- -

Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation

Mostrar el registro sencillo del ítem

Ficheros en el ítem

Thumbnail
Nombre: Expósito;Martín;B ...
Tamaño: 1.629Mb
Formato: PDF
Descripción: Versión editorial
Abrir
dc.contributor.author Expósito, Joana R. es_ES
dc.contributor.author Martín San Román, Sara es_ES
dc.contributor.author Barreno, Eva es_ES
dc.contributor.author Reig-Armiñana, José es_ES
dc.contributor.author García-Breijo, Francisco-José es_ES
dc.contributor.author Catalá, Myriam es_ES
dc.date.accessioned 2021-01-30T04:31:41Z
dc.date.available 2021-01-30T04:31:41Z
dc.date.issued 2019-07 es_ES
dc.identifier.uri http://hdl.handle.net/10251/160303
dc.description.abstract [EN] Lichens are poikilohydrous symbiotic associations between a fungus, photosynthetic partners, and bacteria. They are tolerant to repeated desiccation/rehydration cycles and adapted to anhydrobiosis. Nitric oxide (NO) is a keystone for stress tolerance of lichens; during lichen rehydration, NO limits free radicals and lipid peroxidation but no data on the mechanisms of its synthesis exist. The aim of this work is to characterize the synthesis of NO in the lichen Ramalina farinacea using inhibitors of nitrate reductase (NR) and nitric oxide synthase (NOS), tungstate, and NG-nitro-L-arginine methyl ester (L-NAME), respectively. Tungstate suppressed the NO level in the lichen and caused an increase in malondialdehyde during rehydration in the hyphae of cortex and in phycobionts, suggesting that a plant-like NR is involved in the NO production. Specific activity of NR in R. farinacea was 91 U/mg protein, a level comparable to those in the bryophyte Physcomitrella patens and Arabidopsis thaliana. L-NAME treatment did not suppress the NO level in the lichens. On the other hand, NADPH-diaphorase activity cytochemistry showed a possible presence of a NOS-like activity in the microalgae where it is associated with cytoplasmatic vesicles. These data provide initial evidence that NO synthesis in R. farinacea involves NR. es_ES
dc.description.sponsorship This research was funded by Ministerio de Economia y Competitividad (MINECO - FEDER, Spain) (CGL2016-79158-P) and Generalitat Valenciana (GVA, Excellence in Research, Spain) (PROMETEOIII/2017/039). es_ES
dc.language Inglés es_ES
dc.publisher MDPI es_ES
dc.relation.ispartof Plants es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Trebouxia es_ES
dc.subject Microalgae es_ES
dc.subject Lipid peroxidation es_ES
dc.subject Diaphorase activity es_ES
dc.subject Lichens es_ES
dc.subject Nitric oxide es_ES
dc.subject Nitrate reductase es_ES
dc.subject Nitric oxide synthase es_ES
dc.subject.classification BOTANICA es_ES
dc.title Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.3390/plants8070189 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEO%2F2017%2F039/ES/La simbiosis liquénica como asociación mutualista compleja, paradigma de resiliencia en ambientes adversos. Diversidad genómica, estructural y funcional/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//CGL2016-79158-P/ES/NUEVA PERSPECTIVA INTERDISCIPLINAR SOBRE LA COMPLEJIDAD DE LAS SIMBIOSIS LIQUENICAS: ESTUDIO GENOMICO Y FUNCIONAL DE MICROALGAS Y BACTERIAS/ es_ES
dc.rights.accessRights Abierto es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Ecosistemas Agroforestales - Departament d'Ecosistemes Agroforestals es_ES
dc.description.bibliographicCitation Expósito, JR.; Martín San Román, S.; Barreno, E.; Reig-Armiñana, J.; García-Breijo, F.; Catalá, M. (2019). Inhibition of NO Biosynthetic Activities during Rehydration of Ramalina farinacea Lichen Thalli Provokes Increases in Lipid Peroxidation. Plants. 8(7):1-15. https://doi.org/10.3390/plants8070189 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.3390/plants8070189 es_ES
