Skip to main content
SpringerLink
Log in

Relationships among iron deficit-induced potato callus growth inhibition, Fe distribution, chlorosis, and oxidative stress amplified by reduced antioxidative enzyme activities

  • Original Article
  • Published:
Plant Cell, Tissue and Organ Culture (PCTOC) Aims and scope Submit manuscript

Abstract

Callus cultures were used to investigate and delineate responses of potato to iron (Fe) deficiency conditions over different culture durations. The morphological responses included chlorotic symptoms, reduced fresh weight and area of callus growth on Fe-deficient medium compared to calli grown under Fe sufficient conditions. Biochemically, potato calli under Fe deficit exhibited decreases in chlorophyll and carotenoid contents, reduction in activities of antioxidant enzymes (peroxidase, catalase and ascorbate peroxidase), as well as an increase in ferric chelate reductase (FCR) activity, lipid peroxidation, phenolic production and hydrogen peroxide (H2O2) level. Perls staining revealed sparse Fe distribution in Fe-deficient callus cells whereas Fe was widely distributed and intensely stained among numerous actively dividing cells in Fe-sufficient calli. These responses of calli to Fe deficiency were more pronounced with prolonged exposure to such stress leading to severe chlorosis and/or death of cells in chlorosis-susceptible calli but potential chlorosis-tolerant callus cells maintained their greenness and viability. Over a prolonged period in culture, significantly positive correlations were found among callus fresh weight, chlorophyll and carotenoid contents, antioxidant enzyme activities and lipid peroxidation as Fe supplies to the medium was increased. FCR activity was strongly correlated in a negative manner with Fe deficiency, chlorophyll content and peroxidase activity. The responses of calli to Fe supply can serve as reliable indicators for detecting chlorosis tolerance and/or nutrient deficiency 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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Abadia J, Vazquez S, Rellan-Alvarez R, El-Jendoubi H, Abadia A, A´lvarez-Ferna´ndez A, Lopez-Millan AF (2011) Towards a knowledge-based correction of iron chlorosis. Plant Physiol Biochem 49:471–482

    Article  CAS  PubMed  Google Scholar 

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 52:121–126

    Article  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bairu MW, Aremu AO, Van Staden J (2011) Somaclonal variation in plants: causes and detection methods. Plant Growth Regul 63:147–173

    Article  CAS  Google Scholar 

  • Barton LL, Abadía J (2006) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands

    Book  Google Scholar 

  • Bert P, Bordenave L, Donnart M, He´vin C, Ollat N, Decroocq S (2013) Mapping genetic loci for tolerance to lime-induced iron deficiency chlorosis in grapevine rootstocks (Vitis sp.). Theor Appl Genet 126:451–473

    Article  CAS  PubMed  Google Scholar 

  • Bhaduri AM, Fulekar M (2012) Antioxidant enzyme responses of plants to heavy metal stress. Rev Environ Sci Bio 11:55–69

    Article  CAS  Google Scholar 

  • Bienfait H, Frits D, Letty A, Kramere D (1987) Control of the development of iron-efficiency reactions in potato as a response to iron deficiency is located in the roots. Plant Physiol 83:244–247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boamponsem GA (2017) In vitro selection and characterisation of iron- efficient potato cell lines. PhD Thesis School of Biological Sciences, University of Canterbury, New Zealand

  • Boamponsem GA, Leung DW (2017) Use of compact and friable callus cultures to study adaptive morphological and biochemical responses of potato (Solanum tuberosum) to iron supply. Sci Hort 219:161–172

    Article  CAS  Google Scholar 

  • Boamponsem GA, Leung DWM, Lister C (2017) Insights into resistance to Fe deficiency stress from a comparative study of in vitro-selected novel Fe-efficient and Fe-inefficient potato plants. Front Plant Sci 8:1581

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) 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

    Article  CAS  PubMed  Google Scholar 

  • Bria JF, Curie C, Gaymard F (2007) Iron utilization and metabolism in plants. Curr Opin Plant Biol 10:276–282

    Article  Google Scholar 

  • Broadley M, Brown P, Cakmak I, Rengel Z, Zhao F (2012) Function of nutrient: micronutrients, 3rd edn. Academic press, Elsevier Ltd, London

