- -

Characterization of the responses to saline stress in the symbiotic green microalga Trebouxia sp. TR9

RiuNet: Repositorio Institucional de la Universidad Politécnica de Valencia

Compartir/Enviar a

Citas

Estadísticas

  • Estadisticas de Uso

Characterization of the responses to saline stress in the symbiotic green microalga Trebouxia sp. TR9

Mostrar el registro sencillo del ítem

Ficheros en el ítem

[Cerrado]
Nombre: Hinojosa-Vidal;Ma ...
Tamaño: 2.975Mb
Formato: PDF
Descripción: Versión editorial
Solicitar una copia al autor
dc.contributor.author Hinojosa-Vidal, E. es_ES
dc.contributor.author Marco, F. es_ES
dc.contributor.author Martínez-Alberola, Fernando es_ES
dc.contributor.author Escaray, F.J. es_ES
dc.contributor.author García-Breijo, Francisco-José es_ES
dc.contributor.author Reig-Armiñana, José es_ES
dc.contributor.author Carrasco, P. es_ES
dc.contributor.author Barreno Rodríguez, Eva es_ES
dc.date.accessioned 2020-06-02T05:36:34Z
dc.date.available 2020-06-02T05:36:34Z
dc.date.issued 2018-12 es_ES
dc.identifier.issn 0032-0935 es_ES
dc.identifier.uri http://hdl.handle.net/10251/144797
dc.description.abstract [EN] Main conclusion. For the first time we provide a study on the physiological, ultrastructural and molecular effects of salt stress on a terrestrial symbiotic green microalga, Trebouxia sp. TR9. Although tolerance to saline conditions has been thoroughly studied in plants and, to an extent, free-living microalgae, scientific data regarding salt stress on symbiotic lichen microalgae is scarce to non-existent. Since lichen phycobionts are capable of enduring harsh, restrictive and rapidly changing environments, it is interesting to study the metabolic machinery operating under these extreme conditions. We aim to determine the effects of prolonged exposure to high salt concentrations on the symbiotic phycobiont Trebouxia sp. TR9, isolated from the lichen Ramalina farinacea. Our results suggest that, when this alga is confronted with extreme saline conditions, the cellular structures are affected to an extent, with limited chlorophyll content loss and photosynthetic activity remaining after 72h of exposure to 5M NaCl. Furthermore, this organism displays a rather different molecular response compared to land plants and free-living halophile microalgae, with no noticeable increase in ABA levels and ABA-related gene expression until the external NaCl concentration is raised to 3M NaCl. Despite this, the ABA transduction pathway seems functional, since the ABA-related genes tested are responsive to exogenous ABA. These observations could suggest that this symbiotic green alga may have developed alternative molecular pathways to cope with highly saline environments. es_ES
dc.description.sponsorship Supported by the Ministerio de Economía y Competitividad (MINECO, Spain) and FEDER (CGL2016-79158-P), and the PROMETEO Excellence in Research Program (Generalitat Valenciana, Spain) (PROMETEO/2017/039). Funding for Ernesto Hinojosa-Vidal was also provided by MINECO (BES-2013-065511). es_ES
dc.language Inglés es_ES
dc.publisher Springer-Verlag es_ES
dc.relation.ispartof Planta es_ES
dc.rights Reserva de todos los derechos es_ES
dc.subject ABA es_ES
dc.subject Lichen es_ES
dc.subject Ramalina es_ES
dc.subject Saline stress es_ES
dc.subject Terrestrial microalgae es_ES
dc.subject Trebouxiophyceae es_ES
dc.subject.classification BOTANICA es_ES
dc.title Characterization of the responses to saline stress in the symbiotic green microalga Trebouxia sp. TR9 es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1007/s00425-018-2993-8 es_ES
dc.relation.projectID info:eu-repo/grantAgreement/MINECO//BES-2013-065511/ES/BES-2013-065511/ 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 Cerrado es_ES
dc.contributor.affiliation Universitat Politècnica de València. Departamento de Ecosistemas Agroforestales - Departament d'Ecosistemes Agroforestals es_ES
