (Zea mays L.) leaves: physiological and seasonal variation. Indian J Plant Physiol 1:189–194

    CAS  Google Scholar 

  • Leelahawong C, Srisomsap C, Cherdshewasart W, Chokchaichamnankit D, Vinayavekhin N, Sangvanich P (2016) Comparative protein profiles of Butea superba tubers under seasonal changes. Mol Bio Rep 43:719–736

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Lim PO, Kim HJ, Gil Nam H (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Maillard A, Diquélou S, Billard V et al (2015) Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency. Front Plant Sci 6:317

    Article  PubMed  PubMed Central  Google Scholar 

  • Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193

    Article  CAS  Google Scholar 

  • McAllister CT, Robison HW, Davison PG (2019) Dumortier’s liverwort, Dumortiera hirsuta (Sw.) Nees (hepaticophyta: marchantiales: dumortieraceae) in Arkansas. J Ark Acad Sci 73:151–155

    Google Scholar 

  • Mishra Y, Bhargava P, Thapar R, Srivastava AK, Rai LC (2008) A comparative study of antioxidative defense system in the copper and temperature acclimated strains of Anabaena doliolum. World J Microbiol Biotechnol 24:2997

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Miyata I, Hosokawa T (1961) Seasonal variations of the photosynthetic efficiency and chlorophyll content of epiphytic mosses. Ecology 42:766–775

    Article  CAS  Google Scholar 

  • Nagalakshmi N, Prasad MNV (2001) Responses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmus bijugatus. Plant Sci 160:291–299

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Oliver MJ, Velten J, Wood AJ (2000) Bryophytes as experimental models for the study of environmental stress tolerance: Tortula ruralis and desiccation-tolerance in mosses. Plant Ecol 151:73–84

    Article  Google Scholar 

  • Peters K, Gorzolka K, Bruelheide H, Neumann S (2018) Seasonal variation of secondary metabolites in nine different bryophytes. Ecol Evol 8:9105–9117

    Article  PubMed  PubMed Central  Google Scholar 

  • Pitkin PH (1975) Variability and seasonality of the growth of some corticolous pleurocarpous mosses. J Bryol 8:337–356

    Article  Google Scholar 

  • Polle A, Morawe B (1995) Seasonal changes of the antioxidative systems in foliar buds and leaves of field grown beech trees (Fagus sylvatica, L.) in a stressful climate. Botan Acta 108:314–320

    Article  CAS  Google Scholar 

  • Pradhan R, Singh N, Singh RP (2019) Onset of summer monsoon in Northeast India is preceded by enhanced transpiration. Sci Rep 9:1–11

    Article  Google Scholar 

  • Reski R (2018) Enabling the water-to-land transition . Nat Plants 4:67–68

    Article  CAS  PubMed  Google Scholar 

  • Sagisaka S (1976) The occurrence of peroxide in a perennial plant, Populus gelrica. Plant Physiol 57:308–309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sathish SS, Kavitha R, Kumar SS (2013) Bryophytes in India-the current status. Int J Res Eng Biosci 1:23

    Google Scholar 

  • Schaedle M, Bassham JA (1977) Chloroplast glutathione reductase. Plant Physiol 59:1011–1012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205

    Article  CAS  PubMed  Google Scholar 

  • Sen S, Mukherji S (1998) Seasonal effects on nitrogenous compounds in two crop plants. Environ Ecol 16:871–874

    Google Scholar 

  • Shao HB, Chu LY, Jaleel CA, Zhao CX (2008) Water-deficit stress-induced anatomical changes in higher plants. Comptes Rendus Biol 331:215–225

    Article  Google Scholar 

  • Shaw J, Renzaglia K (2004) Phylogeny and diversification of bryophytes. Am J Bot 91:1557–1581

    Article  PubMed  Google Scholar 

  • Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219

    Article  CAS  PubMed  Google Scholar 

  • Singh SK (2017) Liverwort and hornwort diversity in botanic gardens of Botanical survey of India, Shillong and Barapani. In: Singh P, dash SS (eds) Indian Botanic Gardens Role in conservation. BSI Kolkata, pp 248–259

  • Singh SK, Kumar S (2016) A preliminary study on liverworts and hornworts of Tripura, North-East India. Nelumbo 58:130–151

    Article  Google Scholar 

  • Sivaci A, Duman S (2014) Evaluation of seasonal antioxidant activity and total phenolic compounds in stems and leaves of some almond (Prunus amygdalus L.) varieties. Biol Res 47:1–5

    Article  CAS  Google Scholar 

  • Sývacý A, Sökmen M (2004) Seasonal changes in antioxidant activity, total phenolic and anthocyanin constituent of the stems of two Morus species (Morus alba L. and Morus nigra L.). Plant Growth Regul 44:251–256

    Article  CAS  Google Scholar 

  • Thakur S, Kapila S (2017) Seasonal changes in antioxidant enzymes, polyphenol oxidase enzyme, flavonoids and phenolic content in three leafy liverworts. Lindbergia 40:39–44

    Article  Google Scholar 

  • Vertuani S, Angusti A, Manfredini S (2004) The antioxidants and pro-antioxidants network: an overview. Curr Pharm Des 10:1677–1694

    Article  CAS  PubMed  Google Scholar 

  • Vuleta A, Manitašević Jovanović S, Šešlija D, Tucić B (2010) Seasonal dynamics of foliar antioxidative enzymes and total anthocyanins in natural populations of Iris pumila L. J Plant Ecol 3:59–69

    Article  Google Scholar 

  • Yadav S, Srivastava A, Biswas S, Chaurasia N, Singh SK, Kumar S, Srivastava V, Mishra Y (2020) Comparison and optimization of protein extraction and two-dimensional gel electrophoresis protocols for liverworts. BMC Res Notes 13:1–7

    Article  CAS  Google Scholar 

  • Yamane Y, Hayashi T (2006) Evaluation of environmental conditions for the formation of severe local storms across the Indian subcontinent. Geophys Res Lett 33:L17806

    Article  Google Scholar 

  • Zhang X, Zhao Y, Wang S (2017) Responses of antioxidant defense system of epilithic mosses to drought stress in karst rock desertified areas. Acta Geochim 36:205–212

    Article  CAS  Google Scholar 

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Acknowledgements

Ms. Sandhya Yadav is thankful to University Grant Commission (UGC), New Delhi, India, for senior research fellowship (SRF). Ms. Akanksha Srivastava is thankful to the Department of Science and Technology-Innovation of Science Pursuit for Inspire Research (DST–INSPIRE) fellowship, New Delhi, India. Mr. Subhankar Biswas is thankful to Council of Scientific and Industrial Research (CSIR), New Delhi, India for SRF. The authors are thankful to thank the Head and the Programme Coordinator (CAS) in Botany and Interdisciplinary School of Life Science (ISLS), Universities with Potential for Excellence (UPE) of UGC, at Banaras Hindu University, Varanasi, India, for providing instrumental facilities.

Funding

This research work was supported by the UGC start-up (grant number F.30–86/2014-BSR), New Delhi, India.

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SY, SKS, and YM conceived the idea and designed the experiments; SY, AS, and S. Biswas conducted the experiments; and SY, AS, S. Biswas, S. Basu, SKS, and YM analysed the data and wrote the manuscript.

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Correspondence to Yogesh Mishra.

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Yadav, S., Srivastava, A., Biswas, S. et al. Seasonal Changes in the Antioxidative Defence System of a Liverwort Dumortiera hirsuta. J Plant Growth Regul 41, 1265–1275 (2022). https://doi.org/10.1007/s00344-021-10379-2

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