RESUMEN
The entrapment of NO donors in nanomaterials has emerged as a strategy to protect these molecules from rapid degradation, allowing a more controlled release of NO and prolonging its effect. On the other hand, we have found beneficial effects of S-nitrosoglutathione (GSNO) - a NO donor - supplying to sugarcane plants under water deficit. Here, we hypothesized that GSNO encapsulated into nanoparticles would be more effective in attenuating the effects of water deficit on sugarcane plants as compared to the supplying of GSNO in its free form. The synthesis and characterization of chitosan nanoparticles containing GSNO were also reported. Sugarcane plants were grown in nutrient solution, and then subjected to the following treatments: control (well-hydrated); water deficit (WD); WD + GSNO sprayed in its free form (WDG) or encapsulated (WDG-NP). In general, both GSNO forms attenuated the effects of water deficit on sugarcane plants. However, the encapsulation of this donor into chitosan nanoparticles caused higher photosynthetic rates under water deficit, as compared to plants supplied with free GSNO. The root/shoot ratio was also increased when encapsulated GSNO was supplied, indicating that delayed release of NO improves drought tolerance of sugarcane plants. Our results provide experimental evidence that nanotechnology can be used for enhancing NO-induced benefits for plants under stressful conditions, alleviating the negative impact of water deficit on plant metabolism and increasing biomass allocation to root system.
Asunto(s)
Quitosano/química , Nanopartículas/química , Donantes de Óxido Nítrico/farmacología , S-Nitrosoglutatión/farmacología , Saccharum/efectos de los fármacos , Estrés Fisiológico/efectos de los fármacos , Biomasa , Preparaciones de Acción Retardada/química , Sequías , Portadores de Fármacos/química , Donantes de Óxido Nítrico/síntesis química , Fotosíntesis/efectos de los fármacos , Hojas de la Planta/efectos de los fármacos , Raíces de Plantas/efectos de los fármacos , Brotes de la Planta/efectos de los fármacos , S-Nitrosoglutatión/síntesis químicaRESUMEN
Water deficit is a major environmental constraint on crop productivity and performance and nitric oxide (NO) is an important signaling molecule associated with many biochemical and physiological processes in plants under stressful conditions. This study aims to test the hypothesis that leaf spraying of S-nitrosoglutathione (GSNO), an NO donor, improves the antioxidant defense in both roots and leaves of sugarcane plants under water deficit, with positive consequences for photosynthesis. In addition, the roles of key photosynthetic enzymes ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) and phosphoenolpyruvate carboxylase (PEPC) in maintaining CO2 assimilation of GSNO-sprayed plants under water deficit were evaluated. Sugarcane plants were sprayed with water or GSNO 100 µM and subjected to water deficit, by adding polyethylene glycol (PEG-8000) to the nutrient solution. Sugarcane plants supplied with GSNO presented increases in the activity of antioxidant enzymes such as superoxide dismutase in leaves and catalase in roots, indicating higher antioxidant capacity under water deficit. Such adjustments induced by GSNO were sufficient to prevent oxidative damage in both organs and were associated with better leaf water status. As a consequence, GSNO spraying alleviated the negative impact of water deficit on stomatal conductance and photosynthetic rates, with plants also showing increases in Rubisco activity under water deficit.
