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Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms

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An Erratum to this article was published on 20 October 2009

Abstract

The mechanisms involved in desiccation tolerance of lichens and their photobionts are still poorly understood. To better understand these mechanisms we have studied dehydration rate and desiccation time in Trebouxia, the most abundant chlorophytic photobiont in lichen. Our findings indicate that the drying rate has a profound effect on the recovery of photosynthetic activity of algae after rehydration, greater than the effects of desiccation duration. The basal fluorescence (F′o) values in desiccated algae were significantly higher after rapid dehydration, than after slow dehydration, suggesting higher levels of light energy dissipation in slow-dried algae. Higher values of PSII electron transport were recovered after rehydration of slow-dried Trebouxia erici compared to rapid-dried algae. The main component of non-photochemical quenching after slow dehydration was energy dependent (q E), whereas after fast dehydration it was photoinhibition (q I). Although q E seems to play a role during desiccation recovery, no significant variations were detected in the xanthophyll cycle components. Desiccation did not affect PSI functionality. Classical antioxidant activities like superoxide dismutase or peroxidase decreased during desiccation and early recovery. Dehydrins were detected in the lichen-forming algae T. erici and were constitutively expressed. There is probably a minimal period required to develop strategies which will facilitate transition to the desiccated state in this algae. In this process, the xanthophyll cycle and classical antioxidant mechanisms play a very limited role, if any. However, our results indicate that there is an alternative mechanism of light energy dissipation during desiccation, where activation is dependent on a sufficiently slow dehydration rate.

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Abbreviations

F o :

Minimal fluorescence intensity in dark-adapted samples

F m :

Maximal fluorescence intensity in dark-adapted samples

F v :

Variable fluorescence (F v = F m − F o)

FV/Fm:

Maximal quantum yield of PSII photochemistry

F′m:

Maximum fluorescence intensity in illuminated samples

F′o:

Minimum fluorescence intensity in illuminated samples state

F s :

Fluorescence intensity during exposure to light

F′v/F′m:

Maximum quantum yield of PSII in light-adapted samples

ϕPSII :

Quantum yield of PSII during exposure to light

q P :

Photochemical quenching

q N :

Non-photochemical quenching

q E :

Energy-dependent quenching

q I :

Photoinhibitory quenching

q M :

Middle phase of dark relaxation quenching

A:

Antheraxantin

DPS:

De-epoxidation state of the xanthophyll cycle

PAR:

Photosynthetically active radiation

P700:

Reaction centre of the PSI

PSI, PSII:

Photosystem I (II)

POX:

Peroxidase

RD:

Rapid dehydration

RWC:

Relative water content

SD:

Slow dehydration

SOD:

Superoxide dismutase

V:

Violaxanthin

Z:

Zeaxanthin

References

  • Adams WW III, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou C, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Adv photosynthesis and respiration, vol 19. Springer, The Netherlands, pp 583–604

    Google Scholar 

  • Adams WW III, Demmig-Adams B, Lange OL (1993) Carotenoid composition and metabolism in green and blue-green algal lichens in the field. Oecologia 94:576–584

    Article  Google Scholar 

  • 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 653–660

    Google Scholar 

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

    Google Scholar 

  • Alpert P, Oliver MJ (2002) Drying without dying. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, Oxon, pp 3–43

    Chapter  Google Scholar 

  • Bačkor M, Fahselt D (2005) Tetrazolium reduction as an indicator of environmental stress in lichens and isolated bionts. Environ Exp Bot 53:125–133

    Article  Google Scholar 

  • Bačkor M, Fahselt D, Davidson RD, Wu CT (2003) Effects of copper on wild and tolerant strains of the lichen photobiont Trebouxia erici (Chlorophyta) and possible tolerance mechanisms. Arch Environ Con Tox 45:159–167

    Article  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 

  • Baker NR, Oxborough K (2004) Chlorophyll fluorescence as a probe of photosynthetic productivity. In: Papageorgiou C, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Adv photosynthesis and respiration, vol 19. Springer, The Netherlands, pp 65–82

