Online citations, reference lists, and bibliographies.

Programmed Cell Death Of Plant Tracheary Elements Differentiating In Vitro

Andrew Groover, Natalie DeWitt, Aaron Heidel, Alexis M. Jones
Published 2005 · Biology
Cite This
Download PDF
Analyze on Scholarcy
Share
SummaryWe used various microscopic and labeling techniques to examine events occurring during the programmed cell death (PCD) of plant tracheary elements (TEs) developing in vitro. TEs differentiating in vitro synthesize a secondary cell wall which is complex in composition and pattern at approximately 72 h after hormone manipulation. The timing of PCD events was established relative to this developmental marker. Cytoplasmic streaming continues throughout secondary wall synthesis, which takes 6 h to complete in a typical cell. Vital dye staining and ultrastructural analysis show that the vacuole and plasma membrane are intact during secondary cell wall synthesis, but the cytoplasm becomes less dense in appearance, most likely through the action of confined hydrolysis by small vacuoles which are seen throughout the cell at this time. The final, preeminent step of TE PCD is a rapid collapse of the vacuole occurring after completion of secondary cell wall synthesis. Vacuole collapse is an irreversible commitment to death which results in the immediate cessation of cytoplasmic streaming and leads to the complete degradation of cellular contents, which is probably accomplished by release of hydrolytic enzymes sequestered in the vacuole. This event represents a novel form of PCD. The degradation of nuclear DNA is detectable by TUNEL, an in situ labeling method, and appears to occur near or after vacuole collapse. Our observations indicate that the process of cellular degradation that produces the hollow TE cell corpse is an active and cell-autonomous process which is distinguishable morphologically and kinetically from necrosis. Although TE PCD does not resemble apoptosis morphologically, we describe the production of spherical protoplast fragments by cultured cells that resemble apoptotic bodies but which are not involved in TE PCD. We also present evidence that, unlike the hypersensitive response (HR), TE PCD does not involve an oxidative burst. While this evidence does not exclude a role for reactive oxygen intermediates in TE PCD, it does suggest TE PCD is mechanistically distinct from cell death during the HR.
This paper references
10.1104/pp.65.1.61
Direct Evidence for Cytodifferentiation to Tracheary Elements without Intervening Mitosis in a Culture of Single Cells Isolated from the Mesophyll of Zinnia elegans.
Hiroo Fukuda (1980)
10.1073/pnas.90.3.980
Do all programmed cell deaths occur via apoptosis?
Lawrence M. Schwartz (1993)
10.1016/S0962-8924(00)88932-1
The role of DNA fragmentation in apoptosis.
Carl D Bortner (1995)
10.1016/S0044-328X(77)80263-8
«Plastolysomes» — Plastids Involved in the Autolysis of the Embryo-Suspensor in Phaseolus
Walter Nagl (1977)
10.1093/jnci/86.17.1286
Mechanisms of apoptosis: integration of genetic, biochemical, and cellular indicators.
Bernard W. Stewart (1994)
A (1972) Certain aspects of xylem
L Srivastava (1972)
Isolation of DNA from small amounts of plant tissue
J Doyle (1990)
10.1126/science.8235659
Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species.
D J Kane (1993)
10.1104/pp.90.1.109
Rapid Stimulation of an Oxidative Burst during Elicitation of Cultured Plant Cells : Role in Defense and Signal Transduction.
