Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Do lichens have “memory” of their native nitrogen environment?

  • 231 Accesses

  • 9 Citations

Abstract

This study aimed to deepen the knowledge about intraspecific mechanisms regulating nitrogen tolerance in lichens to wet nitrogen deposition. Thalli of the nitrophilous lichen Xanthoria parietina were collected from environments with different nitrogen availabilities and immersed in 80 mL of ammonium sulphate (NH4)2SO4 solutions with distinct concentrations (0, 0.025, 0.05 and 0.25 M) for 5 h per day during 3 days in a week. After each soaking event, lichens were air dried. After each treatment, maximal PSII efficiency, localization of ammonium ions, concentrations of K+ and Mg2+ and thalli buffer capacity were determined. Our results show that lichens are marked by their native nitrogen environment, since there were important differences between the physiological responses of X. parietina thalli previously grown in an area with high nitrogen deposition (nitrogen emissions of ca. 13,000 t/year) and those previously grown in an unpolluted area (nitrogen emissions of ca. 500 t/year). Greater N availability seems to enable X. parietina to cope better with the effects of nitrogen pollution.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

Abbreviations

Ca2+ :

Calcium ion

CsCl:

Cesium chloride

H2SO4 :

Sulphuric acid

K+ :

Potassium ion

KNO3 :

Potassium nitrate

LaCl3 :

Lanthanum chloride

Mg2+ :

Magnesium ion

N:

Nitrogen

NaOH:

Sodium hydroxide

NiCl2 :

Nickel chloride

NH3 :

Ammonia

NH4 + :

Ammonium ion

NH4Cl:

Ammonium chloride

NH4NO3 :

Ammonium nitrate

(NH4)2SO4 :

Ammonium sulphate

XA:

Xanthoriaparietina from Arrábida

XH:

Xanthoriaparietina from hyppodrome

References

  1. Allen SE (1989) Chemical analysis of ecological materials. Blackwell Scientific, Oxford

  2. Ashraf M, Rahmatullah Ahmad R, Bhatti AS, Afzal M, Sarwar A, Maqsood MA, Kanwal S (2010) Amelioration of salt stress in sugarcane (Saccharum officinarum L.) by supplying potassium and silicon in hydroponics. Pedosphere 20:153–162

  3. Branquinho C, Brown HD, Catarino F (1997) The cellular location of Cu in lichens and its effects on membrane integrity and chlorophyll fluorescence. Environ Exp Bot 38:165–179

  4. Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. J Plant Physiol 159:567–584

  5. Brown DH (1987) The location of mineral elements in lichens: implications for metabolism. Bibl Lichenol 25:361–375

  6. Brown DH, Avalos A (1991) Chemical control of cadmium uptake by Peltigera. Symbiosis 11:299–311

  7. Cape JN, van der Eerden LJ, Sheppard LJ, Leith ID, Sutton MA (2009) Evidence for changing the critical level for ammonia. Environ Pollut 157:1033–1037

  8. Claussen W, Lenz F (1999) Effect of ammonium or nitrate nutrition on net photosynthetic, growth, and activity of the enzymes nitrate reductase and glutamine synthetase in blueberry, raspberry and strawberry. Plant Soil 208:95–102

  9. Cruz C, Bio AF, Domínguez-Valdivia MD, Aparicio-Tejo PM, Lamsfus C, Martins-Loução MA (2006) How does glutamine synthetase activity determine plant tolerance to ammonium? Planta 223:1068–1080

  10. Cruz C, Egsgaard H, Trujillo C, Ambus P, Requena N, Martins-Loução MA, Jacobsen I (2007) Enzymatic evidence for the key role of arginine in nitrogen translocation by arbuscular mycorrhizal fungi. Plant Physiol 144:782–792

  11. Dahlman L, Persson J, Näsholm T, Palmqvist K (2003) Carbon and nitrogen distribution in the green-algal lichens Hypogymnia physodes and Platismatia glauca in relation to nutrient supply. Planta 217:41–48

  12. EMEP (European Monitoring and Evaluation Programme) (2007) Data from the centre on emission inventories and projections http://www.ceip.at/emission-data-webdab/gridded-emissions-in-google-maps/

  13. Feng J, Barker AV (1992) Ethylene evolution and ammonium accumulation by nutrient-stressed tomato plants. J Plant Nutr 1992:137–153

