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Item New insights into nitric oxide biosynthesis underpin lateral root development(Elsevier B.V., 2024) Gupta, Kapuganti Jagadis; Yadav, Nidhi; Kumari, Aprajita; Loake, Gary J.In recent years, nitric oxide (NO) has emerged as a key redox signaling molecule in plants functioning in the regulation of key developmental programs and the orchestration of responses to a plethora of environmental cues (Kolbert et al., 2019). The predominant route for the transfer of NO bioactivity is through S-nitrosylation, the addition of an NO moiety to a protein cysteine thiol to form an S-nitrosothiol (Yun et al., 2011). Specificity for this process is established by the structural constraints imposed by tertiary protein structure in gating access to given cysteine redox switches and associated proteins that can either facilitate the addition or removal of the NO moiety at these residues (Umbreen et al., 2018).Item Nitric oxide, energy and redox-dependent responses to hypoxia(Oxford University Press, 2024) Samant, Sanjib Bal; Yadav, Nidhi; Swain, Jagannath; Joseph, Josepheena; Kumari, Aprajita; Praveen, Afsana; Sahoo, Ranjan Kumar; Manjunatha, Girigowda; Seth, Chandra Shekar; Singla-Pareek, Sneh Lata; Foyer, Christine H; Pareek, Ashwani; Gupta, Kapuganti JagadisHypoxia occurs when the oxygen levels fall below the levels required for mitochondria to support respiration. Regulated hypoxia is associated with quiescence, particularly in storage organs (seeds) and stem cell niches. In contrast, environmentally-induced hypoxia poses significant challenges for metabolically-active cells that are adapted to aerobic respiration. The perception of oxygen availability through cysteine oxidases, which function as oxygen-sensing enzymes in plants that control the N-degron pathway, and the regulation of hypoxia-responsive genes and processes is essential to survival. Functioning together with reactive oxygen species (ROS), particularly hydrogen peroxide and reactive nitrogen species (RNS), such as nitric oxide (•NO), nitrogen dioxide (•NO2), S‐nitrosothiols (SNOs), and peroxynitrite (ONOO−), hypoxia signaling pathways trigger anatomical adaptations such as formation of aerenchyma, mobilization of sugar reserves for anaerobic germination, formation of aerial adventitious roots and hyponastic response. NO and hydrogen peroxide (H2O2) participate in local and systemic signaling pathways that facilitate acclimation to changing energetic requirements, controlling glycolytic fermentation, the GABA shunt and amino acid synthesis. NO enhances antioxidant capacity and contributes to the recycling of redox equivalents energy metabolism through the phytoglobin (Pgb)-NO cycle. Here, we summarize current knowledge, highlighting the central role of NO and redox regulation in adaptive responses that prevent hypoxia-induced death in challenging conditions such as flooding.Item The emerging roles of nitric oxide and its associated scavengers-phytoglobins-in plant symbiotic interactions(Oxford University Press, 2024) Pathak, Pradeep Kumar; Yadav, Nidhi; Kaladhar, Vemula Chandra; Jaiswal, Rekha; Kumari, Aprajita; Igamberdiev, Abir U.; Loake, Gary J.; Gupta, Kapuganti JagadisA key feature in the establishment of symbiosis between plants and microbes is the maintenance of the balance between the production of the small redox-related molecule, nitric oxide (NO), and its cognate scavenging pathways. During the establishment of symbiosis, a transition from a normoxic to a microoxic environment often takes place, triggering the production of NO from nitrite via a reductive production pathway. Plant hemoglobins [phytoglobins (Phytogbs)] are a central tenant of NO scavenging, with NO homeostasis maintained via the Phytogb–NO cycle. While the first plant hemoglobin (leghemoglobin), associated with the symbiotic relationship between leguminous plants and bacterial Rhizobium species, was discovered in 1939, most other plant hemoglobins, identified only in the 1990s, were considered as non-symbiotic. From recent studies, it is becoming evident that the role of Phytogbs1 in the establishment and maintenance of plant–bacterial and plant–fungal symbiosis is also essential in roots. Consequently, the division of plant hemoglobins into symbiotic and non-symbiotic groups becomes less justified. While the main function of Phytogbs1 is related to the regulation of NO levels, participation of these proteins in the establishment of symbiotic relationships between plants and microorganisms represents another