Laboratory of Molecular Biology of the Gene
Department of Chemistry and Biochemistry of Nucleoproteins
Leader: Andrey B. Vartapetian
Plant Direction:
The group headed by Dr. Nina Chichkova has identified phytaspases (plant aspartate-specific proteases) – novel proteolytic enzymes involved in the execution of stress-induced programmed cell death (PCD) in plants (Chichkova et al., Plant Cell 2004; EMBO J. 2010). Phytaspases are highly selective proteases with a strict specificity, as they only cleave after aspartate residues within a defined amino acid motif (Galiullina et al., J. Biol. Chem. 2015) Phytaspase activity becomes apparent in dying plant cells. Phytaspase overexpression significantly enhances PCD induced by biotic and abiotic stresses, whereas inhibition of these enzymes results in suppression of PCD (Chichkova et al., EMBO J. 2010; Vartapetian et al., Cell Death Differ. 2011; Chichkova et al., Physiol. Plant. 2012). Thus, phytaspases apparently represent functional analogues of the animal apoptotic proteases known as caspases.
Structurally, phytaspases belong to the family of subtilisin-like (that is, Ser-dependent) proteases and are thus distinct from caspases. Phytaspases are synthesized as proteolytically inactive precursor proteins, and their activation occurs constitutively via autocatalytic processing of the proenzyme. In healthy plant tissues, phytaspases are secreted from the cells into the intercellular fluid (apoplast). This allows spatial separation of the active enzyme from its intracellular protein targets and thus avoidance of unintended cell death. Upon the induction of PCD, phytaspases are rapidly relocalized from the apoplast to the cytoplasm to gain access to intracellular targets (Chichkova et al., EMBO J. 2010). This retrograde transport of phytaspases involves clathrin-mediated endocytosis (Trusova et al., J. Exp. Bot. 2019) and appears to have no precedent among plant proteases.
Apart from their role in the accomplishment of plant cell death, phytaspases appear to possess multiple functions. A role for phytaspases in mediating defense signaling in plants was illuminated by the finding that phytaspases perform processing of the precursor protein of the wound hormone systemin. Phytaspase-mediated processing generates the bioactive peptide capable of initiating the systemic wound-induced defense response in plants (Beloshistov et al., New Phytol. 2018).
The group collaborated with the laboratories of:
Dr. Michael Taliansky (The James Hutton Institute, UK);
Dr. Andreas Schaller (Institute of Plant Physiology and Biotechnology, University of Hohenheim, Germany);
Dr. Marcin Drag (Wroclaw University of Technology, Poland);
Dr. Patrick Gallois (University of Manchester, UK).
Recent Publications:
Beloshistov RE, Dreizler K, Galiullina RA, Tuzhikov AI, Serebryakova MV, Reichardt S, Shaw J, Taliansky ME, Pfannstiel J, Chichkova NV, Stintzi A, Schaller A and Vartapetian AB (2018) Phytaspase-mediated precursor processing and maturation of the wound hormone systemin. New Phytol. 218, 1167-1178.
Chichkova N.V., Galiullina R.A., Mochalova L.V., Trusova S.V., Sobri Z.M., Gallois P., and Vartapetian A.B. (2018) Arabidopsis thaliana phytaspase: identification and peculiar properties. Funct. Plant Biol. 45, 171-179.
Schaller A, Stintzi A, Rivas S, Serrano I, Chichkova NV, Vartapetian AB, Martinez D, Guiamet JJ, Sueldo DJ, van der Hoorn RAL, Ramirez V, Vera P (2018) From structure to function – a family portrait of plant subtilases. New Phytol. 218, 901-915.
Reichardt S, Repper D, Tuzhikov AI, Galiullina RA, Planas-Marques M, Chichkova NV, Vartapetian AB, Stintzi A, Schaller A (2018) The tomato subtilase family includes several cell death-related proteinases with caspase specificity. Scientific Reports 8(1), 10531.
Trusova S.V., Golyshev S.A., Chichkova N.V., Vartapetian A.B. (2019) Sometimes they come back: endocytosis provides localization dynamics of a subtilase in cells committed to cell death. J. Exp. Botany, in press, https://doi.org/10.1093/jxb/erz014
The group headed by Dr. Nina Chichkova has identified phytaspases (plant aspartate-specific proteases) – novel proteolytic enzymes involved in the execution of stress-induced programmed cell death (PCD) in plants (Chichkova et al., Plant Cell 2004; EMBO J. 2010). Phytaspases are highly selective proteases with a strict specificity, as they only cleave after aspartate residues within a defined amino acid motif (Galiullina et al., J. Biol. Chem. 2015) Phytaspase activity becomes apparent in dying plant cells. Phytaspase overexpression significantly enhances PCD induced by biotic and abiotic stresses, whereas inhibition of these enzymes results in suppression of PCD (Chichkova et al., EMBO J. 2010; Vartapetian et al., Cell Death Differ. 2011; Chichkova et al., Physiol. Plant. 2012). Thus, phytaspases apparently represent functional analogues of the animal apoptotic proteases known as caspases.