dc.description.bibliographicCitation Hinojosa-Vidal, E.; Marco, F.; Martínez-Alberola, F.; Escaray, F.; García-Breijo, F.; Reig-Armiñana, J.; Carrasco, P.... (2018). Characterization of the responses to saline stress in the symbiotic green microalga Trebouxia sp. TR9. Planta. 248(6):1473-1486. https://doi.org/10.1007/s00425-018-2993-8 es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion http://doi.org/10.1007/s00425-018-2993-8 es_ES
dc.description.upvformatpinicio 1473 es_ES
dc.description.upvformatpfin 1486 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 248 es_ES
dc.description.issue 6 es_ES
dc.identifier.pmid 30132152 es_ES
dc.relation.pasarela S\367591 es_ES
dc.contributor.funder Ministerio de Economía y Competitividad es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.description.references Álvarez R, del Hoyo A, Díaz-Rodríguez C et al (2015) Lichen rehydration in heavy metal-polluted environments: Pb modulates the oxidative response of both Ramalina farinacea thalli and its isolated microalgae. Microb Ecol 69:698–709. https://doi.org/10.1007/s00248-014-0524-0 es_ES
dc.description.references Archibald PA (1977) Physiological characteristics of Trebouxia (Chlorophyceae, Chlorococcales) and Pseudotrebouxia (Chlorophyceae, Chlorosarcinales). Phycologia 16:295–300. https://doi.org/10.2216/i0031-8884-16-3-295.1 es_ES
dc.description.references Armstrong RA (2017) Adaptation of lichens to extreme conditions. In: Kumar V, Shukla S, Kumar N (eds) Plant adaptation strategies in changing environment. Springer Singapore, Singapore, pp 1–27 es_ES
dc.description.references Arup U (1995) Littoral species of Caloplaca in North America: a summary and a key. Bryologist 98:129–140. https://doi.org/10.2307/3243649 es_ES
dc.description.references Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:180. https://doi.org/10.3389/fmicb.2016.00180 es_ES
dc.description.references Balarinová K, Barták M, Hazdrová J, Hájek J, Jílková J (2014) Changes in photosynthesis, pigment composition and glutathione contents in two Antarctic lichens during a light stress and recovery. Photosynthetica 52:538–547. https://doi.org/10.1007/s11099-014-0060-7 es_ES
dc.description.references Biosca EG, Flores R, Santander RD, Díez-Gil JL, Barreno E (2016) Innovative approaches using lichen enriched media to improve isolation and culturability of lichen associated bacteria. PLoS One 11:e0160328. https://doi.org/10.1371/journal.pone.0160328 es_ES
dc.description.references Bischoff HW, Bold HC (1963) Some soil algae from Enchanted Rock and related algal species. Phycol Stud 44(1):1–95 es_ES
dc.description.references Borges L, Caldas S, Montes D’Oca MG, Abreu PC (2016) Effect of harvesting processes on the lipid yield and fatty acid profile of the marine microalga Nannochloropsis oculata. Aquac Rep 4:164–168. https://doi.org/10.1016/j.aqrep.2016.10.004 es_ES
dc.description.references Brandt A, Posthoff E, de Vera J-P, Onofri S, Ott S (2016) Characterisation of growth and ultrastructural effects of the Xanthoria elegans photobiont after 1.5 years of space exposure on the International Space Station. Orig Life Evol Biosph 46:311–321. https://doi.org/10.1007/s11084-015-9470-1 es_ES
dc.description.references Brányiková I, Maršálková B, Doucha J et al (2011) Microalgae—novel highly efficient starch producers. Biotechnol Bioeng 108:766–776. https://doi.org/10.1002/bit.23016 es_ES
dc.description.references Callis J, Carpenter T, Sun CW, Vierstra RD (1995) Structure and evolution of genes encoding polyubiquitin and ubiquitin-like proteins in Arabidopsis thaliana ecotype Columbia. Genetics 139:921–939 es_ES
dc.description.references Campenni L, Nobre BP, Santos CA et al (2013) Carotenoid and lipid production by the autotrophic microalga Chlorella protothecoides under nutritional, salinity, and luminosity stress conditions. Appl Microbiol Biotechnol 97:1383–1393. https://doi.org/10.1007/s00253-012-4570-6 es_ES
