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Desiccation tolerance and lichenization: a case study with the aeroterrestrial microalga Trebouxia sp. (Chlorophyta)

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Abstract

Main conclusions

A comparative study of isolated vs. lichenized Trebouxia sp. showed that lichenization does not influence the survival capability of the alga to the photo-oxidative stress derived from prolonged desiccation.

Coccoid algae in the Trebouxia genus are the most common photobionts of chlorolichens but are only sporadically found in soil or bark outside of a lichen. They all appear to be desiccation tolerant, i.e. they can survive drying to water contents of below 10 %. However, little is known about their longevity in the dry state and to which extent lichenization can influence it. Here, we studied the longevity in the dry state of the lichenized alga (LT) Trebouxia sp. in the lichen Parmotrema perlatum, in comparison with axenically grown cultures (CT) isolated from the same lichen. We report on chlorophyll fluorescence emission and reactive oxygen species (ROS) production before desiccation, after 15–45 days in the dry state under different combinations of light and air humidity and after recovery for 1 or 3 days in fully hydrated conditions. Both the CT and the LT were able to withstand desiccation under high light (120 µmol photons m−2 s−1 for 14 h per day), but upon recovery after 45 days in the dry state the performance of the CT was better than that of the LT. By contrast, the quenching of excess light energy was more efficient in the LT, at high relative humidities especially. ROS production in the LT was influenced mostly by light exposure, whereas the CT showed an oxidative burst independent of the light conditions. Although lichenization provides benefits that are essential for the survival of the photobiont in high-light habitats, Trebouxia sp. can withstand protracted periods of photo-oxidative stress even outside of a lichen thallus.

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Abbreviations

Chl a F:

Chlorophyll a fluorescence

CLSM:

Confocal laser scanning microscopy

CT:

Cultured Trebouxia

DCF:

2′,7′-Dichlorofluorescein

DCFH:

2′,7′-Dichlorofluorescin

DCFH-DA:

2′,7′-Dichlorofluorescin diacetate

F 0 and F m :

Minimal and maximal Chl fluorescence intensity in dark-adapted samples, respectively

F′ m :

Maximum quantum yield of photosystem II in illuminated samples

F p :

Maximal Chl fluorescence under non-saturating actinic light

F v :

Variable Chl fluorescence (F v = F m − F 0)

F v/F m :

Maximum quantum yield of photosystem II

LT:

Lichenized Trebouxia

NPQ:

Non photochemical quenching

PPFDIk :

Photosynthetic photon flux density corresponding to the effective maximum value of quantum yield CO2 assimilation

RH:

Air relative humidity

ROS:

Reactive oxygen species

RWC:

Relative water content

References

  • Ahmadjian V (1973) Methods of isolation and culturing lichen symbionts and thalli. In: Ahmadjian V, Hale ME (eds) The lichens. Academic Press, New York, pp 653–659

    Chapter  Google Scholar 

  • Ahmadjian V (1993) The lichen symbiosis. Wiley, Oxford

    Google Scholar 

  • Alpert P (2006) Constraints of tolerance: why are desiccation tolerant organisms so small or rare? J Exp Biol 209:1575–1584

    Article  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Baruffo L, Tretiach M (2007) Seasonal variations of F 0, F m, and F v/F m in an epiphytic population of the lichen Punctelia subrudecta (Nyl.) Krog. Lichenologist 39:555–565

    Article  Google Scholar 

  • Berjak P, Farrant JM, Mycock DJ, Pammenter NW (1990) Recalcitrant homoiohydrous seeds: the enigma of their desiccation-sensitivity. Seed Sci Technol 18:297–310

    Google Scholar 

  • Buitink J, LePrince O (2004) Glass formation in plant anhydrobiotes: survival in the dry state. Cryobiology 48:215–228

    Article  CAS  PubMed  Google Scholar 

  • Buitink J, Claessens MMAE, Hemminga MA, Hoekstra FA (1998) Influence of water content and temperature on molecular mobility and intracellular glasses in seeds and pollen. Plant Physiol 118:531–541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Carvalho P (1996) Microclimate and diversity of cryptogamic epiphytes in a Karst doline (Trieste, NE Italy). Gortania 18:41–68