    Google Scholar 

  • Bewley JD (1979) Physiological aspects of desiccation tolerance. Annu Rev Plant Physiol 30:195–238

    Article  CAS  Google Scholar 

  • Bewley JD, Reynolds TL, Oliver MJ (1993) Evolving strategies in the adaptation to desiccation. In: Close TJ, Bray EA (eds) Plant responses to cellular dehydration during environmental stress, vol 10. American Society of Plant Physiologists, Rockville, Maryland, pp 193–201

    Google Scholar 

  • Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566

    Article  CAS  PubMed  Google Scholar 

  • Buitink J, Hemmings MA, Hoekstra FA (2002) Is there a roll for oligosaccharides in seed longevity? An assessment of intracellular glass stability. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, Oxon, pp 293–318

    Chapter  Google Scholar 

  • Bukhov NG, Kopecky J, Pfundel EE, Klughammer C, Heber U (2001) A few molecules of zeaxanthin per reaction centre of photosystem II permit effective thermal dissipation of light energy in photosystem II of a poikilohydric moss. Planta 212:739–748

    Article  CAS  PubMed  Google Scholar 

  • Calatayud A, Deltoro VI, Barreno E, delValleTascon S (1997) Changes in in vivo chlorophyll fluorescence quenching in lichen thalli as a function of water content and suggestion of zeaxanthin-associated photoprotection. Physiol Plant 101:93–102

    Article  CAS  Google Scholar 

  • Chakir S, Jensen M (1999) How does Lobaria pulmonaria regulate photosystem II during progressive desiccation and osmotic water stress? A chlorophyll fluorescence study at room temperature and at 77 K. Physiol Plant 105:257–265

    Article  CAS  Google Scholar 

  • Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803

    Article  CAS  Google Scholar 

  • Close TJ, Fenton RD, Moonan F (1993) A view of plant dehydrins using antibodies specific to the carboxy terminal peptide. Plant Mol Biol 23:279–286

    Article  CAS  PubMed  Google Scholar 

  • Cooper K, Farrant JM (2002) Recovery of the resurrection plant Craterostigma wilmsii from desiccation: protection versus repair. J Exp Bot 53:1805–1813

    Article  CAS  PubMed  Google Scholar 

  • Crowe JH, Heokstra FA, Crowe LM (1992) Anhydrobiosis. Annu Rev Physiol 54:579–599

    Article  CAS  PubMed  Google Scholar 

  • De las Rivas J, Abadía A, Abadía J (1989) A new reversed-phase-HPLC method resolving all major higher plant photosynthetic pigments. Plant Physiol 91:190–192

    Article  CAS  PubMed  Google Scholar 

  • Deltoro VI, Calatayud A, Gimeno C, Abadía A, Barreno E (1998) Changes in chlorophyll a fluorescent, photosynthetic CO2 assimilation and xanthophyll cycle interconversions during dehydration in desiccation-tolerant and intolerant liverworts. Planta 207:224–228

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW (1993) The xanthophyll cycle, protein turnover, and the high light tolerance of sun acclimated leaves. Plant Physiol 103:1413–1420

    CAS  PubMed  Google Scholar 

  • Fridl T, Büdel B (2008) Photobionts. In: Nash TH, III (ed) Lichen biology. Cambridge University Press, pp 9–26

  • Garty J, Kloog N, Cohen Y (1998) Integrity of lichen cell membranes in relation to concentration of airborne elements. Arch Environ Contam Toxicol 34:136–144

    Article  CAS  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

    CAS  Google Scholar 

  • Goldsmith SJ, Thomas MA, Gries C (1997) A new technique for photobiont culturing and manipulation. Lichenologist 29:559–569

    Google Scholar 

  • Green TGA, Nash TH, III, Lange OL (2008) Physiological ecology of carbon dioxide exchange. In: Nash TH, III (ed) Lichen biology. Cambridge University Press, pp 152–181

