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Cysteine Proteases XCP1 And XCP2 Aid Micro-autolysis Within The Intact Central Vacuole During Xylogenesis In Arabidopsis Roots.
U. Avci, H. Earl Petzold, Ihab O Ismail, E. Beers, C. Haigler
Published 2008 · Biology, Medicine
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Establishing the mechanisms regulating the autolysis of xylem tracheary elements (TEs) is important for understanding this programmed cell death process. These data demonstrate that two paralogous Arabidopsis thaliana proteases, XYLEM CYSTEINE PROTEASE1 (XCP1) and XCP2, participated in micro-autolysis within the intact central vacuole before mega-autolysis was initiated by tonoplast implosion. The data acquisition was aided by the predictable pattern of seedling root xylogenesis, the availability of single and double total knock-out T-DNA lines, anti-sera that recognized XCP1 and XCP2, and the microwave-assisted processing of whole seedlings prior to immunolabeling and observation in the transmission electron microscope. During secondary wall thickening, XCP1 and XCP2 (in wild type), XCP1 (in xcp2 seedlings) or XCP2 (in xcp1 seedlings) were imported into the TE central vacuole. Both XCP1 and XCP2 heavily labeled dense aggregates of material within the vacuole. However, because of XCP1 deficiency in xcp1 and xcp1 xcp2 TEs, non-degraded cellular remnants first accumulated in the vacuole and then persisted in the TE lumen (longer than in the wild type) after the final mega-autolysis was otherwise complete. This delayed TE clearing phenotype in xcp1 was rescued by complementation with wild-type XCP1. Although TEs in the xcp2 single knock-out cleared comparably with wild type, the non-degraded remnants in xcp1 xcp2 TEs were more densely packed than in xcp1 TEs. Therefore, XCP2 has a minor but distinct role in micro-autolysis. After tonoplast implosion, XCP1 and XCP2 remained associated with disintegrating cellular material as mega-autolysis, aided by additional lytic enzymes, destroyed the bulk of the cellular contents.
This paper references
The Xylem and Phloem Transcriptomes from Secondary Tissues of the Arabidopsis Root-Hypocotyl1[w]
C. Zhao (2005)
Mass Transport of Proform of a Kdel-Tailed Cysteine Proteinase (Sh-EP) to Protein Storage Vacuoles by Endoplasmic Reticulum–Derived Vesicle Is Involved in Protein Mobilization in Germinating Seeds
K. Toyooka (2000)
TERE; a novel cis-element responsible for a coordinated expression of genes related to programmed cell death and secondary wall formation during differentiation of tracheary elements.
Hyunjin Pyo (2007)
Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana
J. Alonso (2003)
Vacuum-Microwave Combination for Processing Plant Tissues for Electron Microscopy
William A. Russin (2001)
A proteinase-storing body that prepares for cell death or stresses in the epidermal cells of Arabidopsis.
Y. Hayashi (2001)
Microwave cookbook for microscopists : art and science of visualization
L. P. Kok (1992)
Developmental programmed cell death in plants.
H. Kuriyama (2002)
The Plant Vacuolar Sorting Receptor Atelp Is Involved in Transport of Nh2-Terminal Propeptide-Containing Vacuolar Proteins in Arabidopsis thaliana
S. U. Ahmed (2000)
Proteinase Activity during Tracheary Element Differentiation in Zinnia Mesophyll Cultures
E. Beers (1997)
Sucrose synthase localizes to cellulose synthesis sites in tracheary elements.
V. Salnikov (2001)
Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements
A. W. Roberts (2004)
Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia.
K. Obara (2001)
Activity Profiling of Papain-Like Cysteine Proteases in Plants1
R. V. D. van der Hoorn (2004)
Transcription switches for protoxylem and metaxylem vessel formation.
Minoru Kubo (2005)
Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis.
P. Bozhkov (2005)
Localization of sucrose synthase and callose in freeze-substituted secondary-wall-stage cotton fibers
V. Salnikov (2003)
A Vacuolar Processing Enzyme, δVPE, Is Involved in Seed Coat Formation at the Early Stage of Seed Development
Satoru Nakaune (2005)
Loss of Tonoplast Integrity Programmed in Tracheary Element Differentiation.
Induction of cysteine and serine proteases during xylogenesis in Zinnia elegans
Z. Ye (2004)
Tracheary element differentiation.
S. Turner (2007)
Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases.
C. Zhao (2000)
The immunochemical detection and quantitation of intracellular ubiquitin-protein conjugates.
A. L. Haas (1985)
A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves.
K. Yamada (2001)
Proteasome inhibitors prevent tracheary element differentiation in zinnia mesophyll cell cultures
Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis
Microwave fixation provides excellent preservation of tissue, cells and antigens for light and electron microscopy
G. R. Login (2005)
The S8 serine, C1A cysteine and A1 aspartic protease families in Arabidopsis.
E. Beers (2004)
Processing of the papain precursor. Purification of the zymogen and characterization of its mechanism of processing.
T. Vernet (1991)
Protein dynamics and proteolysis in plant vacuoles.
K. Müntz (2007)
Xylogenesis: the birth of a corpse.
K. Roberts (2000)
In-vitro tracheary element formation: structural studies and the effect of tri-iodobenzoic acid
J. Burgess (2004)
Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips ofNicotiana andArabidopsis
J. Kiss (2005)
A unique mechanism for protein processing and degradation in Arabidopsis thaliana
Enrique Rojo (2003)
The intracellular localization of ribulose-1,5-bisphosphate Carboxylase/Oxygenase in chlamydomonas reinhardtii
Proaleurain vacuolar targeting is mediated by short contiguous peptide interactions.
Barry C. Holwerda (1992)
Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
S. Clough (1998)
XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem.
