Skip to main content
SpringerLink
Log in

Cellular responses of two Latin-American cultivars of Lotus corniculatus to low pH and Al stress

  • Research Article
  • Published:
Central European Journal of Biology

Abstract

Toxic effects of acidic root medium and aluminium were evaluated in two forage cultivars of Lotus corniculatus differing in their tolerance to Al stress. The structural response of most of the root cells exposed to low pH without Al3+ differed markedly from that induced by the combined stress. Conspicuous alteration of the nucleus was present only at low pH 4.0 and disintegration of the cytoplasmic components was more drastic than in the roots exposed to acidic solution containing Al3+. Cells exposed to low pH without Al, did not produce wall thickenings. Severely damaged cytoplasm and localized death in some cortical cells or groups of cells contrasting with almost intact cells exposed to Al3+ stress were found. In this respect, a strong correlation between the occurrence of cell wall thickenings and a better preserved structure of the cytoplasm was observed. The frequency of cell damage in the more tolerant cultivar UFRGS was generally lower, significantly more cortical cells capable of maintaining their resting membrane potential were present than in the sensitive INIA Draco. The difference in their tolerance is related rather to the exudation of citrate and oxalate that was higher in UFRGS than to the accumulation of tannins, which increased after Al treatment in both cultivars.

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

References

  1. Blumenthal M., McGraw R., Lotus adaptation, use and management, In: Beuselinck P., (Ed.), Trefoil: The science and technology of Lotus, American Society of Agronomy, Madison, USA, 1999

    Google Scholar 

  2. Díaz P., Borsani O., Monza J., Lotus related species and their agronomic importance, In: Márquez A.J. (Ed.), Lotus japonicus handbook, Dordrecht: Springer, Dodrecht, Netherlands, 2005

    Google Scholar 

  3. von Uexkull H.R., Mutert E., Global extent, development and economic impact of acid soils. In: Date R.A., Grundon, N.J., Raymet, M.E., Probert M.E. (Eds.), Plant-Soil Interactions at low pH: Principles and Management. Kluwer Academic Publisher, Dodrecht, Netherlands, 1995

    Google Scholar 

  4. Kochian L.V., Cellular mechanisms of aluminium toxicity and resistance in plants, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1995, 46, 237–260

    Article  CAS  Google Scholar 

  5. Yamamoto Y., Profile of modern soil and plant nutrition science (7). Plant growth inhibition mechanism by aluminum ion in acid soil, Agr. Hort., 2001, 76, 819–828

    CAS  Google Scholar 

  6. Rout G.R., Samantaray S., Das P., Aluminium toxicity in plants: a review, Agronomie, 2001, 21, 3–21

    Article  Google Scholar 

  7. Vázquez M.D., Aluminum exclusion mechanism in root tips of maize (Zea mays L.): lysigeny of aluminum hyperaccumulator cells, Plant Biol., 2002, 4, 234–249

    Article  Google Scholar 

  8. Panda S.K., Yamamoto, Y., Kondo, H., Matsumoto, H., Mitochondrial alterations related to programmed cell death in tobacco cells under aluminium stress, C.R. Biologies, 2008, 331, 597–610

    Article  PubMed  CAS  Google Scholar 

  9. Prabagar S., Hodson M., Evans D.E., Silicon amelioration of aluminium toxicity and cell death in suspension cultures of Norway spruce (Picea abies (L.) Karst.), Environ. Exp. Bot., 2011, 70, 266–276

    Article  CAS  Google Scholar 

  10. Rengel Z., Zhang W.H., Role of dynamics of intracellular calcium in aluminium toxicity syndrome, New Phytol., 2003, 159, 295–314

    Article  CAS  Google Scholar 

  11. Nagy N.E., Dalen L.S., Jones D.L., Swensen, B., Fossdal, C.G., Eldhuset, T.D., Cytological and enzymatic responses to aluminium stress in root tips of Norway spruce seedlings, New Phytol., 2004, 163, 595–607

    Article  CAS  Google Scholar 

  12. Eticha D., Stass A., Horst W.J., Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminium resistance, Plant Cell Environ., 2005, 28, 1410–1420

