Skip to main content
SpringerLink
Log in

Modulation of antioxidant enzymes in Juniperus procera needles in relation to habitat environment and dieback incidence

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Oxidative stress and the antioxidant enzymes’ activity are higher in damaged than in healthy Juniperus procera trees, in summer than in winter, and in dry than in wet condition.

Abstract

Many of the small stands of Juniperus procera in Saudi Arabia, confined mainly to Aseer Mountains in the southern part of the country, are suffering from branch dieback. As a part of the project on the structural and functional responses of healthy and dieback-affected trees to local environmental conditions of Al-Ghalab, Al-Yazeed, and Saodah locations, this study quantifies the oxidative stress generated and the consequent modulation of proline accumulation and antioxidant enzymes’ activity, as determined by chemical analysis of needle tissues from samples collected in summer and winter seasons. The level of TBARS, which indicated the extent of oxidative stress, was minimum (10.1 nM g−1 f w) at Al-Ghalab and maximum (28.1 nM g−1 f w) at Al-Yazeed, being relatively higher in summer than in winter. Healthy trees had a lower level of TBARS than those suffering from dieback. Proline content showed 147–54 µg g−1 in healthy trees and 460–99 µg g−1 f w in affected ones. Variation in the activity of superoxide dismutase, ascorbate peroxidase, glutathione reductase, and catalase was around 0.7–3.6, 0.01–0.09, 0.02–0.08, and 0.6–3.0 U mg−1 min−1, respectively, in healthy trees, whereas 2.3–6.1, 0.04–0.3, 0.04–0.3, and 2–5.8 U mg−1 min−1, respectively, in the dieback-affected trees of the different locations. Thus, the oxidative stress and the enzymatic stimulation were higher in damaged than in healthy trees and in summer than in winter season. Water-harvesting efforts at the collection sites showed ameliorative effects. Our observations suggest that J. procera tree can be made more tolerant toward stressful condition, and even the risk of dieback can be avoided or minimized by improving soil–water availability through adequate water-harvesting strategies in the drought-affected areas.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

DDW:

Double distilled water

EDTA:

Ethylene-diamine-tetra-acetic acid

GR:

Gluththione reductase

GSSG:

Glutathione disulfide

ROS:

Reactive oxygen species

TBARS:

Thiobarbituric acid reactive substances

TCA:

Trichloroethanoic acid

References

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  PubMed  Google Scholar 

  • Al-Ghamdi AAM, Jais HM (2012) Study of Juniperus procera and arbuscular mycorhizal fungi (AMF) in Saudi Arabia. Int J Adv Biol Res 2(2):177–183

    Google Scholar 

  • Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Gonzales P, Hogg T, Rigling A, Breshears D et al (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684

    Article  Google Scholar 

  • Anjum NA, Umar S, Iqbal M, Khan NA (2008) Growth characteristics and antioxidant metabolism of mungbean genotypes differing in photosynthetic capacity subjected to water deficit stress. J Plant Interact 3:127–136

    Article  CAS  Google Scholar 

  • Anjum NA, Ahmad I, Mohmood I, Pacheco M, Duarte AC, Pereira E, Umar S, Ahmad A, Khan NA, Iqbal M, Prasad MNV (2012) Modulation of glutathione and its related enzymes in plants’ responses to toxic metals and metalloids—a review. Environ Exp Bot 75:307–324

    CAS  Google Scholar 

  • Anjum NA, Aref IA, Pereira E, Ahmad A, Iqbal M (2014) Glutathione and proline can coordinately make plants withstand the joint attack of osmotic and metal(loid) stresses. Front Plant Sci 5(662):4. doi:10.3389/fpls.2014.00662

    Google Scholar 

  • Anjum NA, Sofo A, Scopa A, Roychoudhury A, Gill SS, Iqbal M, Lukatkin AS, Pereira E, Duarte AC, Ahmad I (2015) Lipids and proteins—major targets of oxidative modifications in abiotic stressed plants. Environ Sci Pollut Res 22:4099–4121. doi:10.1007/s11356-014-3917-1

    Article  CAS  Google Scholar 

  • Anonymous (2011) Methods manual. Soil testing in India. Ministry of Agriculture, Govt of India, New Delhi

  • Aref MI, Ahmed AI, Khan PR, El-Atta H, Iqbal M (2013a) Drought-induced adaptive changes in the seedling anatomy of Acacia ehrenbergiana and Acacia tortilis subsp. raddiana. Trees Struct Funct 27(4):959–971. doi:10.1007/s00468-013-0848-2

