8 research outputs found

    Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus Competition

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    Ramalina farinacea is an epiphytic fruticose lichen that is relatively abundant in areas with Mediterranean, subtropical or temperate climates. Little is known about photobiont diversity in different lichen populations. The present study examines the phycobiont composition of several geographically distant populations of R. farinacea from the Iberian Peninsula, Canary Islands and California as well as the physiological performance of isolated phycobionts. Based on anatomical observations and molecular analyses, the coexistence of two different taxa of Trebouxia (working names, TR1 and TR9) was determined within each thallus of R. farinacea in all of the analysed populations. Examination of the effects of temperature and light on growth and photosynthesis indicated a superior performance of TR9 under relatively high temperatures and irradiances while TR1 thrived at moderate temperature and irradiance. Ramalina farinacea thalli apparently represent a specific and selective form of symbiotic association involving the same two Trebouxia phycobionts. Strict preservation of this pattern of algal coexistence is likely favoured by the different and probably complementary ecophysiological responses of each phycobiont, thus facilitating the proliferation of this lichen in a wide range of habitats and geographic areas. © 2010 Society for Applied Microbiology and Blackwell Publishing Ltd.This study was funded by the Spanish Ministry of Education and Science (CGL2006-12917-C02-01/02), the Spanish Ministry of Science and Innovation (CGL2009-13429-C02-01/02), the AECID (PCI_A/024755/09) and the Generalitat Valenciana (PROMETEO 174/2008 GVA). We are grateful to Dr J. Gimeno-Romeu (University of California, Davis, USA) and to Dr P. J. G. de Nova (IREC, Ciudad Real, Spain), who were the first to isolate DNA from Ramalina farinacea thalli in our group. Wendy Ran revised the manuscript in English.Casano, L.; Del Campo, E.; GarcĂ­a Breijo, FJ.; Reig Armiñana, J.; Gasulla, F.; Del Hoyo, A.; GuĂ©ra, A.... (2011). Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus Competition. Environmental Microbiology. 13(3):806-818. https://doi.org/10.1111/j.1462-2920.2010.02386.xS806818133Angert, A. L., Huxman, T. E., Chesson, P., & Venable, D. L. (2009). Functional tradeoffs determine species coexistence via the storage effect. Proceedings of the National Academy of Sciences, 106(28), 11641-11645. doi:10.1073/pnas.0904512106Baker, N. R., & Oxborough, K. (s. f.). Chlorophyll Fluorescence as a Probe of Photosynthetic Productivity. Advances in Photosynthesis and Respiration, 65-82. doi:10.1007/978-1-4020-3218-9_3Barreno , E. Herrera-Campos , M. GarcĂ­a-Breijo , F. Gasulla , F. Reig-Armiñana , J. 2008 Non photosynthetic bacteria associated to cortical structures on Ramalina and Usnea thalli from Mexico http://192.104.39.110/archive/IAL6abstracts.pdfBECK, A., FRIEDL, T., & RAMBOLD, G. (1998). Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytologist, 139(4), 709-720. doi:10.1046/j.1469-8137.1998.00231.xBilger, W., & Bjïżœrkman, O. (1991). Temperature dependence of violaxanthin de-epoxidation and non-photochemical fluorescence quenching in intact leaves ofGossypium hirsutum L. andMalva parviflora L. Planta, 184(2), 226-234. doi:10.1007/bf01102422Bjïżœrkman, O., & Demmig, B. (1987). Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta, 170(4), 489-504. doi:10.1007/bf00402983Bold, H. C., & Parker, B. C. (1962). Some supplementary attributes in the classification of chlorococcum species. Archiv fïżœr Mikrobiologie, 42(3), 267-288. doi:10.1007/bf00422045Cenis, J. L. (1992). Rapid extraction of fungal DNA for PCR amplification. Nucleic Acids Research, 20(9), 2380-2380. doi:10.1093/nar/20.9.2380Del Campo, E. M., Casano, L. M., Gasulla, F., & Barreno, E. (2010). Suitability of chloroplast LSU rDNA and its diverse group I introns for species recognition and phylogenetic analyses of lichen-forming Trebouxia algae. Molecular Phylogenetics and Evolution, 54(2), 437-444. doi:10.1016/j.ympev.2009.10.024Demmig-Adams, B., & Adams, W. W. (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends in Plant Science, 1(1), 21-26. doi:10.1016/s1360-1385(96)80019-7Demmig-Adams, B., Mïżœguas, C., Adams, W. W., Meyer, A., Kilian, E., & Lange, O. L. (1990). Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue-green phycobionts. Planta, 180(3), 400-409. doi:10.1007/bf01160396DePriest, P. T. (2004). Early Molecular Investigations of Lichen-Forming Symbionts: 1986–2001. Annual Review of Microbiology, 58(1), 273-301. doi:10.1146/annurev.micro.58.030603.123730DOERING, M., & PIERCEY-NORMORE, M. D. (2009). Genetically divergent algae shape an epiphytic lichen community on Jack Pine in Manitoba. The Lichenologist, 41(1), 69-80. doi:10.1017/s0024282909008111Friedl, T. (1989). Comparative ultrastructure of pyrenoids inTrebouxia (Microthamniales, Chlorophyta). Plant Systematics and Evolution, 164(1-4), 145-159. doi:10.1007/bf00940435Gasulla, F., de Nova, P. G., Esteban-Carrasco, A., Zapata, J. M., Barreno, E., & GuĂ©ra, A. (2009). Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta, 231(1), 195-208. doi:10.1007/s00425-009-1019-yGasulla, F., GuĂ©ra, A., & Barreno, E. (2010). “A simple and rapid method for isolating lichen photobionts“. Symbiosis, 51(2), 175-179. doi:10.1007/s13199-010-0064-4Gauze, G. F. (1934). The struggle for existence, by G. F. Gause. doi:10.5962/bhl.title.4489Genty, B., Briantais, J.-M., & Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) - General Subjects, 990(1), 87-92. doi:10.1016/s0304-4165(89)80016-9Gross, K. (2008). Positive interactions among competitors can produce species-rich communities. Ecology Letters, 11(9), 929-936. doi:10.1111/j.1461-0248.2008.01204.xGUZOW-KRZEMIƃSKA, B. (2006). Photobiont flexibility in the lichen Protoparmeliopsis muralis as revealed by ITS rDNA analyses. The Lichenologist, 38(5), 469-476. doi:10.1017/s0024282906005068Haruta, S., Kato, S., Yamamoto, K., & Igarashi, Y. (2009). Intertwined interspecies relationships: approaches to untangle the microbial network. Environmental Microbiology, 11(12), 2963-2969. doi:10.1111/j.1462-2920.2009.01956.xJOHANSEN, S., & HAUGEN, P. (2001). A new nomenclature of group I introns in ribosomal DNA. RNA, 7(7), 935-936. doi:10.1017/s1355838201010500Jones, A. ., Berkelmans, R., van Oppen, M. J. ., Mieog, J. ., & Sinclair, W. (2008). A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences, 275(1641), 1359-1365. doi:10.1098/rspb.2008.0069Kopecky, J., Azarkovich, M., PfĂŒndel, E. E., Shuvalov, V. A., & Heber, U. (2005). Thermal Dissipation of Light Energy is Regulated Differently and by Different Mechanisms in Lichens and Higher Plants. Plant Biology, 7(2), 156-167. doi:10.1055/s-2005-837471Kosugi, M., Arita, M., Shizuma, R., Moriyama, Y., Kashino, Y., Koike, H., & Satoh, K. (2009). Responses to Desiccation Stress in Lichens are Different from Those in Their Photobionts. Plant and Cell Physiology, 50(4), 879-888. doi:10.1093/pcp/pcp043Kranner, 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.0407716102Kroken, S., & Taylor, J. W. (2000). Phylogenetic Species, Reproductive Mode, and Specificity of the Green AlgaTrebouxiaForming Lichens with the Fungal GenusLetharia. The Bryologist, 103(4), 645-660. doi:10.1639/0007-2745(2000)103[0645:psrmas]2.0.co;2Little, A. F. (2004). Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals. Science, 304(5676), 1492-1494. doi:10.1126/science.1095733Loarie, S. R., Duffy, P. B., Hamilton, H., Asner, G. P., Field, C. B., & Ackerly, D. D. (2009). The velocity of climate change. Nature, 462(7276), 1052-1055. doi:10.1038/nature08649Muggia, L., Grube, M., & Tretiach, M. (2008). Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycological Progress, 7(3), 147-160. doi:10.1007/s11557-008-0560-6Niyogi, K. K. (2004). Is PsbS the site of non-photochemical quenching in photosynthesis? Journal of Experimental Botany, 56(411), 375-382. doi:10.1093/jxb/eri056O’Brien, H. E., Miadlikowska, J., & Lutzoni, F. (2005). Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungusPeltigera. European Journal of Phycology, 40(4), 363-378. doi:10.1080/09670260500342647Ohmura, Y., Kawachi, M., Kasai, F., Watanabe, M. M., & Takeshita, S. (2006). Genetic combinations of symbionts in a vegetatively reproducing lichen,Parmotrema tinctorum, based on ITS rDNA sequences. The Bryologist, 109(1), 43-59. doi:10.1639/0007-2745(2006)109[0043:gcosia]2.0.co;2Piercey-Normore, M. D. (2005). The lichen-forming ascomyceteEvernia mesomorphaassociates with multiple genotypes ofTrebouxia jamesii. New Phytologist, 169(2), 331-344. doi:10.1111/j.1469-8137.2005.01576.xPombert, J.