Home LiteratureArticle Details
PMID: 15020745 Published · ppublish English Journal Article Research Support, U.S. Gov't, Non-P.H.S.

Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa.

The Plant cell ·Vol. 16 ·No. 4 ·2004-04-00 ·Pages 857-73

Coffeen WC, Wolpert TJ

Abstract

Victoria blight of Avena sativa (oat) is caused by the fungus Cochliobolus victoriae, which is pathogenic because of the production of the toxin victorin. The victorin-induced response in sensitive A. sativa has been characterized as a form of programmed cell death (PCD) and displays morphological and biochemical features similar to apoptosis, including chromatin condensation, DNA laddering, cell shrinkage, altered mitochondrial function, and ordered, substrate-specific proteolytic events. Victorin-induced proteolysis of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is shown to be prevented by caspase-specific and general protease inhibitors. Evidence is presented for a signaling cascade leading to Rubisco proteolysis that involves multiple proteases. Furthermore, two proteases that are apparently involved in the Rubisco proteolytic cascade were purified and characterized. These proteases exhibit caspase specificity and display amino acid sequences homologous to plant subtilisin-like Ser proteases. The proteases are constitutively present in an active form and are relocalized to the extracellular fluid after induction of PCD by either victorin or heat shock. The role of the enzymes as processive proteases involved in a signal cascade during the PCD response is discussed.

MeSH Terms
Amino Acid Sequence Apoptosis/drug effects,physiology Ascomycota/pathogenicity Avena/chemistry,enzymology,genetics,microbiology Caspase Inhibitors Caspases/genetics,isolation & purification,metabolism Cysteine Proteinase Inhibitors/pharmacology Fungal Proteins/toxicity Genes, Plant Heat-Shock Response Heparin/metabolism Molecular Sequence Data Multigene Family Mycotoxins/toxicity Peptide Mapping Plant Diseases/microbiology Ribulose-Bisphosphate Carboxylase/metabolism Sequence Homology, Amino Acid Serine Endopeptidases/genetics,isolation & purification,metabolism Signal Transduction
Chemicals
Caspase Inhibitors Cysteine Proteinase Inhibitors Fungal Proteins Mycotoxins Victorin protein, Cochliobolus victoriae Heparin Serine Endopeptidases Caspases Ribulose-Bisphosphate Carboxylase
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Coffeen Warren C
Department of Botany and Plant Pathology and Center for Gene Research and Biotechnology, Oregon State University, Corvallis 97331-2902, USA.
Wolpert Thomas J
References (82)
82 references, click to expand
  1. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis.
    Cell. 2002 Mar 22;108(6):743-54 PMID: 11955429
  2. The involvement of poly(ADP-ribose) polymerase in the oxidative stress responses in plants.
    FEBS Lett. 1998 Nov 27;440(1-2):1-7 PMID: 9862413
  3. BRS1, a serine carboxypeptidase, regulates BRI1 signaling in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 2001 May 8;98(10):5916-21 PMID: 11320207
  4. Macluralisin--a serine proteinase from fruits of Maclura pomifera (Raf.) Schneid.
    Planta. 1995;196(1):174-9 PMID: 7767235
  5. A Purified Zinc Protease of Pea Chloroplasts, EP1, Degrades the Large Subunit of Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase.
    Plant Physiol. 1993 Oct;103(2):585-591 PMID: 12231963
  6. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis.
    Science. 2002 Apr 26;296(5568):744-7 PMID: 11976458
  7. Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions.
    Plant Cell. 1996 Oct;8(10):1793-1807 PMID: 12239362
  8. Involvement of poly(ADP-ribose) polymerase and activation of caspase-3-like protease in heat shock-induced apoptosis in tobacco suspension cells.
