Authors:
Judit Kovács University of Szeged, Közép fasor 52, H-6726 Szeged, Hungary

Search for other papers by Judit Kovács in
Current site
Google Scholar
PubMed
Close
,
Péter Poór University of Szeged, Közép fasor 52, H-6726 Szeged, Hungary

Search for other papers by Péter Poór in
Current site
Google Scholar
PubMed
Close
,
Ágnes Szepesi University of Szeged, Közép fasor 52, H-6726 Szeged, Hungary

Search for other papers by Ágnes Szepesi in
Current site
Google Scholar
PubMed
Close
, and
Irma Tari University of Szeged, Közép fasor 52, H-6726 Szeged, Hungary

Search for other papers by Irma Tari in
Current site
Google Scholar
PubMed
Close
Restricted access

The hypersensitive response (HR), a type of programmed cell death (PCD) during biotic stress is mediated by salicylic acid (SA). The aim of this work was to reveal the role of proteolysis and cysteine proteases in the execution of PCD in response of SA. Tomato plants were treated with sublethal (0.1 mM) and lethal (1 mM) SA concentrations through the root system. Treatment with 1 mM SA increased the electrolyte leakage and proteolytic activity and reduced the total protein content of roots after 6 h, while the proteolytic activity did not change in the leaves and in plants exposed to 0.1 mM SA. The expression of the papain-type cysteine protease SlCYP1, the vacuolar processing enzyme SlVPE1 and the tomato metacaspase SlMCA1 was induced within the first three hours in the leaves and after 0.5 h in the roots in the presence of 1 mM SA but the transcript levels did not increase significantly at sublethal SA. The Bax inhibitor-1 (SlBI-1), an antiapoptotic gene was over-expressed in the roots after SA treatments and it proved to be transient in the presence of sublethal SA. Protease inhibitors, SlPI2 and SlLTC were upregulated in the roots by sublethal SA but their expression remained low at 1 mM SA concentration. It is concluded that in contrast to leaves the SA-induced PCD is associated with increased proteolytic activity in the root tissues resulting from a fast up-regulation of specific cysteine proteases and down-regulation of protease inhibitors.

  • 1.

    Benchabane, M., Schlüter, U., Vorster, J., Goulet, M.-C., Michoud, D. (2010) Plant cystatins. Biochemie 92, 16571666.

  • 2.

    Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248254.

    • Search Google Scholar
    • Export Citation
  • 3.

    Chomczynski, P., Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate- phenol-chloroform extraction. Anal. Biochem. 162, 156159.

    • Search Google Scholar
    • Export Citation
  • 4.

    Hatsugai, N., Kuroyanagi, M., Yamada, K., Meshi, T., Tsuda, S., Kondo, M., Hara-Nishimura, I. (2004) A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305, 855858.

    • Search Google Scholar
    • Export Citation
  • 5.

    Hayat, Q., Hayat, S., Irfan, M., Ahmad, A. (2010) Effect of exogenous salicylic acid under changing environment: a review. Environ. Exp. Bot. 68, 1425.

    • Search Google Scholar
    • Export Citation
  • 6.

    Hoeberichts, F. A., Ten Have, A., Woltering, E. J. (2003) A tomato metacaspase gene is upregulated during programmed cell death in Botrytis cinerea-infected leaves. Planta 217, 517522.

    • Search Google Scholar
    • Export Citation
  • 7.

    Horváth, E., Csiszár, J., Gallé, Á., Poór, P., Szepesi, Á., Tari, I. (2015) Hardening with salicylic acid induces concentration-dependent changes in abscisic acid biosynthesis of tomato under salt stress. J. Plant Physiol. 183, 5463.

    • Search Google Scholar
    • Export Citation
  • 8.

    Ishikawa, T., Watabane, N., Nagano, M., Kawai-Yamada, M., Lam, E. (2011) Bax inhibitor-1: a highly conserved endoplasmic reticulum–resident cell death suppressor. Cell Death Diff. 18, 12711278.

