Skip to main content
SpringerLink
Log in

Roles of exogenous glutathione in antioxidant defense system and methylglyoxal detoxification during salt stress in mung bean

  • Original Papers
  • Published:
Biologia Plantarum

Abstract

The protective roles of glutathione (GSH) applied on salt stress-affected mung bean (Vigna radiata L.) seedlings were studied. The salt stress (200 mM NaCl) significantly increased the malondialdehyde (MDA), methylglyoxal (MG), H2O2, and proline (Pro) content, O2 ·− generation rate, and lipoxygenase (LOX) activity and reduced the leaf relative water content (RWC) and chlorophyll (Chl) content. The salt stress also significantly reduced the ascorbate (AsA) content, increased the endogenous GSH and glutathione disulfide (GSSG) content, and reduced the GSH/GSSG ratio. The activities of mono-dehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), and catalase (CAT) decreased; and the activities of ascorbate peroxidase (APX), glutathione reductase (GR), superoxide dismutase (SOD), glutathione S-transferase (GST), and glutathione peroxidase (GPX) increased under the salt stress. The activities of glyoxalase I (Gly I) and glyoxalase II (Gly II) decreased under the salt stress (except the Gly II activity at 48 h). Mung bean seedlings which were treated with NaCl together with GSH showed an improved AsA and GSH content, GSH/GSSG ratio, higher activities of APX (only at 24 h), MDHAR, DHAR, GR, SOD (only at 24 h), CAT, GPX (only at 48 h), GST (only at 24 h), Gly I and Gly II under the salt stress compared with those treated with NaCl alone. The improved antioxidant and glyoxalase systems by GSH application decreased the MDA, H2O2, and MG content, O2 ·− generation rate, as well as increased the leaf RWC and Chl content. Thus, exogenous GSH improved the response of the mung bean seedlings to the salt stress.

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

Similar content being viewed by others

Abbreviations

AO:

ascorbate oxidase

APX:

ascorbate peroxidase

AsA:

ascorbate

BSA:

bovine serum albumin

CAT:

catalase

CDNB:

1-chloro-2,4-dinitrobenzene

Chl:

chlorophyll

DHA:

dehydroascorbate

DHAR:

dehydroascorbate reductase

DTNB:

5,5′-dithio-bis-(2-nitrobenzoic) acid

EDTA:

ethylenediaminetetraacetic acid

Gly:

glyoxalase

GR:

glutathione reductase

GSH:

reduced glutathione

GSSG:

oxidized glutathione

GPX:

glutathione peroxidase

GST:

glutathione S-transferase

LOX:

lipoxygenase

MDA:

malondialdehyde

MDHA:

monodehydroascorbate

MDHAR:

monodehydroascorbate reductase

MG:

methylglyoxal

NADPH:

nicotinamide adenosine dinucleotide phosphate

NTB:

2-nitro-5-thiobenzoic acid

PEG:

polyethylene glycol

Pro:

proline

ROS:

reactive oxygen species

RWC:

relative water content

SLG:

S-D-lactoyl-glutathione

SOD:

superoxide dismutase

TBA:

thiobarbituric acid

TCA:

trichloroacetic acid

References

  • Aghaleh, M., Niknam, V., Ebrahimzadeh, H., Razavi, K.: Antioxidative enzymes in two in vitro cultured Salicornia species in response to increasing salinity. — Biol. Plant. 58: 391–394, 2014.

    Article  CAS  Google Scholar 

  • Alam, M.M., Nahar, K., Hasanuzzaman, M., Fujita, M.: Alleviation of osmotic stress in Brassica napus, B. campestris, and B. juncea by ascorbic acid application. — Biol. Plant. 58: 697–708, 2014.

    Article  CAS  Google Scholar 

  • Arnon, D.T.: Copper enzymes in isolated chloroplasts polyphenal oxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Aziz, A., Larher, F.: Osmotic stress induced changes in lipid composition and peroxidation in leaf discs of Brassica napus L. — J. Plant Physiol. 153: 754–762, 1998.

    Article  CAS  Google Scholar 

  • Aziz, A., Martin-Tanguy, J., Larher, F.: Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. — Physiol. Plant. 104: 195–202, 1998.

    Article  CAS  Google Scholar 

  • Baier, M., Dietz, K.J.: The plant 2-cis-peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin and implications for its specific physiological function in plants. — Plant J. 12: 179–190, 1997.