    FEBS Lett. 2000 May 26;474(1):11-5 PMID: 10828442
  9. Proteolytic activities that mediate apoptosis.
    Annu Rev Physiol. 1998;60:533-73 PMID: 9558476
  10. Yeast KEX2 genes encodes an endopeptidase homologous to subtilisin-like serine proteases.
    Biochem Biophys Res Commun. 1988 Oct 14;156(1):246-54 PMID: 2845974
  11. Gastrulation defective is a serine protease involved in activating the receptor toll to polarize the Drosophila embryo.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9093-7 PMID: 10922064
  12. The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death.
    Plant J. 2002 Feb;29(3):295-312 PMID: 11844107
  13. Apoptosis and predisposition to oral cancer.
    Crit Rev Oral Biol Med. 1999;10(2):139-52 PMID: 10759418
  14. Identification of a 50-kDa systemin-binding protein in tomato plasma membranes having Kex2p-like properties.
    Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11802-6 PMID: 7991538
  15. SEP-1 - a subtilisin-like serine endopeptidase from germinated seeds of Hordeum vulgare L. cv. Morex.
    Planta. 2002 Oct;215(6):885-93 PMID: 12355148
  16. A cysteine endopeptidase with a C-terminal KDEL motif isolated from castor bean endosperm is a marker enzyme for the ricinosome, a putative lytic compartment.
    Planta. 1998 Oct;206(3):466-75 PMID: 9763713
  17. Caspase inhibitors.
    Cell Death Differ. 1999 Nov;6(11):1081-6 PMID: 10578177
  18. Pathogen-induced programmed cell death in plants, a possible defense mechanism.
    Dev Genet. 1997;21(4):279-89 PMID: 9438342
  19. Do plant caspases exist?
    Plant Physiol. 2002 Dec;130(4):1764-9 PMID: 12481059
  20. A C-terminal domain conserved in precursor processing proteases is required for intramolecular N-terminal maturation of pro-Kex2 protease.
    EMBO J. 1994 May 15;13(10):2280-8 PMID: 8194519
  21. Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14159-64 PMID: 10570215
  22. Antisense inhibition of a tomato meiotic proteinase suggests functional redundancy of proteinases during microsporogenesis.
    Genome. 2001 Aug;44(4):644-50 PMID: 11550900
  23. Last exit: senescence, abscission, and meristem arrest in Arabidopsis.
    Plant Cell. 1997 Jul;9(7):1169-79 PMID: 9254934
  24. Activation of cysteine proteases in cowpea plants during the hypersensitive response--a form of programmed cell death.
    Exp Cell Res. 1998 Dec 15;245(2):389-99 PMID: 9851880
  25. Subtilases: the superfamily of subtilisin-like serine proteases.
    Protein Sci. 1997 Mar;6(3):501-23 PMID: 9070434
  26. Characterization of P69E and P69F, two differentially regulated genes encoding new members of the subtilisin-like proteinase family from tomato plants.
    Plant Physiol. 2000 Jan;122(1):67-74 PMID: 10631250
  27. Proteases, proteolysis, and apoptosis.
    Cell Biol Toxicol. 1998 Mar;14(2):121-32 PMID: 9553723
  28. Autoproteolysis and feedback in a protease cascade directing Drosophila dorsal-ventral cell fate.
    EMBO J. 2001 May 15;20(10):2387-93 PMID: 11350927
  29. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis.
    J Biol Chem. 1997 Jul 18;272(29):17907-11 PMID: 9218414
  30. Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death.
    Mol Plant Microbe Interact. 1998 Jun;11(6):544-54 PMID: 9612953
  31. Victorin induction of an apoptotic/senescence-like response in oats.
    Plant Cell. 1999 Feb;11(2):237-49 PMID: 9927641
  32. Cell death in development.
    Cell. 1999 Jan 22;96(2):245-54 PMID: 9988219
  33. Caspases and programmed cell death in the hypersensitive response of plants to pathogens.
    Curr Biol. 1998 Oct 8;8(20):1129-32 PMID: 9778530
  34. A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana.
    Genes Dev. 2000 May 1;14(9):1119-31 PMID: 10809670
  35. Characterization of LRP, a leucine-rich repeat (LRR) protein from tomato plants that is processed during pathogenesis.