important dimension among the other processes in which these key redox-regulatory proteins play a central role.Item Phytoglobin-NO cycle and AOX pathway play a role in anaerobic germination and growth of deepwater rice(John Wiley & Sons, 2021) Kumari, Aprajita; Singh, Pooja; Kaladhar, Vemula Chandra; Manbir; Paul, Debarati; Pathak, Pradeep Kumar; Gupta, Kapuganti JagadisAn important and interesting feature of rice is that it can germinate under anoxic conditions. Though several biochemical adaptive mechanisms play an important role in the anaerobic germination of rice but the role of phytoglobin-nitric oxide cycle and alternative oxidase pathway is not known, therefore in this study we investigated the role of these pathways in anaerobic germination. Under anoxic conditions, deepwater rice germinated much higher and rapidly than aerobic condition and the anaerobic germination and growth were much higher in the presence of nitrite. The addition of nitrite stimulated NR activity and NO production. Important components of phytoglobin-NO cycle such as methaemoglobin reductase activity, expression of Phytoglobin1, NIA1 were elevated under anaerobic conditions in the presence of nitrite. The operation of phytoglobin-NO cycle also enhanced anaerobic ATP generation, LDH, ADH activities and in parallel ethylene levels were also enhanced. Interestingly nitrite suppressed the ROS production and lipid peroxidation. The reduction of ROS was accompanied by enhanced expression of mitochondrial alternative oxidase protein and its capacity. Application of AOX inhibitor SHAM inhibited the anoxic growth mediated by nitrite. In addition, nitrite improved the submergence tolerance of seedlings. Our study revealed that nitrite driven phytoglobin-NO cycle and AOX are crucial players in anaerobic germination and growth of deepwater rice.Item Greenhouse and field experiments revealed that clove oil can effectively reduce bacterial blight and increase yield in pomegranate(John Wiley & Sons, 2021) Kumar, Pavan; Lokesh, Veeresh; Doddaraju, Pushpa; Kumari, Aprajita; Singh, Pooja; Meti, Bharati S.; Sharma, Jyotsana; Gupta, Kapuganti Jagadis; Manjunatha, GirigowdaBacterial blight in pomegranate is a devastating disease caused by bacterial pathogen Xanthomonas axonopodis pv. punicae (XAP), recording huge damage to pomegranate crop worldwide. Antibiotics and copper-based chemicals are being used for the management of this blight, while in this present work, we investigated the effect of eugenol and clove oil either singly or in combination with copper oxychloride (COC) on the induction of plant defense responses and concomitant prevention of bacterial blight. Our results provided evidence that clove oil (0.2%–1%) and eugenol (0.1% and 0.2%) successfully inhibit the growth of XAP in paper disk diffusion assay. Strikingly under the greenhouse condition, clove oil (0.2%) as foliar application 24 h before XAP inoculation recorded the lowest disease severity of 7.34%, whereas eugenol (0.2%) recorded maximum disease severity of 14.56%. However, the combination of clove oil (0.2%) and copper oxychloride (0.3%) recorded the least disease severity of 2.38%. A similar trend was observed in field conditions. Prophylactic application of clove oil leads to enhanced nitrate reductase activity and nitric oxide production which was further enhanced in clove oil pre-treated plants challenged with XAP. Strikingly, the total ROS and H2O2 levels were reduced in response to clove oil application. Clove oil also induced the systemic response by inducing expression levels of defense genes. The reduction of disease severity by clove oil and COC combination also reflected on total yield recording via large-scale field experiments where maximum yield of 14.04 tonnes/acre was observed, whereas streptocycline application recorded 11.12 tonnes/acre. Application of COC and clove oil resulted in a high remunerative value of ₹ 1:5.6, compared to streptocycline (1:4.85) and control (1:1.85). The present study revealed that clove oil as a plant derivative and eugenol as a synthetic option can be effectively used for the successful management of bacterial blight in pomegranate.Item Nitrite and nitric oxide are important in the adjustment of primary metabolism during the hypersensitive response in tobacco(Oxford University Press, 2019) Mur, Luis A. J.; Kumari, Aprajita; Brotman, Yariv; Zeier, Jurgen; Mandon, Julien; Cristescu, Simona M.; Harren, Frans; Kaiser, Werner M.; Fernie, Alisdair R.; Gupta, Kapuganti JagadisNitrate and ammonia deferentially