dc.description.upvformatpinicio 1 es_ES
dc.description.upvformatpfin 15 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 8 es_ES
dc.description.issue 7 es_ES
dc.identifier.eissn 2223-7747 es_ES
dc.identifier.pmid 31247947 es_ES
dc.identifier.pmcid PMC6681199 es_ES
dc.relation.pasarela S\390149 es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.description.references Kranner, I., Beckett, R., Hochman, A., & Nash, T. H. (2008). Desiccation-Tolerance in Lichens: A Review. The Bryologist, 111(4), 576-593. doi:10.1639/0007-2745-111.4.576 es_ES
dc.description.references Kranner, I., Cram, W. J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E., & Pfeifhofer, H. W. (2005). Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proceedings of the National Academy of Sciences, 102(8), 3141-3146. doi:10.1073/pnas.0407716102 es_ES
dc.description.references WILSON, I. D., NEILL, S. J., & HANCOCK, J. T. (2008). Nitric oxide synthesis and signalling in plants. Plant, Cell & Environment, 31(5), 622-631. doi:10.1111/j.1365-3040.2007.01761.x es_ES
dc.description.references Meilhoc, E., Cam, Y., Skapski, A., & Bruand, C. (2010). The Response to Nitric Oxide of the Nitrogen-Fixing Symbiont Sinorhizobium meliloti. Molecular Plant-Microbe Interactions®, 23(6), 748-759. doi:10.1094/mpmi-23-6-0748 es_ES
dc.description.references Feelisch, M., & Martin, J. F. (1995). The early role of nitric oxide in evolution. Trends in Ecology & Evolution, 10(12), 496-499. doi:10.1016/s0169-5347(00)89206-x es_ES
dc.description.references Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7(9), 405-410. doi:10.1016/s1360-1385(02)02312-9 es_ES
dc.description.references Vranova, E. (2002). Signal transduction during oxidative stress. Journal of Experimental Botany, 53(372), 1227-1236. doi:10.1093/jexbot/53.372.1227 es_ES
dc.description.references Millar, A. H., & Day, D. A. (1996). Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Letters, 398(2-3), 155-158. doi:10.1016/s0014-5793(96)01230-6 es_ES
dc.description.references Caro, A., & Puntarulo, S. (1998). Nitric oxide decreases superoxide anion generation by microsomes from soybean embryonic axes. Physiologia Plantarum, 104(3), 357-364. doi:10.1034/j.1399-3054.1998.1040310.x es_ES
dc.description.references BOVERIS, A. D., GALATRO, A., & PUNTARULO, S. (2000). Effect of nitric oxide and plant antioxidants on microsomal content of lipid radicals. Biological Research, 33(2). doi:10.4067/s0716-97602000000200016 es_ES
dc.description.references Wendehenne, D., & Hancock, J. T. (2011). New frontiers in nitric oxide biology in plant. Plant Science, 181(5), 507-508. doi:10.1016/j.plantsci.2011.07.010 es_ES
dc.description.references Gupta, K. J., Fernie, A. R., Kaiser, W. M., & van Dongen, J. T. (2011). On the origins of nitric oxide. Trends in Plant Science, 16(3), 160-168. doi:10.1016/j.tplants.2010.11.007 es_ES
dc.description.references Mallick, N., Mohn, F. H., Soeder, C. J., & Grobbelaar, J. U. (2002). Ameliorative role of nitric oxide on H2O2 toxicity to a chlorophycean alga Scenedesmus obliquus. The Journal of General and Applied Microbiology, 48(1), 1-7. doi:10.2323/jgam.48.1 es_ES
dc.description.references Chen, K., Feng, H., Zhang, M., & Wang, X. (2003). Nitric oxide alleviates oxidative damage in the green algaChlorella pyrenoidosa caused by UV-B radiation. Folia Microbiologica, 48(3), 389-393. doi:10.1007/bf02931372 es_ES
dc.description.references Wilken, M., & Huchzermeyer, B. (1999). Suppression of mycelia formation by NO produced endogenously in Candida tropicalis. European Journal of Cell Biology, 78(3), 209-213. doi:10.1016/s0171-9335(99)80100-9 es_ES
