Publications of NIPGR Scientists
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Item Overexpression of phytoglobin1 in rice leads to enhanced nitrogen use efficiency via modulation of nitric oxide(John Wiley & Sons, 2025) Samant, Sanjib Bal; Swain, Jagannath; Yadav, Nidhi; Yadav, Reena; Singh, Pooja; Rai, Preeti; Sheri, Vijay; Sreeman, Sheshshayee; Subramanyam, Rajagopal; Pareek, Ashwani; Gupta, Kapuganti JagadisNitric oxide (NO) is one of the byproducts of nitrogen metabolism. Excess amount of NO is scavenged by phytoglobins. The role of phytoglobin mediated NO homoeostasis in modulation of nitrate transporters was investigated using NO scavenger cPTIO, phytoglobin overexpressing rice and Arabidopsis. Growing plants under low nitrate leads to generation of reduced levels of NO accompanied by elevated expression of high affinity transporters (HATs) such as NRT2.1, NRT2.3 and NRT2.4. Scavenging of NO by cPTIO under optimal nitrate caused enhanced HATs expression. Phytoglobin overexpressing Arabidopsis showed improved growth and enhanced expression of HATs under low nitrogen in comparison to WT. Pretreatment of optimal nitrate grown plants with NO scavenger cPTIO enhanced HATs expression and shifting of these primed plants from optimal to low nitrate leads to further elevation of HATs expression accompanied by enhanced nitrogen uptake and its accumulation with positive effect on growth. Phytoglobin overexpression in rice leads to enhanced HATs expression, improved growth, nitrogen accumulation under low nitrate. Pgb OE lines showed enhanced accumulation of amino acids. Taken together our results suggest an important role of phytoglobins in nitrogen uptake and assimilation.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 Nitric oxide regulates mitochondrial biogenesis in plants(John Wiley & Sons, 2023) Kumari, Aprajita; Kaladhar, Vemula Chandra; Yadav, Nidhi; Singh, Pooja; Reddy, Kishorekumar; Gupta, Kapuganti JagadisThe site of nitric oxide (NO) production in mitochondrial cytochrome c oxidase and the role of NO in mitochondrial biogenesis are not known in plants. By imposing osmotic stress and recovery on Arabidopsis seedlings we investigated the site of NO production and its role in mitochondrial biogenesis. Osmotic stress reduced growth and mitochondrial number while increasing NO production. During the recovery phase the mitochondrial number increased and this increase was higher in wild type and the high NO-producing Pgb1 silencing line in comparison to the NO-deficient nitrate reductase double mutant (nia1/nia2). Application of nitrite stimulated NO production and mitochondrial number in the nia1/nia2 mutant. Osmotic stress induced COX6b−3 and COA6-L genes encoding subunits of COX. The mutants cox6b-3 and coa6-l were impaired both in NO production and mitochondrial number during stress to recovery suggesting the involvement of these subunits in nitrite-dependent NO production. Transcripts encoding the mitochondrial protein import machinery showed reduced expression in cox6b-3 and coa6-l mutants. Finally, COX6b-3 and COA6-L interacted with the VQ27 motif-containing protein in the presence of NO. The vq27 mutant was impaired in mitochondrial biogenesis. Our results suggest the involvement of COX derived NO in mitochondrial biogenesis.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 The power of the phytoglobin-NO cycle in the regulation of nodulation and symbiotic nitrogen fixation(John Wiley & Sons, Inc., 2020) Singh, Pooja; Kumari, Aprajita; Foyer, Christine H.; Gupta, Kapuganti JagadisRecent years have seen a large increase in our understanding of the multifaceted roles of nitric oxide (NO) in plant biology, particularly in the regulation of symbiotic interactions with soil microorganisms. NO serves key functions in the initiation and maintenance of legume–rhizobium symbiosis. Extensive molecular crosstalk between the host legume and the soil rhizobium results in the initiation of symbiosis and the establishment of a highly specialized organ called the nodule, which provides the conditions required for bacterial nitrogen fixation. Within the nodules, the rhizobium bacteria are housed in bacteroids, in which the oxygen is maintained at very low levels allowing the bacterial nitrogenase to function. This enzyme is oxygen sensitive (half maximal inhibitory concentration (IC50) oxygen for nitrogenase is 2.9 µM; Goldberg et al., 1987). Hence, a key feature of the nodule is the maintenance of a strong oxygen diffusion barrier, in which leghaemoglobin is used to transfer oxygen to the plant mitochondria to sustain respiration.Item The PHYTOGLOBIN-NO cycle regulates plant mycorrhizal symbiosis(Elsevier B.V., 2019) Kumari, Aprajita; Pathak, Pradeep Kumar; Loake, Gary J.; Gupta, Kapuganti JagadisThe production of the redox-active signaling molecule, NO, has long been associated with interactions between microbes and their host plants. Emerging evidence now suggests that specific NO signatures and cognate patterns of PHYTOGLOBIN1 (PHYTOGB1) expression, a key regulator of cellular NO homeostasis, may help determine either symbiosis or pathogenicity.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 Pathways of nitric oxide metabolism and operation of phytoglobins in legume nodules: missing links and future directions(John Wiley & Sons, 2018) Berger, Antoine; Brouquisse, Renaud; Pathak, Pradeep Kumar; Hichri, Imène; Singh, Inderjit; Bhatia, Sabhyata; Boscari, Alexandre; Igamberdiev, Abir U.; Gupta, Kapuganti JagadisThe interaction between legumes and rhizobia leads to the establishment of a beneficial symbiotic relationship. Recent advances in legume - rhizobium symbiosis revealed that various reactive oxygen and nitrogen species including nitric oxide (NO) play important roles during this process. Nodule development occurs with a transition from a normoxic environment during the establishment of symbiosis to a microoxic environment in functional nodules. Such oxygen dynamics are required for activation and repression of various NO production and scavenging pathways. Both the plant and bacterial partners participate in the synthesis and degradation of NO. However, the pathways of NO production and degradation as well as their cross-talk and involvement in the metabolism are still a matter of debate. The plant-originated reductive pathways are known to contribute to the NO production in nodules under hypoxic conditions. Non-symbiotic hemoglobin (phytoglobin) (Pgb) possesses high NO oxygenation capacity, buffers and scavenges NO. Its operation, through a respiratory cycle called Pgb-NO cycle, leads to the maintenance of redox and energy balance in nodules. The role of Pgb/NO cycle under fluctuating NO production from soil needs further investigation for complete understanding of NO regulatory mechanism governing nodule development to attain optimal food security under changing environment.