Plant and Soil

, Volume 347, Issue 1–2, pp 363–376

Patterns of nitrate reductase activity vary according to the plant functional group in a Mediterranean maquis

  • Teresa Dias
  • Domingos Neto
  • Maria Amélia Martins-Loução
  • Lucy Sheppard
  • Cristina Cruz
Regular Article


Since little is known about how the Mediterranean Basin ecosystems are affected by nitrogen deposition, we aimed to understand the use of nitrogen by distinct plant functional groups (PFG: summer semi-deciduous and evergreen sclerophylls) present in the Mediterranean maquis in order to assess which may be more affected by changes in nitrogen availability. The availability of soil inorganic nitrogen, leaf nitrate concentrations and nitrate reductase activity (in vivo and in vitro) were measured during the year in three plant species from each PFG. The patterns of in vitro NRA along the shoot and through the day were also determined. Although summer semi deciduous species occupied soil patches richer in nitrate, their leaf NRA were significantly lower than that of evergreen sclerophylls species. The pattern of nitrate and ammonium availabilities along the year also distinguished the PFG. Results show that each PFG is composed of a number of physiologically similar species. Patterns of NRA varied according to the PFG, which may represent distinct specializations of co-occurring species to access nitrogen. Therefore, the NRA can be used as an indicator of the nitrate availability taking into consideration the time of the year, the plant species and its PFG.


Mediterranean Plant functional groups Nitrate Ammonium Pattern of nitrate reductase activity Nitrogen strategies 