    Plant J. 1996 Aug;10(2):315-30 PMID: 8771787
  36. Reinforcing the idea of signalling in the stomatal pathway.
    Trends Genet. 2002 Dec;18(12):597-600 PMID: 12446135
  37. Characterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill.).
    Plant Mol Biol. 1999 Mar;39(4):749-60 PMID: 10350089
  38. Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors.
    Mol Plant Microbe Interact. 2001 Apr;14(4):477-86 PMID: 11310735
  39. Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis
    Plant Physiol. 1999 Feb;119(2):375-84 PMID: 9952432
  40. The biochemistry of apoptosis.
    Nature. 2000 Oct 12;407(6805):770-6 PMID: 11048727
  41. Activation of caspase-like proteases and induction of apoptosis by isopentenyladenosine in tobacco BY-2 cells.
    Planta. 2002 May;215(1):158-66 PMID: 12012253
  42. Maturation and secretion of a serine proteinase is associated with events of late microsporogenesis.
    Plant J. 1997 Dec;12(6):1261-71 PMID: 9450340
  43. Effect of the Specific Toxin in Helminthosporium victoriae on Host Cell Membranes.
    Plant Physiol. 1968 Jan;43(1):21-8 PMID: 16656731
  44. Ara12 subtilisin-like protease from Arabidopsis thaliana: purification, substrate specificity and tissue localization.
    Biochem J. 2003 Feb 15;370(Pt 1):57-67 PMID: 12413398
  45. Constitutive caspase-like machinery executes programmed cell death in plant cells.
    Cell Death Differ. 2002 Jul;9(7):726-33 PMID: 12058273
  46. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants.
    Plant Cell. 1999 Mar;11(3):431-44 PMID: 10072402
  47. Changes in Permeability Induced by Victorin.
    Science. 1962 Sep 21;137(3534):983-4 PMID: 17782735
  48. Furin: the prototype mammalian subtilisin-like proprotein-processing enzyme. Endoproteolytic cleavage at paired basic residues of proproteins of the eukaryotic secretory pathway.
    Enzyme. 1991;45(5-6):257-70 PMID: 1843280
  49. A New Helminthosporium Blight of Oats.
    Science. 1946 Nov 1;104(2705):413-4 PMID: 17814758
  50. Comparison of the molecular forms of the Kex2/subtilisin-like serine proteases SPC2, SPC3, and furin in neuroendocrine secretory vesicles reveals differences in carboxyl-terminus truncation and membrane association.
    J Neurochem. 1995 Nov;65(5):2318-26 PMID: 7595521
  51. Interaction of heparin and antithrombin III. The role of O-sulfate groups.
    Eur J Biochem. 1988 Oct 1;176(3):637-40 PMID: 3169017
  52. Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats.
    Plant J. 2001 Oct;28(1):13-26 PMID: 11696183
  53. Taraxalisin -- a serine proteinase from dandelion Taraxacum officinale Webb s.l.
    FEBS Lett. 1998 Oct 23;437(3):237-40 PMID: 9824298
  54. Chemical-induced apoptotic cell death in tomato cells: involvement of caspase-like proteases.
    Planta. 2000 Oct;211(5):656-62 PMID: 11089678
  55. A genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants.
    J Biol Chem. 1999 Jan 22;274(4):2360-5 PMID: 9891003
  56. Apoptosis: (2) characteristics of apoptosis.
    J Formos Med Assoc. 1999 Aug;98(8):531-42 PMID: 10502906
  57. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death.
    EMBO J. 2003 Jan 2;22(1):60-9 PMID: 12505984
  58. The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity.
    Plant J. 2004 Apr;38(2):244-59 PMID: 15078328
  59. Pathogenesis-related proteins of tomato : p-69 as an alkaline endoproteinase.
    Plant Physiol. 1988 May;87(1):58-63 PMID: 16666127
  60. Early stages of seed development in Brassica napus: a seed coat-specific cysteine proteinase associated with programmed cell death of the inner integument.