dc.description.references Casano LM, del Campo EM, García-Breijo FJ et al (2011) Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition? Environ Microbiol 13:806–818. https://doi.org/10.1111/j.1462-2920.2010.02386.x es_ES
dc.description.references Chettri M, Cook C, Vardaka E, Sawidis T, Lanaras L (1998) The effect of Cu, Zn and Pb on the chlorophyll content of the lichens Cladonia convoluta and Cladonia rangiformis. Environ Exp Bot 39:1–10. https://doi.org/10.1016/S0098-8472(97)00024-5 es_ES
dc.description.references Cornillon P-A (2012) R for statistics. CRC Press, Boca Raton es_ES
dc.description.references Cowan AK, Rose PD, Horne LG (1992) Dunaliella salina: a model system for studying the response of plant cells to stress. J Exp Bot 43:1535–1547. https://doi.org/10.1093/jxb/43.12.1535 es_ES
dc.description.references Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139:5–17. https://doi.org/10.1104/pp.105.063743 es_ES
dc.description.references Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32:40–52. https://doi.org/10.1016/j.biotechadv.2013.09.006 es_ES
dc.description.references Delmail D, Labrousse P, Hourdin P et al (2013) Micropropagation of Myriophyllum alterniflorum (Haloragaceae) for stream rehabilitation: first in vitro culture and reintroduction assays of a heavy-metal hyperaccumulator immersed macrophyte. Int J Phytoremediation 15:647–662. https://doi.org/10.1080/15226514.2012.723068 es_ES
dc.description.references Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Energy 88:3331–3335. https://doi.org/10.1016/j.apenergy.2011.03.012 es_ES
dc.description.references Duarte AWF, Passarini MRZ, Delforno TP et al (2016) Yeasts from macroalgae and lichens that inhabit the South Shetland Islands, Antarctica. Environ Microbiol Rep 8:874–885. https://doi.org/10.1111/1758-2229.12452 es_ES
dc.description.references Durgbanshi A, Arbona V, Pozo O et al (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography–electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442. https://doi.org/10.1021/JF050884B es_ES
dc.description.references Einspahr KJ, Maeda M, Thompson GA (1988) Concurrent changes in Dunaliella salina ultrastructure and membrane phospholipid metabolism after hyperosmotic shock. J Cell Biol 107:529–538. https://doi.org/10.1083/JCB.107.2.529 es_ES
dc.description.references Gasulla F, de Nova PG, Esteban-Carrasco A et al (2009) Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta 231:195–208. https://doi.org/10.1007/s00425-009-1019-y es_ES
dc.description.references Gasulla F, Guéra A, Barreno E (2010) A simple and rapid method for isolating lichen photobionts. Symbiosis 51:175–179. https://doi.org/10.1007/s13199-010-0064-4 es_ES
dc.description.references Gómez-Cadenas A, Arbona V, Jacas J, Primo-Millo E, Talon M (2002) Abscisic acid reduces leaf abscission and increases salt tolerance in citrus plants. J Plant Growth Regul 21:234–240. https://doi.org/10.1007/s00344-002-0013-4 es_ES
dc.description.references Green TGA, Brabyn L, Beard C, Sancho LG (2012) Extremely low lichen growth rates in Taylor Valley, Dry Valleys, continental Antarctica. Polar Biol 35:535–541. https://doi.org/10.1007/s00300-011-1098-7 es_ES
dc.description.references Grube M, Blaha J (2005) Halotolerance and lichen symbioses. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Berlin, pp 471–488 es_ES
dc.description.references Guéra A, Calatayud A, Sabater B, Barreno E (2004) Involvement of the thylakoidal NADH-plastoquinone-oxidoreductase complex in the early responses to ozone exposure of barley (Hordeum vulgare L.) seedlings. J Exp Bot 56:205–218. https://doi.org/10.1093/jxb/eri024 es_ES
dc.description.references Gustavs L, Eggert A, Michalik D, Karsten U (2010) Physiological and biochemical responses of green microalgae from different habitats to osmotic and matric stress. Protoplasma 243:3–14. https://doi.org/10.1007/s00709-009-0060-9 es_ES