  • Guéra A, Calatayud A, Sabater B, Barreno E (2005) 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

    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, Bilger W, Shuvalov VA (2006a) Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation. J Exp Bot 57:2993–3006

    Article  CAS  PubMed  Google Scholar 

  • Heber U, Lange OL, Shuvalov VA (2006b) Conservation and dissipation of light energy as complementary processes: homoiohydric and poikilohydric autotrophs. J Exp Bot 57:1211–1223

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Horton P, Hague A (1988) Studies on the induction of chlorophyll fluorescence in isolated barley protoplasts. Resolution of non-photochemical quenching. Biochim Biophys Acta 932:107–115

    Article  CAS  Google Scholar 

  • Ingram J, Bartels D (1996) The molecular basis of dehydration tolerance in plants. Annu Rev Plant Physiol Plant Mol Biol 47:377–403

    Article  CAS  PubMed  Google Scholar 

  • Kim SJ, Lee CH, Hope AB, Chow WS (2001) Inhibition of photosystems I and II and enhanced back flow of photosystem I electrons in cucumber leaf discs chilled in the light. Plant Cell Physiol 42:842–848

    Article  CAS  PubMed  Google Scholar 

  • Kopecky J, Azarkovich M, Pfundel EE, Shuvalov VA, Heber U (2005) Thermal dissipation of light energy is regulated differently and by different mechanisms in lichens and higher plants. Plant Biol (Stuttg) 7:156–167

    Article  CAS  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 symbionts. Plant Cell Physiol. doi:10.10093/pcp/pcp043

  • Kramer DM, Johnson G, Kiirats O, Edwards GE (2004) New fluorescence parameters for the determination of Q(A) redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  CAS  PubMed  Google Scholar 

  • Kranner I (2002) Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytol 154:451–460

    Article  CAS  Google Scholar 

  • Kranner I, Birtic F (2005) A modulation role for antioxidants in desiccation tolerance. Integr Comp Biol 45:734–740

    Article  CAS  Google Scholar 

  • Kranner I, Zorn M, Turk B, Wornik S, Beckett RR, Batic F (2003) Biochemical traits of lichens differing in relative desiccation tolerance. New Phytol 160:167–176

    Article  CAS  Google Scholar 

  • Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, Pfeifhofer HW (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  Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgiou C, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Adv photosynthesis and respiration, vol 19. Springer, The Netherlands, pp 463–495

    Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis—the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Logan BA, Adams WW III, Demmig-Adams B (2007) Avoiding common pitfalls of chlorophyll fluorescence analysis under field conditions. Funct Plant Biol 34:853–859

    Article  CAS  Google Scholar 

  • Luwe MWF, Takahama U, Heber U (1993) Role of ascorbate in detoxifying ozone in the apoplast of spinach (Spinacea oleracea L.). Plant Physiol 101:969–976

    CAS  PubMed  Google Scholar 

  • Mantoura RFC, Llewellyn CA (1983) The rapid-determination of algal chlorophyll and carotenoid pigments and their breakdown products in natural waters by reverse-phase high performance liquid chromatography. Anal Chim Acta 151:297–314

    Article  CAS  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 X-P, Niyogi KK (2001) Non-photochemical quenching: a response to excess light energy. Plant Physiol 125:1558–1566

    Article  PubMed  Google Scholar 

  • Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371

    Article  CAS  PubMed  Google Scholar 

  • Niyogi KK, Li XP, Rosenberg V, Jung HS (2004) Is psbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382

    Article  PubMed  Google Scholar 

  • O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021

    PubMed  Google Scholar 

  • Oliver MJ, Bewley JD (1997) Desiccation tolerance of plant tissues: a mechanistic overview. Horticult Rev 18:171–214

    Google Scholar 

  • Oliver MJ, Velten J, Mishler BD (2005) Desiccation tolerance in bryophytes: a reflection of the primitive strategy for plant survival in dehydrating habitats? Integr Comp Biol 45:788–799

