Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata
Abstract
In the genus Azolla rapid abscission of roots from floating fronds occurs within minutes in response to a variety of stresses, including exposure to nitrite. We found that hydrogen peroxide, though itself not an inducer of root abscission, modulates nitrite-induced root abscission by Azolla pinnata in a dose-dependent manner, with 2 mM H2O2 significantly diminishing the responsiveness to 2 mM NaNO2, and 10 mM H2O2 slightly enhancing it. Hypoxia, which has been found in other plants to result in autogenic production of H2O2, dramatically stimulated root abscission of A. pinnata in response to nitrite, especially for plants previously cultivated in medium containing 5 mM KNO3 compared to plants cultivated under N2-fixing conditions without combined nitrogen. Plants, including Azolla, produce the small signaling molecule nitric oxide (NO) from nitrite using nitrate reductase. We found Azolla plants to display dose-dependent root abscission in response to the NO donor spermine NONOate. Treatment of plants with the thiol-modifying agents S-methyl methanethiosulfonate or glutathione inhibited the nitrite-induced root abscission response. Synchrotron radiation-based Fourier transform infrared spectromicroscopy revealed higher levels of carbonylation in the abscission zone of dropped roots, indicative of reaction products of polysaccharides with potent free radical oxidants. Lastly, we hypothesize that metabolic productsmore »
- Authors:
-
- Sonoma State Univ., Rohnert Park, CA (United States); Okinawa Inst. of Science and Technology, Okinawa (Japan)
- Univ. of the Ryukyus, Nishihara (Japan)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1257258
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Frontiers in Plant Science
- Additional Journal Information:
- Journal Volume: 6; Journal ID: ISSN 1664-462X
- Publisher:
- Frontiers Research Foundation
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY; root abscission; apoplast; free radical cleavage; FTIR spectromicroscopy; hydrogen peroxide; nitric oxide; nitrite; plant cell wall loosening
Citation Formats
Cohen, Michael F., Gurung, Sushma, Birarda, Giovanni, Holman, Hoi-Ying N., and Yamasaki, Hideo. Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata. United States: N. p., 2015.
Web. doi:10.3389/fpls.2015.00518.
Cohen, Michael F., Gurung, Sushma, Birarda, Giovanni, Holman, Hoi-Ying N., & Yamasaki, Hideo. Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata. United States. https://doi.org/10.3389/fpls.2015.00518
Cohen, Michael F., Gurung, Sushma, Birarda, Giovanni, Holman, Hoi-Ying N., and Yamasaki, Hideo. Thu .
"Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata". United States. https://doi.org/10.3389/fpls.2015.00518. https://www.osti.gov/servlets/purl/1257258.
@article{osti_1257258,
title = {Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata},
author = {Cohen, Michael F. and Gurung, Sushma and Birarda, Giovanni and Holman, Hoi-Ying N. and Yamasaki, Hideo},
abstractNote = {In the genus Azolla rapid abscission of roots from floating fronds occurs within minutes in response to a variety of stresses, including exposure to nitrite. We found that hydrogen peroxide, though itself not an inducer of root abscission, modulates nitrite-induced root abscission by Azolla pinnata in a dose-dependent manner, with 2 mM H2O2 significantly diminishing the responsiveness to 2 mM NaNO2, and 10 mM H2O2 slightly enhancing it. Hypoxia, which has been found in other plants to result in autogenic production of H2O2, dramatically stimulated root abscission of A. pinnata in response to nitrite, especially for plants previously cultivated in medium containing 5 mM KNO3 compared to plants cultivated under N2-fixing conditions without combined nitrogen. Plants, including Azolla, produce the small signaling molecule nitric oxide (NO) from nitrite using nitrate reductase. We found Azolla plants