    Google Scholar 

  • Bruggemann W, Maas-Kantel K, Moog PR (1993) Iron uptake by leaf mesophyll cells: the role of the plasma membrane-bound ferric-chelate reductase. Planta 190:151–155

    Article  Google Scholar 

  • Chatterjee C, Gopal R, Dube BK (2006) Impact of iron stress on biomass, yield, metabolism and quality of potato (Solanum tuberosum L.). Sci Hort 108:1–6

    Article  CAS  Google Scholar 

  • Connolly EL, Campbel NH, Grotz N, Prichard CL, Guerinot ML (2003) Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiol 133:1102–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cvitanich C, Przybyłowicz WJ, Urbanski DF, Jurkiewicz AM, Mesjasz-Przybyłowicz J, Blair MW et al (2010) Iron and ferritin accumulate in separate cellular locations in Phaseolus seeds. BMC Plant Biol 10:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Darbani B, Briat J, Holm PB, Husted S, Noeparvar S, Borg S (2013) Dissecting plant iron homeostasis under short and long-term iron fluctuations. Biotechnol Adv 31:1292–1307

    Article  CAS  PubMed  Google Scholar 

  • Daudi A, O’Brien JA (2012) Detection of hydrogen peroxide by DAB staining in Arabidopsis leaves. Bio Protoc 2:e263

    Article  PubMed  PubMed Central  Google Scholar 

  • De la Guardia MD, Alcántara E (2002) Bicarbonate and low iron level increase root to total plant weight ratio in olive and peach rootstock. J Plant Nutr 25:1021–1032

    Article  Google Scholar 

  • Demiral T, Türkan I (2005) Comparative lipid peroxidation, antioxidant defense systems and proline content in roots of two rice cultivars differing in salt tolerance. Environ Exp Bot 53:247–257

    Article  CAS  Google Scholar 

  • Dolcet-Sanjuan R, Mok DWS, Mok M (1992) Characterization and in vitro selection for iron efficiency in Pyrus and Cydonia. In Vitro Cell Dev Biol Plant 28:25–29

    Article  Google Scholar 

  • Donnini S, Dell’Orto M, Zocchi G (2011) Oxidative stress responses and root lignification induced by Fe deficiency conditions in pear and quince genotypes. Tree Physiol 31:102–113

    Article  CAS  PubMed  Google Scholar 

  • Eide DJ, Broderiu M, Fett J, Guerinot ML (1996) A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Nat Acad Sci 93:5624–5628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • García-Mina JM, Bacaicoa E, Fuentes M, Casanova E (2013) Fine regulation of leaf iron use efficiency and iron root uptake under limited iron bioavailability. Plant Sci 198:39–45

    Article  PubMed  Google Scholar 

  • Graziano M, Lamattina L (2005) Nitric oxide and iron in plants: an emerging and con-verging story. Trends Plant Sci 10:4–8

    Article  CAS  PubMed  Google Scholar 

  • Green L, Rogers EE (2004) FRD3 controls iron localization in Arabidopsis thaliana. Plant Physiol 136:2523–2531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruber B, Kosegarten H (2002) Depressed growth of nonchlorotic vine grown in calcareous soil is an iron deficiency symptom prior to leaf chlorosis. J Plant Nutr Soil Sci 165:111

    Article  CAS  Google Scholar 

  • Grusak MA, Welch RM, Kochian LV (1990) Does iron deficiency in Pisum sativum enhance the activity of the root plasmalemma iron transport protein? Plant Physiol 94:1353–1357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guerinot ML, Yi Y (1994) Iron: nutritious, noxious, and not readily available. Plant Physiol 104:815–820

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagen SR, Muneta P, LeTourneau D, Brown J (1991) Effect of temperature on the starch content of potato callus tissue. Am Potato J 68:191–195

    Article  CAS  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansch R, Mendel RR (2009) Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Curr Opin Plant Biol 12:259–266

    Article  PubMed  Google Scholar 

  • Hansen NC, Hopkins BG, Ellsworth JW, Jolley VD (2006) Iron nutrition in field crops. In: Barton LL, Abadía J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 23–59