    Article  Google Scholar 

  • Proctor MCF, Pence VC (2002) Vegetative tissues: bryophytes, vascular resurrection plants, and vegetative propogules. In: Black M, Pritchard HW (eds) Desiccation and survival in plants: drying without dying. CABI Publishing, Wallingford, Oxon, pp 207–237

    Chapter  Google Scholar 

  • Proctor MC, Smirnoff N (2000) Rapid recovery of photosystems on rewetting desiccation-tolerant mosses: chlorophyll fluorescence and inhibitor experiments. J Exp Bot 51:1695–1704

    Article  CAS  PubMed  Google Scholar 

  • Proctor MCF, Tuba Z (2002) Poikilohydry and homoiohydric: antithesis or spectrum of possibilities. New Phytol 156:327–349

    Article  Google Scholar 

  • Quick WP, Stitt M (1989) An examination of factors contributing to non-photochemical quenching of chlorophyll fluorescence in barley leaves. Biochim Biophys Acta 977:287–296

    Article  CAS  Google Scholar 

  • Rundel PW (1988) Water relations. In: Galun M (ed) Handbook of lichenology, vol II. CRC Press, Boca Raton, Fla, pp 17–36

    Google Scholar 

  • Schonbeck MW, Bewley JD (1981) Responses of the moss Tortula ruralis to desiccation treatments I. Effects of minimum water content and rates of dehydration and rehydration. Can J Bot 59:2698–2706

    CAS  Google Scholar 

  • Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and nonphotochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51–62

    Article  CAS  Google Scholar 

  • Silberstein L, Siegel BZ, Siegel SM, Mukhtar A, Galun M (1996) Comparative studies on Xanthoria parietina, a pollution-resistant lichen, and Ramalina duriaei, a sensitive species. 1. Effects of air pollution on physiological processes. Lichenologist 28:355–365

    Google Scholar 

  • Walters RG, Horton P (1990) The use of light-pulses to investigate the relaxation in the dark of chlorophyll fluorescence quenching in barley leaves. Curr Res Photosynthesis 1–4:A631–A634

    Google Scholar 

  • Walters RG, Horton P (1991) Resolution of components of nonphotochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121–133

    Article  CAS  Google Scholar 

  • Weissman L, Garty J, Hochman A (2005) Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydration. Appl Environ Microbiol 71:6508–6514

    Article  CAS  PubMed  Google Scholar 

  • Zapata JM, Sabater B, Martin M (1998) Identification of a thylakoid peroxidase of barley which oxidizes hydroquinone. Phytochemistry 48:1119–1123

    Article  CAS  Google Scholar 

  • Zapata JM, Gasulla F, Esteban-Carrasco A, Barreno E, Guéra A (2006) Inactivation of a plastid evolutionary conserved gene affects PSII electron transport, life span and fitness of tobacco plants. New Phytol 174:357–366

    Article  Google Scholar 

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Authors and Affiliations

  1. Dpto. de Botánica, Fac. de Biología, Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universitat de València, 46100, Burjassot, Valencia, Spain

    Francisco Gasulla, Pedro Gómez de Nova & Eva Barreno

  2. Dpto. de Biología Vegetal, Fac. de Biología, Universidad de Alcalá, Edificio de Ciencias, Campus Universitario, 28871, Alcalá de Henares, Madrid, Spain

    Alberto Esteban-Carrasco, José M. Zapata & Alfredo Guéra

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  1. Francisco Gasulla
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  2. Pedro Gómez de Nova
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  3. Alberto Esteban-Carrasco
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  4. José M. Zapata
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  5. Eva Barreno
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  6. Alfredo Guéra
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Correspondence to Alfredo Guéra.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s00425-009-1030-3

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Gasulla, F., de Nova, P.G., Esteban-Carrasco, A. et al. Dehydration rate and time of desiccation affect recovery of the lichenic algae Trebouxia erici: alternative and classical protective mechanisms. Planta 231, 195–208 (2009). https://doi.org/10.1007/s00425-009-1019-y

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