Izydor Apostol (1989)
10.1007/BF00411135
In-vitro tracheary element formation: structural studies and the effect of tri-iodobenzoic acid
Jeremy Burgess (2004)
10.1016/0092-8674(94)90218-6
Arabidopsis mutants simulating disease resistance response
Robert A. Dietrich (1994)
10.1126/science.273.5283.1853
Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide
Thorsten Jabs (1996)
10.1007/978-1-4684-4544-2_29
Disease Lesion Mimic Mutations
Virginia Walbot (1983)
10.1139/b72-225
Certain aspects of xylem differentiation in corn
Lalit Mohan Srivastava (1972)
10.1016/0168-9452(95)04095-C
Microscopy of the interaction of hrp mutants of Pseudomonas syringae pv. phaseolicola with a nonhost plant
William F. Fett (1995)
10.1038/bjc.1972.33
Apoptosis: A Basic Biological Phenomenon with Wide-ranging Implications in Tissue Kinetics
J. F. R. Kerr (1972)
10.1104/pp.103.3.805
Gene Expression Patterns Associated with in Vitro Tracheary Element Formation in Isolated Single Mesophyll Cells of Zinnia elegans
Zheng-Hua Ye (1993)
10.1146/annurev.cb.07.110191.003311
Mechanisms and functions of cell death.
Ronald E. Ellis (1991)
10.1016/0092-8674(94)90217-8
Programmed cell death in plants: A pathogen-triggered response activated coordinately with multiple defense functions
Jean T Greenberg (1994)
10.1104/pp.108.2.503
Hrp Mutant of Pseudomonas syringae pv phaseolicola Induces Cell Wall Alterations but Not Membrane Damage Leading to the Hypersensitive Reaction in Lettuce
Charles S. Bestwick (1995)
10.1073/pnas.90.3.853
Apoptosis in C3H/10T1/2 mouse embryonic cells: evidence for internucleosomal DNA modification in the absence of double-strand cleavage.
Louis David Tomei (1993)
10.1104/pp.105.2.467
Active Oxygen Species in Plant Defense against Pathogens
Mona C. Mehdy (1994)
10.1104/pp.110.3.759
The Active Oxygen Response of Cell Suspensions to Incompatible Bacteria Is Not Sufficient to Cause Hypersensitive Cell Death
J. A. Glazener (1996)
10.1007/BF00174615
Developmental cell death: morphological diversity and multiple mechanisms
Peter G. H. Clarke (2004)
10.1086/336211
A View of Ultrastructure of Cucurbita xylem
Katherine Esau (1963)
10.1086/336157
Further Experiments on Wound-Vessel Formation in Stem Wounds of Coleus
Lorin Watson Roberts (1962)
10.1104/pp.65.1.57
Establishment of an Experimental System for the Study of Tracheary Element Differentiation from Single Cells Isolated from the Mesophyll of Zinnia elegans.
Hiroo Fukuda (1980)
10.1007/BF00019005
Isolation and characterization of cDNAs encoding xylogenesis-associated and wounding-induced ribonucleases in Zinnia elegans
Zheng-Hua Ye (2004)
10.1086/336070
Experiments on Xylem Regeneration in Stem Wound Responses in Coleus
Lorin Watson Roberts (1960)
10.1002/j.1537-2197.1967.tb06899.x
ABSCISIN, AUXIN, AND GIBBERELLIN EFFECTS ON THE DEVELOPMENTAL ASPECTS OF ABSCISSION IN COTTON (GOSSYPIUM HIRSUTUM)
Chris H. Bornman (1967)
Nuclear changes during the differentiation of xylem vessel elements
V Lai (1976)
10.1002/j.1537-2197.1973.tb05967.x
ORGANIZATION AND BREAKDOWN OF THE PROTOPLAST DURING MATURATION OF PINE TRACHEIDS
Tomasz J. Wodzicki (1973)
Extracellular superoxide initiates runaway cell death in an Arabidopsis mutant
W Jacobs (1996)
10.1016/S0960-9822(02)00510-9
Calcium-mediated apoptosis in a plant hypersensitive disease resistance response
Alex Levine (1996)
10.1016/S0040-8166(72)80028-4
Cytodifferentiation of maturing pine tracheids: the final stage.
