Expression of phytoglobin affects nitric oxide metabolism and energy state of barley plants exposed to anoxia

Cochrane, Devin W.; Shah, Jash; Hebelstrup, Kim H.; Igamberdiev, Abir U.

doi:10.1016/j.plantsci.2017.10.001

Cited by 31 publications

(33 citation statements)

References 33 publications

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“…NO also plays a significant role as a signaling intermediate in ABA-induced stomatal closure (Neill et al , 2008; Gayatri et al , 2013). Since the leaf internal NO levels are influenced by the NO–phytoglobin cycle in transgenic Arabidopsis and barley plants with altered phytoglobin expression (Hebelstrup et al , 2012, 2014; Cochrane et al , 2017), the stomatal opening could also be changed, affecting NO diffusion and hence NO fixation. The stomatal conductance in WT and transgenic barley was similar (Supplementary Fig.…”

Section: Discussionmentioning

confidence: 99%

Phytoglobin overexpression promotes barley growth in the presence of enhanced level of atmospheric nitric oxide

Zhang

Buegger

Albert

et al. 2019

Journal of Experimental Botany

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To investigate the effect of high atmospheric NO concentrations on crop plants and the role of phytoglobins under these conditions, we performed a long-term study on barley ‘Golden Promise’ wild type (WT), class 1 phytoglobin knockdown (HvPgb1.1−) and class 1 phytoglobin overexpression (HvPgb1.1+) lines. Plants were cultivated with nitrogen-free nutrient solution during the entire growth period and were fumigated with different NO concentration (ambient, 800, 1500, and 3000 ppb). Analysis of fresh weight, stem number, chlorophyll content, and effective quantum yield of PSII showed that NO fumigation promoted plant growth and tillering significantly in the HvPgb1.1+ line. After 80 d of NO fumigation, dry matter weight, spikes number, kernel number, and plant kernel weight were significantly increased in HvPgb1.1+ plants with increasing NO concentration. In contrast, yield decreased in WT and HvPgb1.1− plants the higher the NO level. Application of atmospheric 15NO and 15NO2 demonstrated NO specificity of phytoglobins. 15N from 15NO could be detected in RNA, DNA, and proteins of barley leaves and the 15N levels were significantly higher in HvPgb1.1+ plants in comparison with HvPgb1.1− and WT plants. Our results demonstrate that overexpression of phytoglobins allows plants to more efficiently use atmospheric NO as N source.

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Section: Discussionmentioning

confidence: 99%

Phytoglobin overexpression promotes barley growth in the presence of enhanced level of atmospheric nitric oxide

Zhang

Buegger

Albert

et al. 2019

Journal of Experimental Botany

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“…To test the plants under oxygen deficiency, they were placed in a custom-built, sealed, 2 L, dark chamber for 4 h. A steady inflow of nitrogen gas was maintained at 120 mL min −1 (Alphagaz 1 grade having ∼0.001% oxygen) at one opening and unidirectional air valves facing outward in the openings to maintain ambient pressure within the chamber while preventing ambient air from entering (Cochrane et al, 2017). In a few experiments, the nitrogen gas contained either 0.1% or 3% oxygen.…”

Section: Normoxia Hypoxia and Reoxygenation Treatmentsmentioning

confidence: 99%

“…The extraction of ATP and ADP was modified from Dordas et al (2003) as described earlier (Cochrane et al, 2017). Fresh leaf biomass (100 mg) was rapidly frozen in liquid nitrogen and homogenized in 1 mL of 2.4 M HCl using a mortar and pestle.…”