  1. Arslan H, Güleryüz G (2005) A study on nitrate reductase activity (NRA) of geophytes from Mediterranean environment. Flora 200:434–443Google Scholar
  2. Arslan H, Kirmizi S, Sakar S, Güleryüz G (2009) Nitrate reductase activity (NRA) in some shrub species from Mediterranean Environment. Ekoloji 18:49–56CrossRefGoogle Scholar
  3. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59PubMedCrossRefGoogle Scholar
  4. Canadell J, Jackson RB, Ehleringer JR, Mooney HA, Sala OE, Schulze ED (1996) Maximum rooting depth of vegetation types at the global scale. Oecologia 108:583–595CrossRefGoogle Scholar
  5. Cardinale BJ, Wright JP, Cadotte MW, Carroll IT, Hector A, Srivastava DS, Loreau M, Weis JJ (2007) Impacts of plant diversity on biomass production increase through time because of species complementarity. PNAS 104:18123–18128PubMedCrossRefGoogle Scholar
  6. Chapin FS III, Matson PA, Mooney HA (2002) Principles of terrestrial ecosystem ecology. Springer, United States of AmericaGoogle Scholar
  7. Correia OA (1988) Contribuição da fenologia e ecofisiologia em estudos da sucessão e dinâmica da vegetação mediterrânica. Dissertation, Universidade de LisboaGoogle Scholar
  8. Cowling RM, Rundel PW, Lamont BB, Arroyo MK, Arianoutsou M (1996) Plant diversity in Mediterranean-climate regions. Tree 11:362–366PubMedGoogle Scholar
  9. Craine JM (2009) Resource strategies of wild plants. Princeton University PressGoogle Scholar
  10. Cruz C, Martins-Loução MA (2000) Nitrogen in a sustainable environment: a matter of integration. In: Martins-Loução MA, Lips SH (eds) Nitrogen in a sustainable ecosystem. Backhuys, The Netherlands, pp 415–419Google Scholar
  11. Cruz C, Dias T, Matos S, Tavares A, Neto D, Martins-Loução MA (2003) Nitrogen availability and plant cover: the importance of nitrogen pools. In: Tiezzi E, Brebbia CA, Usó JL (eds) Ecosystems and sustainable development IV. WIT Press, Southampton, Boston, pp 123–135Google Scholar
  12. Cruz C, Bio AMF, Jullioti A, Dias T, Martins-Loução MA (2008) Heterogeneity of soil surface ammonium concentration and other characteristics, related to plant specific variability in a Mediterranean-type ecosystem. Environ Pollut 154:414–423PubMedCrossRefGoogle Scholar
  13. Dias T, Malveiro S, Martins-Loução MA, Sheppard LJ, Cruz C (2011) Linking N-driven biodiversity changes with soil N availability in a Mediterranean ecosystem. Plant Soil 341:125–136CrossRefGoogle Scholar
  14. EMEP (2008) European Monitoring and Evaluation ProgrammeGoogle Scholar
  15. Emmett BA (2007) Nitrogen saturation of terrestrial ecosystems: some recent findings and their implications for our conceptual framework. Water Air Soil Pollut 7:99–109CrossRefGoogle Scholar
  16. Fitter AH, Hay RKM (2002) Environmental physiology of plants. Academic, San DiegoGoogle Scholar
  17. Foyer CH, Valadier M-H, Migge A, Becker TW (1998) Drought-induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiol 117:283–292PubMedCrossRefGoogle Scholar
  18. Gallardo A, Paramá R, Covelo F (2006) Differences between soil ammonium and nitrate spatial pattern in six plant communites. Simulated effect on plant populations. Plant Soil 279:333–346CrossRefGoogle Scholar
  19. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Towsend AR, Vorosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226CrossRefGoogle Scholar
  20. Gebauer G, Melzer A, Rehder H (1984) Nitrate content and nitrate reductase activity in Rumex obtusifolius L. I. Differences in organs and diurnal changes. Oecologia 63:136–142CrossRefGoogle Scholar
  21. Gratani L, Bombelli A (2000) Correlation between leaf age and other leaf traits in three Mediterranean maquis shrub species: Quercus ilex, Phillyrea latifolia and Cistus incanus. Environ Exp Bot 43:141–153CrossRefGoogle Scholar
  22. Gruber N, Galloway JN (2008) An Earth-system perspective of the global nitrogen cycle. Nature 451:293–296PubMedCrossRefGoogle Scholar
  23. Hageman RH, Hucklesby DP (1971) Nitrate reductase from higher plants. In: San Pietro A (ed) Methods in enzimology. Academic, London-New York, pp 491–503Google Scholar
  24. Havill DC, Lee JA, Stewart GR (1974) Nitrate utilization by species from acidic and calcareous soils. New Phytol 73:1221–1231CrossRefGoogle Scholar
  25. Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecol 87:1244–1255CrossRefGoogle Scholar
  26. Kaiser WM, Huber SC (2001) Post-translational regulation of nitrate reductase: mechanism, physiological relevance and environmental triggers. J Exp Bot 52:1981–1989PubMedCrossRefGoogle Scholar
  27. Kaiser WM, Spill D (1991) Rapid modulation of spinach leaf nitrate reductase by photosynthesis II. In vitro modulation by ATP and AMP. Plant Physiol 96:368–375PubMedCrossRefGoogle Scholar
  28. Kaiser WM, Kandlbinder A, Stoimenova M, Glaab J (2000) Discrepancy between nitrate reduction rates in intact leaves and nitrate reductase activity in leaf extracts: what limits nitrate reduction in situ? Planta 210:801–807PubMedCrossRefGoogle Scholar
  29. Kaiser WM, Weiner H, Kandlbinder A, Tsai C-B, Rockel P, Sonoda M, Planchet E (2002) Modulation of nitrate reductase: some new insights, an unusual case and a potentially important side reaction. J Exp Bot 53:875–882PubMedCrossRefGoogle Scholar
  30. Karavatas S, Manetas Y (1999) Seasonal patterns of photosystem 2 photochemical efficiency in evergreen sclerophylls and drought semi-deciduous shrubs under Mediterranean field conditions. Photosynthetica 36:41–49CrossRefGoogle Scholar
  31. Kummerow J (1973) Comparative anatomy of sclerophylls of Mediterranean climatic areas. In: diCastri F, Mooney HA (eds) Mediterranean type ecosystems: origin and structure. Springer Verlag, Berlin, pp 157–167Google Scholar
  32. Lee JA, Stewart GR (1978) Ecological aspects of nitrogen metabolism. Adv Bot Res 6:1–43CrossRefGoogle Scholar