    Article  CAS  Google Scholar 

  13. Tahara K., Norisada M., Hogetsu T., Kojima K., Aluminum tolerance and aluminum-induced deposition of callose and lignin in the root tips of Melaleuca and Eucalyptus species, J. For. Res., 2005, 10, 325–333

    Article  CAS  Google Scholar 

  14. Pan W., Shou J., Zhou X., Zha X., Guo T., Zhu M., et al., Al-induced cell wall hydroxyproline-rich glycoprotein accumulation is involved in alleviating Al toxicity in rice, Acta Physiol. Plant., 2011, 33, 601–608

    Article  CAS  Google Scholar 

  15. Vitorello V.A., Capaldi F,R., Stefanuto V.A., Recent advances in aluminum toxicity and resistance in higher plants, Braz. J. Plant Physiol., 2005, 17, 129–143

    Article  CAS  Google Scholar 

  16. Pavlovkin J., Pal’ove-Balang P., Kolarovič L., Zelinová V., Growth and functional responses of different cultivars of Lotus corniculatus to aluminum and low pH stress, J. Plant Physiol., 2009, 166, 1479–1487

    Article  PubMed  CAS  Google Scholar 

  17. Bose J., Babourina O., Shabala S., Rengel Z., Aluminum-dependent dynamics of ion transport in Arabidopsis: specificity of low pH and aluminum responses, Physiol. Plantarum, 2010, 139, 401–412

    CAS  Google Scholar 

  18. Koyama H., Toda T., Hara T., Brief exposure to low-pH stress causes irreversible damage to the growing root in Arabidopsis thaliana: pectin-Ca interaction may play an important role in proton rhizotoxicity, J. Exp. Bot., 2001, 52, 361–368

    Article  PubMed  CAS  Google Scholar 

  19. Larger I., Andreasson O., Dunbar T.L., Andreasson E., Escobar M.A., Rasmusson A.G., Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses, Plant Cell Environ., 2010, 33, 1513–1528

    Google Scholar 

  20. Zelinová V., Halušková Ľ., Huttová J., Illéš P., Mistrík I., Valentovičová K., et al., Short-term aluminiuminduced changes in barley root tips, Protoplasma 2011, 248, 523–530

    Article  PubMed  Google Scholar 

  21. Barceló J., Poschenrieder C., Fast root growth responses, root exudates, and internal detoxification as clues to the mechanisms of aluminium toxicity and resistance: A review, Environ. Exp. Bot., 2002, 48, 75–92

    Article  Google Scholar 

  22. Tolrá R., Barceló J., Poschenrieder C., Constitutive and aluminium-induced patterns of phenolic compounds in two maize varieties differing in aluminium tolerance, J. Inorg. Biochem., 2009, 103, 1486–1490

    Article  PubMed  Google Scholar 

  23. Kinraide T.B., Parker D.R., Zobel R.W., Organic acid secretion as a mechanism of aluminium toxicity and tolerance in higher plants: a model incorporation the root cortex, epidermis and the external unstirred layer, J. Exp. Bot., 2005, 56, 1853–1865

    Article  PubMed  CAS  Google Scholar 

  24. Delhaize E., Gruber B.D., Ryan P.R., The roles of organic anion permeases in aluminium resistance and mineral nutrition, FEBS Lett., 2007, 581, 2255–2262

    Article  PubMed  CAS  Google Scholar 

  25. Handberg K., Stougaard J., Lotus japonicus diploid legume species for classical and molecular genetics, Plant J., 1992, 2, 487–496

    Article  Google Scholar 

  26. Pavlovkin J., Mistrík I., Zajchenko A.M., Dugovič L., Some aspects of phytotoxic action of trichothecene mycotoxin roridin H on corn roots, Biologia, 1993, 48, 435–439

    CAS  Google Scholar 

  27. Edmeades D.C., Blamey F.P.C., Asher C.J., Edwards D.G., Effects of pH and aluminium on the growth of temperate pasture species. II. Growth and nodulation of legumes, Aust. J. Agricult. Res., 1991, 42, 893–900

    Article  Google Scholar 

  28. Correa O.S., Aranda A., Barneix A.J., Effects of pH on growth and nodulation of two forage legumes, J. Plant Nutr., 2001, 24, 1367–1375