    Article  Google Scholar 

  • Aref IM, El-Atta H, Al-Shahrani T, Alazba A, Ahmed AI (2013b) Evaluation of the physiological and growth response of Juniperus procera Hochst. ex Endlicher to some types of microcatchments. Int J Plant Anim Environ Sci 3(1):234–241

    Google Scholar 

  • Aref MI, El-Atta H, El-Obeid M, Ahmed AI, Khan PR, Iqbal M (2013c) Effect of water stress on relative water and chlorophyll contents of Juniperus procera Hochst. ex Endlicher in Saudi Arabia. Life Sci J 10(4):681–685

    Google Scholar 

  • Aref MI, Khan PR, Al-Mefarrej H, Al-Shahrani T, Ahmed AI, Iqbal M (2014) Cambial periodicity and wood production in Acacia ehrenbergiana Hayne growing on dry sites of Saudi Arabia. J Environ Biol 35(2):301–310

    PubMed  Google Scholar 

  • Arshi A, Ahmad A, Aref IM, Iqbal M (2010) Effect of calcium against salinity-induced inhibition in growth, ion accumulation and proline contents in Cichorium intybus L. J Environ Biol 31:939–944

    CAS  PubMed  Google Scholar 

  • Arshi A, Ahmad A, Aref IM, Iqbal M (2012) Comparative studies on antioxidant enzyme action and ion accumulation in soybean cultivars under salinity stress. J Environ Biol 33:9–20

    CAS  PubMed  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51(2):163–190

    Article  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 

  • Bhattacharjee S (2012) The language of reactive oxygen species signaling in plants. J Bot 2012:22. doi:10.1155/2012/985298

    Google Scholar 

  • Bloedner C, Majcherczyk A, Kues U, Polle A (2007) Early drought-induced changes to the needle proteome of Norway spruce. Tree Physiol 27:1423–1431

    Article  CAS  Google Scholar 

  • Cakmak I, Horst J (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 

  • Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Environ Sci 2(53):13. doi:10.3389/fenvs.2014.00053

    Google Scholar 

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence correlated with increased level of membrane permeability, lipid peroxidation and decreased level of SOD and CAT. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • El-Atta H, Aref IM (2010) Effect of terracing on rainwater harvesting and growth of Juniperus procera Hochst ex Endlicher. Int J Environ Sci Technol 7(1):59–66

    Article  Google Scholar 

  • Favaretto VF, Martinez CA, Soriani HH, Furriel RPM (2011) Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions. Environ Exp Bot 70:20–28

    Article  CAS  Google Scholar 

  • Fink T (2011) Signal transduction by reactive oxygen species. J Cell Biol 194(1):7–15

    Article  Google Scholar 

  • Foyer CH, Noctor G (2003) Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119:355–364

    Article  CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016

    Article  CAS  PubMed  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signalling networks. Front Plant Sci 5:art 151:10. doi:10.3389/fpls.2014.00151

    Google Scholar 

  • Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: Physiological, biochemical and molecular characterization. Int J Genom. doi:10.1155/2014/701596 (Art. ID 701596)

    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 7:11. doi:10.4161/psb.21949

    Google Scholar 

  • Impa SM, Nadaradjan S, Jagadish SVK (2012) Drought stress induced reactive oxygen species and antioxidants in plants. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, pp 131–147

    Chapter  Google Scholar 

  • Iqbal M, Bano R, Wali B (2005) Plant growth responses to air pollution. In: Chaturvedi SN, Singh KP (eds) Plant biodiversity, microbial interaction and environmental biology. Avishkar Publishers, Jaipur, pp 166–188

    Google Scholar 

  • Iqbal M, Mahmooduzzafar, Aref IM, Khan PR (2010) Behavioural responses of leaves and vascular cambium of Prosopis cineraria (L.) Druce to different regimes of coal-smoke pollution. J Plant Interact 5(2):117–133

    Article  CAS  Google Scholar 

  • Iqbal M, Ahmad A, Ansari MKA, Qureshi MI, Aref MI, Khan PR, Hegazy SS, El-Atta H, Husen A, Hakeem KR (2015) Improving the phytoextraction capacity of plants to scavenge metal(loid)-contaminated sites. Environ Rev 23(1):44–65. doi:10.1139/er-2014-0043

    Article  CAS  Google Scholar 

  • Jabeen R, Ahmad A, Iqbal M (2009) Phytoremediation of heavy metals: physiological and molecular aspects. Bot Rev 75:339–364

    Article  Google Scholar 

  • Jackson ML (1967) Soil chemical analysis, 7th edn. Prentice Hall (India) Pvt Ltd, New Delhi, p 498