dc.description.references Maier, J., Hecker, R., Rockel, P., & Ninnemann, H. (2001). Role of Nitric Oxide Synthase in the Light-Induced Development of Sporangiophores in Phycomyces blakesleeanus. Plant Physiology, 126(3), 1323-1330. doi:10.1104/pp.126.3.1323 es_ES
dc.description.references Kong, W., Huang, C., Chen, Q., Zou, Y., & Zhang, J. (2012). Nitric oxide alleviates heat stress-induced oxidative damage in Pleurotus eryngii var. tuoliensis. Fungal Genetics and Biology, 49(1), 15-20. doi:10.1016/j.fgb.2011.12.003 es_ES
dc.description.references Song, N.-K., Jeong, C.-S., & Choi, H.-S. (2000). Identification of nitric oxide synthase in Flammulina velutipes. Mycologia, 92(6), 1027-1032. doi:10.1080/00275514.2000.12061247 es_ES
dc.description.references Catalá, M., Gasulla, F., Pradas del Real, A. E., García-Breijo, F., Reig-Armiñana, J., & Barreno, E. (2010). Fungal-associated NO is involved in the regulation of oxidative stress during rehydration in lichen symbiosis. BMC Microbiology, 10(1), 297. doi:10.1186/1471-2180-10-297 es_ES
dc.description.references Weissman, L., Garty, J., & Hochman, A. (2005). Rehydration of the Lichen Ramalina lacera Results in Production of Reactive Oxygen Species and Nitric Oxide and a Decrease in Antioxidants. Applied and Environmental Microbiology, 71(4), 2121-2129. doi:10.1128/aem.71.4.2121-2129.2005 es_ES
dc.description.references Catalá, M., Gasulla, F., Pradas del Real, A. E., García-Breijo, F., Reig-Armiñana, J., & Barreno, E. (2013). The organic air pollutant cumene hydroperoxide interferes with NO antioxidant role in rehydrating lichen. Environmental Pollution, 179, 277-284. doi:10.1016/j.envpol.2013.04.015 es_ES
dc.description.references Wendehenne, D., Pugin, A., Klessig, D. F., & Durner, J. (2001). Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends in Plant Science, 6(4), 177-183. doi:10.1016/s1360-1385(01)01893-3 es_ES
dc.description.references Bogdan, C. (2001). Nitric oxide and the regulation of gene expression. Trends in Cell Biology, 11(2), 66-75. doi:10.1016/s0962-8924(00)01900-0 es_ES
dc.description.references Yamasaki, H., Sakihama, Y., & Takahashi, S. (1999). An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends in Plant Science, 4(4), 128-129. doi:10.1016/s1360-1385(99)01393-x es_ES
dc.description.references Berges, J. (1997). Miniview: algal nitrate reductases. European Journal of Phycology, 32(1), 3-8. doi:10.1080/09541449710001719315 es_ES
dc.description.references Chamizo-Ampudia, A., Sanz-Luque, E., Llamas, Á., Ocaña-Calahorro, F., Mariscal, V., Carreras, A., … Fernández, E. (2016). A dual system formed by the ARC and NR molybdoenzymes mediates nitrite-dependent NO production inChlamydomonas. Plant, Cell & Environment, 39(10), 2097-2107. doi:10.1111/pce.12739 es_ES
dc.description.references Corpas, F. J., & Barroso, J. B. (2017). Nitric oxide synthase-like activity in higher plants. Nitric Oxide, 68, 5-6. doi:10.1016/j.niox.2016.10.009 es_ES
dc.description.references Foresi, N., Correa-Aragunde, N., Parisi, G., Caló, G., Salerno, G., & Lamattina, L. (2010). Characterization of a Nitric Oxide Synthase from the Plant Kingdom: NO Generation from the Green Alga Ostreococcus tauri Is Light Irradiance and Growth Phase Dependent    . The Plant Cell, 22(11), 3816-3830. doi:10.1105/tpc.109.073510 es_ES
dc.description.references Moya, P., Molins, A., Martínez-Alberola, F., Muggia, L., & Barreno, E. (2017). Unexpected associated microalgal diversity in the lichen Ramalina farinacea is uncovered by pyrosequencing analyses. PLOS ONE, 12(4), e0175091. doi:10.1371/journal.pone.0175091 es_ES
dc.description.references Cueto, M., Hernández-Perera, O., Martín, R., Bentura, M. L., Rodrigo, J., Lamas, S., & Golvano, M. P. (1996). Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Letters, 398(2-3), 159-164. doi:10.1016/s0014-5793(96)01232-x es_ES