    Google Scholar 

  • Catalá M, Gasulla F, Pradas del Real AE, 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 Microbiol 10:297

    Article  PubMed Central  PubMed  Google Scholar 

  • Cruz de Carvalho R, Català M, Marques da Silva J, Branquinho C, Barreno E (2012) The impact of dehydration rate on the production and cellular location of reactive oxygen species in an acquatic moss. Ann Bot Lond 110:1007–1016

    Article  CAS  Google Scholar 

  • Dahmen H, Staub T, Schwinn FJ (1983) Technique for long-term preservation of phytopathogenic fungi in liquid nitrogen. Phytopathology 73:241–246

    Article  Google Scholar 

  • Dietz S, Büdel B, Lange OL, Bilger W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibl Lichenol 75:171–182

    Google Scholar 

  • Fernández-Marín B, Becerril JM, García-Plazaola JI (2010) Unravelling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria. Planta 231:1335–1342

    Article  PubMed  Google Scholar 

  • Fernández-Marín B, Kranner I, San Sebastían M, Artexte U, Laza JM, Vilas JL, Pritchard HW, Nadajaran J, Míguez F, Becerril JM, García-Plazaola JI (2013) Evidence for the absence of enzymatic reactions in the glassy state. A case study of xanthophyll cycle pigments in the desiccation-tolerant moss Syntrichia ruralis. J Exp Bot 64:3033–3043

    Article  PubMed Central  PubMed  Google Scholar 

  • Franks F, Hatley RHM, Mathias S (1991) Materials science and the production of shelf-stable biologicals. Biopharmaceuticals 4:38–42

    CAS  Google Scholar 

  • Gauslaa Y, Solhaug KA (2000) High-light-intensity damage to the foliose lichen Lobaria pulmonaria within natural forest: the applicability of chlorophyll fluorescence methods. Lichenologist 32:271–289

    Article  Google Scholar 

  • Gauslaa Y, Coxson DS, Solhaug KA (2012) The paradox of higher light tolerance during desiccation in rare old forest cyanolichens than in more widespread co-occurring chloro- and cephalolichens. New Phytol 195:812–822

    Article  PubMed Central  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Gerotto C, Alboresi A, Giacometti GM, Bassi R, Morosinotto T (2011) Role of PSBS and LHCSR in Physcomitrella patens acclimation to high light and low temperature. Plant Cell Environ 34:922–932

    Article  CAS  PubMed  Google Scholar 

  • Gilmore AM, Hazlett TL, Govindjee (1994) Xanthophyll cycle-dependent quenching of photosystem II chlorophyll a fluorescence: formation of a quenching complex with a short fluorescent lifetime. Proc Natl Acad Sci USA 92:2273–2277

    Article  Google Scholar 

  • Govindarajulu M, Pfeffer PE, Jin H, Abubaker J, Douds DD, Allen JW, Bücking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823

    Article  CAS  PubMed  Google Scholar 

  • Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1255

    Article  CAS  PubMed  Google Scholar 

  • Heber U (2008) Photoprotection of green plants: a mechanism of ultra-fast thermal energy dissipation in desiccated lichens. Planta 228:641–650

    Article  CAS  PubMed  Google Scholar 

  • Heber U, Azarkovich M, Shuvalov V (2007) Activation of mechanisms of photoprotection by desiccation and by light: poikilohydric photoautotrophs. J Exp Bot 58:2745–2759

    Article  CAS  PubMed  Google Scholar 

  • Honegger R (1991) Functional aspects of the lichen symbiosis. Annu Rev Plant Biol 42:553–578

    Article  CAS  Google Scholar 

  • Honegger R (2003) The impact of different long term storage conditions on the viability of lichen-forming ascomycetes and their green algal photobiont, Trebouxia spp. Plant Biol 5:324–330

    Article  Google Scholar 

  • Kosugi 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 Cell Physiol 50:879–888

    Article  CAS  PubMed  Google Scholar 

  • Kosugi M, Kashino Y, Satoh K (2010) Comparative analysis of light response curves of Ramalina yasudae and freshly isolated Trebouxia sp. revealed the presence of intrinsic protection mechanisms independent of upper cortex for the photosynthetic system of algal symbionts in lichen. Lichenology 9:1–10