Tomasz J. Wodzicki (1972)
10.1083/jcb.119.3.493
Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation
Y Gavrieli (1992)
10.1002/j.1537-2197.1952.tb14277.x
THE ROLE OF AUXIN IN DIFFERENTIATION OF XYLEM AROUND A WOUND
Wm. P. Jacobs (1952)
10.1093/jxb/17.1.151
The Behaviour of Lysosome-like Particles during Cell Differentiation
Peter B. Gahan (1966)
10.1105/tpc.8.3.393
Cleavage of Nuclear DNA into Oligonucleosomal Fragments during Cell Death Induced by Fungal Infection or by Abiotic Treatments.
Douglas E. Ryerson (1996)
10.1016/S1360-1385(96)90005-9
Logjam at the Styx: programmed cell death in plants
Alan M. Jones (1996)
10.1105/tpc.8.3.375
Apoptosis: A Functional Paradigm for Programmed Plant Cell Death Induced by a Host-Selective Phytotoxin and Invoked during Development.
Huiquan Wang (1996)
10.1105/tpc.7.1.29
Coordinated Activation of Programmed Cell Death and Defense Mechanisms in Transgenic Tobacco Plants Expressing a Bacterial Proton Pump.
Ron Mittler (1995)
10.1007/BF00393688
Identification and purification of a nuclease from Zinnia elegans L.: a potential molecular marker for xylogenesis
Michael P. Thelen (2004)
10.1016/0968-0004(94)90170-8
Dicing with death: dissecting the components of the apoptosis machinery.
S J Martin (1994)
10.1210/endo-124-6-3083
Glucocorticoid endangerment of hippocampal neurons does not involve deoxyribonucleic acid cleavage.
Jeffrey Masters (1989)
10.1016/0739-6260(84)90046-7
Comparison of tracheary element differentiation in intact leaves and isolated mesophyll cells of Zinnia elegans
Jeremy Burgess (1984)
10.1093/nar/20.19.5243
A simple and rapid method for detection of apoptosis in human cells.
Frank Dr Roesl (1992)
Disease lesions mimic mutations
V Walbot (1983)
10.1104/pp.108.2.489
In Situ Detection of nDNA Fragmentation during the Differentiation of Tracheary Elements in Higher Plants
Ron Mittler (1995)
10.1002/j.1460-2075.1990.tb07486.x
A 125 bp promoter fragment is sufficient for strong elicitor-mediated gene activation in parsley.
U van de Löcht (1990)
Apoptosis : a functional paradigm fer programmed cell death induced by a hostselec211 tive phytotoxin and invoked during development
C Meredith (1996)
10.1016/0092-8674(94)90544-4
H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response
Alex Levine (1994)
10.1104/pp.107.4.1241
Plasma Membrane Redox Enzyme Is Involved in the Synthesis of O2- and H2O2 by Phytophthora Elicitor-Stimulated Rose Cells
C. K. Auh (1995)
10.1016/S0074-7696(08)62312-8
Cell death: the significance of apoptosis.
Andrew H. Wyllie (1980)



This paper is referenced by
10.1007/978-3-642-36491-4_1
Xylem Development in Trees: From Cambial Divisions to Mature Wood Cells
Jörg Fromm (2013)
10.1007/s00425-005-1545-1
Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae)
Arunika Hlan Gunawardena (2005)
10.1111/j.1365-313X.2008.03777.x
A unique program for cell death in xylem fibers of Populus stem.
Charleen Laetitia Courtois-Moreau (2009)
10.1016/S0070-2153(05)71007-3
Cell death and organ development in plants.
Hilary J Rogers (2005)
10.1023/A:1026532223173
Programmed cell death of tracheary elements as a paradigm in plants
Hiroo Fukuda (2004)
10.1007/978-94-007-2220-0_3
Stress in Plantation Crops: Adaptation and Management
Kunnummal Kurungara Vinod (2012)
Programmed cell death and tissue remodeling in plants
Arunika Hlan Gunawardena (2007)
Cellular changes of tracheids and ray parenchyma cells from cambium to heartwood in Cunninghamia lanceolata.
