|
Tracheary Element Differentiation Uses a Novel Mechanism
Coordinating Programmed Cell Death and Secondary
Cell Wall
Synthesis1
Andrew Groover2, * and
Alan M. Jones
Department of Biology, University of North Carolina, Chapel Hill,
North Carolina 27599
Tracheary
element differentiation requires strict coordination of secondary cell
wall synthesis and programmed cell death (PCD) to produce a functional
cell corpse. The execution of cell death involves an influx of
Ca2+ into the cell and is manifested by rapid collapse of
the large hydrolytic vacuole and cessation of cytoplasmic streaming.
This precise means of effecting cell death is a prerequisite for
postmortem developmental events, including autolysis and chromatin
degradation. A 40-kD serine protease is secreted during secondary cell
wall synthesis, which may be the coordinating factor between secondary cell wall synthesis and PCD. Specific proteolysis of the extracellular matrix is necessary and sufficient to trigger Ca2+ influx,
vacuole collapse, cell death, and chromatin degradation, suggesting
that extracellular proteolysis plays a key regulatory role during PCD.
We propose a model in which secondary cell wall synthesis and cell
death are coordinated by the concomitant secretion of the 40-kD
protease and secondary cell wall precursors. Subsequent cell death is
triggered by a critical activity of protease or the arrival of
substrate signal precursor corresponding with the completion of a
functional secondary cell wall.
1
Supported in part by the Development Mechanisms
Program of the National Science Foundation. A.G. was supported by
fellowships from the Institute of Marine and Agricultural Research and
by the Graduate School and Department of Biology of the University of
North Carolina at Chapel Hill.
2
Present address: Cold Spring Harbor Laboratory,
P.O. Box 100, Cold Spring Harbor, NY 11724.
*
Corresponding author; e-mail groover{at}cshl.org; fax
1-516-367-8369.
Plant Physiol. (1999) 119: 375-384
Copyright Clearance Center: 0032-0889/99/119//10
© 1999 American Society of Plant Physiologists
This article has been cited by other articles:
|
|
|
|
 
A. Helmersson, S. von Arnold, and P. V. Bozhkov
The Level of Free Intracellular Zinc Mediates Programmed Cell Death/Cell Survival Decisions in Plant Embryos
Plant Physiology,
July 1, 2008;
147(3):
1158 - 1167.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Li, G. Brader, and E. T. Palva
Kunitz Trypsin Inhibitor: An Antagonist of Cell Death Triggered by Phytopathogens and Fumonisin B1 in Arabidopsis
Mol Plant,
May 1, 2008;
1(3):
482 - 495.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Kuthanova, Z. Opatrny, and L. Fischer
Is internucleosomal DNA fragmentation an indicator of programmed death in plant cells?
J. Exp. Bot.,
May 1, 2008;
59(8):
2233 - 2240.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Vizcay-Barrena and Z. A. Wilson
Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant.
J. Exp. Bot.,
August 1, 2006;
57(11):
2709 - 2717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. Pesquet, P. Ranocha, S. Legay, C. Digonnet, O. Barbier, M. Pichon, and D. Goffner
Novel Markers of Xylogenesis in Zinnia Are Differentially Regulated by Auxin and Cytokinin
Plant Physiology,
December 1, 2005;
139(4):
1821 - 1839.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Karlsson, M. Melzer, I. Prokhorenko, T. Johansson, and G. Wingsle
Hydrogen peroxide and expression of hipI-superoxide dismutase are associated with the development of secondary cell walls in Zinnia elegans
J. Exp. Bot.,
August 1, 2005;
56(418):
2085 - 2093.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Chen and M. B. Dickman
Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides
J. Exp. Bot.,
December 1, 2004;
55(408):
2617 - 2623.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. C. Coffeen and T. J. Wolpert
Purification and Characterization of Serine Proteases That Exhibit Caspase-Like Activity and Are Associated with Programmed Cell Death in Avena sativa
PLANT CELL,
April 1, 2004;
16(4):
857 - 873.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
U. Ryser, M. Schorderet, R. Guyot, and B. Keller
A new structural element containing glycine-rich proteins and rhamnogalacturonan I in the protoxylem of seed plants
J. Cell Sci.,
March 1, 2004;
117(7):
1179 - 1190.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Oh, S. Park, and K.-H. Han
Transcriptional regulation of secondary growth in Arabidopsis thaliana
J. Exp. Bot.,
December 1, 2003;
54(393):
2709 - 2722.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Mele, N. Ori, Y. Sato, and S. Hake
The knotted1-like homeobox gene BREVIPEDICELLUS regulates cell differentiation by modulating metabolic pathways
Genes & Dev.,
September 1, 2003;
17(17):
2088 - 2093.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. N. Gushwa, D. Hayashi, A. Kemper, B. Abram, J. E. Taylor, J. Upton, C. F. Tay, S. Fiedler, S. Pullen, L. P. Miller, et al.