dc.description.references Hauser F, Rainer W, Schroeder JI (2011) Evolution of abscisic acid synthesis and signaling mechanisms. Curr Biol 21:346–355. https://doi.org/10.1016/j.cub.2011.03.015.Hauser es_ES
dc.description.references Hayashi H, Alia L, Mustardy L, Ida M, Murata N (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycine betaine and enhanced tolerance to salt and cold stress. Plant J 12:133–142. https://doi.org/10.1046/j.1365-313X.1997.12010133.x es_ES
dc.description.references Hiremath S, Mathad P (2010) Impact of salinity on the physiological and biochemical traits of Chlorella vulgaris Beijerinck. J Algal Biomass Util 1:51–59 es_ES
dc.description.references Hirsch R, Hartung W, Gimmler H (1989) Abscisic acid content of algae under stress. Bot Acta 102:326–334. https://doi.org/10.1111/j.1438-8677.1989.tb00113.x es_ES
dc.description.references Jameson P (1993) Plant hormones in the algae. Prog Phycol Res 9:239–279 es_ES
dc.description.references Kibbe WA (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35:W43–W46. https://doi.org/10.1093/nar/gkm234 es_ES
dc.description.references Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Ainsworth and Bisby’s dictionary of the fungi, 9th edn. CABI Publishing, Wallingford, UK es_ES
dc.description.references Kline KG, Barrett-Wilt GA, Sussman MR (2010) In planta changes in protein phosphorylation induced by the plant hormone abscisic acid. Proc Natl Acad Sci USA 107:15986–15991. https://doi.org/10.1073/pnas.1007879107 es_ES
dc.description.references Koizumi M, Yamaguchi-Shinozaki K, Tsuji H, Shinozaki K (1993) Structure and expression of two genes that encode distinct drought-inducible cysteine proteinases in Arabidopsis thaliana. Gene 129:175–182. https://doi.org/10.1016/0378-1119(93)90266-6 es_ES
dc.description.references Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349. https://doi.org/10.1146/annurev.pp.42.060191.001525 es_ES
dc.description.references Lan SB, Wu L, Zhang DL, Hu CX, Liu YD (2010) Effects of drought and salt stresses on man-made cyanobacterial crusts. Eur J Soil Biol 46:381–386. https://doi.org/10.1016/j.ejsobi.2010.08.002 es_ES
dc.description.references Leavitt SD, Kraichak E, Nelsen MP et al (2015) Fungal specificity and selectivity for algae play a major role in determining lichen partnerships across diverse ecogeographic regions in the lichen-forming family Parmeliaceae (Ascomycota). Mol Ecol 24:3779–3797. https://doi.org/10.1111/mec.13271 es_ES
dc.description.references Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/METH.2001.1262 es_ES
dc.description.references Lu Y, Xu J (2015) Phytohormones in microalgae: a new opportunity for microalgal biotechnology? Trends Plant Sci 20:273–282. https://doi.org/10.1016/j.tplants.2015.01.006 es_ES
dc.description.references Malaspina P, Giordani P, Pastorino G, Modenesi P, Mariotti MG (2015) Interaction of sea salt and atmospheric pollution alters the OJIP fluorescence transient in the lichen Pseudevernia furfuracea (L.) Zopf. Ecol Indic 50:251–257. https://doi.org/10.1016/j.ecolind.2014.11.015 es_ES
dc.description.references Mane AV, Karadge BA, Samant JS (2010) Salt stress induced alteration in photosynthetic pigments and polyphenols of Pennisetum alopecuroides (L.). J Ecophysiol Occup Health 10:177–182. https://doi.org/10.18311/jeoh/2010/18339 es_ES
dc.description.references Maphangwa KW, Musil CF, Raitt L, Zedda L (2012) Experimental climate warming decreases photosynthetic efficiency of lichens in an arid South African ecosystem. Oecologia 169:257–268. https://doi.org/10.1007/s00442-011-2184-9 es_ES
dc.description.references Margulis L, Barreno E (2003) Looking at lichens. Bioscience 53:776–778. https://doi.org/10.1641/0006-3568(2003)053%5b0776:lal%5d2.0.co;2 es_ES
dc.description.references Maršálek B, Zahradníčková H, Hronková M (1992) Extracellular abscisic acid produced by cyanobacteria under salt stress. J Plant Physiol 139:506–508. https://doi.org/10.1016/S0176-1617(11)80503-1 es_ES