Asunto(s)
Donantes de Óxido Nítrico/farmacología , Fosfoenolpiruvato Carboxilasa/efectos de los fármacos , Ribulosa-Bifosfato Carboxilasa/efectos de los fármacos , S-Nitrosoglutatión/farmacología , Saccharum/efectos de los fármacos , Antioxidantes/metabolismo , Catalasa/metabolismo , Deshidratación , Oxidación-Reducción , Fosfoenolpiruvato Carboxilasa/metabolismo , Fotosíntesis/efectos de los fármacos , Hojas de la Planta/efectos de los fármacos , Hojas de la Planta/enzimología , Hojas de la Planta/fisiología , Raíces de Plantas/efectos de los fármacos , Raíces de Plantas/enzimología , Raíces de Plantas/fisiología , Estomas de Plantas/efectos de los fármacos , Estomas de Plantas/enzimología , Estomas de Plantas/fisiología , Transpiración de Plantas/efectos de los fármacos , Ribulosa-Bifosfato Carboxilasa/metabolismo , Saccharum/enzimología , Saccharum/fisiología , Superóxido Dismutasa/metabolismo , Agua/fisiologíaRESUMEN
MAIN CONCLUSION: Nitric oxide (NO)-mediated redox signaling plays a role in alleviating the negative impact of water stress in sugarcane plants by improving root growth and photosynthesis. Drought is an environmental limitation affecting sugarcane growth and yield. The redox-active molecule nitric oxide (NO) is known to modulate plant responses to stressful conditions. NO may react with glutathione (GSH) to form S-nitrosoglutathione (GSNO), which is considered the main reservoir of NO in cells. Here, we investigate the role of NO in alleviating the effects of water deficit on growth and photosynthesis of sugarcane plants. Well-hydrated plants were compared to plants under drought and sprayed with mock (water) or GSNO at concentrations ranging from 10 to 1000 µM. Leaf GSNO sprayed plants showed significant improvement of relative water content and leaf and root dry matter under drought compared to mock-sprayed plants. Additionally, plants sprayed with GSNO (≥ 100 µM) showed higher leaf gas exchange and photochemical activity as compared to mock-sprayed plants under water deficit and after rehydration. Surprisingly, a raise in the total S-nitrosothiols content was observed in leaves sprayed with GSH or GSNO, suggesting a long-term role of NO-mediated responses to water deficit. Experiments with leaf discs fumigated with NO gas also suggested a role of NO in drought tolerance of sugarcane plants. Overall, our data indicate that the NO-mediated redox signaling plays a role in alleviating the negative effects of water stress in sugarcane plants by protecting the photosynthetic apparatus and improving shoot and root growth.
Asunto(s)
Sequías , Óxido Nítrico/farmacología , Fotosíntesis/efectos de los fármacos , Saccharum/efectos de los fármacos , Análisis de Varianza , Dióxido de Carbono/metabolismo , Deshidratación , Óxido Nítrico/metabolismo , Donantes de Óxido Nítrico/metabolismo , Donantes de Óxido Nítrico/farmacología , Oxidación-Reducción/efectos de los fármacos , Hojas de la Planta/efectos de los fármacos , Hojas de la Planta/crecimiento & desarrollo , Hojas de la Planta/metabolismo , Raíces de Plantas/efectos de los fármacos , Raíces de Plantas/crecimiento & desarrollo , Raíces de Plantas/metabolismo , Brotes de la Planta/efectos de los fármacos , Brotes de la Planta/crecimiento & desarrollo , Brotes de la Planta/metabolismo , S-Nitrosoglutatión/metabolismo , S-Nitrosoglutatión/farmacología , Saccharum/crecimiento & desarrollo , Saccharum/metabolismo , Agua/metabolismo , Agua/farmacologíaRESUMEN
Stability is a key trait for plant growth and development in a changing environment, involving homeostasis and resilience. While homeostasis refers to the maintenance of the internal structural and functional plant integrity, resilience is associated with the plant ability in returning to the initial conditions after a given disturbance. Such concepts are especially relevant for perennial and semi-perennial plants facing seasonal and frequent stress conditions. Although plant memory is closely associated with plant performance under recurrent stresses, to date, there is no study evaluating how stress memory is linked to stability under varying water conditions. Herein, we evaluated the association between drought stability and memory in sugarcane plants and proposed a new stability index to evaluate plant memory. Two datasets were analyzed, the first deals with leaf gas exchange and photochemistry of sugarcane plants grown in nutrient solution and exposed to one, two or three water deficit cycles. The second takes into account the physiological performance of sugarcane propagules obtained by vegetative propagation from plants that faced drought. To quantify sugarcane stability, we estimated the drought impact, the disturbance rate (DR), drought perturbation, and recovery rate (RR) for plants from both datasets. Drought memory - given by improved performance after previous stress events or when origin material faced drought - was detected in both datasets, changing either DR or RR. Based on these indices, we proposed the overall stability (OSt), defined as the ratio between RR and DR. While DR is associated to plant homeostasis, RR is a measure of plant resilience. Sugarcane plants exposed to three cycles of water deficit or those propagules originated from stressed plants presented the highest OSt values, showing higher RR and/or lower DR when compared to well-watered plants or to propagules from well-watered plants. Regarding the physiological traits evaluated, leaf CO2 assimilation and stomatal conductance were the most consistent variables in revealing drought stability and memory. Concluding, OSt revealed consistently patterns of response associated with plant memory, besides quantifying plant stability under stressful conditions.