    Chapter  Google Scholar 

  • Hindt MN, Guerinot ML (2012) Getting a sense for signals: regulation of the plant iron deficiency response. Biochim Biophys Acta 1823:1521–1530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iturbe-Ormaetxe I, Morán JF, Arrese-Igor C, Gogorcena Y, Klucas RV, Becana M (1995) Activated oxygen and antioxidant defences in iron-deficient pea plants. Plant Cell Environ 18:421–429

    Article  CAS  Google Scholar 

  • Ivanov R, Brumbarova T, Bauer P (2012) Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Mol Plant 5:27–42

    Article  CAS  PubMed  Google Scholar 

  • Jbir-Koubaa R, Charfeddine S, Ellouz W et al (2015) Investigation of the response to salinity and to oxidative stress of interspecific potato somatic hybrids grown in a greenhouse. Plant Cell Tiss Organ Cult 120:933

    Article  CAS  Google Scholar 

  • Jelali N, Dell’Orto M, Rabhi M, Zocchi G, Abdelly C, Gharsalli M (2010) Physiological and biochemical responses for two cultivars of Pisum sativum (‘‘Merveille de Kelvedon’’ and ‘‘Lincoln’’) to iron deficiency conditions. Sci Hort 124:116–121

    Article  CAS  Google Scholar 

  • Jelali N, Moez S, Dhifi W, Mnif W, Abdelly C, Gharsalli M (2012) Secondary metabolism responses in two Pisum sativum L. cultivars cultivated under Fe deficiency conditions. Afr J Biotechnol 11:14828–14836

    CAS  Google Scholar 

  • Jeong J, Cohu C, Kerkeb L, Pilon M, Connolly EL, Guerinot ML (2008) Chloroplast Fe (III) chelate reductase activity is essential for seedling viability under iron limiting conditions. Proc Natl Acad Sci 105:10619–10624

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jin CW, You GY, He YF, Tang C, Wu P, Zheng SJP (2007) Iron deficiency-induced secretion of phenolic facilitates the reutilization of root apoplastic iron in red clover. Plant Physiol 144:278–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kabir AH, Rahman MM, Haider SA, Paul NK (2015) Mechanisms associated with differential tolerance to Fe deficiency in okra (Abelmoschus esculentus Moench). Environ Exp Bot 112:16–26

    Article  CAS  Google Scholar 

  • Kerkeb L, Connolly EL (2006) Iron transport and metabolism in plants. In Genetic Engineering. Springer, New York, pp 119–140

    Google Scholar 

  • Kim SA, Guerinot ML (2007) Mining iron: iron uptake and transport in plants. FEBS Lett 581:2273–2280

    Article  CAS  PubMed  Google Scholar 

  • Kumar P, Tewari RK, Sharma PN (2010) Sodium nitroprusside-mediated alleviation of iron deficiency and modulation of antioxidant responses in maize plants. AoB Plants plq002:1–11

    Google Scholar 

  • Legay S, Guignard C, Ziebel J, Evers D (2012) Iron uptake and homeostasis related genes in potato cultivated in vitro under iron deficiency and overload. Plant Physiol Biochem 60:180–189

    Article  CAS  PubMed  Google Scholar 

  • López-Millán AF, Grusak MA, Abadía A, Abadía J (2013) Iron deficiency in plants: an insight from proteomic approaches. Front Plant Sci 4:254

    Article  PubMed  PubMed Central  Google Scholar 

  • M’sehli W, Houmani H, Donnini S, Zocchi G, Abdelly C, Gharsalli M (2014) Iron deficiency tolerance at leaf level in Medicago ciliaris plants. Am J Plant Sci 5:2541–2553

    Article  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Padmanabhan P, Shukla MR, Sullivan JA et al (2017) Iron supplementation promotes in vitro shoot induction and multiplication of Baptisia australis. Plant Cell Tissue Organ Cult 129:145

    Article  CAS  Google Scholar 

  • Panda SK (2012) Assay guided comparison for enzymatic and non-enzymatic antioxidant Activities with special reference to medicinal plants. In: El-Missiry MA (ed) Antioxidant Enzyme, vol 14. InTech, pp 382–400

  • Perron NR, Brumaghim JL (2009) A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem Biophys 53:75–100