dc.description.references Chow, F., Capociama, F. V., Faria, R., & Oliveira, M. C. de. (2007). Characterization of nitrate reductase activity in vitro in Gracilaria caudata J. Agardh (Rhodophyta, Gracilariales). Revista Brasileira de Botânica, 30(1). doi:10.1590/s0100-84042007000100012 es_ES
dc.description.references Groß, F., Durner, J., & Gaupels, F. (2013). Nitric oxide, antioxidants and prooxidants in plant defence responses. Frontiers in Plant Science, 4. doi:10.3389/fpls.2013.00419 es_ES
dc.description.references Xiong, J., Fu, G., Yang, Y., Zhu, C., & Tao, L. (2011). Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? Journal of Experimental Botany, 63(1), 33-41. doi:10.1093/jxb/err268 es_ES
dc.description.references Sakihama, Y., Nakamura, S., & Yamasaki, H. (2002). Nitric Oxide Production Mediated by Nitrate Reductase in the Green Alga Chlamydomonas reinhardtii: an Alternative NO Production Pathway in Photosynthetic Organisms. Plant and Cell Physiology, 43(3), 290-297. doi:10.1093/pcp/pcf034 es_ES
dc.description.references Mallick, N., Rai, L. C., Mohn, F. H., & Soeder, C. J. (1999). Studies on nitric oxide (NO) formation by the green alga Scenedesmus obliquus and the diazotrophic cyanobacterium Anabaena Doliolum. Chemosphere, 39(10), 1601-1610. doi:10.1016/s0045-6535(99)00058-2 es_ES
dc.description.references Medina-Andrés, R., Solano-Peralta, A., Saucedo-Vázquez, J. P., Napsucialy-Mendivil, S., Pimentel-Cabrera, J. A., Sosa-Torres, M. E., … Lira-Ruan, V. (2015). The Nitric Oxide Production in the Moss Physcomitrella patens Is Mediated by Nitrate Reductase. PLOS ONE, 10(3), e0119400. doi:10.1371/journal.pone.0119400 es_ES
dc.description.references Cánovas, D., Marcos, J. F., Marcos, A. T., & Strauss, J. (2016). Nitric oxide in fungi: is there NO light at the end of the tunnel? Current Genetics, 62(3), 513-518. doi:10.1007/s00294-016-0574-6 es_ES
dc.description.references Slot, J. C., & Hibbett, D. S. (2007). Horizontal Transfer of a Nitrate Assimilation Gene Cluster and Ecological Transitions in Fungi: A Phylogenetic Study. PLoS ONE, 2(10), e1097. doi:10.1371/journal.pone.0001097 es_ES
dc.description.references Kopincová, J., Púzserová, A., & Bernátová, I. (2012). L-NAME in the cardiovascular system – nitric oxide synthase activator? Pharmacological Reports, 64(3), 511-520. doi:10.1016/s1734-1140(12)70846-0 es_ES
dc.description.references Gross, B. H., Kreutz, K. J., Osterberg, E. C., McConnell, J. R., Handley, M., Wake, C. P., & Yalcin, K. (2012). Constraining recent lead pollution sources in the North Pacific using ice core stable lead isotopes. Journal of Geophysical Research: Atmospheres, 117(D16), n/a-n/a. doi:10.1029/2011jd017270 es_ES
dc.description.references Kim, D., Yamaguchi, K., & Oda, T. (2006). Nitric oxide synthase-like enzyme mediated nitric oxide generation by harmful red tide phytoplankton, Chattonella marina. Journal of Plankton Research, 28(6), 613-620. doi:10.1093/plankt/fbi145 es_ES
dc.description.references Valentovičová, K., Halušková, L., Huttová, J., Mistrík, I., & Tamás, L. (2010). Effect of cadmium on diaphorase activity and nitric oxide production in barley root tips. Journal of Plant Physiology, 167(1), 10-14. doi:10.1016/j.jplph.2009.06.018 es_ES
dc.description.references Thomas, T. E., & Harrison, P. J. (1988). A Comparison of In Vitro and In Vivo Nitrate Reductase Assays in Three Intertidal Seaweeds. Botanica Marina, 31(2). doi:10.1515/botm.1988.31.2.101 es_ES
dc.description.references Granbom, M., Chow, F., Lopes, P. F., de Oliveira, M. C., Colepicolo, P., de Paula, E. J., & Pedersén, M. (2004). Characterisation of nitrate reductase in the marine macroalga Kappaphycus alvarezii (Rhodophyta). Aquatic Botany, 78(4), 295-305. doi:10.1016/j.aquabot.2003.11.001 es_ES