  14. Frati L, Santoni S, Nicolardi V, Gaggi C, Brunialti G, Guttova A, Gaudino S, Pati A, Pirintsos SA, Loppi S (2007) Lichen biomonitoring of ammonia emission and nitrogen deposition around a pig stockfarm. Environ Pollut 146:311–316

  15. Gaio-Oliveira G, Branquinho C, Máguas C, Martins-Loução MA (2001) The concentration of nitrogen in nitrophilous and non-nitrophilous lichen species. Symbiosis 31:187–199

  16. Gaio-Oliveira G, Dahlman L, Palmqvist K, Máguas C (2005a) Responses of the lichen Xanthoria parietina (L.) Th. Fr. to varying thallus nitrogen concentrations. Lichenologist 37:171–179

  17. Gaio-Oliveira G, Dahlman L, Palmqvist K, Martins-Louçáo MA, Máguas C (2005b) Nitrogen uptake in relation to excess supply and its effects on the lichens Evernia prunastri (L.) Ach. and Xanthoria parietina (L.) Th. Fr. Planta 220:794–803

  18. Gloser V, Gloser J (2000) Nitrogen and base cation uptake in seedlings of Acer pseudoplatanus and Calamagrotis villosa exposed to an acidified environment. Plant Soil 226:71–77

  19. Hallbom L, Bergman B, Rai AN (1986) Immunogold localization of glutamine synthetase in the cyanobionts of the lichens Peltigera aphthosa and Peltigera canina. Lichen Physiol Biochem 1:27–34

  20. Hauck M (2010) Ammonium and nitrate tolerance in lichens. Environ Pollut 158:1127–1133

  21. Heeb NV, Saxer CJ, Forss AM, Brühlmann S (2008) Trends of NO-, NO2-, and NH3-emissions from gasoline-fueled Euro-3- to Euro-4-passenger cars. Atmos Environ 42:2543–2554

  22. Hölldampf B, Barker AV (1993) Effects of ammonium on elemental nutrition of red spruce and indicator plants grown in acid soil. Commun Soil Sci Plant Anal 24:1945–1957

  23. Janson S, Rai AN, Bergman B (1993) The marine lichen Lichina confinis (O.F. Müll.) C. Ag.: ultrastructure and localization of nitrogenase, glutamine synthetase, phycoerythrin and ribulose 1, 5-bisphosphate carboxylase/oxygenase in the cyanobiont. New Phytol 124:149–160

  24. Kraft M, Eikmann T, Kappos A, Künzli N, Rapp R, Schneider K, Seitz H, Voss J, Wichmann HE (2005) The German view: effects of nitrogen dioxide on human health–derivation of health-related short-term and long-term values. Int J Hyg Environ Health 208:305–318

  25. Kronzucker HJ, Szczerba MW, Britto DT (2003) Cytosolic potassium homeostatis revisited: 42K-tracer analysis reveals setpointvariations in [K+]. Planta 217:540–546

  26. Krupa SV (2003) Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environ Pollut 124:179–221

  27. McKersie BD, Hucl P, Beversdorf WD (1982) Solute leakage from susceptible and tolerant cultivars of Phaseolus vulgaris following ozone exposure. Can J Bot 60:73–78

  28. Miller JE, Brown DH (1999) Studies of ammonia uptake and loss by lichen. Lichenologist 31:85–93

  29. Munzi S, Pirintsos AS, Loppi S (2009a) Chlorophyll degradation and inhibition of polyamines biosynthesis in the lichen Xanthoria parietina under nitrogen stress. Ecotoxicol Environ Saf 72:281–285

  30. Munzi S, Pisani T, Loppi S (2009b) The integrity of lichen cell membrane is a suitable parameter for monitoring early biological effects of acute nitrogen pollution. Ecotoxicol Environ Saf 72:2009–2012

  31. Nieboer E, Richardson DHS, Tomassini FD (1978) Mineral uptake and release by lichens. Bryologist 81:226–246

  32. Paoli L, Pirintsos SA, Kotzabasis K, Pisani T, Navakoudis E, Loppi S (2010) Effects of ammonia from livestock farming on lichen photosynthesis. Environ Pollut 158:2258–2265

  33. Pinho P, Augusto S, Martins-Loução MA, Pereira MJ, Soares A, Máguas C, Branquinho C (2008) Causes of change in nitrophytic and oligotrophic lichen species in a Mediterranean climate: impact of land cover and atmospheric pollutants. Environ Pollut 154:380–389

