The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers

H2O2 is a widespread molecule in many biological systems. It is created enzymatically in living cells during various oxidation reactions and by leakage of electrons from the electron transport chains. Depending on the concentration H2O2 can induce cell protective responses, programmed cell death, or necrosis. Here we provide evidence that H2O2 may function as a developmental signal in the differentiation of secondary walls in cotton (Gossypium hirsutum) fibers. Three lines of evidence support this conclusion: (a) the period of H2O2 generation coincided with the onset of secondary wall deposition, (b) inhibition of H2O2 production or scavenging the available H2O2 from the system prevented the wall differentiation process, and (c) exogenous addition of H2O2 prematurely promoted secondary wall formation in young fibers. Furthermore, we provide support for the concept that H2O2 generation could be mediated by the expression of the small GTPase Rac, the accumulation of which was shown previously to be strongly induced during the onset of secondary wall differentiation. In support of Rac's role in the activation of NADPH oxidase and the generation of reactive oxygen species, we transformed soybean (Glycine max) and Arabidopsis cells with mutated Rac genes. Transformation with a dominantly activated cotton Rac13 gene resulted in constitutively higher levels of H2O2, whereas transformation with the antisense and especially with dominant-negative Rac constructs decreased the levels of H2O2.

[1]  G. De Lorenzo,et al.  Oligogalacturonides stimulate pericycle cell wall thickening and cell divisions leading to stoma formation in tobacco leaf explants , 1998, Planta.

[2]  R. Dixon,et al.  A Plant Homolog of the Neutrophil NADPH Oxidase gp91phox Subunit Gene Encodes a Plasma Membrane Protein with Ca2+ Binding Motifs , 1998, Plant Cell.

[3]  H. Asard,et al.  Solubilization and Separation of a Plant Plasma Membrane NADPH-O2- Synthase from Other NAD(P)H Oxidoreductases , 1997, Plant physiology.

[4]  A. Allan,et al.  Two Distinct Sources of Elicited Reactive Oxygen Species in Tobacco Epidermal Cells. , 1997, The Plant cell.

[5]  A. Mithöfer,et al.  Involvement of an NAD(P)H oxidase in the elicitor-inducible oxidative burst of soybean , 1997 .

[6]  C. Langebartels,et al.  Changes in the biochemical status of plant cells induced by the environmental pollutant ozone , 1997 .

[7]  T. Jabs,et al.  Elicitor-stimulated ion fluxes and O2- from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[8]  J. Zweier,et al.  Mitogenic Signaling Mediated by Oxidants in Ras-Transformed Fibroblasts , 1997, Science.

[9]  J. Blein,et al.  Tobacco cells contain a protein, immunologically related to the neutrophil small G protein Rac2 and involved in elicitor‐induced oxidative burst , 1997, FEBS letters.

[10]  E. Blumwald,et al.  Race-specific elicitors of Cladosporium fulvum promote translocation of cytosolic components of NADPH oxidase to the plasma membrane of tomato cells. , 1997, The Plant cell.

[11]  M. Bennett,et al.  Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. , 1997, The Plant cell.

[12]  G. Kotliar,et al.  The Metal-Insulator Transition in Correlated Disordered Systems , 1996, Science.

[13]  T. K. Prasad.  Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities , 1996 .

[14]  D. Delmer,et al.  Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[15]  T. Jabs,et al.  Initiation of Runaway Cell Death in an Arabidopsis Mutant by Extracellular Superoxide , 1996, Science.

[16]  Jonathan D. G. Jones,et al.  rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. , 1996, The Plant journal : for cell and molecular biology.

[17]  V. Ferrans,et al.  Regulation of reactive-oxygen-species generation in fibroblasts by Rac1. , 1996, The Biochemical journal.

[18]  A. Abo,et al.  Rac “Insert Region” Is a Novel Effector Region That Is Implicated in the Activation of NADPH Oxidase, but Not PAK65* , 1996, The Journal of Biological Chemistry.

[19]  H. Fukuda.  XYLOGENESIS: INITIATION, PROGRESSION, AND CELL DEATH. , 1996, Annual review of plant physiology and plant molecular biology.

[20]  M. Symons,et al.  Rho family GTPases: the cytoskeleton and beyond. , 1996, Trends in biochemical sciences.

[21]  G. Bolwell.  The origin of the oxidative burst in plants. , 1996, Biochemical Society transactions.

[22]  C. Lamb,et al.  Calcium-mediated apoptosis in a plant hypersensitive disease resistance response , 1996, Current Biology.

[23]  É. Hideg,et al.  UV-B induced free radical production in plant leaves and isolated thylakoid membranes , 1996 .

[24]  P. Low,et al.  Plant and human neutrophil oxidative burst complexes contain immunologically related proteins. , 1996, Biochimica et biophysica acta.

[25]  P. Low,et al.  The oxidative burst in plant defense: Function and signal transduction , 1996 .

[26]  T. Murphy,et al.  The Superoxide Synthases of Plasma Membrane Preparations from Cultured Rose Cells , 1996, Plant physiology.