    • Search Google Scholar
    • Export Citation
  • 9.

    Jones, J. D., Dangl, J. L. (2006) The plant immune system. Nature 444, 323329.

  • 10.

    Kawai-Yamada, M., Ohori, Y., Uchimiya, H. (2004) Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death. Plant Cell 16, 2132.

    • Search Google Scholar
    • Export Citation
  • 11.

    Kim, I., Xu, W., Reed, J. C. (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nature reviews drug discovery 7, 10131030.

    • Search Google Scholar
    • Export Citation
  • 12.

    Livak, K. J., Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-??CT method. Methods 25, 402408.

    • Search Google Scholar
    • Export Citation
  • 13.

    Lu, S., Faris, J. D., Sherwood, R., Edwards, M. C. (2013) Dimerization and protease resistance: new insight into the function of PR-1. J. Plant Physiol. 170, 105110.

    • Search Google Scholar
    • Export Citation
  • 14.

    Morris, K., Mackerness, S. A. H., Page, T., John, C. F., Murphy, A. M., Carr, J. P., Buchanan-Wollaston, V. (2000) Salicylic acid has a role in regulating gene expression during leaf senescence. Plant J. 23, 677685.

    • Search Google Scholar
    • Export Citation
  • 15.

    Pereira, D. A., Ramos, M. V., Souza, D. P., Portela, T. C., Guimarães, J. A., Madeira, S. V., Freitas, C. D. (2010) Digestibility of defense proteins in latex of milkweeds by digestive proteases of Monarch butterflies, Danaus plexippus L.: a potential determinant of plant–herbivore interactions. Plant Sci. 179, 348355.

    • Search Google Scholar
    • Export Citation
  • 16.

    Poór, P. (2013) Investigation of salt stress- and salicylic acid-induced physiological changes in tomato plants: acclimation or programmed cell death. PhD Thesis, in Hungarian, University of Szeged, Hungary, pp. 6168.

    • Search Google Scholar
    • Export Citation
  • 17.

    Poór, P., Kovács, J., Szopkó, D., Tari, I. (2013) Ethylene signaling in salt stress- and salicylic acidinduced programmed cell death in tomato suspension cells. Protoplasma 250, 273284.

    • Search Google Scholar
    • Export Citation
  • 18.

    Poór, P., Borbély, P., Kovács, J., Papp, A., Szepesi, Á., Takács, Z., Tari, I. (2014) Opposite extremes in ethylene/nitric oxide ratio induce cell death in suspension culture and root apices of tomato exposed to salt stress. Acta Biol. Hung. 65, 428438.

    • Search Google Scholar
    • Export Citation
  • 19.

    Roberts, I. N., Caputo, C., Criado, M. V., Funk, C. (2012) Senescence-associated proteases in plants. Physiol. Plant. 145, 130139.

  • 20.

    Rossano, R., Larocca, M., Riccio, P. (2011) 2-D zymographic analysis of broccoli (Brassica oleracea L. var. Italica) florets proteases: Follow up of cysteine protease isotypes in the course of post-harvest senescence. J. Plant Physiol. 168, 15171525.

    • Search Google Scholar
    • Export Citation
  • 21.

    Sanmartín, M., Jaroszewski, L., Raikhel, N. V., Rojo, E. (2005) Caspases. Regulating death since the origin of life. Plant Physiol. 137, 841847.

    • Search Google Scholar
    • Export Citation
  • 22.

    Shindo, T., van der Horn, R. A. L. (2008) Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders. Mol. Plant Pathol. 9, 119125.

    • Search Google Scholar
    • Export Citation
  • 23.

    Shindo, T., Misas-Villami, J. C., Hörger, A. J., Song, J., van der Horn, R. A. L. (2012) A role in immunity for Arabidopsis cysteine protease RD21, the ortholog of the tomato immune protease C14. PloS ONE 7(1) e29317. doi:10.1371/journal.pone.0029317

    • Search Google Scholar
    • Export Citation
  • 24.

