Nitric oxide triggers a transient metabolic reprogramming in Arabidopsis

[EN] Nitric oxide (NO) regulates plant growth and development as well as responses to stress that enhanced its endogenous production. Arabidopsis plants exposed to a pulse of exogenous NO gas were used for untargeted global metabolomic analyses thus allowing the identification of metabolic processes affected by NO. At early time points after treatment, NO scavenged superoxide anion and induced the nitration and the S-nitrosylation of proteins. These events preceded an extensive though transient metabolic reprogramming at 6 h after NO treatment, which included enhanced levels of polyamines, lipid catabolism and accumulation of phospholipids, chlorophyll breakdown, protein and nucleic acid turnover and increased content of sugars. Accordingly, lipid-related structures such as root cell membranes and leaf cuticle altered their permeability upon NO treatment. Besides, NO-treated plants displayed degradation of starch granules, which is consistent with the increased sugar content observed in the metabolomic survey. The metabolic profile was restored to baseline levels at 24 h post-treatment, thus pointing up the plasticity of plant metabolism in response to nitroxidative stress conditions.This work was supported by grants BIO2011-27526 and BIO2014-56067-P from the Spanish Ministry of Economy and Competitiveness and FEDER funds. We thank support and comments from Danny Alexander (Metabolon Inc., USA) on metabolomic analyses.Leon Ramos, J.; Costa-Broseta, Á.; Castillo López Del Toro, MC. (2016). Nitric oxide triggers a transient metabolic reprogramming in Arabidopsis. Scientific Reports. 6:1-14. doi:10.1038/srep37945S1146Arc, E., Galland, M., Godin, B., Cueff, G. & Rajjou, L. Nitric oxide implication in the control of seed dormancy and germination. Front. Plant Sci. 4, 346 (2013).Beligni, M. V. & Lamattina, L. Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210, 215–221 (2000).Lozano-Juste, J. & León, J. Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol. 156, 1410–1123 (2011).He, Y. et al. Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968–1971 (2004).Tsai, Y. C., Delk, N. A., Chowdhury, N. I. & Braam, J. Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering. Plant Signal. Behav. 2, 446–454 (2007).Manjunatha, G., Lokesh, V. & Neelwarne, B. Nitric oxide in fruit ripening: trends and opportunities. Biotechnol. Adv. 28, 489–499 (2010).Liu, F. & Guo, F. Q. Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. PLoS One 8(2), e56345 (2013).Du, J. et al. Nitric oxide induces cotyledon senescence involving co-operation of the NES1/MAD1 and EIN2-associated ORE1 signalling pathways in Arabidopsis. J. Exp. Bot. 65, 4051–4063 (2014).Siddiqui, M. H., Al-Whaibi, M. H. & Basalah, M. O. Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248, 447–455 (2011).Arasimowicz-Jelonek, M. & Floryszak-Wieczorek, J. Nitric oxide: an effective weapon of the plant or the pathogen? Mol. Plant Pathol. 15, 406–416 (2014).Thomas, D. D. Breathing new life into nitric oxide signaling: A brief overview of the interplay between oxygen and nitric oxide. Redox Biol. 5, 225–33 (2015).Groβ, F., Durner, J. & Gaupels, F. Nitric oxide, antioxidants and prooxidants in plant defence responses. Front. Plant Sci. 4, 419 (2013).Astier, J. & Lindermayr, C. Nitric oxide-dependent posttranslational modification in plants: an update. Int. J. Mol. Sci. 13, 15193–15208 (2012).Hess, D. T. & Stamler, J. S. Regulation by S-nitrosylation of protein post-translational modification. J. Biol. Chem. 287, 4411–4418 (2012).Guerra, D. D. & Callis, J. Ubiquitin on the move: the ubiquitin modification system plays diverse roles in the regulation of endoplasmic reticulum- and plasma membrane-localized proteins. Plant Physiol. 160, 56–64 (2012).Skalska, K., Miller, J. S. & Ledakowicz, S. Trends in NO(x) abatement: a review. Sci. Total Environ. 408, 3976–3989 (2010).Pilegaard, K. Processes regulating nitric oxide emissions from soils. Phil. Transac. Royal Soc. London. Ser. B, Biol. Sci. 368, 20130126 (2013).Jaegle, L., Steinberger, L., Martin, R. V. & Chance, K. Global partitioning of NOx sources using satellite observations: Relative roles of fossil fuel combustion, biomass burning and soil emissions. Faraday Discus. 