    Google Scholar 

  • Kosugi M, Miyake H, Yamanakawa H, Shibata Y, Miyazawa A, Sugimura T, Satoh K, Itoh S, Kashino Y (2013) Arabitol provided by lichenous fungi enhances ability to dissipate excess light energy in symbiotic green alga under desiccation. Plant Cell Physiol 54:1316–1325

    Article  CAS  PubMed  Google Scholar 

  • Kranner I, Cram JW, Zorn M et al (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Natl Acad Sci USA 102:3141–3146

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kranner I, Beckett RP, Hochman A, Nash TH III (2008) Desiccation tolerance in lichens: a review. Bryologist 111:576–593

    Article  Google Scholar 

  • Lange OL (1953) Hitze- und Trockenresistenz der Flechten in Beziehung zu ihrer Verbreitung. Flora 140:39–47

    Google Scholar 

  • Lange OL, Pfanz H, Killian E, Mayer A (1990) Effect of low water potential on photosynthesis in intact lichens and their liberated algal components. Planta 182:467–472

    Article  CAS  PubMed  Google Scholar 

  • Lazár D, Nauš J (1998) Statistical properties of chlorophyll fluorescence induction parameters. Photosynthetica 35:121–127

    Article  Google Scholar 

  • Leliaert F, Smith DR, Moreau H, Herron MD, Verbruggen H, Delwiche CF, De Clerck O (2012) Phylogeny and molecular evolution of the green algae. Crit Rev Plant Sci 31:1–46

  • Lüttge U, Büdel B (2010) Resurrection kinetics of photosynthesis in desiccation-tolerant terrestrial green algae (Chlorophyta) on tree bark. Plant Biol 123:437–444

    Article  Google Scholar 

  • MacKenzie TDB, Król M, Huner NPA, Campbell DA (2002) Seasonal changes in chlorophyll fluorescence quenching and the induction and capacity of the photoprotective xanthophyll cycle in Lobaria pulmonaria. Can J Bot 80:255–261

    Article  CAS  Google Scholar 

  • Malloch DW, Pirozynski KA, Raven PH (1980) Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review). Proc Natl Acad Sci USA 77:2113–2118

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matthes-Sears U, Gerrath JA, Gerrath JF, Larson DW (1999) Community structure of epilithic and endolithic algae and cyanobacteria on cliffs of the Niagara Escarpment. J Veg Sci 10:587–598

    Article  Google Scholar 

  • Minibayeva F, Beckett RP (2001) High rates of extracellular superoxide production in bryophytes and lichens, and an oxidative burst in response to rehydration following desiccation. New Phytol 152:333–341

    Article  CAS  Google Scholar 

  • Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed Central  PubMed  Google Scholar 

  • Nardini A, Marchetto A, Tretiach M (2013) Water relation parameters of six Peltigera species correlate with their habitat preferences. Fungal Ecol 6:397–407

  • Nash TH III (2008) Lichen biology, 2nd edn. Cambridge University Press, New York

    Book  Google Scholar 

  • Nash TH III, Reiner A, Demmig-Adams B, Kilian E, Kaiser WM, Lange OL (1990) The effect of osmotic water stress on photosynthesis and dark respiration of lichens. New Phytol 116:269–276

    Article  Google Scholar 

  • Nimis PL, Martellos S (2008) ITALIC—the information system on Italian lichens. Version 4.0. http://dbiodbs-univ.trieste.it. Accessed 1 Apr 2012 

  • Pellegrini E, Bertuzzi S, Candotto Carniel F, Lorenzini G, Nali C, Tretiach M (2014) Ozone tolerance in lichens: a possible explanation from biochemical to physiological level using Flavoparmelia caperata as test organism. J Plant Physiol 171:1514–1523

    Article  CAS  PubMed  Google Scholar 

  • Piccotto M, Tretiach M (2010) Photosynthesis in chlorolichens the influence of the habitat light regime. J Plant Res 123:763–775

    Article  CAS  PubMed  Google Scholar 

  • Roháček K (2002) Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40:13–29

    Article  Google Scholar 

  • Scherrer S, De Vries OMH, Dudler R, Wessels JGH, Honegger R (2000) Interfacial self-assembly of fungal hydrophobins of the lichen-forming ascomycetes Xanthoria parietina and X. ectaneoides. Fungal Genet Biol 30:81–93