modulate primary metabolism during the hypersensitive response in tobacco. In this study, tobacco RNAi lines with low nitrite reductase (NiRr) levels were used to investigate the roles of nitrite and nitric oxide (NO) in this process. The lines accumulate NO2-, with increased NO generation, but allow sufficient reduction to NH4+ to maintain plant viability. For wild-type (WT) and NiRr plants grown with NO3-, inoculation with the non-host biotrophic pathogen Pseudomonas syringae pv. phaseolicola induced an accumulation of nitrite and NO, together with a hypersensitive response (HR) that resulted in decreased bacterial growth, increased electrolyte leakage, and enhanced pathogen resistance gene expression. These responses were greater with increases in NO or NO2- levels in NiRr plants than in the WT under NO3- nutrition. In contrast, WT and NiRr plants grown with NH4+ exhibited compromised resistance. A metabolomic analysis detected 141 metabolites whose abundance was differentially changed as a result of exposure to the pathogen and in response to accumulation of NO or NO2-. Of these, 13 were involved in primary metabolism and most were linked to amino acid and energy metabolism. HR-associated changes in metabolism that are often linked with primary nitrate assimilation may therefore be influenced by nitrite and NO production.Item Nitric oxide accelerates germination via the regulation of respiration in chickpea(Oxford University Press, 2019) Pandey, Sonika; Kumari, Aprajita; Shree, Manu; Kumar, Vinod; Singh, Pooja; Bharadwaj, Chellapilla; Loake, Gary J.; Parida, Swarup K.; Masakapalli, Shyam Kumar; Gupta, Kapuganti JagadisSeed germination is crucial for the plant life cycle. We investigated the role of nitric oxide (NO) in two chickpea varieties that differ in germination capacity: Kabuli, which has a low rate of germination and germinates slowly, and Desi, which shows improved germination properties. Desi produced more NO than Kabuli and had lower respiratory rates. As a result of the high respiration rates, Kabuli had higher levels of reactive oxygen species (ROS). Treatment with the NO donor S-nitroso-N-acetyl-D,L-penicillamine (SNAP) reduced respiration in Kabuli and decreased ROS levels, resulting in accelerated germination rates. These findings suggest that NO plays a key role in the germination of Kabuli. SNAP increased the levels of transcripts encoding enzymes involved in carbohydrate metabolism and the cell cycle. Moreover, the levels of amino acids and organic acids were increased in Kabuli as a result of SNAP treatment. 1 H-nuclear magnetic resonance analysis revealed that Kabuli has a higher capacity for glucose oxidation than Desi. An observed SNAP-induced increase in 13C incorporation into soluble alanine may result from enhanced oxidation of exogenous [13C]glucose via glycolysis and the pentose phosphate pathway. A homozygous hybrid that originated from a recombinant inbred line population of a cross between Desi and Kabuli germinated faster and had increased NO levels and a reduced accumulation of ROS compared with Kabuli. Taken together, these findings demonstrate the importance of NO in chickpea germination via the control of respiration and ROS accumulation.Item Alternative oxidase is an important player in the regulation of nitric oxide levels under normoxic and hypoxic conditions in plants(Oxford University Press, 2019) Kumari, Aprajita; Pathak, Pradeep Kumar; Bulle, Mallesham; Igamberdiev, Abir U; Gupta, Kapuganti JagadisPlant mitochondria possess two different pathways for electron transport from ubiquinol: the cytochrome pathway and the alternative oxidase (AOX) pathway. The AOX pathway plays an important role in stress tolerance and is induced by various metabolites and signals. Previously, several lines of evidence suggested that the AOX pathway prevents overproduction of superoxide and other reactive oxygen species. More recent evidence suggests that AOX also plays a role in regulation of nitric oxide (NO) production and signalling. The AOX pathway is induced under low phosphate, hypoxia, pathogen infections and elicitor treatments. The induction of AOX under aerobic conditions in response to various stresses can reduce electron transfer through complexes III and IV and thus prevents the leakage of electrons to nitrite and the subsequent accumulation of NO. Excess of NO under various stresses can inhibit complex IV, thus the AOX pathway minimizes nitrite-dependent NO synthesis that would arise from enhanced electron leakage in the cytochrome pathway. By preventing