    Article  CAS  Google Scholar 

  29. Abreu Jr. C.H., Muraoka T., Lavorante A. F., Exchangeable aluminum evaluation in acid soils, Sci. Agr., 2003, 60, 543–548

    CAS  Google Scholar 

  30. Probst A., Liu H., Fanjul M., Liao B., Hollande E., Response of Vicia faba L. to metal toxicity on mine tailing substrate: Geochemical and morphological changes in leaf and root, Environ. Exp. Bot., 2009, 66, 297–308

    Article  CAS  Google Scholar 

  31. Pan J., Zhu M., Chen H., Aluminum-induced cell death in root-tip cells of barley, Environ. Exp. Bot., 2001, 46, 71–79

    Article  PubMed  CAS  Google Scholar 

  32. Delisle G., Champoux M., Houde M., Characterization of Oxalate Oxidase and Cell Death in Al-Sensitive and Tolerant Wheat Roots, Plant Cell Physiol., 2001, 42, 324–333

    Article  PubMed  CAS  Google Scholar 

  33. Panda S.K., Matsumoto H., Molecular physiology of aluminum toxicity and tolerance in plants, Bot. Rev., 2007, 73, 326–347

    Article  Google Scholar 

  34. Schmohl N., Horst W.J., Cell wall pectin content modulates aluminium sensitivityof Zea mays (L.) cells grown in suspension culture, Plant Cell Environ., 2000, 23, 735–742

    Article  CAS  Google Scholar 

  35. Jones D.L., Blancaflor E.B., Kochian L.V., Gilroy S., Spatial coordination of aluminium uptake, production of reactive oxygen species, callose production and wall rigidification in maize roots, Plant Cell Environ., 2006, 29, 1309–1318

    Article  PubMed  CAS  Google Scholar 

  36. Stoutjesdijk P.A., Sale P.W., Larkin P.J., Possible involvement of condensed tannins in aluminium tolerance of Lotus pedunculatus, Aust. J. Plant Physiol., 2001, 28, 1063–1074

    CAS  Google Scholar 

  37. Osawa H., Endo I., Hara Y., Matsushima Y., Tange T., Transient Proliferation of Proanthocyanidin-Accumulating Cells on the Epidermal Apex Contributes to Highly Aluminum-Resistant Root Elongation in Camphor Tree, Plant Physiol., 2011, 155, 433–446

    Article  PubMed  CAS  Google Scholar 

  38. Wang J.-P., Raman H., Zhang G.-P. Mendham N., Zhou M.-X., Aluminium tolerance in barley (Hordeum vulgare L.): physiological mechanisms, genetics and screening methods, J. Zhenjang Univ. Sci. B, 2006, 7, 1862–1783

    Google Scholar 

  39. Zhao Z.Q., Ma J.F., Sato K., Takeda K., Differential Al resistance and citrate secretion in barley (Hordeum vulgare L.), Planta, 2006, 217, 794–800

    Article  Google Scholar 

  40. Silva I.R., Smyth T.J., Raper C.D., Carter T.E., Rufty T.W., Differential aluminum tolerance in soybean: An evaluation of the role of organic acids, Physiol. Plantarum, 2001, 112, 200–210

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Botany, Slovak Academy of Sciences, SK-84523, Bratislava, Slovak Republic

    Peter Paľove-Balang, Milada Čiamporová, Veronika Zelinová, Ján Pavlovkin, Erika Gurinová & Igor Mistrík

  2. Institute of Biological and Ecological Sciences, Faculty of Natural Sciences, P. J. Šafárik University in Košice, SK-04001, Košice, Slovak Republic

    Peter Paľove-Balang

Authors
  1. Peter Paľove-Balang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Milada Čiamporová
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Veronika Zelinová
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ján Pavlovkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Erika Gurinová
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Igor Mistrík
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peter Paľove-Balang.

About this article

Cite this article

Paľove-Balang, P., Čiamporová, M., Zelinová, V. et al. Cellular responses of two Latin-American cultivars of Lotus corniculatus to low pH and Al stress. cent.eur.j.biol. 7, 1046–1054 (2012). https://doi.org/10.2478/s11535-012-0098-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11535-012-0098-0

Keywords

Search

Navigation