Publications of NIPGR Scientists
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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 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 Recommendations on terminology and experimental best practice associated with plant nitric oxide research(John Wiley & Sons, 2020) Gupta, Kapuganti Jagadis; Hancock, John T.; Petrivalsky, Marek; Kolbert, Zsuzsanna; Lindermayr, Christian; Durner, Jorg; Barroso, Juan B.; Palma, José M.; Brouquisse, Renaud; Wendehenne, David; Corpas, Francisco J.; Loake, Gary J.Nitric oxide (NO) emerged as a key signal molecule in plants. During the last two decades impressive progress has been made in plant NO research. This small, redox‐active molecule is now known to play an important role in plant immunity, stress responses, environmental interactions, plant growth and development. To more accurately and robustly establish the full spectrum of NO bioactivity in plants, it will be essential to apply methodological best practice. In addition, there are some instances of conflicting nomenclature within the field, which would benefit from standardisation. In this context, we attempt to provide some helpful guidance for best practice associated with NO research and also suggestions for the cognate terminology.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 Interaction of nitric oxide with the components of plant mitochondrial electron transport chain(Oxford University Press, 2018) Gupta, Kapuganti Jagadis; Kumari, Aprajita; Florez-Sarasa, Igor; Fernie, Alisdair R; Igamberdiev, Abir UMitochondria are not only major sites for energy production but also participate in several alternative functions, among these generation of nitric oxide (NO) and its different impacts on this organelle is increasing attention. The inner mitochondrial membrane contains the chain of protein complexes, and electron transfer via oxidation of various organic acids and reducing equivalents leads to generation of proton gradient that results in energy production. Recent evidence suggests that these complexes are sources and targets for NO. Complex I and rotenone-insensitive NAD(P)H dehydrogenases regulate hypoxic NO production, while complex I also participates in the formation of supercomplex with complex III under hypoxia. Complex II is a target for NO which by inhibiting Fe-S centres regulates ROS generation, and complex III is one of the major sites for NO production and the produced NO participates in the phytoglobin-NO cycle that leads to the maintenance of redox level and limited energy production under hypoxia. Expression of the alternative oxidase (AOX) is induced by NO under various stress conditions, and evidence exists that AOX can regulate mitochondrial NO production. Complex IV is another major site for NO production which can also be linked to ATP generation via the phytoglobin-NO cycle. Inhibition of complex IV by NO can prevent oxygen depletion at the frontier of anoxia. The NO production and action on various complexes play a major role in NO signalling and energy metabolism.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.Item Nitric oxide is essential for the development of aerenchyma in wheat roots under hypoxic stress(John Wiley & Sons, 2017) Wany, Aakanksha; Kumari, Aprajita; Gupta, Kapuganti JagadisIn response to flooding/waterlogging, plants develop various anatomical changes including the formation of lysigenous aerenchyma for the delivery of oxygen to roots. Under hypoxia, plants produce high levels of nitric oxide (NO) but the role of this molecule in plant-adaptive response to hypoxia is not known. Here, we investigated whether ethylene-induced aerenchyma requires hypoxia-induced NO. Under hypoxic conditions, wheat roots produced NO apparently via nitrate reductase and scavenging of NO led to a marked reduction in aerenchyma formation. Interestingly, we found that hypoxically induced NO is important for induction of the ethylene biosynthetic genes encoding ACC synthase and ACC oxidase. Hypoxia-induced NO accelerated production of reactive oxygen species, lipid peroxidation, and protein tyrosine nitration. Other events related to cell death such as increased conductivity, increased cellulase activity, DNA fragmentation, and cytoplasmic streaming occurred under hypoxia, and opposing effects were observed by scavenging NO. The NO scavenger cPTIO (2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide potassium salt) and ethylene biosynthetic inhibitor CoCl2 both led to reduced induction of genes involved in signal transduction such as phospholipase C, G protein alpha subunit, calcium-dependent protein kinase family genes CDPK, CDPK2, CDPK 4, Ca-CAMK, inositol 1,4,5-trisphosphate 5-phosphatase 1, and protein kinase suggesting that hypoxically induced NO is essential for the development of aerenchyma.Item Moving nitrogen to the centre of plant defence against pathogens(Oxford University Press, 2017) Mur, Luis A.J.; Simpson, Catherine; Kumari, Aprajita; Gupta, Alok Kumar; Gupta, Kapuganti JagadisBackground Plants require nitrogen (N) for growth, development and defence against abiotic and biotic stresses. The extensive use of artificial N fertilizers has played an important role in the Green Revolution. N assimilation can involve a reductase series (NO–3→ NO–2 → NH+4) followed by transamination to form amino acids. Given its widespread use, the agricultural impact of N nutrition on disease development has been extensively examined. Scope: When a pathogen first comes into contact with a host, it is usually nutrient starved such that rapid assimilation of host nutrients is essential for successful pathogenesis. Equally, the host may reallocate its nutrients to defence responses or away from the site of attempted infection. Exogenous application of N fertilizer can, therefore, shift the balance in favour of the host or pathogen. In line with this, increasing N has been reported either to increase or to decrease plant resistance to pathogens, which reflects differences in the infection strategies of discrete pathogens. Beyond considering only N content, the use of NO-3 or NH+4 fertilizers affects the outcome of plant–pathogen interactions. NO-3 feeding augments hypersensitive response- (HR) mediated resistance, while ammonium nutrition can compromise defence. Metabolically, NO–3 enhances production of polyamines such as spermine and spermidine, which are established defence signals, with NH+4 nutrition leading to increased γ-aminobutyric acid (GABA) levels which may be a nutrient source for the pathogen. Within the defensive N economy, the roles of nitric oxide must also be considered. This is mostly generated from NO–2 by nitrate reductase and is elicited by both pathogen-associated microbial patterns and gene-for-gene-mediated defences. Nitric oxide (NO) production and associated defences are therefore NO-3 dependent and are compromised by NH+4. Conclusion:This review demonstrates how N content and form plays an essential role in defensive primary and secondary metabolism and NO-mediated events.