    Singh, M., Bhogal, D., Goel, A., Kumar, A. (2011) Cloning, in silico characterization and interaction of cysteine protease and cystatin for establishing their role in early blight disease in tomato. J. Plant Biochem. Biotech. 20, 110117.

    • Search Google Scholar
    • Export Citation
  • 25.

    Trobacher, C. P., Senatore, A., Greenwood, J. S. (2006) Masterminds or minions? Cysteine proteinases in plant programmed cell death. This review is one of a selection of papers published in the Special Issue on Plant Cell Biology. Botany 84, 651667.

    • Search Google Scholar
    • Export Citation
  • 26.

    van Doorn, W. G. (2011) Classes of programmed cell death in plants, compared to those in animals. J. Exp. Bot. 62, 47494761.

  • 27.

    Woltering, E. J. (2004) Death proteases come alive. Trends Plant Sci. 9, 469472.

  • 28.

    Woltering, E. J. (2010) Death proteases: alive and kicking. Trends Plant Sci. 15, 185188.

  • 29.

    Yamada, K., Nishimura, M., Hara-Nishimura, I. (2004) The slow wound-response of ?VPE is regulated by endogenous salicylic acid in Arabidopsis. Planta 218, 599605.

    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Editorial Board

    1. Csányi, Vilmos (Göd)
    1. Dudits, Dénes (Szeged)
    1. Falus, András (Budapest)
    1. Fischer, Ernő (Pécs)
    1. Gábriel, Róbert (Pécs)
    1. Gulya, Károly (Szeged)
    1. Gulyás, Balázs (Stockholm)
    1. Hajós, Ferenc (Budapest)
    1. Hámori, József (Budapest)
    1. Heszky, László (Gödöllő)
    1. Hideg, Éva (Szeged)
    1. E. Ito (Sanuki)
    1. Janda, Tibor (Martonvásár)
    1. Kavanaugh, Michael P. (Missoula)
    1. Kása, Péter (Szeged)
    1. Klein, Éva (Stockholm)
    1. Kovács, János (Budapest)
    1. Brigitte Mauch-Mani (Neuchâtel)
    1. Nässel, Dick R. (Stockholm)
    1. Nemcsók, János (Szeged)
    1. Péczely, Péter (Gödöllő)
    1. Roberts, D. F. (Newcastle-upon-Tyne)
    1. Sakharov, Dimitri A. (Moscow)
    1. Singh, Meharvan (Fort Worth)
    1. Sipiczky, Mátyás (Debrecen)
    1. Szeberényi, József (Pécs)
    1. Székely, György (Debrecen)
    1. Tari, Irma (Szeged)
    1. Vágvölgyi, Csaba (Szeged),
    1. L. Zaborszky (Newark)

 

Acta Biologica Hungarica
P.O. Box 35
H-8237 Tihany, Hungary
Phone: (36 87) 448 244 ext. 103
Fax: (36 87) 448 006
E-mail: elekes@tres.blki.hu

Indexing and Abstracting Services:

  • Biological Abstracts
  • BIOSIS Previews
  • CAB Abstracts
  • Chemical Abstracts
  • Current Contents: Agriculture
  • Biology and Environmental Sciences
  • Elsevier BIOBASE
  • Global Health
  • Index Medicus
  • Index Veterinarius
  • Medline
  • Referativnyi Zhurnal
  • Science Citation Index
  • Science Citation Index Expanded (SciSearch)
  • SCOPUS
  • The ISI Alerting Services
  • Zoological Abstracts

 

Acta Biologica Hungarica
Language English
Size  
Year of
Foundation
1950
Publication
Programme
changed title
Volumes
per Year
 
Issues
per Year
 
Founder Magyar Tudományos Akadémia
Founder's
Address
H-1051 Budapest, Hungary, Széchenyi István tér 9.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 0236-5383 (Print)
ISSN 1588-256X (Online)