Skip to main content

Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism

Protoplasma volume 251, pages 1007–1019 (2014)Cite this article

Abstract

We investigated the influence of exogenously sourced ethylene (200 μL L−1 ethephon) in the protection of photosynthesis against 200 mg kg−1 soil each of nickel (Ni)- and zinc (Zn)-accrued stress in mustard (Brassica juncea L.). Plants grown with Ni or Zn but without ethephon exhibited increased activity of 1-aminocyclopropane carboxylic acid synthase, and ethylene with increased oxidative stress measured as H2O2 content and lipid peroxidation compared with control plants. The oxidative stress in Ni-grown plants was higher than Zn-grown plants. Under metal stress, ethylene protected photosynthetic potential by efficient PS II activity and through increased activity of ribulose-1,5-bisphosphate carboxylase and photosynthetic nitrogen use efficiency (P-NUE). Application of 200 μL L−1 ethephon to Ni- or Zn-grown plants significantly alleviated toxicity and reduced the oxidative stress to a greater extent together with the improved net photosynthesis due to induced activity of ascorbate peroxidase and glutathione (GSH) reductase, resulting in increased production of reduced GSH. Ethylene formation resulting from ethephon application alleviated Ni and Zn stress by reducing oxidative stress caused by stress ethylene production and maintained increased GSH pool. The involvement of ethylene in reversal of photosynthetic inhibition by Ni and Zn stress was related to the changes in PS II activity, P-NUE, and antioxidant capacity was confirmed using ethylene action inhibitor, norbornadiene.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology, 2nd edn. Academic, San Diego

    Google Scholar 

  • Avni A, Bailey BA, Mattoo AK, Anderson JD (1994) Induction of ethylene biosynthesis in Nicotiana tabacum by a Trichoderma viridae xylanase is correlated to the accumulation of 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase transcripts. Plant Physiol 106:1049–1055

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Baker NR, Rosenquist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621

    CAS  PubMed  Article  Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    CAS  PubMed  Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of proteins utilising the principle of protein-dye binding. Anal Biochem 72:248–254

    CAS  PubMed  Article  Google Scholar 

  • Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. CLEAN-Soil Air Water 37:304–313

    CAS  Article  Google Scholar 

  • Chen JW, Zhang Q, Li XS, Cao KF (2011) Steady and dynamic photosynthetic responses of seedlings from contrasting successional groups under low-light growth conditions. Physiol Plant 141:84–95

    CAS  PubMed  Article  Google Scholar 

  • Cui Y, Zhao N (2011) Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant Soil Environ 57:34–39

    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 dismutase and catalase. J Exp Bot 32:93–101

    CAS  Article  Google Scholar 

  • Fiorani F, Bogemann GM, Visser EJW, Lambers H, Voesenek LACJ (2002) Ethylene emission and responsiveness to applied ethylene vary among Poa species that inherently differ in leaf elongation rates. Plant Physiol 129:1382–1390

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25

    CAS  PubMed  Article  Google Scholar 

  • Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Gajewska E, Skłodowska M (2005) Antioxidative responses and proline level in leaves and roots of pea plants subjected to nickel stress. Acta Physiol Plant 27:329–339

    CAS  Google Scholar 

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

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Gratao PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal-stressed plants a little easier. Funct Plant Biol 32:481–494

    CAS  Article  Google Scholar 

  • Griffith OW (1980) Determination of glutathione disulphide using glutathione reductase and 2 vinylpyridine. Anal Biochem 106:207–212

    CAS  PubMed  Article  Google Scholar 

  • Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard. J Exp Bot 62:4955–4963

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Iqbal N, Nazar R, Khan MIR, Khan NA (2012) Variation in photosynthesis and growth of mustard cultivars: role of ethylene sensitivity. Sci Hortic 135:1–6

    CAS  Article  Google Scholar 

  • Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA (2013) Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 73:128–138

    CAS  PubMed  Google Scholar 

  • Ivanov YV, Savochkin YV, Kuznetsov VV (2012) Scots pine as a model plant for studying the mechanisms of conifers adaptation to heavy metal action: 2. Functioning of antioxidant enzymes in pine seedlings under chronic zinc action. Russ J Plant Physiol 59:50–58

    CAS  Google Scholar 

  • Kanwar MK, Bhardwaj R, Chowdhary SP, Arora P, Sharma P, Kumar S (2013) Isolation and characterization of 24-epibrassinolide from Brassica juncea L. and its effects on growth, Ni ion uptake, antioxidant defense of Brassica plants and in vitro cytotoxicity. Acta Physiol Plant 35:1351–1362

    CAS  Google Scholar 

  • Khan NA (2004a) An evaluation of the effects of exogenous ethephon, an ethylene releasing compound, on photosynthesis of mustard (Brassica juncea) cultivars that differ in photosynthetic capacity. BMC Plant Biol 4:21

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Khan NA (2004b) Activity of 1-aminocyclopropane carboxylic acid synthase in two mustard (Brassica juncea L.) cultivars differing in photosynthetic capacity. Photosynthetica 42:477–480