    Article  CAS  PubMed  Google Scholar 

  • Barrs, H.D., Weatherley, P.E.: A re-examination of the relative turgidity technique for estimating water deficits in leaves. — Aust. J. biol. Sci. 15: 413–428, 1962.

    Google Scholar 

  • Bates, L.S., Waldren, R.P., Teari, D.: Rapid determination of free proline for water stress studies. — Plant Soil 39: 205–207, 1973.

    Article  CAS  Google Scholar 

  • Bergmann, L., Rennenberg, H.: Glutathione metabolism in plants. — In: De Kok, L.J., Stulen, I., Rennenberg, H., Brunold, C., Rauser, W.E. (ed.): Sulfur Nutrition and Sulfur Assimilation in Higher Plants. Pp. 109–123. SPB Academic Publishers, The Hague 1993.

    Google Scholar 

  • Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J.H., Jiang, H.W., Hsieh, E.J., Chen, H.Y., Chien. C.T., Hsieh, H.L., Lin, T.P.: Drought and salt stress tolerance of an Arabidopsis glutathione S-transferase U17 knockout mutant are attributed to the combined effect of glutathione and abscisic acid. — Plant Physiol. 158: 340–351, 2012.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Del Río, L.A., Corpas, F.J., Sandalio, L.M., Palma, J.M., Gómez, M., Barroso, J.B.: Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. — J. exp. Bot. 53: 1255–1272, 2002.

    Article  PubMed  Google Scholar 

  • Dixon, D.P., Skipsey, M., Edwards, R.: Roles for glutathione transferases in plant secondary metabolism. — Phytochemistry 71: 338–350, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Dixon, D.P., Skipsey, M., Grundy, N.M., Edwards, R.: Stressinduced protein S-glutathionylation in Arabidopsis. — Plant Physiol. 138: 2233–2244, 2005.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Doderer, A., Kokkelink, I., Van der Veen, S., Valk, B., Schram, A., Douma, A.: Purification and characterization of two lipoxygenase isoenzymes from germinating barley. — Biochem. biophys. Acta 112: 97–104, 1992.

    Google Scholar 

  • Elia, A.C., Galarini, R., Taticchi, M.I., Dorr, A.J.M., Mantilacci, L.: Antioxidant responses and bioaccumulation in Ictalurus melas under mercury exposure. — Ecotoxicol. Environ. Safety 55: 162–167, 2003.

    Article  CAS  PubMed  Google Scholar 

  • El-Shabrawi, H., Kumar, B., Kaul, T., Reddy, M.K., Singla-Pareek, S.L., Sopory, S.K.: Redox homeostasis, antioxidant defense, and methylglyoxal detoxification as markers for salt tolerance in Pokkali rice. — Protoplasma 245: 85–96, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Elstner, E.F., Heupel, A.: Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. — Anal. Biochem. 70: 616–620, 1976.

    Article  CAS  PubMed  Google Scholar 

  • Foyer, C.H., Noctor, G.: Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. — Physiol. Plant 119: 355–364, 2003.

    Article  CAS  Google Scholar 

  • Foyer, C.H., Theodoulou, F.L., Delrot, S.: The functions of inter- and intracellular glutathione transport systems in plants. — Trends Plant Sci. 6: 486–492, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Garg, N., Manchanda, G.: ROS generation in plants: boon or bane? — Plant Biosyst. 143: 81–96, 2009.

    Article  Google Scholar 

  • Gill, S.S., Anjum, N.A., Hasanuzzaman, M., Gill, R., Trivedi, D.K., Ahmad, I., Pereira E., Tuteja, N.: Glutathione reductase and glutathione: a boon in disguise for plant abiotic stress defense operations. — Plant Physiol. Biochem. 70: 204–212, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Gill, S.S., Tuteja, N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. — Plant Physiol. Biochem. 48: 909–930, 2010.

    Article  CAS  PubMed  Google Scholar 

  • Grill, E., Loffler, S., Winnacker, E.L., Zenk, M.H.: Phytochelatins, the heavy-metal-binding peptides of plants, are synthesized from glutathione by a specific gammaglutamylcysteine dipeptidyltranspeptidase (phytochelatin synthase). — Proc. nat. Acad. Sci. USA 86: 6838–6842, 1989.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hajlaoui, H., Denden, M., El-Ayeb, N.: Changes in fatty acid composition, hydrogen peroxide and lipid peroxidation of salt-stressed corn (Zea mays L.) roots. — Acta Physiol. Plant. 31: 787–796, 2009.