Structurally, phytaspases belong to the family of subtilisin-like (that is, Ser-dependent) proteases and are thus distinct from caspases. Phytaspases are synthesized as proteolytically inactive precursor proteins, and their activation occurs constitutively via autocatalytic processing of the proenzyme. In healthy plant tissues, phytaspases are secreted from the cells into the intercellular fluid (apoplast). This allows spatial separation of the active enzyme from its intracellular protein targets and thus avoidance of unintended cell death. Upon the induction of PCD, phytaspases are rapidly relocalized from the apoplast to the cytoplasm to gain access to intracellular targets (Chichkova et al., EMBO J. 2010). This retrograde transport of phytaspases involves clathrin-mediated endocytosis (Trusova et al., J. Exp. Bot. 2019) and appears to have no precedent among plant proteases.
Apart from their role in the accomplishment of plant cell death, phytaspases appear to possess multiple functions. A role for phytaspases in mediating defense signaling in plants was illuminated by the finding that phytaspases perform processing of the precursor protein of the wound hormone systemin. Phytaspase-mediated processing generates the bioactive peptide capable of initiating the systemic wound-induced defense response in plants (Beloshistov et al., New Phytol. 2018).
The group collaborated with the laboratories of:
Dr. Michael Taliansky (The James Hutton Institute, UK);
Dr. Andreas Schaller (Institute of Plant Physiology and Biotechnology, University of Hohenheim, Germany);
Dr. Marcin Drag (Wroclaw University of Technology, Poland);
Dr. Patrick Gallois (University of Manchester, UK).
Recent Publications:
Beloshistov RE, Dreizler K, Galiullina RA, Tuzhikov AI, Serebryakova MV, Reichardt S, Shaw J, Taliansky ME, Pfannstiel J, Chichkova NV, Stintzi A, Schaller A and Vartapetian AB (2018) Phytaspase-mediated precursor processing and maturation of the wound hormone systemin. New Phytol. 218, 1167-1178.
Chichkova N.V., Galiullina R.A., Mochalova L.V., Trusova S.V., Sobri Z.M., Gallois P., and Vartapetian A.B. (2018) Arabidopsis thaliana phytaspase: identification and peculiar properties. Funct. Plant Biol. 45, 171-179.
Schaller A, Stintzi A, Rivas S, Serrano I, Chichkova NV, Vartapetian AB, Martinez D, Guiamet JJ, Sueldo DJ, van der Hoorn RAL, Ramirez V, Vera P (2018) From structure to function – a family portrait of plant subtilases. New Phytol. 218, 901-915.
Reichardt S, Repper D, Tuzhikov AI, Galiullina RA, Planas-Marques M, Chichkova NV, Vartapetian AB, Stintzi A, Schaller A (2018) The tomato subtilase family includes several cell death-related proteinases with caspase specificity. Scientific Reports 8(1), 10531.
Trusova S.V., Golyshev S.A., Chichkova N.V., Vartapetian A.B. (2019) Sometimes they come back: endocytosis provides localization dynamics of a subtilase in cells committed to cell death. J. Exp. Botany, in press, https://doi.org/10.1093/jxb/erz014
Articles
- Galiullina R.A., Pigidanov A.A., Safronov G.G., Trusova S.V., Teplova A.D., Golyshev S.A., Serebryakova M.V., Kovaleva I.E., Litvinova A.V., Chichkova N.V., Vartapetian A.B.(2025) Retrograde transport of tobacco phytaspase is mediated by its partner, Tubby-like F-box protein 8. International Journal of Molecular Sciences, >>
- Galiullina R.A., Chichkova N.V., Safronov G.G., Vartapetian A.B.(2023) Characterization of Phytaspase Proteolytic Activity Using Fluorogenic Peptide Substrates. Methods in molecular biology (Clifton, N.J.), >>
- Galiullina R.A., Dyugay I.A., Vartapetian A.B., Chichkova N.V.(2023) Purification of Phytaspases Using a Biotinylated Peptide Inhibitor. Methods in molecular biology (Clifton, N.J.), >>
- Teplova Anastasia D., Pigidanov Artemii A., Serebryakova Marina V., Golyshev Sergei A., Galiullina Raisa A., Chichkova Nina V., Vartapetian Andrey B.(2023) Phytaspase is Capable of Detaching the Endoplasmic Reticulum Retrieval Signal from Tobacco Calreticulin-3. International Journal of Molecular Sciences, >>
- Teplova A.D., Serebryakova M.V., Galiullina R.A., Chichkova N.V., Vartapetian A.B.(2021) Identification of Phytaspase Interactors via the Proximity-Dependent Biotin-Based Identification Approach. International Journal of Molecular Sciences, >>
- Beloshistov RE, Dreizler K., Galiullina RA, Tuzhikov AI, Serebryakova MV, Reichardt S., Shaw J., Taliansky ME, Pfannstiel J., Chichkova NV, Stintzi A., Schaller A., Vartapetian AB(2018) Phytaspase-mediated precursor processing and maturation of the wound hormone systemin. New Phytologist, >>
- Schaller A., Stintzi A., Rivas S., Serrano I., Chichkova NV, Vartapetian AB, Martinez D., Guiamet JJ, Sueldo DJ, van_der_Hoorn RAL, Ramirez V., Vera P.(2018) From structure to function – a family portrait of plant subtilases. New Phytologist, >>
- Torosian T.A., Barsukova A.I., Chichkova N.V., Vartapetian A.B.(2024) Phytaspase Does Not Require Proteolytic Activity for Its Stress-Induced Internalization. International Journal of Molecular Sciences, >>