    Article  CAS  PubMed  Google Scholar 

  • Phillips RL, Kaeppler SM, Olhoft P (1994) Genetic instability of plant tissue cultures: breakdown of normal controls. Proc Natl Acad Sci 91:5222–5226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piagnani C, Nisi PD, Espen L, Zocchi G (2003) Adaptive responses to iron-deficiency in callus cultures of two cultivars of Vitis spp. J Plant Physiol 160:865–870

    Article  CAS  PubMed  Google Scholar 

  • Ramírez L, Bartoli CG, Lamattina L (2013) Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency. J Exp Bot. https://doi.org/10.1093/jxb/ert153

    PubMed  Google Scholar 

  • Ranieri A, Castagna A, Lorenzini G, Soldatini G (1997) Changes in thylakoid protein patterns and antioxidant levels in two wheat cultivars with different sensitivity to sulfur dioxide. Environ Exp Bot 37:125–135

    Article  CAS  Google Scholar 

  • Ranieri A, Castagna A, Baldan B, Soldatini GF (2001) Iron deficiency differently affects peroxidase isoforms in sunflower. J Exp Bot 52:25–35

    Article  CAS  PubMed  Google Scholar 

  • Robinson NJ, Groom SJ, Groom QJ (1997) The froh gene family from Arabidopsis thaliana: putative iron-chelate reductases. Plant Soil 196:245–248

    Article  CAS  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Celma J, Vázquez-Reina S, Orduna J, Abadía A, Abadía J, Álvarez-Fernández A, López-Millán AF (2011) Characterization of flavins in roots of Fe-deficient strategy I plants, with a focus on Medicago truncatula. Plant Cell Physiol 52:2173–2189

    Article  PubMed  Google Scholar 

  • Rodríguez-Celma J, Lin W, Fu G, Abadía J, López-Míllán A, Schmidt W (2013) Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula. Plant Physiol 162:1473–1485

    Article  PubMed  PubMed Central  Google Scholar 

  • Römheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180

    Article  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Conéjéro G, Curie C, Mari S (2009) Identification of the endodermal vacuole as the iron storage compartment in the Arabidopsis embryo. Plant Physiol 151:1329–1338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Grillet L, Isaure MP, Conéjéro G, Ortega R, Curie C, Mari S (2011) Plant cell nucleolus as a hot spot for iron. J Biol Chem 286:27863–27866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roschzttardtz H, Conéjéro G, Divol F, Alcon C, Verdeil J, Curie C, Mari S (2013) New insights into Fe localization in plant tissues. Front Plant Sci 4:1–11

    Article  Google Scholar 

  • Rout JR, Behera S, Keshari N, Ram SS, Bhar S, Chakraborty A et al (2015) Effect of iron stress on Withania somnifera L.: antioxidant enzyme response and nutrient elemental uptake of in vitro grown plants. Ecotoxicology 24:401–413

    Article  CAS  PubMed  Google Scholar 

  • Salama ZAE, El-Beltagi HS, El-Hariri DM (2009) Effect of Fe deficiency on antioxidant system in leaves of three flax cultivars. Not Bot Hort Agrobot Cluj 37:122–128

    CAS  Google Scholar 

  • Schmidt W, Tittel J, Schikora A (2000) Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiol 122:1109–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simko I, Van Den Berg JH, Vreugdenhil D, Ewing EE (2008) Mapping loci for chlorosis associated with chlorophyll b deficiency in potato. Euphytica 162:99–107

    Article  CAS  Google Scholar 

  • Spanos GA, Wrolstad RE (1990) Influence of processing and storage on the phenolic composition of Thompson seedless grape juice. J Agric Food Chem 38:1565–1571

    Article  CAS  Google Scholar 

  • Sperotto RA, Boff T, Duarte GL, Fett JP (2008) Increased senescence-associated gene expression and lipid peroxidation induced by iron deficiency in rice roots. Plant Cell Rep 27:183–195

    Article  CAS  PubMed  Google Scholar 

  • Sun B, Jing Y, Chen K, Song L, Chen F, Zhang L (2007) Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays). J Plant Physiol 164:536–543