Thermotolerant Guard Cell Protoplasts of Tree Tobacco Do Not Require Exogenous Hormones to Survive in Culture and Are Blocked from Reentering the Cell Cycle at the G1-to-S Transition
Plant Physiology,
August 1, 2003;
132(4):
1925 - 1940.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. M. Eklund and J. Edqvist
Localization of Nonspecific Lipid Transfer Proteins Correlate with Programmed Cell Death Responses during Endosperm Degradation in Euphorbia lagascae Seedlings
Plant Physiology,
July 1, 2003;
132(3):
1249 - 1259.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. T. Groover, J. R. Fontana, J. M. Arroyo, C. Yordan, W. R. McCombie, and R. A. Martienssen
Secretion Trap Tagging of Secreted and Membrane-Spanning Proteins Using Arabidopsis Gene Traps
Plant Physiology,
June 1, 2003;
132(2):
698 - 708.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. J. Woltering, A. van der Bent, and F. A. Hoeberichts
Do Plant Caspases Exist?
Plant Physiology,
December 1, 2002;
130(4):
1764 - 1769.
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. GIULIANI, G. CONSONNI, G. GAVAZZI, M. COLOMBO, and S. DOLFINI
Programmed Cell Death during Embryogenesis in Maize
Ann. Bot.,
August 1, 2002;
90(2):
287 - 292.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Aharoni, L. C.P. Keizer, H. C. Van Den Broeck, R. Blanco-Portales, J. Munoz-Blanco, G. Bois, P. Smit, R. C.H. De Vos, and A. P. O'Connell
Novel Insight into Vascular, Stress, and Auxin-Dependent and -Independent Gene Expression Programs in Strawberry, a Non-Climacteric Fruit
Plant Physiology,
July 1, 2002;
129(3):
1019 - 1031.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. S. Reddy, G. S. Ali, and A. S. N. Reddy
Genes Encoding Calmodulin-binding Proteins in the Arabidopsis Genome
J. Biol. Chem.,
March 15, 2002;
277(12):
9840 - 9852.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Kuroyanagi, M. Nishimura, and I. Hara-Nishimura
Activation of Arabidopsis Vacuolar Processing Enzyme by Self-Catalytic Removal of an Auto-Inhibitory Domain of the C-Terminal Propeptide
Plant Cell Physiol.,
February 1, 2002;
43(2):
143 - 151.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. A. Harding, J. Leshkevich, V. L. Chiang, and C.-J. Tsai
Differential Substrate Inhibition Couples Kinetically Distinct 4-Coumarate:Coenzyme A Ligases with Spatially Distinct Metabolic Roles in Quaking Aspen
Plant Physiology,
February 1, 2002;
128(2):
428 - 438.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. V. Dyachok, M. Wiweger, L. Kenne, and S. von Arnold
Endogenous Nod-Factor-Like Signal Molecules Promote Early Somatic Embryo Development in Norway Spruce
Plant Physiology,
February 1, 2002;
128(2):
523 - 533.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Funk, B. Kositsup, C. Zhao, and E. P. Beers
The Arabidopsis Xylem Peptidase XCP1 Is a Tracheary Element Vacuolar Protein That May Be a Papain Ortholog
Plant Physiology,
January 1, 2002;
128(1):
84 - 94.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. C. McCann, N. J. Stacey, P. Dahiya, D. Milioni, P.-E. Sado, and K. Roberts
Zinnia. Everybody Needs Good Neighbors
Plant Physiology,
December 1, 2001;
127(4):
1380 - 1382.