    Article  CAS  PubMed  Google Scholar 

  • Schofield SC, Campbell DA, Funk C, MacKenzie TDB (2003) Changes in macromolecular allocation in nondividing algal symbionts allow for photosynthetic acclimation in the lichen Lobaria pulmonaria. New Phytol 159:709–718

    Article  CAS  Google Scholar 

  • Solhaug KA, Gauslaa Y (1996) Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia 108:412–418

    Article  Google Scholar 

  • Štepigová J, Gauslaa Y, Cempírková-Vráblíková H, Solhaug KA (2008) Irradiance prior to and during desiccation improves the tolerance to excess irradiance in the desiccated state of the old forest lichen Lobaria pulmonaria. Photosynthetica 46:286–290

  • Tretiach M, Adamo P, Bargagli R, Baruffo L, Carletti L, Crisafulli P, Giordano S, Modenesi P, Orlando S, Pittao E (2007a) Lichen and moss bags as monitoring devices in urban areas. Part I: influence of exposure on sample vitality. Environ Pollut 146:380–391

    Article  CAS  PubMed  Google Scholar 

  • Tretiach M, Piccotto M, Baruffo L (2007b) Effect of ambient NOx on chlorophyll a fluorescence in transplanted Flavoparmelia caperata (Lichen). Environ Sci Technol 46:2978–2984

    Article  Google Scholar 

  • Tschermak-Woess E (1989) Developmental studies in trebouxioid algae and taxonomical consequences. Plant Syst Evol 164:161–195

    Article  Google Scholar 

  • Vráblíková H, Barták M, Wonish A (2005) Changes in glutathione and xanthophyll cycle pigments in the high light-stressed lichens Umbilicaria antartica and Lasallia pustulata. J Photochem Photobiol, B 79:35–41

    Article  Google Scholar 

  • 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. Appl Environ Microbiol 71:2121–2129

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wellburn AR (1964) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  Google Scholar 

  • Yamamoto M, Kinoshita Y, Yoshimura I (2002) Photobiont culturing. In: Kranner I, Beckett RP, Varma AK (eds) Protocols in lichenology. Culturing, biochemistry, ecophysiology and use in biomonitoring. Springer, Berlin, pp 34–42

    Google Scholar 

  • Zia A, Johnson MP, Ruban AV (2011) Acclimation- and mutation-induced enhancement of PsbS levels affects the kinetics of non-photochemical quenching in Arabidopsis thaliana. Planta 233:1253–1264

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank A. Montagner for help in the laboratory, G. Baj for assistance at the confocal microscopy, D. Kodnik for field work, L. Muggia for assessing the phylogenetic position of our photobiont and P. Crisafulli for the culture inclusions. A special thanks goes to Professor I. Kranner (University of Innsbruck) for the critical comments to the manuscript and the constructive discussion about this work. This study was supported by the Italian Ministry of Education, University and Research (20082WWM9A to M.T.), and by the University of Trieste (F.R.A. 2011 to M.T.).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Dipartimento di Scienze della Vita, Università degli Studi di Trieste, Via L. Giorgieri, 10, 34127, Trieste, Italy

    Fabio Candotto Carniel, Davide Zanelli, Stefano Bertuzzi & Mauro Tretiach

  2. Institute of Botany, University of Innsbruck, Sternwartestraße 15, 6020, Innsbruck, Austria

    Fabio Candotto Carniel

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  1. Fabio Candotto Carniel
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  2. Davide Zanelli
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  3. Stefano Bertuzzi
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  4. Mauro Tretiach
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Correspondence to Fabio Candotto Carniel.

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Special topic: Desiccation Biology.

Guest editors: Olivier Leprince and Julia Buitink.

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Candotto Carniel, F., Zanelli, D., Bertuzzi, S. et al. Desiccation tolerance and lichenization: a case study with the aeroterrestrial microalga Trebouxia sp. (Chlorophyta). Planta 242, 493–505 (2015). https://doi.org/10.1007/s00425-015-2319-z

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