NO generation, AOX can reduce peroxynitrite formation and tyrosine nitration. In contrast to its function under normoxia, AOX has a specific role under hypoxia, where AOX can facilitate nitrite-dependent NO production. This reaction drives the phytoglobin-NO cycle to increase energy efficiency under hypoxia.Item Nitrate nutrition influences multiple factors in order to increase energy efficiency under hypoxia in Arabidopsis(Oxford University Press, 2019) Wany, Aakanksha; Gupta, Alok Kumar; Kumari, Aprajita; Mishra, Sonal; Singh, Namrata; Pandey, Sonika; Vanvari, Rhythm; Igamberdiev, Abir U.; Fernie, Alisdair R.; Gupta, Kapuganti JagadisBACKGROUND AND AIMS: Nitrogen (N) levels vary between ecosystems, while the form of available N has a substantial impact on growth, development and perception of stress. Plants have the capacity to assimilate N in the form of either nitrate (NO3-) or ammonium (NH4+). Recent studies revealed that NO3- nutrition increases nitric oxide (NO) levels under hypoxia. When oxygen availability changes, plants need to generate energy to protect themselves against hypoxia-induced damage. As the effects of NO3- or NH4+ nutrition on energy production remain unresolved, this study was conducted to investigate the role of N source on group VII transcription factors, fermentative genes, energy metabolism and respiration under normoxic and hypoxic conditions. METHODS : We used Arabidopsis plants grown on Hoagland medium with either NO3- or NH4+ as a source of N and exposed to 0.8 % oxygen environment. In both roots and seedlings, we investigated the phytoglobin-nitric oxide cycle and the pathways of fermentation and respiration; furthermore, NO levels were tested using a combination of techniques including diaminofluorescein fluorescence, the gas phase Griess reagent assay, respiration by using an oxygen sensor and gene expression analysis by real-time quantitative reverse transcription-PCR methods. KEY RESULTS : Under NO3- nutrition, hypoxic stress leads to increases in nitrate reductase activity, NO production, class 1 phytoglobin transcript abundance and metphytoglobin reductase activity. In contrast, none of these processes responded to hypoxia under NH4+ nutrition. Under NO3- nutrition, a decreased total respiratory rate and increased alternative oxidase capacity and expression were observed during hypoxia. Data correlated with decreased reactive oxygen species and lipid peroxidation levels. Moreover, increased fermentation and NAD+ recycling as well as increased ATP production concomitant with the increased expression of transcription factor genes HRE1, HRE2, RAP2.2 and RAP2.12 were observed during hypoxia under NO3- nutrition. CONCLUSIONS: The results of this study collectively indicate that nitrate nutrition influences multiple factors in order to increase energy efficiency under hypoxia.Item A discrete role for alternative oxidase under hypoxia to increase nitric oxide and drive energy production(Elsevier B.V., 2018) Vishwakarma, Abhaypratap; Kumari, Aprajita; Mur, Luis A.J.; Gupta, Kapuganti JagadisAlternative oxidase (AOX) is an integral part of the mitochondrial electron transport and can prevent reactive oxygen species (ROS) and nitric oxide (NO) production under non-stressed, normoxic conditions. Here we assessed the roles of AOX by imposing stress under normoxia in comparison to hypoxic conditions using AOX over expressing (AOX OE) and anti-sense (AOX AS) transgenic Arabidopsis seedlings and roots. Under normoxic conditions stress was induced with the defence elicitor flagellin (flg22). AOX OE reduced NO production whilst this was increased in AOX AS. Moreover AOX AS also exhibited an increase in superoxide and therefore peroxynitrite, tyrosine nitration suggesting that scavenging of NO by AOX can prevent toxic peroxynitrite formation under normoxia. In contrast, during hypoxia interestingly we found that AOX is a generator of NO. Thus, the NO produced during hypoxia, was enhanced in AOX OE and suppressed in AOX AS. Additionally, treatment of WT or AOX OE with the AOX inhibitor SHAM inhibited hypoxic NO production. The enhanced levels of NO correlated with expression of non-symbiotic haemoglobin, increased NR activity and ATP production. The ATP generation was suppressed in nia1,2 mutant and non symbiotic haemoglobin antisense line treated with SHAM. Taken together these results suggest that hypoxic NO generation mediated by AOX has a discrete role by feeding into the haemoglobin-NO cycle to drive energy efficiency under conditions of low oxygen tension.