    Plant J. 2002 Apr;30(1):1-10 PMID: 11967088
  61. Characterization of the binding site on heparan sulfate for macrophage inflammatory protein 1alpha.
    Blood. 2002 Sep 1;100(5):1543-50 PMID: 12176868
  62. A novel subtilase from common bean leaves.
    FEBS Lett. 2002 Oct 23;530(1-3):163-8 PMID: 12387886
  63. The gastrulation defective gene of Drosophila melanogaster is a member of the serine protease superfamily.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6819-24 PMID: 9618496
  64. Gastrulation defective, a complement factor C2/B-like protease, interprets a ventral prepattern in Drosophila.
    EMBO Rep. 2001 Aug;2(8):721-6 PMID: 11493599
  65. Identification of a new pathogen-induced member of the subtilisin-like processing protease family from plants.
    J Biol Chem. 1997 May 30;272(22):14412-9 PMID: 9162080
  66. Cytochrome c release and caspase activation during menadione-induced apoptosis in plants.
    FEBS Lett. 1999 Dec 3;462(3):317-21 PMID: 10622718
  67. Apoptotic DNA fragmentation.
    Exp Cell Res. 2000 Apr 10;256(1):12-8 PMID: 10739646
  68. Differential Phytotoxicity of Metabolic By-Products of Helminthosporium victoriae.
    Science. 1947 Sep 19;106(2751):270-1 PMID: 17777075
  69. Primary structure and expression of a pathogen-induced protease (PR-P69) in tomato plants: Similarity of functional domains to subtilisin-like endoproteases.
    Proc Natl Acad Sci U S A. 1996 Jun 25;93(13):6332-7 PMID: 8692815
  70. Heparin-protein interactions.
    Angew Chem Int Ed Engl. 2002 Feb 1;41(3):391-412 PMID: 12491369
  71. Cucumisin, a serine protease from melon fruits, shares structural homology with subtilisin and is generated from a large precursor.
    J Biol Chem. 1994 Dec 30;269(52):32725-31 PMID: 7806492
  72. Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis.
    Plant Physiol. 1999 Aug;120(4):1015-24 PMID: 10444084
  73. LeSBT1, a subtilase from tomato plants. Overexpression in insect cells, purification, and characterization.
    J Biol Chem. 2000 Feb 18;275(7):5193-9 PMID: 10671566
  74. Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation.
    Plant Mol Biol. 1999 Jan;39(2):273-87 PMID: 10080694
  75. Conversion of ribulose-1,5-bisphosphate carboxylase to an acidic and catalytically inactive form by extracts of osmotically stressed Lemna minor fronds.
    Planta. 1989 Nov;179(4):448-55 PMID: 24201768
  76. Molecular cloning and characterization of a cDNA and a gene for subtilisin-like serine proteases from rice (Oryza sativa L.) and Arabidopsis thaliana.
    Biosci Biotechnol Biochem. 2000 Sep;64(9):1947-57 PMID: 11055401
  77. Activation of a protease cascade involved in patterning the Drosophila embryo.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5055-60 PMID: 11296245
  78. A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants.
    Development. 2001 Dec;128(23):4681-9 PMID: 11731449
  79. Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants.
    FEBS Lett. 1999 Dec 10;463(1-2):151-4 PMID: 10601657
  80. A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber.
    Plant Physiol. 2000 Jul;123(3):917-27 PMID: 10889240
  81. Phytepsin, a barley vacuolar aspartic proteinase, is highly expressed during autolysis of developing tracheary elements and sieve cells.
    Plant J. 1998 Jul;15(1):139-45 PMID: 9744102
  82. The ricinosomes of senescing plant tissue bud from the endoplasmic reticulum.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5353-8 PMID: 11296243
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2004-04-00
Epub
2004-00-12
Pages
857-73
Language
English
Region
England
NLM ID
9208688
PMCID
PMC412861
Subset
IM
Databases
GENBANK
A55800, BAB89803, CAA76724, CAA76725, T06577
RefSeq
NP_569048
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]