dc.description.references Lopes, P. F., Oliveira, M. C., & Colepicolo, P. (1997). DIURNAL FLUCTUATION OF NITRATE REDUCTASE ACTIVITY IN THE MARINE RED ALGA GRACILARIA TENUISTIPITATA (RHODOPHYTA)1. Journal of Phycology, 33(2), 225-231. doi:10.1111/j.0022-3646.1997.00225.x es_ES
dc.description.references Chow, F., de Oliveira, M. C., & Pedersén, M. (2004). In vitro assay and light regulation of nitrate reductase in red alga Gracilaria chilensis. Journal of Plant Physiology, 161(7), 769-776. doi:10.1016/j.jplph.2004.01.002 es_ES
dc.description.references Zhao, M.-G., Chen, L., Zhang, L.-L., & Zhang, W.-H. (2009). Nitric Reductase-Dependent Nitric Oxide Production Is Involved in Cold Acclimation and Freezing Tolerance in Arabidopsis. Plant Physiology, 151(2), 755-767. doi:10.1104/pp.109.140996 es_ES
dc.description.references Hwang, S.-P. L., Williams, S. L., & Brinkhuis, B. H. (1987). Changes in Internal Dissolved Nitrogen Pools as Related to Nitrate Uptake and Assimilation in Gracilaria tikvahiae McLachlan (Rhodophyta)). Botanica Marina, 30(1). doi:10.1515/botm.1987.30.1.11 es_ES
dc.description.references Berges, J. A., & Harrison, P. J. (1995). Nitrate reductase activity quantitatively predicts the rate of nitrate incorporation under steady state light limitation: A revised assay and characterization of the enzyme in three species of marine phytoplankton. Limnology and Oceanography, 40(1), 82-93. doi:10.4319/lo.1995.40.1.0082 es_ES
dc.description.references Botsoglou, N. A., Fletouris, D. J., Papageorgiou, G. E., Vassilopoulos, V. N., Mantis, A. J., & Trakatellis, A. G. (1994). Rapid, Sensitive, and Specific Thiobarbituric Acid Method for Measuring Lipid Peroxidation in Animal Tissue, Food, and Feedstuff Samples. Journal of Agricultural and Food Chemistry, 42(9), 1931-1937. doi:10.1021/jf00045a019 es_ES
dc.description.references Du, Z., & Bramlage, W. J. (1992). Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. Journal of Agricultural and Food Chemistry, 40(9), 1566-1570. doi:10.1021/jf00021a018 es_ES
dc.description.references Reilly, C. A., & Aust, S. D. (1999). Measurement of Lipid Peroxidation. Current Protocols in Toxicology, 00(1). doi:10.1002/0471140856.tx0204s00 es_ES
dc.description.references Nussler, A. K., Glanemann, M., Schirmeier, A., Liu, L., & Nüssler, N. C. (2006). Fluorometric measurement of nitrite/nitrate by 2,3-diaminonaphthalene. Nature Protocols, 1(5), 2223-2226. doi:10.1038/nprot.2006.341 es_ES
dc.description.references Hope, B. T., & Vincent, S. R. (1989). Histochemical characterization of neuronal NADPH-diaphorase. Journal of Histochemistry & Cytochemistry, 37(5), 653-661. doi:10.1177/37.5.2703701 es_ES
dc.description.references Hope, B. T., Michael, G. J., Knigge, K. M., & Vincent, S. R. (1991). Neuronal NADPH diaphorase is a nitric oxide synthase. Proceedings of the National Academy of Sciences, 88(7), 2811-2814. doi:10.1073/pnas.88.7.2811 es_ES
dc.description.references Griess, P. (1879). Bemerkungen zu der Abhandlung der HH. Weselsky und Benedikt „Ueber einige Azoverbindungen”. Berichte der deutschen chemischen Gesellschaft, 12(1), 426-428. doi:10.1002/cber.187901201117 es_ES
dc.description.references Chaki, M., Valderrama, R., Fernández-Ocaña, A. M., Carreras, A., Gómez-Rodríguez, M. V., Pedrajas, J. R., … Barroso, J. B. (2010). Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. Journal of Experimental Botany, 62(6), 1803-1813. doi:10.1093/jxb/erq358 es_ES
dc.description.references Noble, J. E., & Bailey, M. J. A. (2009). Chapter 8 Quantitation of Protein. Guide to Protein Purification, 2nd Edition, 73-95. doi:10.1016/s0076-6879(09)63008-1 es_ES


Este ítem aparece en la(s) siguiente(s) colección(ones)

Mostrar el registro sencillo del ítem