Kunlin Song (2011)
10.1163/22941932-90000149
SEASONAL VARIATION IN WOOD FORMATION OF CEDRELA FISSILIS (MELIACEAE)
Carmen Regina Marcati (2006)
10.1007/s10265-010-0384-8
Nuclear DNA fragmentation during cell death of short-lived ray tracheids in the conifer Pinus densiflora
Satoshi Nakaba (2010)
TRACHEARY ELEMENT DIFFERENTIATION AND SECONDARY CELL-WALL FORMATION IN CELL CULTURES OF CONIFEROUS GYMNOSPERMS*
Rickard Möller (2006)
10.1007/s00425-004-1435-y
Cellular re-distribution of flavin-containing polyamine oxidase in differentiating root and mesocotyl of Zea mays L. seedlings
Alessandra Cona (2004)
10.3732/ajb.0800343
In vivo study of developmental programmed cell death using the lace plant (Aponogeton madagascariensis; Aponogetonaceae) leaf model system.
Humberto Wright (2009)
10.1111/plb.12391
The mystery of underground death: cell death in roots during ontogeny and in response to environmental factors.
Agnieszka Bagniewska-Zadworna (2016)
10.1111/tpj.12141
Set-point control of RD21 protease activity by AtSerpin1 controls cell death in Arabidopsis.
Nardy Lampl (2013)
Xylem tissue sp cification , patter ing , and differentiation chanisms thias
Maria Greco (2012)
10.1007/PL00000786
Glycine-rich proteins as structural components of plant cell walls
Christoph Ringli (2001)
10.1146/annurev.arplant.57.032905.105236
Tracheary element differentiation.
Simon R. Turner (2007)
10.1242/jcs.00966
A new structural element containing glycine-rich proteins and rhamnogalacturonan I in the protoxylem of seed plants
Ulrich Ryser (2004)
10.1038/sj.cdd.4400940
Mitochondrial involvement in tracheary element programmed cell death
X-H Yu (2002)
Physique et biologie moléculaire de la vulnérabilité du xylème à la cavitation
Aude Tixier (2013)
CELL SUICIDE OR PROGRAMMED CELL DEATH
Medhat M. Elsahookie مدحت مجيد الساهوكي (2009)
10.1186/s12870-019-1671-8
Transcriptomic profiling identifies differentially expressed genes associated with programmed cell death of nucellar cells in Ginkgo biloba L.
Dahui Li (2019)
Xylem cells cooperate in the control of lignification and cell death during plant vascular development
Sacha Escamez (2016)
10.1093/jxb/eru057
Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal.
Sacha Escamez (2014)
Hydraulic properties of Zinnia elegans : from cellular development in vitro to performance in planta
Peter Twumasi (2007)
10.1177/002215540205000801
An Antigen Expressed During Plant Vascular Development Crossreacts with Antibodies Towards KLH (Keyhole Limpet Hemocyanin)
Anna-Stina Höglund (2002)
10.1104/pp.103.026591
Ozone-Induced Cell Death in Tobacco Cultivar Bel W3 Plants. The Role of Programmed Cell Death in Lesion Formation
Stefania Pasqualini (2003)
10.1007/s00299-009-0753-8
Functional analysis of a cotton cellulose synthase A4 gene promoter in transgenic tobacco plants
Ai-min Wu (2009)
10.1007/PL00000784
Arabinogalactan-proteins: structure, expression and function
Allan M. Showalter (2001)
10.1093/jxb/erm189
Programmed cell death and tissue remodelling in plants.
Arunika Hlan Gunawardena (2008)
10.1016/B978-0-12-385851-1.00004-4
The Botanical Dance of Death: Programmed Cell Death in Plants
Joanna Kacprzyk (2011)
See more
Semantic Scholar Logo Some data provided by SemanticScholar