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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Nitrogen tolerance in the lichen Xanthoria parietina: the sensitive side of a resistant species

Silvana Munzi A B C , Cristina Branquinho A , Cristina Cruz A and Stefano Loppi B
+ Author Affiliations
- Author Affiliations

A Universidade de Lisboa, Faculdade de Ciências, Centro de Biologia Ambiental, Campo Grande, Bloco C2, 1749-016 Lisboa, Portugal.

B Department of Environmental Science, University of Siena, via P. Mattioli 4, I-53100 Siena, Italy.

C Corresponding author. Email: ssmunzi@fc.ul.pt

Functional Plant Biology 40(3) 237-243 https://doi.org/10.1071/FP12127
Submitted: 24 April 2012  Accepted: 12 October 2012   Published: 7 November 2012

Abstract

To investigate the mechanisms of nitrogen (N) tolerance in lichens, we examined the physiological responses to increased N availability in different functional groups. Thalli of the nitrophytic Xanthoria parietina (L.) Th.Fr. previously grown both in an N-poor environment (~2 kg N ha–1 year–1) and in an N-rich environment (~52 kg N ha–1 year–1) were compared with the oligotrophic species Evernia prunastri (L.) Ach. and Usnea sp. Lichens were submitted to ammonium treatments. Maximum PSII efficiency, redistribution of the ions between the intra- and extracellular compartments and potassium and magnesium concentrations were the parameters used to check for the effects of N supply. The buffering capacity of the lichen extracts was also determined in untreated lichen thalli to check if different lichen behaviours were due to their ability to maintain the pH. The results showed a more similar response between X. parietina from the N-poor environment and the N-sensitive species than between X. parietina from the N-poor and N-rich environments, suggesting that X. parietina achieved N-tolerance after long-term exposure to N-rich environment. These results are important in understanding the effects of chronic ammonium pollution on one of the most sensitive components of the ecosystem, linking physiological response and ecological consequences.

Additional keywords: adaptation, ammonium, buffer capacity, cell membrane damage, cellular homeostasis, Fv/Fm.


References

Bassi P, Basile A, Ferraro M, Masi M, Migliaccio D, Morelli G, Napolitano E (2006) Plasticity of repetitive DNA in response to metal stress in Bryophytes. Plant Biosystems 140, 80–86.
Plasticity of repetitive DNA in response to metal stress in Bryophytes.Crossref | GoogleScholarGoogle Scholar |

Branquinho C, Brown HD, Catarino F (1997) The cellular location of Cu in lichens and its effects on membrane integrity and chlorophyll fluorescence. Environmental and Experimental Botany 38, 165–179.
The cellular location of Cu in lichens and its effects on membrane integrity and chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtVGht7k%3D&md5=ca659a881640ee1ceb31dc3280d798c6CAS |

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

Carreras HA, Gudiño GL, Pignata ML (1998) Comparative biomonitoring of atmospheric quality in five zones of Córdoba city (Argentina) employing the transplanted lichen Usnea sp. Environmental Pollution 103, 317–325.
Comparative biomonitoring of atmospheric quality in five zones of Córdoba city (Argentina) employing the transplanted lichen Usnea sp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXotVWqtbw%3D&md5=e1520fe733fec67abdb7e7743f06ee30CAS |

Cruz C, Biol AFM, 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.
How does glutamine synthetase activity determine plant tolerance to ammonium?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XivVegtro%3D&md5=54447e274ade6aa4cae28b8ff95824e4CAS |

Cullis CA (1976) Environmentally induced changes in ribosomal RNA cistron number in flax. Heredity 36, 73–79.
Environmentally induced changes in ribosomal RNA cistron number in flax.Crossref | GoogleScholarGoogle Scholar |

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.

Davies L, Bates JW, Bell JNB, James PW, Purvis OW (2007) Diversity and sensitivity of epiphytes to oxides of nitrogen in London. Environmental Pollution 146, 299–310.
Diversity and sensitivity of epiphytes to oxides of nitrogen in London.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit12hur8%3D&md5=9c5145416e97b99231ca6e86ee398976CAS |

Dias T, Malveiro S, Martins-Loução MA, Sheppard L, Cruz C (2011) Linking N-driven biodiversity changes with soil N availability in a Mediterranean ecosystem. Plant and Soil 341, 125–136.
Linking N-driven biodiversity changes with soil N availability in a Mediterranean ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjt1Wjs7s%3D&md5=784de4bcf3fdc9e49cfa56106fff84e8CAS |

EMEP (European Monitoring and Evaluation Programme) (2007) Data from the Centre on Emission Inventories and Projections. Available at http://www.ceip.at/emission-data-webdab/gridded-emissions-in-google-maps/ [Accessed 15 January 2011]

Evans GM, Durrant A, Rees H (1966) Associated nuclear changes in the induction of flax genotrophs. Nature 212, 697–699.
Associated nuclear changes in the induction of flax genotrophs.Crossref | GoogleScholarGoogle Scholar |

Gadsdon SR, Dagley JR, Wolseley PA, Power SA (2010) Relationships between lichen community composition and concentrations of NO2 and NH3. Environmental Pollution 158, 2553–2560.
Relationships between lichen community composition and concentrations of NO2 and NH3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXos1yktrg%3D&md5=c6e74c26894ca3a5fb9074a18a14e759CAS |

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.