[27]  G. Paliyath,et al.  Ultraviolet-B- and Ozone-Induced Biochemical Changes in Antioxidant Enzymes of Arabidopsis thaliana , 1996, Plant physiology.

[28]  D. Loisance,et al.  Inhibition of hydroxyl radical production by lactobionate, adenine, and tempol. , 1995, Free radical biology & medicine.

[29]  F. Farzaneh,et al.  Quantitative multiwell myeloid differentiation assay using dichlorodihydrofluorescein diacetate (H2DCF-DA) or dihydrorhodamine 123 (H2R123). , 1995, Journal of immunological methods.

[30]  J P Knox,et al.  Developmentally regulated proteoglycans and glycoproteins of the plant cell surface , 1995, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[31]  M. Bennett,et al.  Hrp Mutant of Pseudomonas syringae pv phaseolicola Induces Cell Wall Alterations but Not Membrane Damage Leading to the Hypersensitive Reaction in Lettuce , 1995, Plant physiology.

[32]  Z. Oltvai,et al.  Reactive oxygen species and the regulation of cell death by the Bcl-2 gene family. , 1995, Biochimica et biophysica acta.

[33]  R. Dixon,et al.  Function of the oxidative burst in hypersensitive disease resistance. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[34]  D. Delmer,et al.  A mutant of Arabidopsis thaliana displaying altered patterns of cellulose deposition , 1995 .

[35]  Alex Levine,et al.  H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response , 1994, Cell.

[36]  A. Abo,et al.  Interaction of Rac with p67phox and regulation of phagocytic NADPH oxidase activity. , 1994, Science.

[37]  M. Mehdy.  Active Oxygen Species in Plant Defense against Pathogens , 1994, Plant physiology.

[38]  P. Schopfer.  Histochemical Demonstration and Localization of H2O2 in Organs of Higher Plants by Tissue Printing on Nitrocellulose Paper , 1994, Plant physiology.

[39]  F. Civoli,et al.  Flow cytometric detection of hydrogen peroxide production induced by doxorubicin in cancer cells. , 1994, Free radical biology & medicine.

[40]  A. Abo,et al.  Activation of NADPH oxidase involves the dissociation of p21rac from its inhibitory GDP/GTP exchange protein (rhoGDI) followed by its translocation to the plasma membrane. , 1994, The Biochemical journal.

[41]  T. Lam,et al.  Covalent Cross-Links in the Cell Wall , 1994, Plant physiology.

[42]  K. Aston,et al.  Evaluation of activity of putative superoxide dismutase mimics. Direct analysis by stopped-flow kinetics. , 1993, The Journal of biological chemistry.

[43]  B. Robertsen,et al.  Elicitation of H2 O2 production in cucumber hypocotyl segments by oligo-1,4-α-D-galacturonides and an oligo-β-glucan preparation from cell walls of Phythophthora megasperma f. sp. glycinea. , 1993, Physiologia plantarum.

[44]  P. Low,et al.  Characterization of the Oligogalacturonide-Induced Oxidative Burst in Cultured Soybean (Glycine max) Cells , 1993, Plant physiology.

[45]  H. Ischiropoulos,et al.  Evaluation of 2',7'-dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. , 1993, Archives of biochemistry and biophysics.

[46]  D. Tew,et al.  Studies on the inhibitory mechanism of iodonium compounds with special reference to neutrophil NADPH oxidase. , 1993, The Biochemical journal.

[47]  A. Abo,et al.  The biochemical basis of the NADPH oxidase of phagocytes. , 1993, Trends in biochemical sciences.

[48]  Anne J. Ridley,et al.  The small GTP-binding protein rac regulates growth factor-induced membrane ruffling , 1992, Cell.

[49]  C. Lamb,et al.  Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response , 1992, Cell.

[50]  P. Low,et al.  Rapid Stimulation of an Oxidative Burst during Elicitation of Cultured Plant Cells : Role in Defense and Signal Transduction. , 1989, Plant physiology.

[51]  D. Delmer,et al.  UDP-Glucose: (1→3)-β-Glucan Synthases from Mung Bean and Cotton Differential Effects of Ca2+ and Mg2+ on Enzyme Properties and on Macromolecular Structure of the Glucan Product , 1987 .

[52]  D. Delmer,et al.  beta-1,3-Glucan in Developing Cotton Fibers: Structure, Localization, and Relationship of Synthesis to That of Secondary Wall Cellulose. , 1979, Plant physiology.

[53]  D. Delmer,et al.  Changes in biochemical composition of the cell wall of the cotton fiber during development. , 1977, Plant physiology.

[54]  D. Updegraff.  Semimicro determination of cellulose in biological materials. , 1969, Analytical biochemistry.

[55]  F. D. Snell,et al.  Colorimetric Methods of Analysis , 1945 .

[56]  H. Fukuda.  Tracheary Element Formation as a Model System of Cell Differentiation , 1992 .

[57]  N. O'neill,et al.  Early responses during plant-bacteria interactions in tobacco cell suspensions , 1991 .

[58]  A. Basra,et al.  Development of the Cotton Fiber , 1984 .