    Article  CAS  Google Scholar 

  • Hasanuzzaman, M., Hossain, M.A., Da Silva, J.A.T., Fujita, M.: Plant responses and tolerance to abiotic oxidative stress: antioxidant defense is a key factor. — In: Bandi, V., Shanker, A.K., Shanker, C., Mandapaka, M. (ed.): Crop Stress and its Management: Perspectives and Strategies. Pp. 261–316. Springer, Berlin 2012.

    Chapter  Google Scholar 

  • Hasanuzzaman, M., Hossain, M.A., Fujita, M.: Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. — Plant Biotechnol. Rep. 5: 353–365, 2011a.

    Article  Google Scholar 

  • Hasanuzzaman, M., Hossain, M.A., Fujita, M.: Seleniuminduced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinityinduced damage in rapeseed seedlings. — Biol. Trace Element Res. 143: 1704–1721, 2011b.

    Article  CAS  Google Scholar 

  • Hasanuzzaman, M., Nahar, K., Alam, M.M., Roychowdhury, R., Fujita, M.: Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. — Int. J. mol. Sci. 14: 9643–9684, 2013.

    Article  PubMed Central  PubMed  Google Scholar 

  • Heath, R.L., Packer, L.: Photoperoxidation in isolated chloroplast. I. kinetics and stoichiometry of fatty acid peroxidation. — Arch. Biochem. Biophys. 125: 189–198, 1968.

    Article  CAS  PubMed  Google Scholar 

  • Herschbach, C., Van Der Zalm, E., Schneider, A., Jouanin, L., De Kok, L.J.: Rennenberg H.: Regulation of sulfur nutrition in wild-type and transgenic poplar by over-expressing gamma glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. — Plant Physiol. 124: 461–473, 2000.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hossain, M.A., Fujita, M.: Evidence for a role of exogenous glycinebetaine and proline in antioxidant defense and methylglyoxal detoxification systems in mung bean seedlings under salt stress. — Physiol. mol. Biol. Plants. 16: 19–29, 2010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hossain, M.A., Hasanuzzaman, M., Fujita, M.: Coordinate induction of antioxidant defense and glyoxalase system by exogenous proline and glycinebetaine is correlated with salt tolerance in mung bean. — Front. Agr. China 5: 1–14, 2011.

    Article  Google Scholar 

  • Hossain, M.A., Hossain, M.D., Fujita, M.: Induction of pumpkin glutathione S-transferase by different stresses and its possible mechanisms. — Biol. Plant. 50: 210–218, 2006.

    Article  CAS  Google Scholar 

  • Hossain, M.A., Nakano, Y., Asada, K.: Monodehydroascorbate reductase in spinach chloroplasts and its participation in the regeneration of ascorbate for scavenging hydrogen peroxide. — Plant Cell Physiol. 25: 385–395, 1984.

    CAS  Google Scholar 

  • Huang, C., He, W., Guo, J., Chang, X., Su, P., Zhang, L.: Increased sensitivity to salt stress in ascorbate deficient Arabidopsis mutant. — J. exp. Bot. 56: 3041–3049, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Job, C., Rajjou, L., Lovigny, Y., Belghazi, M., Job, D.: Patterns of protein oxidation in Arabidopsis seeds and during germination. — Plant Physiol. 138: 790–802, 2005.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Katerji, N., Van Hoorn, J.W., Hamdy, A., Mastrorilli, M., Moukarzel, E.: Osmotic adjustment of sugar beets in response to soil salinity and its influence on stomatal conductance, growth and yield. — Agr. Water Manage. 34: 57–69, 1997.

    Article  Google Scholar 

  • Kattab, H.: Role of glutathione and polyadenylic acid on the oxidative defense systems of two different cultivars of canola seedlings grown under saline condition. — Aust. J. basic appl. Sci. 1: 323–332, 2007.

    CAS  Google Scholar 

  • Khedr, A.H.A., Abbas, M.A., Wahid, A.A.A., Quick, W.P., Abogadallah, G.M.: Proline induces the expression of saltstress responsive proteins and may improve the adaptation of Pancratium maritimum L. to salt-stress. — J. exp. Bot. 54: 2553–2562, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Lappartient, A.G., Touraine, B.: Demand-driven control of root ATP sulfurylase activity and SO4 2- uptake in intact canola. The role of phloem-translocated glutathione. — Plant Physiol. 111: 147–157, 1996.