to display dose-dependent root abscission in response to the NO donor spermine NONOate. Treatment of plants with the thiol-modifying agents S-methyl methanethiosulfonate or glutathione inhibited the nitrite-induced root abscission response. Synchrotron radiation-based Fourier transform infrared spectromicroscopy revealed higher levels of carbonylation in the abscission zone of dropped roots, indicative of reaction products of polysaccharides with potent free radical oxidants. Lastly, we hypothesize that metabolic products of nitrite and NO react with H2O2 in the apoplast leading to free-radical-mediated cleavage of structural polysaccharides and consequent rapid root abscission.},
doi = {10.3389/fpls.2015.00518},
journal = {Frontiers in Plant Science},
number = ,
volume = 6,
place = {United States},
year = {Thu Jul 09 00:00:00 EDT 2015},
month = {Thu Jul 09 00:00:00 EDT 2015}
}
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Works referenced in this record:
Leaf-goldenning induced by high light inFicus microcarpa L. f., a tropical fig
journal, June 1995
- Yamasaki, Hideo; Heshiki, Rika; Ikehara, Norikatsu
- Journal of Plant Research, Vol. 108, Issue 2
Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth
journal, August 2003
- Liszkay, Anja; Kenk, Barbara; Schopfer, Peter
- Planta, Vol. 217, Issue 4
Use of FT-IR Spectra and PCA to the Bulk Characterization of Cell Wall Residues of Fruits and Vegetables Along a Fraction Process
journal, December 2012
- Szymanska-Chargot, Monika; Zdunek, Artur
- Food Biophysics, Vol. 8, Issue 1
Separation of abscission zone cells in detached Azolla roots depends on apoplastic pH
journal, January 2013
- Fukuda, Kazuma; Yamada, Yoshiya; Miyamoto, Kensuke
- Journal of Plant Physiology, Vol. 170, Issue 1
Controlled free radical attack in the apoplast: A hypothesis for roles of O, N and S species in regulatory and polysaccharide cleavage events during rapid abscission by Azolla
journal, March 2014
- Cohen, Michael F.; Gurung, Sushma; Fukuto, Jon M.
- Plant Science, Vol. 217-218
Response of six Azolla species to transient high-temperature stress
journal, May 1999
- Uheda, Eiji; Kitoh, Shunji; Shiomi, Nobuyuki
- Aquatic Botany, Vol. 64, Issue 1
Hydroxyl radical formation resulting from the interaction of nitric oxide and hydrogen peroxide
journal, March 1998
- Nappi, Anthony J.; Vass, Emily
- Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1380, Issue 1
Yellowing and IR-changes of spruce wood as result of UV-irradiation
journal, February 2003
- Müller, Uwe; Rätzsch, Manfred; Schwanninger, Manfred
- Journal of Photochemistry and Photobiology B: Biology, Vol. 69, Issue 2
Synchrotron IR Spectromicroscopy: Chemistry of Living Cells
journal, November 2010
- Holman, Hoi-Ying N.; Bechtel, Hans A.; Hao, Zhao
- Analytical Chemistry, Vol. 82, Issue 21
Formation of Cysteine Sulfenic Acid by Oxygen Atom Transfer from Nitrite
journal, June 2010
- Heinecke, Julie; Ford, Peter C.
- Journal of the American Chemical Society, Vol. 132, Issue 27
Small Molecule Signaling Agents: The Integrated Chemistry and Biochemistry of Nitrogen Oxides, Oxides of Carbon, Dioxygen, Hydrogen Sulfide, and Their Derived Species
journal, February 2012
- Fukuto, Jon M.; Carrington, Samantha J.; Tantillo, Dean J.
- Chemical Research in Toxicology, Vol. 25, Issue 4
628. Infrared spectra of periodate-oxidised cellulose
journal, January 1960
- Spedding, H.
- Journal of the Chemical Society (Resumed)
Oxidative scission of plant cell wall polysaccharides by ascorbate-induced hydroxyl radicals
journal, June 1998
- Fry, Stephen C.
- Biochemical Journal, Vol. 332, Issue 2
Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth: Hydroxyl radicals, cell-wall loosening and elongation growth
journal, December 2001
- Schopfer, Peter
- The Plant Journal, Vol. 28, Issue 6
Anoxic stress leads to hydrogen peroxide formation in plant cells
journal, June 2001
- Blokhina, Olga B.; Chirkova, Tamara V.; Fagerstedt, Kurt V.