C. Zhao (2008)
Programmed cell death of plant tracheary elements differentiating in vitro
A. Groover (2005)
Regulation of viability and cell death by hormones in cereal aleurone
P. Bethke (2001)
Microwave processing techniques for electron microscopy: a four-hour protocol.
Richard T. Giberson (1999)
Fixation and imaging of biological elements: heavy metals, diffusible substances, ions, peptides, and lipids.
V. Mizuhira (2000)
Pattern of Differentiation of the First Vascular Elements in the Embryo and Seedling of Arabidopsis thaliana
J. Busse (1999)
High pressure freezing and freeze substitution reveal new aspects of fine structure and maintain protein antigenicity in barley aleurone cells
J. Lonsdale (1999)
Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean.
M. Otegui (2005)
Microwave energy fixation of plant tissue: an alternative approach that provides excellent preservation of ultrastructure and antigenicity.
N. Benhamou (1991)
Positional cloning in Arabidopsis. Why it feels good to have a genome initiative working for you.
W. Lukowitz (2000)
Blotting Index of Dissimilarity: use to study immunological relatedness of plant and animal High Mobility Group (HMG) chromosomal proteins
S. Spiker (2004)
Transient and specific expression of a cysteine endopeptidase associated with autolysis during differentiation of Zinnia mesophyll cells into tracheary elements.
A. Minami (1995)
The Arabidopsis xylem peptidase XCP1 is a tracheary element vacuolar protein that may be a papain ortholog.
Vanessa L Funk (2002)
Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development.
J. S. Greenwood (2005)
Cellular organisation of the Arabidopsis thaliana root.
L. Dolan (1993)
Microwave-stimulated glutaraldehyde and osmium tetroxide fixation of plant tissue: ultrastructural preservation in seconds
H. Heumann (2004)
This paper is referenced by
Transcriptional networks orchestrating programmed cell death during plant development.
Marta Cubría-Radío (2019)
Molecular control of cell specification and cell differentiation during procambial development.
K. Furuta (2014)
Arabidopsis NAC Domain Proteins, VND1 to VND5, Are Transcriptional Regulators of Secondary Wall Biosynthesis in Vessels
J. Zhou (2014)
Sacha Escamez (2016)
Subclassification and Biochemical Analysis of Plant Papain-Like Cysteine Proteases Displays Subfamily-Specific Characteristics1[C][W]
Kerstin H. Richau (2012)
Whole-genome re-sequencing of two Italian tomato landraces reveals sequence variations in genes associated with stress tolerance, fruit quality and long shelf-life traits
Valentina Tranchida-Lombardo (2018)
Papain-like peptidases: structure, function, and evolution
Marko Novinec (2013)
[Molecular mechanism of AtGA3OX1 and AtGA3OX2 genes affecting secondary wall thickening in stems in Arabidopsis].
Z. Wang (2013)
Expression and functions of proteases in vascular tissues.
H. Petzold (2012)
Cell death patterns in Arabidopsis cells subjected to four physiological stressors indicate multiple signalling pathways and cell cycle phase specificity
Ranjith Pathirana (2016)
γVPE plays an important role in programmed cell death for xylem fiber cells by activating protease CEP1 maturation in Arabidopsis thaliana.
Ziyi Cheng (2019)
Plant life needs cell death, but does plant cell death need Cys proteases?
Daniela J. Sueldo (2017)
ARACNe-based inference, using curated microarray data, of Arabidopsis thaliana root transcriptional regulatory networks
Ricardo A Chávez Montes (2013)
A unique program for cell death in xylem fibers of Populus stem.
C. Courtois-Moreau (2009)
Ultrastructure of autophagy in plant cells
W. G. van Doorn (2013)
Xylem development - from the cradle to the grave.
Kamil Růžička (2015)
A regular paper for PCP Running title : Protein S-nitrosylation regulates xylem formation Corresponding
Harunori Kawabe (2017)
A distinct subfamily of papain-like cystein proteinases regulated by senescence and stresses in Glycine max.
Belén Esteban-García (2010)
Comparative study of salt stress-induced physiological and molecular responses in tomato (Solanum lycopersicum L.)
Kovács Judit (2017)
Elucidating gene function and function evolution through comparison of co-expression networks of plants
B. O. Hansen (2014)
Induction of a ricinosomal-protease and programmed cell death in tomato endosperm by gibberellic acid
Christopher P. Trobacher (2012)
Temporal analysis of Arabidopsis genes activated by Eucalyptus grandis NAC transcription factors associated with xylem fibre and vessel development
Maritz Laubscher (2018)
Involvement of papain and legumain proteinase in the senescence process of Medicago truncatula nodules.
O. Pierre (2014)
Xylogenesis in zinnia (Zinnia elegans) cell cultures: unravelling the regulatory steps in a complex developmental programmed cell death event
E. Iakimova (2017)
Xylem Development in Trees: From Cambial Divisions to Mature Wood Cells
Jörg Fromm (2013)
Cellular dynamics of the primary shoot and root meristem
Lam Dai Vu (2016)
Plant proteases during developmental programmed cell death.
Rafael Andrade Buono (2019)
Regulation of secondary wall synthesis and cell death by NAC transcription factors in the monocot Brachypodium distachyon
E. R. Valdivia (2013)
Towards Identifying Cis and Trans Regulators of Expression of Xylem Cysteine Protease 1 ( XCP 1 ) in Arabidopsis thaliana
W. Stroud (2009)
The role of the transcription factor ZHOUPI in endosperm Programmed Cell Death during Arabidopsis thaliana seed development
Andrew J. Waters (2014)
The proteasome is responsible for caspase-3-like activity during xylem development.
Jiajia Han (2012)
Quantitative proteomics reveals protein profiles underlying major transitions in aspen wood development
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