    CAS  Article  Google Scholar 

  • Khan NA, Mir MR, Nazar R, Singh S (2008) The application of ethephon (an ethylene releaser) increases growth, photosynthesis and nitrogen accumulation in mustard (Brassica juncea L.) under high nitrogen levels. Plant Biol 10:534–538

    CAS  PubMed  Article  Google Scholar 

  • Khan MIR, Iqbal N, Masood A, Per TS, Khan NA (2013) Salicylic acid alleviates adverse effects of heat stress on photosynthesis through changes in proline production and ethylene formation. Plant Signal Behav 8(11):e26374

    PubMed Central  PubMed  Article  Google Scholar 

  • Khudsar T, Mahmooduzzafar IM, Sairam RK (2004) Zinc-induced changes in morpho-physiological and biochemical parameters in Artemisia annua. Biol Plant 48:255–260

    CAS  Article  Google Scholar 

  • Klee HJ (2004) Ethylene signal transduction. Moving beyond Arabidopsis. Plant Physiol 135:660–667

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Krall JP, Edwards GE (1992) Relationship between photosystem II activity and CO2 fixation in leaves. Physiol Plant 86:180–187

    CAS  Article  Google Scholar 

  • Kuo TM, Warner RL, Kleinhofs A (1982) In vitro stability of nitrate reductase from barley leaves. Phytochemistry 21:531–533

    CAS  Article  Google Scholar 

  • Larbi A, Abadía A, Morales F, Abadía J (2004) Fe resupply to Fe-deficient sugar beet plants leads to rapid changes in the violaxanthin cycle and other photosynthetic characteristics without significant de novo chlorophyll synthesis. Photosynth Res 79:59–69

    CAS  PubMed  Article  Google Scholar 

  • Li S, Yang W, Yang T, Chen Y, Ni W (2013) Effects of cadmium stress on leaf chlorophyll fluorescence and photosynthesis of Elsholtzia argyi—a cadmium accumulating plant. Int J Phyto. doi:10.1080/15226514.2013.828020

    Google Scholar 

  • Lindner RC (1944) Rapid analytical methods for some of the more common inorganic constituents of plant tissues. Plant Physiol 19:70–89

    Google Scholar 

  • Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29:177–187

    CAS  Google Scholar 

  • Malik A (2004) Metal bioremediation through growing cells. Environ Int 30:261–278

    CAS  PubMed  Article  Google Scholar 

  • Masood A, Iqbal N, Khan NA (2012) Role of ethylene in alleviation of cadmium-induced photosynthetic capacity inhibition by sulphur in mustard. Plant Cell Environ 35:524–533

    CAS  PubMed  Article  Google Scholar 

  • Maxwell K, Johnson G (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    CAS  PubMed  Article  Google Scholar 

  • McLaughlin MJ, Parker DR, Clarke JM (1999) Metals and micronutrients—food safety issues. Field Crop Res 60:143–163

    Article  Google Scholar 

  • Mobin M, Khan NA (2007) Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. J Plant Physiol 164:601–610

    CAS  PubMed  Article  Google Scholar 

  • Nakagawa H, Poulle M, Oaks A (1984) Characterization of nitrate reductase from corn leaves (Zea mays cv. W64A × W182E). Plant Physiol 75:285–289

    CAS  PubMed Central  PubMed  Article  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 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249–279

    CAS  PubMed  Google Scholar 

  • Noctor G, Mhamdi A, Chaouch S, Han Y, Neukermans J, Marquez-Garcia B, Queval G, Foyer CH (2012) Glutathione in plants: an integrated overview. Plant Cell Environ 35:454–484

    CAS  PubMed  Article  Google Scholar 

  • Okuda T, Matsuda Y, Yamanaka A, Sagisaka S (1991) Abrupt increase in the level of hydrogen peroxide in leaves of winter wheat is caused by cold treatment. Plant Physiol 97:1265–1267

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Pallas JE, Kays SJ (1982) Inhibition of photosynthesis by ethylene: a stomatal effect. Plant Physiol 70:598–601

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Pell EJ, Schlagnhaufer CD, Arteca RN (1997) Ozone-induced oxidative stress: mechanisms of action and reaction. Physiol Plant 100:264–273

    CAS  Article  Google Scholar 

  • Perata P, Voesenek LA (2007) Submergence tolerance in rice requires Sub1A, an ethylene response-factor-like gene. Trends Plant Sci 12:43–46

    CAS  PubMed  Article  Google Scholar 

  • Pierik R, Tholen D, Poorter H, Visser EJW, Voesenek LACJ (2006) The Janus face of ethylene: growth inhibition and stimulation. Trends Plant Sci 11:176–183

    CAS  PubMed  Article  Google Scholar 

  • Prasad SM, Dwivedi R, Zeeshan M (2005) Growth, photosynthetic electron transport, and antioxidant responses of young soybean seedlings to simultaneous exposure of nickel and UV-B stress. Photosynthetica 43:177–185

    CAS  Article  Google Scholar 

  • Sarvari E (2005) Effects of heavy metals on chlorophyll-protein complexes in higher plants: Causes and consequences. In: Pessarakli M (ed) Handbook of photosynthesis. CRC Press, Boca Raton, pp 865–888