130, 407–423 (2005).Gupta, K. J., Fernie, A. R., Kaiser, W. M. & van Dongen, J. T. On the origins of nitric oxide. Trends Plant Sci. 16, 160–168 (2011).Mur, L. A. et al. Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5, pls052 (2013).Correa-Aragunde, N., Foresi, N. & Lamattina, L. Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J. Exp. Bot. 66, 2913–2921 (2015).Noctor, G., Lelarge-Trouverie, C. & Mhamdi, A. The metabolomics of oxidative stress. Phytochemistry 112, 33–53 (2015).Allan, W. L., Simpson, J. P., Clark, S. M. & Shelp, B. J. Gamma-hydroxybutyrate accumulation in Arabidopsis and tobacco plants is a general response to abiotic stress: putative regulation by redox balance and glyoxylate reductase isoforms. J. Exp. Bot. 59, 2555–2564 (2008).Romero, L. C., Aroca, M. Á., Laureano-Marín, A. M., Moreno, I., García, I. & Gotor, C. Cysteine and cysteine-related signaling pathways in Arabidopsis thaliana. Mol. Plant 7, 264–276 (2014).Noctor, G. et al. Glutathione in plants: an integrated overview. Plant Cell Environ. 35, 454–484 (2012).Feussner, I. & Wasternack, C. The lipoxygenase pathway. Ann. Rev. Plant Biol. 53, 275–297 (2002).Green, M. A. & Fry, S. C. Vitamin C degradation in plant cells via enzymatic hydrolysis of 4-O-oxalyl-L-threonate. Nature 433, 83–87 (2005).Szarka, A., Tomasskovics, B. & Bánhegyi, G. The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int. J. Mol. Sci. 13, 4458–4483 (2012).Hurlock, A. K., Roston, R. L., Wang, K. & Benning, C. Lipid trafficking in plant cells. Traffic 15, 915–932 (2014).Blokhina, O., Virolainen, E. & Fagerstedt, K. V. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91, 179–194 (2003).Yeats, T. H. & Rose, J. K. The formation and function of plant cuticles. Plant Physiol. 163, 5–20 (2013).Lozano-Juste, J. & León, J. Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 152, 891–903 (2010).Hörtensteiner, S. Update on the biochemistry of chlorophyll breakdown. Plant Mol Biol. 82, 505–17 (2013).Pruzinská, A. et al. Chlorophyll breakdown in senescent Arabidopsis leaves: characterization of chlorophyll catabolites and of chlorophyll catabolic enzymes involved in the degreening reaction. Plant Physiol. 139, 52–63 (2005).Hirashima, M., Tanaka, R. & Tanaka, A. Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol. 50, 719–29 (2009).Zottini, M., Costa, A., De Michele, R., Ruzzene, M., Carimi, F. & Lo Schiavo, F. Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot. 58, 1397–1405 (2007).Mainz, E. R. et al. Monitoring intracellular nitric oxide production using microchip electrophoresis and laser-induced fluorescence detection. Analytical Methods 4, 414–420 (2012).Vandelle, E. & Delledonne, M. Peroxynitrite formation and function in plants. Plant Sci. 181, 534–539 (2011).Minocha, R., Majumdar, R. & Minocha, S. C. Polyamines and abiotic stress in plants: a complex relationship. Front. Plant Sci. 5, 175 (2014).Parsons H. T., Yasmin, T. & Fry, S. C. Alternative pathways of dehydroascorbic acid degradation in vitro and in plant cell cultures: novel insights into vitamin C catabolism. Biochem. J. 440, 375–383 (2011).Hou, Q., Ufer, G. & Bartels, D. Lipid signalling in plant responses to abiotic stress. Plant Cell Environ. 39, 1029–4108 (2016).Zhou, X. R., Callahan, D. L., Shrestha, P., Liu, Q., Petrie, J. R. & Singh, S. P. Lipidomic analysis of Arabidopsis seed genetically engineered to contain DHA. Front. Plant Sci. 5, 41 (2014).Pohl, C. H. & Kock, J. L. Oxidized fatty acids as inter-kingdom signaling molecules. Molecules 19, 1273–1285 (2014).Araújo, W. L., Tohge, T., Ishizaki, K., Leaver, C. J. & Fernie, A. R. Protein degradation-an alternative respiratory substrate for stressed plants. Trends Plant Sci. 16, 489–498 (2011).Sakamoto, W. & Takami, T. Nucleases in higher plants and their possible involvement in DNA degradation during leaf senescence. J. Exp. Bot. 65, 3835–3843 (2014).Del Duca, S., Serafini-Fracassini, D. & Cai, G. Senescence and programmed cell death in plants: polyamine action mediated by transglutaminase. Front. Plant Sci. 5, 120 (2014).Franco, M. C. & Estévez, A. G. Tyrosine nitration as mediator of cell death. Cell. Mol. Life Sci. 71, 3939–3950 (2014).Palumbo, A., Fiore, G., Di Cristo, C., Di Cosmo, A. & d’Ischia, M. NMDA receptor stimulation induces temporary alpha-tubulin degradation signalled by nitric oxide-mediated tyrosine nitration in the nervous system of Sepia officinalis. Biochem. Biophys. Res. Commun. 