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu, J.J., Lin, S.H., Xu, P.L., Wang, X.J., Bai, J.G.: Effects of exogenous silicon on the activities of antioxidant enzymes and lipid peroxidation in chilling-stressed cucumber leaves. — Agr. Sci. China 8: 1075–1086, 2009.

    Article  CAS  Google Scholar 

  • Lynch, D.L., Thompson, J.E.: Lipoxygenase-mediated production of superoxide anion in senescing plant tissue. — FEBS Lett. 173: 251–254, 1984.

    Article  CAS  Google Scholar 

  • Marrs, K.A.: The functions and regulation of glutathione S-transferases in plants. — Annu. Rev. Plant Physiol. Plant mol. Biol. 47: 127–157, 1996.

    Article  CAS  PubMed  Google Scholar 

  • Mishra, P., Bhoomika, K., Dubey, R.S.: Differential responses of antioxidative defense system to prolonged salinity stress in salt-tolerant and salt-sensitive Indica rice (Oryza sativa L.) seedlings. — Protoplasma 250: 3–19, 2013.

    Article  CAS  PubMed  Google Scholar 

  • Molassiotis, A., Sotiropoulos, T., Tanou, G., Diamantidis, G., Therios, I.: Boron induced oxidative damage and antioxidant and nucleolytic responses in shoot tips culture of the apple rootstock EM9 (Malus domestica Borkh). — Environ. exp. Bot. 56: 54–62, 2006.

    Article  CAS  Google Scholar 

  • Moller, I.M., Jensen, P.E., Hansson, A.: Oxidative modifications to cellular components in plants. — Annu. Rev. Plant Biol. 58: 459–481, 2007.

    Article  PubMed  Google Scholar 

  • Nahar, K., Hasanuzzaman, M., Alam, M.M., Fujita, M.: Exogenous glutathione confers high temperature stress tolerance in mung bean (Vigna radiata L.) by modulating antioxidant defense and methylglyoxal detoxification system. — Environ. exp. Bot. 112: 44–54, 2015a.

    Article  CAS  Google Scholar 

  • Nahar, K., Hasanuzzaman, M., Alam, M.M., Fujita, M.: Glutathione-induced drought stress tolerance in mung bean: Coordinated roles of the antioxidant defense and methylglyoxal detoxification systems. — AoB Plants. DOI: 10.1093/aobpla/plv069, 2015b.

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

    CAS  Google Scholar 

  • Naliwajski, M.R., SkŁodowska, M.: The oxidative stress and antioxidant systems in cucumber cells during acclimation to salinity. — Biol. Plant. 58: 47–54, 2014.

    Article  CAS  Google Scholar 

  • Paradiso, A., Berardino, R., De Pinto, M., Di Toppi, L.S., Storelli, F.T, De Gara, L.: Increase in ascorbate-glutathione metabolism as local and precocious systemic responses induced by cadmium in durum wheat plants. — Plant Cell Physiol. 49: 362–374, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Principato, G.B., Rosi, G., Talesa, V., Govannini, E., Uolila, L.: Purification and characterization of two forms of glyoxalase II from rat liver and brain of Wistar rats. — Biochem. biophys. Acta. 911: 349–355, 1987.

    CAS  PubMed  Google Scholar 

  • Rennenberg, H., Schmitz, K., Bergmann, L.: Long distance transport of sulfur in Nicotiana tabacum. — Planta 147: 57–82, 1979.

    Article  CAS  PubMed  Google Scholar 

  • Roychoudhury, A., Basu, S., Sengupta, D.N.: Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of Indica rice differing in their level of salt tolerance. — J. Plant Physiol. 168: 317–328, 2011.

    Article  CAS  PubMed  Google Scholar 

  • Schneider, A., Schatten, T., Rennenberg, H.: Exchange between phloem and xylem during long distance transport of glutathione in spruce trees (Picea abies [Karst.]L.). — J. exp. Bot. 45: 457–462, 1994.

    Article  CAS  Google Scholar 

  • Shringarpure, R., Davies K.J.: Protein turnover by the proteasome in aging and disease. — Free Radical Biol. Med. 32: 1084–1089, 2002.

    Article  CAS  Google Scholar 

  • Song, X.S., Hu, W.H., Mao, W.H., Ogweno, J.O., Zhou, Y.H., Yu, J.Q.: Response of ascorbate peroxidase isoenzymes and ascorbate regeneration system to abiotic stresses in Cucumis sativus L. — Plant Physiol. Biochem. 43: 1082–1088, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Srivalli, S., Khanna-Chopra, R.: Role of glutathione in abiotic stress tolerance. — In: Khan, N.A., Singh, S., Umar, S. (ed.): Sulfur Assimilation and Abiotic Stress in Plants. Pp. 207–225. Springer, Berlin 2008.