Asunto(s)
Botánica/métodos , Sequías , Saccharum/fisiología , Estrés FisiológicoRESUMEN
Drought stress can imprint marks in plants after a previous exposure, leading to plant acclimation and a permissive state that facilitates a more effective response to subsequent stress events. Such stress imprints would benefit plants obtained through vegetative propagation (propagules). Herein, our hypothesis was that the propagules obtained from plants previously exposed to water deficit would perform better under water deficit as compared to those obtained from plants that did not face stressful conditions. Sugarcane plants were grown under well-hydrated conditions or subjected to three cycles of water deficit by water withholding. Then, the propagules were subjected to water deficit. Leaf gas exchange was reduced under water deficit and the propagules from plants that experienced water deficit presented a faster recovery of CO2 assimilation and higher instantaneous carboxylation efficiency after rehydration as compared to the propagules from plants that never faced water deficit. The propagules from plants that faced water deficit also showed the highest leaf proline concentration under water deficit as well as higher leaf H2O2 concentration and leaf ascorbate peroxidase activity regardless of water regime. Under well-watered conditions, the propagules from plants that faced stressful conditions presented higher root H2O2 concentration and higher activity of catalase in roots as compared to the ones from plants that did not experience water shortage. Such physiological changes were associated with improvements in leaf area and shoot and root dry matter accumulation in propagules obtained from stressed plants. Our results suggest that root H2O2 concentration is a chemical signal associated with improved sugarcane performance under water deficit. Taken together, our findings bring a new perspective to the sugarcane production systems, in which plant acclimation can be explored for improving drought tolerance in rainfed areas.
Asunto(s)
Dióxido de Carbono/metabolismo , Osmorregulación , Hojas de la Planta/crecimiento & desarrollo , Raíces de Plantas/crecimiento & desarrollo , Saccharum/crecimiento & desarrollo , Agua/metabolismo , Deshidratación , Peróxido de Hidrógeno/metabolismoRESUMEN
Under field conditions, plants are exposed to cycles of dehydration and rehydration during their lifespan. In this study, we hypothesized that sugarcane plants previously exposed to cycles of water deficits will perform better than plants that have never faced water deficits when both are subjected to low water availability. Sugarcane plants were grown in a nutrient solution and exposed to one (1WD), two (2WD) or three (3WD) water deficit cycles. As the reference, plants were grown in a nutrient solution without adding polyethylene glycol. Under water deficits, leaf gas exchange was significantly reduced in 1WD and 2WD plants. However, 3WD plants showed similar CO2 assimilation and lower stomatal conductance compared to the reference plants, with increases in intrinsic water-use efficiency. Abscisic acid concentrations were lower in 3WD plants than in 1WD plants. Our data revealed root H2O2 concentration as an important chemical signal, with the highest root H2O2 concentrations found in 3WD plants. These plants presented higher root dry matter and root:shoot ratios compared to the reference plants, as well as higher biomass production when water was available. Our data suggest that sugarcane plants were able to store information from previous stressful events, with plant performance improving under water deficits. In addition, our findings provide a new perspective for increasing drought tolerance in sugarcane plants under nursery conditions.
Asunto(s)
Sequías , Saccharum/fisiología , Agua/metabolismo , Ácido Abscísico/metabolismo , Peróxido de Hidrógeno/metabolismo , Hojas de la Planta/anatomía & histología , Hojas de la Planta/química , Hojas de la Planta/fisiología , Raíces de Plantas/fisiología , Saccharum/anatomía & histología , Saccharum/química , Transducción de Señal/fisiologíaRESUMEN
Exogenous supply of nitric oxide (NO) increases drought tolerance in sugarcane plants. However, little is known about the role of NO produced by plants under water deficit. The aim of this study was to test the hypothesis that drought-tolerance in sugarcane is associated with NO production and metabolism, with the more drought-tolerant genotype presenting higher NO accumulation in plant tissues. The sugarcane genotypes IACSP95-5000 (drought-tolerant) and IACSP97-7065 (drought-sensitive) were submitted to water deficit by adding polyethylene glycol (PEG-8000) in nutrient solution to reduce the osmotic potential to -0.4 MPa. To evaluate short-time responses to water deficit, leaf and root samples were taken after 24 h under water deficit. The drought-tolerant genotype presented higher root extracellular NO content, which was accompanied by higher root nitrate reductase (NR) activity as compared to the drought-sensitive genotype under water deficit. In addition, the drought-tolerant genotype had higher leaf intracellular NO content than the drought-sensitive one. IACSP95-5000 exhibited decreases in root S-nitrosoglutathione reductase (GSNOR) activity under water deficit, suggesting that S-nitrosoglutathione (GSNO) is less degraded and that the drought-tolerant genotype has a higher natural reservoir of NO than the drought-sensitive one. Those differences in intracellular and extracellular NO contents and enzymatic activities were associated with higher leaf hydration in the drought-tolerant genotype as compared to the sensitive one under water deficit.