  33. Lloret F, Casanovas C, Peñuelas J (1999) Seedling survival of Mediterranean shrubland species in relation to root: shoot ratio, seed size and water and nitrogen use. Funct Ecol 13:210–216CrossRefGoogle Scholar
  34. Maestre FT, Reynolds JF (2006) Spatial heterogeneity in soil nutrient supply modulates nutrient and biomass responses to multiple global change drivers in model grassland communities. Glob Chang Biol 12:2431–2441CrossRefGoogle Scholar
  35. Matsumura S, Witjaksono G (1999) Modification of the Cataldo method for the determination of nitrate in soil extracts by potassium chloride. Soil Sci Plant Nutr 45:231–235Google Scholar
  36. Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M (2001a) The immediate cause of the diurnal changes of nitrogen metabolism in leaves of nitrate-replete tobacco: a major imbalance between the rate of nitrate reduction and the rates of nitrate uptake and ammonium metabolism during the first part of the light period. Plant Cell Environ 24:177–190CrossRefGoogle Scholar
  37. Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M (2001b) Elevated carbon dioxide increases nitrate uptake and nitrate reductase activity when tobacco is growing on nitrate, but increases ammonium uptake and inhibits nitrate reductase activity when tobacco is growing on ammonium nitrate. Plant Cell Environ 24:1119–1137CrossRefGoogle Scholar
  38. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185PubMedCrossRefGoogle Scholar
  39. Montès N, Maestre F, Ballini C, Baldy V, Gauquelin T, Planquette M, Greff S, Dupouyet S, Perret J-B (2008) On the relative importance of the effects of selection and complementarity of diversity-productivity relationships in Mediterranean shrublands. Oikos 117:1345–1350CrossRefGoogle Scholar
  40. Naeem S (2009) Gini in the bottle. Nature 458:579–580PubMedCrossRefGoogle Scholar
  41. Oaks A, Aslam M, Boesel I (1977) Ammonium and amino acids as regulators of nitrate reductase in corn roots. Plant Physiol 59:391–394PubMedCrossRefGoogle Scholar
  42. Ochoa-Hueso R, Allen EB, Branquinho C, Cruz C, Dias T, Fenn ME, Manrique E, Perez-Corona ME, Sheppard LJ, Stock WD (2011) Nitrogen effects on Mediterranean-type ecosystems: an ecological assessment. Environ Pollut In pressGoogle Scholar
  43. Oliveira G, Peñuelas J (2004) The effect of winter cold stress on photosynthesis and photochemical efficiency of PSII of two Mediterranean woody species—Cistus albidus and Quercus ilex. Plant Ecol 175:179–191CrossRefGoogle Scholar
  44. Orebamjo TO, Stewart GR (1975) Ammonium repression of nitrate reductase formation in Lemna minor L. Planta 122:27–36CrossRefGoogle Scholar
  45. Phoenix GK, Hicks WK, Cinderby S, Kuylenstierna JCI, Stock WD, Dentener FJ, Giller KE, Austin AT, Lefroy RDB, Gimeno BS, Ashmore MR, Ineson P (2006) Atmospheric nitrogen deposition in world biodiversity hotspots: the need for a greater global perspective in assessing N deposition impacts. Glob Chang Biol 12:470–476CrossRefGoogle Scholar
  46. Pinho P, Branquinho C, Cruz C, Tang S, Dias T, Rosa AP, Máguas C, Martins-Loução MA, Sutton MA (2009) Assessment of critical levels of atmospheric ammonia for lichen diversity in a cork-oak woodland, Portugal. In: Sutton MA, Reis S, Baker S (eds) Atmospheric Ammonia. Springer, pp 109–120Google Scholar
  47. Pinho P, Dias T, Cruz C, Tang S, Sutton MA, Martins-Loução MA, Máguas C, Branquinho C (2011) Using lichen functional-diversity to assess the effects of atmospheric ammonia in Mediterranean woodlands. J Appl Ecol In pressGoogle Scholar
  48. Poorter H, van de Vijver CADM, Boot RGA, Lambers H (1995) Growth and carbon economy of a fast-growing and a slow-growing grass species as dependent on nitrate supply. Plant Soil 171:217–227CrossRefGoogle Scholar
  49. Rockström J, Steffen W, Noone K, Persson A, Chapin FS III, Lambin EF, Lenton T, Scheffer M, Folke C, Schellnhuber HJ, Nykvist B, de Wit CA, Hughes T, van der Leeuw S, Rodhe H, Sörlin S, Snyder PK, Costanza R, Svedin U, Falkenmark M, Karlberg L, Corell RW, Fabry VJ, Hansen J, Walker B, Leiverman D, Richardson K, Crutzen P, Foley JA (2009) A safe operating space for humanity. Nature 461:472–475PubMedCrossRefGoogle Scholar
  50. Rutigliano FA, Castaldi S, D'Ascoli R, Papa S, Carfora A, Marzaioli R, Fioretto A (2009) Soil activities related to nitrogen cycle under three plant cover types in Mediterranean environment. Appl Soil Ecol 43:40–46CrossRefGoogle Scholar
  51. Sakar FS, Arslan H, Kirmizi S, Güleryüz G (2010) Nitrate reductase activity (NRA) in Asphodelus aestivus Brot. (Liliaceae): distribution among organs, seasonal variation and differences among populations. Flora 205:527–531Google Scholar
  52. Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Sci 287:1770–1774CrossRefGoogle Scholar
  53. Valladares F, Gianoli R (2007) How much ecology do we need to know to restore Mediterranean ecosystems? Restor Ecol 15:363–368CrossRefGoogle Scholar
  54. Werner C, Correia O, Beyschlag W (1999) Two different strategies of Mediterranean macchia plants to avoid photoinhibitory damage by excessive radiation levels during summer drought. Acta Oecologica 20:15–23CrossRefGoogle Scholar
  55. Werner C, Ryel RJ, Correia O, Beyschlag W (2001) Effects of photoinhibition on whole-plant carbon gain assessed with a photosynthesis model. Plant Cell Environ 24:27–40CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Teresa Dias
    • 1
  • Domingos Neto
    • 1
    • 2
  • Maria Amélia Martins-Loução
    • 1
  • Lucy Sheppard
    • 3
  • Cristina Cruz
    • 1
  1. 1.Faculdade de Ciências, Centro de Biologia Ambiental (CBA)Universidade de LisboaLisboaPortugal
  2. 2.Universidade Agostinho NetoLuandaAngola
  3. 3.Centre of Ecology and Hydrology (CEH)PenicuikUK

Personalised recommendations