    Google Scholar 

  • Lee BR, Li LS, Jung WJ, Jin YLJC, Avice JC, Ourry A, Kim TH (2009) Water deficit-induced oxidative stress and the activation of antioxidant enzymes in white clover leaves. Biol Plant 53:505–510

    Article  Google Scholar 

  • Mantry N, Patade V, Penna S, Ford R, Pang E (2012) Abiotic stress responses in plants: present and future. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, pp 1–19

    Chapter  Google Scholar 

  • Mendrey KJ (2013) Metal response of Douglas-fir: a comparison of foliar metals and phytochelatin production in trees planted in soils amended with biosolids or metal salts. MS Thesis, University of Washington, USA, p 185

  • Miller GAD, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 35:299–319

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • NCWCD, JICA (2006) The management plan for conservation of juniper woodlands. The Final Report of the joint study of National Commission of Wildlife Conservation and Development (NCWCD) and Japan International Cooperation Agency (JICA). pp 142 + 2 appendices

  • Qureshi MI, Israr M, Abdin MZ, Iqbal M (2005) Responses of Artemisia annua L. to lead and salt-induced oxidative stress. Environ Exp Bot 53:185–193

    Article  CAS  Google Scholar 

  • Qureshi MI, Abdin MZ, Qadir S, Iqbal M (2007) Lead-induced oxidative stress and metabolic alterations in Cassia angustifolia Vahl. Biol Plant 51:121–128

    Article  CAS  Google Scholar 

  • Qureshi MI, Abdin MZ, Ahmad J, Iqbal M (2013) Effect of long-term salinity on cellular antioxidants, compatible solute and fatty-acid profile of Sweet annie (Artemisia annua L.). Phytochemistry 95:215–223

    Article  CAS  PubMed  Google Scholar 

  • Rao MV (1992) Cellular detoxification mechanisms to determine age dependent injury in tropical plant exposed to SO2. J Plant Physiol 140:737–740

    Article  Google Scholar 

  • Sahu S, Das P, Ray M, Sabat SC (2010) Osmolyte-modulated enhanced rice leaf catalase activity under salt stress. Adv Biosci Biotechnol 1:39–46

    Article  CAS  Google Scholar 

  • Spano C, Bruno M, Bottega S (2013) Calystegia soldanella: dune versus laboratory plants to highlight key adaptive physiological traits. Acta Physiol Plant 35(4):1329–1336

    Article  CAS  Google Scholar 

  • Subbaiah BV, Asija GL (1956) A rapid procedure for determination of available nitrogen in soils. Curr Sci 25:259–260

    Google Scholar 

  • Suzuki N, Koussevitzky S, Mittler R, Miller G (2012) ROS and redox signaling in the response of plants to abiotic stress. Plant Cell Environ 35:259–270

    Article  CAS  PubMed  Google Scholar 

  • Sweetlove LJ, Moller IM (2009) Oxidation of proteins in plants—mechanisms and consequences. Adv Bot Res 52:1–23

    Article  CAS  Google Scholar 

  • Watanabe FS, Olsen SR (1965) Test of an ascorbic acid method for determining P in water and NaHCO3 extract from soil. Soil Sci Soc Am Proc 29:677–678

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Financial support provided by the National Plan for Sciences, Technology and Innovation, Saudi Arabia, for sponsoring this study under the research project #10-AGRI 1310-02 is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Department of Plant Production, College of Food and Agricultural Sciences, King Saud University, Post Box 2460, Riyadh, 11451, Saudi Arabia

    Ibrahim M. Aref, Pervaiz R. Khan, Hashim El-Atta & Abdalla I. Ahmed

  2. Department of Botany and Microbiology, College of Science, King Saud University, Post Box 2455, Riyadh, 11451, Saudi Arabia

    Salim Khan

  3. Department of Botany, Faculty of Science, Jamia Hamdard, Hamdard Nagar, New Delhi, 110062, India

    Muhammad Iqbal

Authors
  1. Ibrahim M. Aref
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pervaiz R. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Salim Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hashim El-Atta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abdalla I. Ahmed
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Muhammad Iqbal
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muhammad Iqbal.

Ethics declarations

Conflict of interest

The authors have no conflict of interest.

Additional information

Communicated by W. Bilger.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aref, I.M., Khan, P.R., Khan, S. et al. Modulation of antioxidant enzymes in Juniperus procera needles in relation to habitat environment and dieback incidence. Trees 30, 1669–1681 (2016). https://doi.org/10.1007/s00468-016-1399-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-016-1399-0

Keywords

Search

Navigation