    Google Scholar 

  • Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277

    CAS  Google Scholar 

  • Shangguan Z, Shao M, Dyckmans J (2000) Effects of nitrogen nutrition and water deficit on net photosynthetic rate and chlorophyll fluorescence in winter wheat. J Plant Physiol 156:46–51

    CAS  Article  Google Scholar 

  • Shaw BP, Sahu SK, Mishra RK (2004) Heavy metal induced oxidative damage in terrestrial plants. In: Prasad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystems. Narosa Publishing House, New Delhi, pp 84–126

    Chapter  Google Scholar 

  • Shikazono N, Zakir HM, Sudo Y (2008) Zinc contamination in river water and sediments at Taisyu Zn–Pb mine area, Tsushima Island, Japan. J Geochem Explor 98:80–88

    CAS  Article  Google Scholar 

  • Sytar O, Kumar A, Latowski D, Kuczynska P, Strzałka K, Prasad MNV (2013) Heavy metal-induced oxidative damage, defense reactions, and detoxification mechanisms in plants. Acta Physiol Plant 35:985–999

    CAS  Google Scholar 

  • Tholen D, Pons TL, Voesenek LACJ, Poorter H (2007) Ethylene insensitivity results in the down-regulation of Rubisco expression and photosynthetic capacity in tobacco. Plant Physiol 144:1305–1315

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Tsonev T, Lidon FJC (2012) Zinc in plants—an overview. Emir J Food Agric 24:322–333

    Google Scholar 

  • Usuda H (1985) The activation state of ribulose 1,5-bisphosphate carboxylase in maize leaves in dark and light. Plant Cell Physiol 91:455–463

    Google Scholar 

  • Vaillant N, Monnet F, Hitmi A, Sallanon H, Coudret A (2005) Comparative study of responses in four Datura species to a zinc stress. Chemosphere 59:1005–1013

    CAS  PubMed  Article  Google Scholar 

  • Ventrella A, Catucci L, Piletska E, Piletsky S, Agostiano A (2011) Interactions between heavy metals and photosynthetic materials studied by optical techniques. Bioelectrochemistry 77:19–25

    Article  Google Scholar 

  • Verstraeten S, Aimo L, Oteiza P (2008) Aluminium and lead: molecular mechanisms of brain toxicity. Arch Toxicol 82:789–802

    CAS  PubMed  Article  Google Scholar 

  • Von Cammerer S, Farquhar GD (1981) Some relationship between the biochemistry of photosynthesis and the gas exchange of leaves. Planta 153:376–387

    Article  Google Scholar 

  • Wi SJ, Jang SJ, Park KY (2010) Inhibition of biphasic ethylene production enhances tolerance to abiotic stress by reducing the accumulation of reactive oxygen species in Nicotiana tabacum. Mol Cells 30:37–49

    CAS  PubMed  Article  Google Scholar 

  • Wise RR, Naylor AW (1988) Stress ethylene does not originate directly from lipid peroxidation during chilling-enhanced photooxidation. J Plant Physiol 133:62–66

    CAS  Article  Google Scholar 

  • Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis mutants that overproduce ethylene are affected in the post-transcriptional regulation of 1-aminocyclopropane-1-carboxylic synthase. Plant Physiol 30:81–86

    Google Scholar 

  • Yoshida S, Tamaoki M, Ioki M, Ogawa D, Sato Y, Aono M, Kubo A, Saji S, Saji H, Satoh S, Nakajima N (2009) Ethylene and salicylic acid control glutathione biosynthesis in ozone-exposed Arabidopsis thaliana. Physiol Plant 136:284–298

    CAS  PubMed  Article  Google Scholar 

  • Zhang W, Wen CK (2010) Preparation of ethylene gas and comparison of ethylene responses induced by ethylene, ACC, and ethephon. Plant Physiol Biochem 48:45–53

    PubMed  Google Scholar 

  • Zhang W, Hu W, Wen CK (2010) Ethylene preparation and its application to physiological experiments. Plant Signal Behav 5:453–457

    CAS  PubMed Central  PubMed  Article  Google Scholar 

Download references

Acknowledgments

The first author gratefully acknowledges the award of Moulana Azad National Fellowship by the University Grants Commission, New Delhi.

Conflict of interest

There is no conflict of interest.

Author information

Affiliations

  1. Plant Physiology and Biochemistry Section, Department of Botany, Aligarh Muslim University, Aligarh, 202 002, India

    M. Iqbal R. Khan & Nafees A. Khan

Authors
  1. M. Iqbal R. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nafees A. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nafees A. Khan.

Additional information

Handling Editor: Bhumi Nath Tripathi

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Khan, M.I.R., Khan, N.A. Ethylene reverses photosynthetic inhibition by nickel and zinc in mustard through changes in PS II activity, photosynthetic nitrogen use efficiency, and antioxidant metabolism. Protoplasma 251, 1007–1019 (2014). https://doi.org/10.1007/s00709-014-0610-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-014-0610-7

Keywords

  • Antioxidant system
  • Ethylene
  • Nickel
  • Photosynthetic-NUE
  • PS II activity
  • Zinc