    Chapter  Google Scholar 

  • Steudle, E.: Water uptake by roots: effects of water deficit. — J. exp. Bot. 51: 1531–1542, 2000.

    Article  CAS  PubMed  Google Scholar 

  • Sudhir, P., Murthy, S.D.S.: Effects of salt stress on basic processes of photosynthesis. — Photosynthetica 42: 481–486, 2004.

    Article  CAS  Google Scholar 

  • Sumithra, K., Jutur, P.P., Carmel, B.D., Reddy, A.R.: Salinityinduced changes in two cultivars of Vigna radiata: responses of antioxidative and proline metabolism. — Plant Growth Regul. 50: 11–22, 2006.

    Article  CAS  Google Scholar 

  • Wang, H., Liu, J., Wu, L.: Methylglyoxal-induced mitochondrial dysfunction in vascular smooth muscle cells. — Biochem. Pharmacol. 77: 1709–1716, 2009.

    Article  CAS  PubMed  Google Scholar 

  • Wild, R., Ooi, L., Srikanth, V., Münch, G.: A quick, convenient and economical method for the reliable determination of methylglyoxal in millimolar concentrations: the N-acetyl-L-cysteine assay. — Anal Bioanal. Chem. 403: 2577–2581, 2012.

    Article  CAS  PubMed  Google Scholar 

  • Xu, L.H., Wang, W.Y., Guo, J.J., Qin, J., Shi, D.Q., Li, Y.L., Xu, J.: Zinc improves salt tolerance by increasing reactive oxygen species scavenging and reducing Na+ accumulation in wheat seedlings. — Biol. Plant. 58: 751–757, 2014.

    Article  CAS  Google Scholar 

  • Yadav, S.K., Singla-Pareek, S.L., Ray, M., Reddy, M.K., Sopory, S.K.: Methylglyoxal levels in plants under salinity stress are dependent on glyoxalase I and glutathione. — Biochem. biophys. Res. Commun. 337: 61–67, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Yadav, S.K., Singla-Pareek, S.L., Sopory, S.K.: An overview on the role of methylglyoxal and glyoxalases in plants. — Drug Metab. Drug Interact. 23: 51–68, 2008.

    Article  CAS  Google Scholar 

  • Yang, H., Shi, G., Wang, H., Xu, Q.: Involvement of polyamines in adaptation of Potamogeton crispus L. to cadmium stress. — Aquat. Toxicol. 100: 282–288, 2010.

    Article  PubMed  Google Scholar 

  • Yu, C.W., Murphy, T.M., Lin, C.H.: Hydrogen peroxideinduces chilling tolerance in mung beans mediated through ABA-independent glutathione accumulation. — Funct. Plant Biol. 30: 955–963, 2003.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Plant Stress Responses, Department of Applied Biological Science, Faculty of Agriculture, Kagawa University, Miki-cho, Kita-gun, Kagawa, 761-0795, Japan

    K. Nahar, M. M. Alam & M. Fujita

  2. Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka, 1207, Bangladesh

    K. Nahar

  3. Department of Agronomy, Faculty of Agriculture, Sher-e-Bangla Agricultural University, Sher-e-Bangla Nagar, Dhaka, 1207, Bangladesh

    M. Hasanuzzaman

Authors
  1. K. Nahar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Hasanuzzaman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. M. Alam
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Fujita
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Fujita.

Additional information

Acknowledgements: The first author is grateful to the Ministry of Education, Culture, Sports, Science and Technology (MEXT), Japan, for financial support. We acknowledge Dr Md Motiar Rohman, the Senior Scientific Officer, theBangladesh Agricultural Research Institute, for his cooperation and help in measuring enzymatic activities and other biochemical parameters. We thankfully acknowledge Dennis Murphy, Ehime University, Japan, for a critical review and English language correction.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nahar, K., Hasanuzzaman, M., Alam, M.M. et al. Roles of exogenous glutathione in antioxidant defense system and methylglyoxal detoxification during salt stress in mung bean. Biol Plant 59, 745–756 (2015). https://doi.org/10.1007/s10535-015-0542-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10535-015-0542-x

Additional key words

Search

Navigation