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Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata.

Cohen MF, Gurung S, Birarda G, Holman HY, Yamasaki H - Front Plant Sci (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Sonoma State University, Rohnert Park, CA USA ; Biological Systems Unit, Okinawa Institute of Science and Technology, Okinawa Japan.

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. 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.

No MeSH data available.


Related in: MedlinePlus

Combined effect of nitrite and H2O2 on root abscission of Azolla pinnata plants. Abscission was measured 90 min after 2 mM nitrite was added. 2, 4, 6, 8, or 10 mM H2O2 were added (A) simultaneous with or (B) 60 min before addition of nitrite. (C) 2 mM H2O2 was added simultaneously with 2, 4, 6, 8, or 10 mM nitrite (A, n = 7; B, n = 8, C, n = 2, mean ± SE; means with the same letter are not significantly different).
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Figure 1: Combined effect of nitrite and H2O2 on root abscission of Azolla pinnata plants. Abscission was measured 90 min after 2 mM nitrite was added. 2, 4, 6, 8, or 10 mM H2O2 were added (A) simultaneous with or (B) 60 min before addition of nitrite. (C) 2 mM H2O2 was added simultaneously with 2, 4, 6, 8, or 10 mM nitrite (A, n = 7; B, n = 8, C, n = 2, mean ± SE; means with the same letter are not significantly different).

Mentions: In other plant systems Sakamoto et al. (2008) have described a H2O2 burst coinciding with leaf abscission that would presumably provide substrate for ⋅OH generation (Liszkay et al., 2003). This H2O2 burst is apparently distinct from the lower level of H2O2 production that functions in the abscission signaling process. We have previously reported that treatment of A. pinnata plants with up to 10 mM H2O2 alone does not induce root abscission (Gurung et al., 2012). However, in combination with the known abscission-inducing agent nitrite, treatment of plants with H2O2 exhibited a pronounced effect that depended on the concentration and timing of the H2O2 treatment relative to exposure to nitrite (Figures 1A,B). The inhibitory effect of 2 mM H2O2 on root abscission induced by 2 mM nitrite could be overridden by the further addition of nitrite (>4 mM nitrite; Figure 1C).


Bimodal effect of hydrogen peroxide and oxidative events in nitrite-induced rapid root abscission by the water fern Azolla pinnata.

Cohen MF, Gurung S, Birarda G, Holman HY, Yamasaki H - Front Plant Sci (2015)

Combined effect of nitrite and H2O2 on root abscission of Azolla pinnata plants. Abscission was measured 90 min after 2 mM nitrite was added. 2, 4, 6, 8, or 10 mM H2O2 were added (A) simultaneous with or (B) 60 min before addition of nitrite. (C) 2 mM H2O2 was added simultaneously with 2, 4, 6, 8, or 10 mM nitrite (A, n = 7; B, n = 8, C, n = 2, mean ± SE; means with the same letter are not significantly different).
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4496558&req=5

Figure 1: Combined effect of nitrite and H2O2 on root abscission of Azolla pinnata plants. Abscission was measured 90 min after 2 mM nitrite was added. 2, 4, 6, 8, or 10 mM H2O2 were added (A) simultaneous with or (B) 60 min before addition of nitrite. (C) 2 mM H2O2 was added simultaneously with 2, 4, 6, 8, or 10 mM nitrite (A, n = 7; B, n = 8, C, n = 2, mean ± SE; means with the same letter are not significantly different).
Mentions: In other plant systems Sakamoto et al. (2008) have described a H2O2 burst coinciding with leaf abscission that would presumably provide substrate for ⋅OH generation (Liszkay et al., 2003). This H2O2 burst is apparently distinct from the lower level of H2O2 production that functions in the abscission signaling process. We have previously reported that treatment of A. pinnata plants with up to 10 mM H2O2 alone does not induce root abscission (Gurung et al., 2012). However, in combination with the known abscission-inducing agent nitrite, treatment of plants with H2O2 exhibited a pronounced effect that depended on the concentration and timing of the H2O2 treatment relative to exposure to nitrite (Figures 1A,B). The inhibitory effect of 2 mM H2O2 on root abscission induced by 2 mM nitrite could be overridden by the further addition of nitrite (>4 mM nitrite; Figure 1C).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Sonoma State University, Rohnert Park, CA USA ; Biological Systems Unit, Okinawa Institute of Science and Technology, Okinawa Japan.

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. 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.

No MeSH data available.


Related in: MedlinePlus