293, 1536–1543 (2002).Wang, Y. Y., Lin, S. Y., Chuang, Y. H., Mao, C. H., Tung, K. C. & Sheu, W. H. Protein nitration is associated with increased proteolysis in skeletal muscle of bile duct ligation-induced cirrhotic rats. Metabolism 59, 468–472 (2010).Castillo, M. C., Lozano-Juste, J., González-Guzmán, M., Rodriguez, L., Rodriguez, P. L. & León, J. Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci. Signal. 8(392), ra89 (2015).Blaise, G. A., Gauvin, D., Gangal, M. & Authier, S. Nitric oxide, cell signaling and cell death. Toxicology 208, 177–192 (2005).Brüne, B. Nitric oxide: NO apoptosis or turning it ON? Cell Death Differ. 10, 864–869 (2003).Wang, Y., Chen, C., Loake, G. J. & Chu, C. Nitric oxide: promoter or suppressor of programmed cell death? Prot. Cell 1, 133–142 (2010).Serrano, I., Romero-Puertas, M. C., Sandalio, L. M. & Olmedilla, A. The role of reactive oxygen species and nitric oxide in programmed cell death associated with self-incompatibility. J. Exp. Bot. 66, 2869–2876 (2015).Huang, S., Hill, R. D. & Stasolla, C. Plant hemoglobin participation in cell fate determination. Plant Signal. Behavior 9, e29485 (2014).Maes, M. B., Scharpé, S. & De Meester, I. Dipeptidyl peptidase II (DPPII), a review. Clin. Chim. Acta 380, 31–49 (2007).Gibbs, D. J. et al. Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol. Cell 53, 369–379 (2014).Kitamura, K. Inhibition of the Arg/N-end rule pathway-mediated proteolysis by dipeptide-mimetic molecules. Amino Acids 48, 235–243 (2016).Duek, P. D., Elmer, M. V., van Oosten, V. R. & Fankhauser C. The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr Biol. 14, 2296–2301 (2004)

Cardiovascular Risk Factors in an Eastern Caribbean Island: Prevalence of Non-communicable Chronic Diseases and Associated Lifestyle Risk Factors for Cardiovascular Morbidity and Mortality in the British Virgin Islands

Background: The epidemiological transition has seen a trend from communicable to non-com-municable diseases in developing countries. At the pinnacle of these chronic diseases is hypertension, pre-hypertension, diabetes and obesity. This leads to increased cardiovascular morbidity and mortality worldwide. In addition, environmental and behavioural changes such as lifestyle habits represent modifiable risk factors for the development of cardiovascular diseases. The Caribbean is not immune to this trend. Methods: This was a cross-sectional survey conducted between June and September 2009 and involved individuals 15–74 years of age. Age-gender was weighted to get as close a representative sample of the general population living in the British Virgin Islands (BVI) for more than two years to a total of 301 (n = 301, M: 144, F: 157; CI 95% ± error 5%). The study was carried out using a handout ques-tionnaire that included variables on age, gender, socio-economic status (SES), income level, cigarette smoking, physical activity, weight, height, body mass index (BMI), blood pressure, fasting blood glucose and cholesterol. Results: This study shows a prevalence of hypertension of 16.6%, pre-hypertension – 29.9%, diabetes mellitus – 10.0% [M: 5.6%, F: 14%, p 30) – 23.6% (M: 17.4%, F: 29.3%, p < 0.001) [all significantly higher in women], smoking habits – 16.6% and alcohol – 51.2% [significantly higher in men: 22.5% and 56.7%, respectively]. Of the respondents, 43.2% had a low/inactive physical activity level. Clustering of greater than one risk factor was more pronounced for women than for men 29.6% (M: 27.1%, F: 31.8%, p < 0.05). Sedentary lifestyle (low/inactive physical activity) and obesity were the only risk factors that had a positive correlation with all four chronic diseases (p < 0.05). Conclusion: The above results indicate that a national strategy needs to be implemented to control