Geiser LH, Jovan ES, Glavich DA, Porter MK (2010) Lichen-based critical loads for atmospheric nitrogen deposition in Western Oregon and Washington Forests, USA. Environmental Pollution 158, 2412–2421.
Lichen-based critical loads for atmospheric nitrogen deposition in Western Oregon and Washington Forests, USA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVWjs7w%3D&md5=2e388d229ad3b53ce02c479bc65d7d54CAS |

Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451, 293–296.
An earth-system perspective of the global nitrogen cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Cqsg%3D%3D&md5=bb4aabfa39c07e855e5159534b47f798CAS |

Hauck M (2010) Ammonium and nitrate tolerance in lichens. Environmental Pollution 158, 1127–1133.
Ammonium and nitrate tolerance in lichens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmt1Knt7w%3D&md5=2ea7fb23c1648d283d83e24a6f4a5d68CAS |

McKersie BD, Hucl P, Beversdorf WD (1982) Solute leakage from susceptible and tolerant cultivars of Phaseolus vulgaris following ozone exposure. Canadian Journal of Botany 60, 73–78.
Solute leakage from susceptible and tolerant cultivars of Phaseolus vulgaris following ozone exposure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XhtFOisLw%3D&md5=7d058b463f9ee7e742e4e22c32367413CAS |

Munzi S, Pirintsos SA, Loppi S (2009a) Chlorophyll degradation and inhibition of polyamine biosynthesis in the lichen Xanthoria parietina under nitrogen stress. Ecotoxicology and Environmental Safety 72, 281–285.
Chlorophyll degradation and inhibition of polyamine biosynthesis in the lichen Xanthoria parietina under nitrogen stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlaqtbnK&md5=22fedd2cb71c8388c897ba1561fe1209CAS |

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. Ecotoxicology and Environmental Safety 72, 2009–2012.
The integrity of lichen cell membrane is a suitable parameter for monitoring early biological effects of acute nitrogen pollution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFGqtLvN&md5=17815b57678821b8d90449a9524b4a2dCAS |

Munzi S, Pisani T, Paoli L, Loppi S (2010) Time- and dose-dependency of the effects of nitrogen pollution on lichens. Ecotoxicology and Environmental Safety 73, 1785–1788.
Time- and dose-dependency of the effects of nitrogen pollution on lichens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Wlsr3M&md5=9fc11588272e9f000007dd854398f6e5CAS |

Munzi S, Loppi S, Cruz C, Branquinho C (2011) Do lichen have ‘memory’ of their native nitrogen environment? Planta 233, 333–342.
Do lichen have ‘memory’ of their native nitrogen environment?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVemu7c%3D&md5=458b82fce2b87ecbc5a6c31b23457dcfCAS |

Pinho P, Dias T, Cruz C, Tang YS, Sutton MA, Martins-Loução MA, Máguas C, Branquinho C (2011) Using lichen functional diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands. Journal of Applied Ecology 48, 1107–1116.
Using lichen functional diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVWjsbrM&md5=fa78a129de6a77bfa86a47b5dccd44f5CAS |

Pirintsos SA, Munzi S, Loppi S, Kotzabasis K (2009) Do polyamines alter the sensitivity of lichens to nitrogen stress? Ecotoxicology and Environmental Safety 72, 1331–1336.
Do polyamines alter the sensitivity of lichens to nitrogen stress?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1Oqs7g%3D&md5=84cfdac67ea5092a5e202e175882105fCAS |

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.
Physiological effects of a geothermal element: boron excess in the epiphytic lichen Xanthoria parietina (L.) Th.Fr.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVaqu74%3D&md5=3ccb7d385f8954524df23d9974a28b1cCAS |

Rhine ED, Sims GK, Mulvaney RL, Pratt EJ (1998) Improving the Berthelot reaction for determining ammonium in soil extracts and water. Soil Science Society of America Journal 62, 473–480.
Improving the Berthelot reaction for determining ammonium in soil extracts and water.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXivF2is74%3D&md5=76e1769690c0474d6f31bcb97a6c2aa6CAS |

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 ‘Atmospheric ammonia – detecting emission changes and environmental impacts’. (Eds MA Sutton, S Reis, SMH Baker) pp. 49–58. (Springer: Berlin)

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

Sparrius LB (2007) Response of epiphytic lichen communities to decreasing ammonia air concentrations in a moderately polluted area of the Netherlands. Environmental Pollution 146, 375–379.
Response of epiphytic lichen communities to decreasing ammonia air concentrations in a moderately polluted area of the Netherlands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit12gsr8%3D&md5=91992ca83f0bf955a263010f0a8fe42cCAS |

Szczerba MW, Britto DT, Ali SA, Balkos KD, Kronzucker HJ (2008) NH4 +-stimulated and -inhibited components of K+ transport in rice (Oryza sativa L.). Journal of Experimental Botany 59, 3415–3423.
NH4 +-stimulated and -inhibited components of K+ transport in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWit7vF&md5=68067b572741f416296266066bd3f3cfCAS |

van Herk CM, Mathijssen-Spiekman EAM, de Zwart D (2003) Long distance nitrogen air pollution effects on lichens in Europe. Lichenologist 35, 347–359.
Long distance nitrogen air pollution effects on lichens in Europe.Crossref | GoogleScholarGoogle Scholar |

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.
Intracellular and extracellular ammonium (NH4+) uptake and its toxic effects on the aquatic biomonitor Fontinalis antipyretica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFegurnP&md5=a9c79d81f915da1f3781a0ce0229d935CAS |