- Journal of Experimental Botany, Vol. 52, Issue 359
Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro
journal, January 2002
- Rockel, Peter; Strube, Frank; Rockel, Andra
- Journal of Experimental Botany, Vol. 53, Issue 366
Events associated with the rapid separation of cells from detached roots ofAzolla filiculoidesdepend on pH
journal, January 1994
- Uheda, Eiji; Nakamura, Sumio; Kitoh, Shunji
- Journal of Experimental Botany, Vol. 45, Issue 10
Rapid Shedding of Roots from Azolla filiculoides Plants in Response to Inhibitors of Respiration
journal, January 1994
- Uheda, Eiji; Kitoh, Shunji
- Plant and Cell Physiology, Vol. 35, Issue 1, 37-43
Abscission of Azolla Branches Induced by Ethylene and
Sodium Azide
journal, December 2000
- Uheda, Eiji; Nakamura, Sumio
- Plant and Cell Physiology, Vol. 41, Issue 12
Synergistic Effect of Deoxyanthocyanins from Symbiotic FernAzollaspp. onhrmAGene Induction in the CyanobacteriumNostoc punctiforme
journal, September 2002
- Cohen, Michael F.; Sakihama, Yasuko; Takagi, Yojiro C.
- Molecular Plant-Microbe Interactions®, Vol. 15, Issue 9
Imaging Cell Wall Architecture in Single Zinnia elegans Tracheary Elements
journal, June 2010
- Lacayo, Catherine I.; Malkin, Alexander J.; Holman, Hoi-Ying N.
- Plant Physiology, Vol. 154, Issue 1
Ascorbate and Glutathione: The Heart of the Redox Hub
journal, January 2011
- Foyer, Christine H.; Noctor, Graham
- Plant Physiology, Vol. 155, Issue 1
Polyamines Interact with Hydroxyl Radicals in Activating Ca2+ and K+ Transport across the Root Epidermal Plasma Membranes
journal, October 2011
- Zepeda-Jazo, Isaac; Velarde-Buendía, Ana María; Enríquez-Figueroa, René
- Plant Physiology, Vol. 157, Issue 4
The Azolla, Anabaena azollae Relationship
journal, June 1974
- Peters, Gerald A.; Mayne, Berger C.
- Plant Physiology, Vol. 53, Issue 6
Citrus leaf abscission. Regulatory role of exogenous auxin and ethylene on peroxidases and endogenous growth substances
journal, September 1978
- Gaspar, T.; Goren, R.; Huberman, M.
- Plant, Cell and Environment, Vol. 1, Issue 3
The NO world for plants: achieving balance in an open system
journal, January 2005
- Yamasaki, H.
- Plant, Cell and Environment, Vol. 28, Issue 1
P LANT P LASMA M EMBRANE H + -ATPases: Powerhouses for Nutrient Uptake
journal, June 2001
- Palmgren, Michael G.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 52, Issue 1
Polyamine-Induced Rapid Root Abscission in Azolla pinnata
journal, September 2012
- Gurung, Sushma; Cohen, Michael F.; Fukuto, Jon
- Journal of Amino Acids, Vol. 2012
Endogenous generation of reactive oxidants and electrophiles and their reactions with DNA and protein
journal, March 2003
- Marnett, Lawrence J.; Riggins, James N.; West, James D.
- Journal of Clinical Investigation, Vol. 111, Issue 5
Effects of Seasonal Changes on Pigment Composition ofAzolla filiculoidesLam.
journal, April 2014
- Kösesakal, Taylan
- American Fern Journal, Vol. 104, Issue 2
Reactive oxygen species in leaf abscission signaling
journal, November 2008
- Sakamoto, Masaru; Munemura, Ikuko; Tomita, Reiko
- Plant Signaling & Behavior, Vol. 3, Issue 11
Works referencing / citing this record:
d-Cysteine-Induced Rapid Root Abscission in the Water Fern Azolla Pinnata: Implications for the Linkage between d-Amino Acid and Reactive Sulfur Species (RSS) in Plant Environmental Responses
journal, September 2019
- Yamasaki, Hideo; Ogura, Masahiro P.; Kingjoe, Katsumi A.
- Antioxidants, Vol. 8, Issue 9
d-Cysteine-Induced Rapid Root Abscission in the Water Fern Azolla Pinnata: Implications for the Linkage between d-Amino Acid and Reactive Sulfur Species (RSS) in Plant Environmental Responses
journal, September 2019
- Yamasaki, Hideo; Ogura, Masahiro P.; Kingjoe, Katsumi A.
- Antioxidants, Vol. 8, Issue 9