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Lehmann, B. Hause, D. Altmann, and M. Kock
Tomato Ribonuclease LX with the Functional Endoplasmic Reticulum Retention Motif HDEF Is Expressed during Programmed Cell Death Processes, Including Xylem Differentiation, Germination, and Senescence
Plant Physiology,
October 1, 2001;
127(2):
436 - 449.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Y. Hayashi, K. Yamada, T. Shimada, R. Matsushima, N. K. Nishizawa, M. Nishimura, and I. Hara-Nishimura
A Proteinase-Storing Body that Prepares for Cell Death or Stresses in the Epidermal Cells of Arabidopsis
Plant Cell Physiol.,
September 1, 2001;
42(9):
894 - 899.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. Obara, H. Kuriyama, and H. Fukuda
Direct Evidence of Active and Rapid Nuclear Degradation Triggered by Vacuole Rupture during Programmed Cell Death in Zinnia
Plant Physiology,
February 1, 2001;
125(2):
615 - 626.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
S. Endo, T. Demura, and H. Fukuda
Inhibition of Proteasome Activity by the TED4 Protein in Extracellular Space: a Novel Mechanism for Protection of Living Cells from Injury Caused by Dying Cells
Plant Cell Physiol.,
January 1, 2001;
42(1):
9 - 19.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. M. Jones
Programmed Cell Death in Development and Defense
Plant Physiology,
January 1, 2001;
125(1):
94 - 97.
[Full Text]
|
|
|
|
|
|
|
H. Mergemann and M. Sauter
Ethylene Induces Epidermal Cell Death at the Site of Adventitious Root Emergence in Rice
Plant Physiology,
October 1, 2000;
124(2):
609 - 614.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
L. H. Stevens, G. M. Stoopen, I. J.W. Elbers, J. W. Molthoff, H. A.C. Bakker, A. Lommen, D. Bosch, and W. Jordi
Effect of Climate Conditions and Plant Developmental Stage on the Stability of Antibodies Expressed in Transgenic Tobacco
Plant Physiology,
September 1, 2000;
124(1):
173 - 182.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
T. Pechan, L. Ye, Y.-m. Chang, A. Mitra, L. Lin, F. M. Davis, W. P. Williams, and D. S. Luthe
A Unique 33-kD Cysteine Proteinase Accumulates in Response to Larval Feeding in Maize Genotypes Resistant to Fall Armyworm and Other Lepidoptera
PLANT CELL,
July 1, 2000;
12(7):
1031 - 1040.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
V. G.R. Delorme, P. F. McCabe, D.-J. Kim, and C. J. Leaver
A Matrix Metalloproteinase Gene Is Expressed at the Boundary of Senescence and Programmed Cell Death in Cucumber
Plant Physiology,
July 1, 2000;
123(3):
917 - 928.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
C. Zhao, B. J. Johnson, B. Kositsup, and E. P. Beers
Exploiting Secondary Growth in Arabidopsis. Construction of Xylem and Bark cDNA Libraries and Cloning of Three Xylem Endopeptidases
Plant Physiology,
July 1, 2000;
123(3):
1185 - 1196.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
K.-H. Im, D. J. Cosgrove, and A. M. Jones
Subcellular Localization of Expansin mRNA in Xylem Cells
Plant Physiology,
June 1, 2000;
123(2):
463 - 470.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
Y. Xu and M. R. Hanson
Programmed Cell Death during Pollination-Induced Petal Senescence in Petunia
Plant Physiology,
April 1, 2000;
122(4):
1323 - 1334.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
L. Filonova, P. Bozhkov, V. Brukhin, G Daniel, B Zhivotovsky, and S von Arnold
Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce
J. Cell Sci.,
January 12, 2000;
113(24):
4399 - 4411.
[Abstract]
[PDF]
|
|
|
|
|
|
|
H. Kuriyama
Loss of Tonoplast Integrity Programmed in Tracheary Element Differentiation
Plant Physiology,
November 1, 1999;
121(3):
763 - 774.
[Abstract]
[Full Text]
|
|
|
|
|
|
|
T. Yang and B. W. Poovaiah
An Early Ethylene Up-regulated Gene Encoding a Calmodulin-binding Protein Involved in Plant Senescence and Death
J. Biol. Chem.,
December 1, 2000;
275(49):
38467 - 38473.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