    Article  CAS  PubMed  Google Scholar 

  • Tarrahi R, Rezanejad F (2013) Callogenesis and production of anthocyanin and chlorophyll in callus cultures of vegetative and floral explants in Rosa gallica and Rosa hybrida (Rosaceae). Turk J Bot 37:1145–1154

    Article  CAS  Google Scholar 

  • Tewari RK, Kumar P, Sharma PN (2005) Signs of oxidative stress in the chlorotic leaves of iron starved plants. Plant Sci 169:1037–1045

    Article  CAS  Google Scholar 

  • Tewari RK, Hadacek F, Sassmann S, Lang I (2013) Iron deprivation-induced reactive oxygen species generation leads to non-autolytic PCD in Brassica napus leaves. Environ Exp Bot 91:74–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomine S, Vert G (2013) Iron transport in plants: better be safe than sorry. Curr Opin Plant Biol 16:322–327

    Article  CAS  PubMed  Google Scholar 

  • Vasconcelos MW, Grusak MA (2014) Morpho-physiological parameters affecting iron deficiency chlorosis in soybean (Glycine max L.). Plant Soil 374:161–172

    Article  CAS  Google Scholar 

  • Vázquez AM (2001) Insight into somaclonal variation. Plant Biosyst-Int J Dealing Asp Plant Biol 135:57–62

    Google Scholar 

  • Wang QM, Gao F-Z, Gao X, Zou F-Y, Sui X, Wang M, Wang L (2011) Regeneration of Clivia miniata and assessment of clonal fidelity of plantlets. Plant Cell Tissue Organ Cult 109:191–200

    Article  Google Scholar 

  • Waters BM, Blevins DG, Eide DJ (2002) Characterization of FRO1, a pea ferric-chelate reductase involved in root iron acquisition. Plant Physiol 129:85–94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellburn A, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Adv Photosyn Res 2:9–12

    Article  CAS  Google Scholar 

  • Xu J, Liu B, Liu X, Gao H, Deng X (2011) Carotenoids synthesized in citrus callus of different genotypes. Acta Physiol Plant 33:745–753

    Article  CAS  Google Scholar 

  • Yi Y, Guerinot ML (1996) Genetic evidence that induction of root Fe (III) chelate reductase activity is necessary for iron uptake under iron deficiency. Plant J 10:835–844

    Article  CAS  PubMed  Google Scholar 

  • Yoon KS, Leung DW (2004) Relative importance of maltose and sucrose supplied during a 2-step potato microtuberization process. Acta Physiol Plant 26:47–52

    Article  CAS  Google Scholar 

  • Zamboni A, Zanin L, Tomasi N, Pezzotti M, Pinton R, Varanini Z, Cesco C (2012) Genome-wide microarray analysis of tomato roots showed defined responses to iron deficiency. BMC Genomics 13:101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr. Louis Boamponsem and Dr. Seyedardalan Ashrafadeh for their excellent technical advice on methodologies and statistical analysis. Special thanks to Graeme Bull, Manfred Ingerfeld and Keum-Ah Lee for assistance with microscopy analysis and lab preparations.

Author information

Authors and Affiliations

  1. School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, 8140, New Zealand

    Georgina A. Boamponsem & David W. M. Leung

  2. The New Zealand Institute for Plant & Food Research Limited, Plant & Food Research Canterbury Agriculture & Science Centre, Gerald St, Lincoln, 7608, New Zealand

    Carolyn Lister

Authors
  1. Georgina A. Boamponsem
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David W. M. Leung
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolyn Lister
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All three authors developed the laboratory analyses and reviewed the research. DWML and GAB designed the research project, read and revised the manuscript. GAB carried out the laboratory experiments and drafted manuscript. CL guided the laboratory analyses and reviewed results. DWML critically revised manuscript and approved final version to be published.

Corresponding author

Correspondence to Georgina A. Boamponsem.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Communicated by Sergio J. Ochatt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 306 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Boamponsem, G.A., Leung, D.W.M. & Lister, C. Relationships among iron deficit-induced potato callus growth inhibition, Fe distribution, chlorosis, and oxidative stress amplified by reduced antioxidative enzyme activities. Plant Cell Tiss Organ Cult 132, 393–412 (2018). https://doi.org/10.1007/s11240-017-1338-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11240-017-1338-9

Keywords

Search

Navigation