cardiovascular diseases, educate the population and promote healthy lifestyle habits with particular attention to low physical inactivity and obesity. Keywords: British Virgin Islands, cardiovascular risk, Eastern Caribbean, diabetes mellitus, hypertension, impaired fasting glucose, lifestyle, obesity, pre-hypertension "Factores de Riesgo Cardiovascular en una isla del Caribe Oriental: Prevalencia de las Enfermedades Crónicas no Comunicables y Factores de Riesgo Asociados con el Estilo de Vida en Relación con la Morbilidad y la Mortalidad Cardiovasculares en las Islas Vírgenes Británicas" RESUMEN Antecedentes: La transición epidemiológica ha visto una tendencia a pasar de enfermedades comunicables a enfermedades no comunicables en los países en vías de desarrollo. En la cima de estas enfermedades crónicas se hallan la hipertensión, la pre-hipertensión, la diabetes y la obesidad. Esto conduce al aumento de la morbilidad y la mortalidad cardiovasculares a nivel mundial. Además, los cambios medioambientales y conductuales tales como los hábitos de estilo de vida, representan factores de riesgo modificables para el desarrollo de las enfermedades cardiovasculares. El Caribe no es ajeno a esta tendencia. Métodos: Se trata de un estudio transversal llevado a cabo entre junio y septiembre de 2009, el cual incluyó individuos de 15–74 años de edad. Se ponderó la edad-género con el propósito de obtener una muestra tan representativa como fuera posible de la población general que vive en las Islas Vírgenes Británicas (IVB) por más de dos años para un total de 301 (n = 301, M: 144, F: 157; CI 95% error ± 5%). El estudio fue llevado a cabo usando hojas informativas con un cuestionario que incluían las variables: edad, género, estatus socioeconómico (ESE), nivel de ingresos, hábito de fumar, actividad física, peso, altura, índice de masa corporal (IMC), presión sanguínea, y prueba de colesterol y de glucosa en sangre en ayunas. Resultados: Este estudio muestra una prevalencia de hipertensión de 16.6%, pre-hipertensión 29.9%, diabetes mellitus 10.0% [M: 5.6%, F: 14%, p 30) 23.6% (M: 17.4%, F: 29.3%, p < 0.001) [todos significativamente más altos en las mujeres], hábito de fumar 16.6% y consumo de alcohol 51.2% [significativamente más altos en los hombres 22.5% y 56.7%, respectivamente]. De los encuestados, el 43.2% tenían un nivel de actividad física inactivo/bajo. La existencia de más de un factor de riesgo fue más pronunciada en las mujeres que en los hombres 29.6% (M: 27.1%, F: 31.8%, p < 0.05). El estilo de vida sedentario (actividad física inactiva/baja) y la obesidad fueron los únicos factores de riesgo que tuvieron una correlación positiva con las cuatro enfermedades crónicas (p < 0.05). Conclusión: Los resultados enumerados indican que es necesario implementar una estrategia nacional a fin de controlar las enfermedades cardiovasculares, educar, y promover hábitos de estilo de vida saludables con atención particular a la actividad física baja y la obesidad. Palabras claves: Islas Vírgenes Británicas, riesgo cardiovascular, Caribe oriental, diabetes mellitus, hipertensión, glucosa en ayunas alterada, estilo de vida, obesidad, pre-hipertensió

Plastid Transient and Stable Interactions with Other Cell Compartments

International audiencePlastids are organelles delineated by two envelopes that play important roles in different cellular processes such as energy production or lipid biosynthesis. To regulate their biogenesis and their function, plastids have to communicate with other cellular compartments. This communication can be mediated by signaling molecules and by the establishment of direct contacts between the plastid envelope and other organelles such as the endoplasmic reticulum, the mitochondria, the plasma membrane, the peroxisomes and the nucleus. These interactions are highly dynamic and respond to different biotic and abiotic stresses. However, the mechanisms involved in the formation of plastid-organelle contact sites and their functions are still enigmatic. In this chapter, we summarize our current knowledge about plastid contact sites and their role in the regulation of plastid biogenesis and function