-F., Lemieux, C., & Turmel, M. (2006). BMC Biology, 4(1), 3. doi:10.1186/1741-7007-4-3Rambold, G., Friedl, T., & Beck, A. (1998). Photobionts in Lichens: Possible Indicators of Phylogenetic Relationships? The Bryologist, 101(3), 392. doi:10.1639/0007-2745(1998)101[392:pilpio]2.0.co;2Romeike, J., Friedl, T., Helms, G., & Ott, S. (2002). Genetic Diversity of Algal and Fungal Partners in Four Species of Umbilicaria (Lichenized Ascomycetes) Along a Transect of the Antarctic Peninsula. Molecular Biology and Evolution, 19(8), 1209-1217. doi:10.1093/oxfordjournals.molbev.a004181Rosenberg, E., Sharon, G., & Zilber-Rosenberg, I. (2009). The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework. Environmental Microbiology, 11(12), 2959-2962. doi:10.1111/j.1462-2920.2009.01995.xSchreiber, U., Schliwa, U., & Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research, 10(1-2), 51-62. doi:10.1007/bf00024185Skaloud, P., & Peksa, O. (2010). Evolutionary inferences based on ITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Molecular Phylogenetics and Evolution, 54(1), 36-46. doi:10.1016/j.ympev.2009.09.035Wegley, L., Edwards, R., Rodriguez-Brito, B., Liu, H., & Rohwer, F. (2007). Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environmental Microbiology, 9(11), 2707-2719. doi:10.1111/j.1462-2920.2007.01383.xWeis, E., & Berry, J. A. (1987). Quantum efficiency of Photosystem II in relation to ‘energy’-dependent quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 894(2), 198-208. doi:10.1016/0005-2728(87)90190-3Wornik, S., & Grube, M. (2009). Joint Dispersal Does Not Imply Maintenance of Partnerships in Lichen Symbioses. Microbial Ecology, 59(1), 150-157. doi:10.1007/s00248-009-9584-yYAHR, R., VILGALYS, R., & DEPRIEST, P. T. (2004). Strong fungal specificity and selectivity for algal symbionts in Florida scrub Cladonia lichens. Molecular Ecology, 13(11), 3367-3378. doi:10.1111/j.1365-294x.2004.02350.xYahr, R., Vilgalys, R., & DePriest, P. T. (2006). Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytologist, 171(4), 847-860. doi:10.1111/j.1469-8137.2006.01792.xZoller, S. (2003). Slow algae, fast fungi: exceptionally high nucleotide substitution rate differences between lichenized fungi Omphalina and their symbiotic green algae Coccomyxa. Molecular Phylogenetics and Evolution, 29(3), 629-640. doi:10.1016/s1055-7903(03)00215-

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

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    [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.Supported by the Ministerio de EconomĂ­a 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).Hinojosa-Vidal, E.; Marco, F.; MartĂ­nez-Alberola, F.; Escaray, F.; GarcĂ­a-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/s00425-018-2993-8S147314862486Álvarez R, del Hoyo A, DĂ­az-RodrĂ­guez 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/s00248-014-0524-0Archibald PA (1977) Physiological characteristics of Trebouxia (Chlorophyceae, Chlorococcales) and Pseudotrebouxia (Chlorophyceae, Chlorosarcinales). Phycologia 16:295–300. https://doi.org/10.2216/i0031-8884-16-3-295.1Armstrong 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 1–27Arup U (1995) Littoral species of Caloplaca in North America: a summary and a key. Bryologist 98:129–140. https://doi.org/10.2307/3243649Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:180. https://doi.org/10.3389/fmicb.2016.00180BalarinovĂĄ K, BartĂĄk M, HazdrovĂĄ J, HĂĄjek J, JĂ­lkovĂĄ 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/s11099-014-0060-7Biosca EG, Flores R, Santander RD, DĂ­ez-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.0160328Bischoff HW, Bold HC (1963) Some soil algae from Enchanted Rock and related algal species. Phycol Stud 44(1):1–95Borges 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.2016.10.004Brandt 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/s11084-015-9470-1BrĂĄnyikovĂĄ I, MarĆĄĂĄlkovĂĄ B, Doucha J et al (2011) Microalgae—novel highly efficient starch producers. Biotechnol Bioeng 108:766–776. https://doi.org/10.1002/bit.23016Callis 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 139:921–939Campenni 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/s00253-012-4570-6Casano LM, del Campo EM, GarcĂ­a-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.xChettri 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)00024-5Cornillon