dc.description.references Martínez-Alberola F (2015) Genome characterization of the symbiotic microalga Trebouxia sp. TR9 isolated from the lichen Ramalina farinacea (L.) Ach. by means of NGS techniques. PhD Dissertation. Universitat de València. http://roderic.uv.es/handle/10550/48824 es_ES
dc.description.references Mishra A, Jha B (2009) Isolation and characterization of extracellular polymeric substances from micro-algae Dunaliella salina under salt stress. Bioresour Technol 100:3382–3386. https://doi.org/10.1016/j.biortech.2009.02.006 es_ES
dc.description.references Molins A, Moya P, García-Breijo FJ, Reig-Arminana J, Barreno E (2018) A multi-tool approach to assess microalgal diversity in lichens: isolation, Sanger sequencing, HTS and ultrastructural correlations. Lichenologist 50:123–138. https://doi.org/10.1017/S0024282917000664 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:e0175091. https://doi.org/10.1371/journal.pone.0175091 es_ES
dc.description.references Nash TH III, Lange OL (1988) Responses of lichens to salinity: concentration and time-course relationships and variability among Californian species. New Phytol 109:361–367. https://doi.org/10.1111/j.1469-8137.1988.tb04206.x es_ES
dc.description.references Neale PJ, Melis A (1989) Salinity-stress enhances photoinhibition of photosynthesis in Chlamydomonas reinhardtii. J Plant Physiol 134:619–622. https://doi.org/10.1016/S0176-1617(89)80158-0 es_ES
dc.description.references Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Ann Bot 119:1–11. https://doi.org/10.1093/aob/mcw191 es_ES
dc.description.references Qiao K, Takano T, Liu S (2015) Discovery of two novel highly tolerant NaHCO3 Trebouxiophytes: identification and characterization of microalgae from extreme saline–alkali soil. Algal Res 9:245–253. https://doi.org/10.1016/j.algal.2015.03.023 es_ES
dc.description.references Ruzin SE (2000) Plant microtechnique and microscopy. New Phytol 148:57–58 es_ES
dc.description.references Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR (1997) Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276:1872–1874. https://doi.org/10.1126/science.276.5320.1872 es_ES
dc.description.references Škaloud P, Peksa O (2010) Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Mol Phylogenet Evol 54:36–46. https://doi.org/10.1016/J.YMPEV.2009.09.035 es_ES
dc.description.references Spribille T, Tuovinen V, Resl P et al (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492. https://doi.org/10.1126/science.aaf8287 es_ES
dc.description.references Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165. https://doi.org/10.1104/pp.108.132407 es_ES
dc.description.references Takagi M, Karseno YT (2006) Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J Biosci Bioeng 101:223–226. https://doi.org/10.1263/jbb.101.223 es_ES
dc.description.references Takahagi T, Yamamoto Y, Kinoshita Y, Takeshita S, Yamada T (2002) Inhibitory effects of sodium chloride on induction of tissue cultures of lichens of Ramalina species. Plant Biotechnol 19:53–55. https://doi.org/10.5511/plantbiotechnology.19.53 es_ES
dc.description.references Tietz A, Kasprik W (1986) Identification of abscisic acid in a green alga. Biochem Physiol Pflanz 181:269–274. https://doi.org/10.1016/S0015-3796(86)80093-2 es_ES
dc.description.references Wani SH, Kumar V, Shriram V, Sah SK (2016) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4:162–176. https://doi.org/10.1016/j.cj.2016.01.010 es_ES
dc.description.references Wellburn AR, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls A and B of leaf extracts in different solvents. In: Sybesma C (ed) Advances in photosynthesis research. Springer, Dordrecht, pp 9–12 es_ES
dc.description.references Zhang J, Jia W, Yang J, Ismail AM (2006) Role of ABA in integrating plant responses to drought and salt stresses. Field Crop Res 97:111–119. https://doi.org/10.1016/j.fcr.2005.08.018 es_ES


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

Mostrar el registro sencillo del ítem