  34. Pinho P, Branquinho C, Cruz C, Tang SY, Dias T, Rosa AP, Máguas C, Loução MAM, Sutton MA (2009) Assessment of critical levels of atmospheric ammonia for lichen diversity in cork-oak woodland, Portugal. In: Sutton MA, Reis S, Baker SMH (eds) Atmospheric ammonia—detecting emission changes and environmental impacts. Springer, Berlin, pp 109–120

  35. Pirintsos SA, Munzi S, Loppi S, Kotzabasis K (2009) Do polyamines alter the sensitivity of lichens to nitrogen stress? Ecotoxicol Environ Saf 72:1331–1336

  36. Pisani T, Munzi S, Paoli L, Bačkor M, Loppi S (2009) Physiological effects of a geothermal element: boron excess in the epiphytic lichen Xanthoria parietina (L.) Th. Fr. Chemosphere 76:921–926

  37. Reis MA, Alves LC, Freitas MC, Van Os B, de Goeij J, Wolterbeek HTH (2002) Calibration of lichen transplants considering faint memory effects. Environ Pollut 120:87–95

  38. Sanità di Toppi L, Pawlik-Skowrońska B, Vurro E, Vattuone Z, Kalinowska R, Restivo FM, Musetti R, Skowroński T (2008) First and second line mechanisms of cadmium detoxification in the lichen photobiont Trebouxia impressa (Chlorophyta). Environ Pollut 151:280–286

  39. Santa-María GE, Danna CH, Czibener C (2000) High-affinity potassium transport in barley roots. Ammonium-sensitive and—insensitive pathways. Plant Physiol 62:665–669

  40. Sheppard LJ, Leith ID, Crossley A, van Dijk N, Fowler D, Sutton MA (2009) Long-term cumulative exposure exacerbates the effects of atmospheric ammonia on an ombrotrophic bog: implications for critical levels. In: Sutton MA, Reis S, Baker SMH (eds) Atmospheric ammonia—detecting emission changes and environmental impacts. Springer, Berlin, pp 49–58

  41. Sutton MA, Dragosits U, Tang YS, Fowler D (2000) Ammonia emissions from non-agricultural sources in the UK. Atmos Environ 34:855–869

  42. Sutton MA, Pitcairn CER, Whitfield CP (eds) (2004) Introduction: bioindicators and biomonitoring for atmospheric nitrogen. Bioindicator and biomonitoring methods for assessing the effects of atmospheric nitrogen on statutory nature conservation sites. Jt Nat Conserv Comm Rep 356

  43. Szczerba MW, Britto DT, Ali SA, Balkos KD, Kronzucker HJ (2008) NH4+-stimulated and—inhibited components of K+ transport in rice (Oryza sativa L.). J Exp Bot 59:3415–3423

  44. van Dobben HF, ter Braak CJF (1998) Effects of atmospheric NH3 on epiphytic lichens in The Netherlands: the pitfalls of biological monitoring. Atmos Environ 32:551–557

  45. van Herk CM (1999) Mapping of ammonia pollution with epiphytic lichens in The Netherlands. Lichenologist 31:9–20

  46. van Herk CM (2001) Bark pH and susceptibility to toxic air pollutants as independent causes of changes in epiphytic lichen composition in space and time. Lichenologist 33:419–442

  47. Vieira AR, Gonzales C, Martins-Louçáo MA, Branquinho C (2009) Intracellular and extracellular ammonium (NH4 +) uptake and its toxic effects on the aquatic biomonitor Fontinalis antipyretica. Ecotoxicology 18:1087–1094

  48. Yamamoto Y, Hamade R, Kinoshita Y, Higuchi M, Yoshimura I, Sekiya J, Yamada Y (1994) Biological approaches using lichen-derived cultures: growth and primary metabolism. Symbiosis 16:203–217

  49. Zhang YS, Sun X, Ying QZ (1990) The effect of organic manure and potassium in preventing ammonium toxicity in barley. Acta Pedol Sinica 27:80–86

Download references

Author information

Correspondence to Stefano Loppi.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Munzi, S., Loppi, S., Cruz, C. et al. Do lichens have “memory” of their native nitrogen environment?. Planta 233, 333–342 (2011). https://doi.org/10.1007/s00425-010-1300-0

Download citation

Keywords

  • Ammonium load
  • Buffer capacity
  • Chlorophyll fluorescence
  • Electrolyte leakage
  • Membrane damage
  • Xanthoria