Section: Adenylatesmentioning

confidence: 99%

Roles for Plant Mitochondrial Alternative Oxidase Under Normoxia, Hypoxia, and Reoxygenation Conditions

et al. 2020

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Alternative oxidase (AOX) is a non-energy conserving terminal oxidase in the plant mitochondrial electron transport chain (ETC) that has a lower affinity for oxygen than does cytochrome (cyt) oxidase. To investigate the role(s) of AOX under different oxygen conditions, wild-type (WT) Nicotiana tabacum plants were compared with AOX knockdown and overexpression plants under normoxia, hypoxia (near-anoxia), and during a reoxygenation period following hypoxia. Paradoxically, under all the conditions tested, the AOX amount across plant lines correlated positively with leaf energy status (ATP/ADP ratio). Under normoxia, AOX was important to maintain respiratory carbon flow, to prevent the mitochondrial generation of superoxide and nitric oxide (NO), to control lipid peroxidation and protein S-nitrosylation, and possibly to reduce the inhibition of cyt oxidase by NO. Under hypoxia, AOX was again important in preventing superoxide generation and lipid peroxidation, but now contributed positively to NO amount. This may indicate an ability of AOX to generate NO under hypoxia, similar to the nitrite reductase activity of cyt oxidase under hypoxia. Alternatively, it may indicate that AOX activity simply reduces the amount of superoxide scavenging of NO, by reducing the availability of superoxide. The amount of inactivation of mitochondrial aconitase during hypoxia was also dependent upon AOX amount, perhaps through its effects on NO amount, and this influenced carbon flow under hypoxia. Finally, AOX was particularly important in preventing nitro-oxidative stress during the reoxygenation period, thereby contributing positively to the recovery of energy status following hypoxia. Overall, the results suggest that AOX plays a beneficial role in low oxygen metabolism, despite its lower affinity for oxygen than cytochrome oxidase.

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“…The main important physiological role of phytoglobins is best known for class 1 and implies cellular NO scavenging since they are rapidly induced in hypoxia, increasing plant survival in such stress conditions for several species such as maize, Arabidopsis and alfalfa 7 , 20 , 76 , 77 . In order to keep NO metabolism functional for a physiologically relevant time, hemoglobins have to be resistant to autoxidation or need an efficient electron donating partner to reduce back the ferric hemoglobin generated during autoxidation; the latter option would be an energy consuming situation.…”

Section: Resultsmentioning

confidence: 99%

Redox control and autoxidation of class 1, 2 and 3 phytoglobins from Arabidopsis thaliana

Moţ

Pușcaș

Miclea

et al. 2018

Sci Rep

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Despite a recent increase in interest towards phytoglobins and their importance in plants, much is still unknown regarding their biochemical/biophysical properties and physiological roles. The present study presents data on three recombinant Arabidopsis phytoglobins in terms of their UV-vis and Raman spectroscopic characteristics, redox state control, redox potentials and autoxidation rates. The latter are strongly influenced by pH for all three hemoglobins – (with a fundamental involvement of the distal histidine), as well as by added anion concentrations – suggesting either a process dominated by nucleophilic displacement of superoxide for AtHb2 or an inhibitory effect for AtHb1 and AtHb3. Reducing agents, such as ascorbate and glutathione, are found to either enhance– (presumably via direct electron transfer or via allosteric regulation) or prevent autoxidation. HbFe3+ reduction was possible in the presence of high (presumably not physiologically relevant) concentrations of NADH, glutathione and ascorbate, with differing behaviors for the three globins. The iron coordination sphere is found to affect the autoxidation, redox state interconversion and redox potentials in these three phytoglobins.

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Expression of phytoglobin affects nitric oxide metabolism and energy state of barley plants exposed to anoxia

Cited by 31 publications

References 33 publications

Phytoglobin overexpression promotes barley growth in the presence of enhanced level of atmospheric nitric oxide

Phytoglobin overexpression promotes barley growth in the presence of enhanced level of atmospheric nitric oxide

Roles for Plant Mitochondrial Alternative Oxidase Under Normoxia, Hypoxia, and Reoxygenation Conditions

Redox control and autoxidation of class 1, 2 and 3 phytoglobins from Arabidopsis thaliana

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