P-A (2012) R for statistics. CRC Press, Boca RatonCowan 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/43.12.1535Czechowski 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.105.063743Danquah 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.2013.09.006Delmail 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/10.1080/15226514.2012.723068Dragone 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.2011.03.012Duarte 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/10.1111/1758-2229.12452Durgbanshi 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/JF050884BEinspahr 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.107.2.529Gasulla 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-yGasulla F, GuĂ©ra A, Barreno E (2010) A simple and rapid method for isolating lichen photobionts. Symbiosis 51:175–179. https://doi.org/10.1007/s13199-010-0064-4GĂłmez-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/s00344-002-0013-4Green 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/s00300-011-1098-7Grube M, Blaha J (2005) Halotolerance and lichen symbioses. In: Gunde-Cimerman N, Oren A, PlemenitaĆĄ A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Berlin, pp 471–488GuĂ©ra 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/eri024Gustavs 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/s00709-009-0060-9Hauser 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.HauserHayashi 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.xHiremath S, Mathad P (2010) Impact of salinity on the physiological and biochemical traits of Chlorella vulgaris Beijerinck. J Algal Biomass Util 1:51–59Hirsch 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.xJameson P (1993) Plant hormones in the algae. Prog Phycol Res 9:239–279Kibbe WA (2007) OligoCalc: an online oligonucleotide properties calculator. Nucleic Acids Res 35:W43–W46. https://doi.org/10.1093/nar/gkm234Kirk PM, Cannon PF, David JC, Stalpers JA (2001) Ainsworth and Bisby’s dictionary of the fungi, 9th edn. CABI Publishing, Wallingford, UKKline 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.1007879107Koizumi 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)90266-6Krause 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.42.060191.001525Lan 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.2010.08.002Leavitt 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.13271Livak 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.2001.1262Lu 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.2015.01.006Malaspina 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.2014.11.015Mane 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/2010/18339Maphangwa 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/s00442-011-2184-9Margulis 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;2MarĆĄĂĄlek B, ZahradníčkovĂĄ H, HronkovĂĄ 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)80503-1MartĂ­nez-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 ValĂšncia. http://roderic.uv.es/handle/10550/48824Mishra 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.2009.02.006Molins A, Moya P, GarcĂ­a-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/S0024282917000664Moya P, Molins A, MartĂ­nez-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.0175091Nash 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.xNeale 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)80158-0NegrĂŁo 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/mcw191Qiao 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.2015.03.023Ruzin SE (2000) Plant microtechnique and microscopy. New Phytol 148:57–58Schwartz 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.276.5320.1872Ć kaloud 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.2009.09.035Spribille 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.aaf8287Stepien 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.108.132407Takagi 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.101.223Takahagi 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.19.53Tietz 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)80093-2Wani 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.2016.01.010Wellburn 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 9–12Zhang 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.2005.08.01
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