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Nitrogen resorption in Acer platanoides and Acer saccharum: influence of light exposure and leaf pigmentation

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Abstract

We investigated the effects of leaf color change in the fall on photosynthetic production and nitrogen resorption. Seedlings of Acer platanoides L. and A. saccharum Marsh. were grown in a shade house for 5 months in either 21 % (intermediate light, M) or 4.9 % (low light, L) of incident irradiance. After this period, a subset of the intermediate-light grown seedlings was transferred to a high-light stress treatment (H). Gas exchange, chlorophyll fluorescence, pigments, antioxidant activity, and nitrogen (N) resorption were examined at three leaf senescence stages during September and October. Our results show that plants of both species produce more anthocyanins in the H treatment. In comparison with plants grown in the L and M treatments, plants of both species in the H treatments had lower chlorophyll, carotenoid and chlorophyll fluorescence parameters (F v/F m, Φ PSII, NPQ and ETR) at the third sampling date (October 12–18), and indicating higher levels of photoinhibition in the seedlings exposed to high light. Our results imply that autumn leaf redness is inducible and closely linked to photo-oxidative stress. However, anthocyanins did not enhance antioxidant capacity in red leaves in either species, when exposed to high light. For both species, our results showed a higher N-resorption for high-light stressed plants. We also observed that the number of abscised leaves at the second sampling dates (September 10) was higher than at the third sampling dates. The intra-leaf distribution of anthocyanin, the association between anthocyanin production and the high-light environments, the retention of red leaves, the substantial physiological gain of photosynthetic activity, as well as the links between anthocyanins and increased N resorption led us to assume that one primary role of autumn anthocyanin could be to protect the photosynthetic apparatus from photo-oxidative damage as light filters rather than as antioxidant. Another major role is to extend carbon capture and help supply the energy needed for N resorption from senescing leaves in both A. saccharum and A. Platanoides during high-light stress. Nevertheless, photoprotective capacity of anthocyanins was not able to fully compensate for photoinhibitory stress as the anthocyanins are not optimally located to efficiently reduce light within the leaves.

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Abbreviations

A sat :

Photosynthetic rates at saturating irradiance

Chl:

Chlorophyll

Φ PSII :

Effective PSII quantum yield

ETR:

Electron transport rate

F v/F m :

Maximal PSII quantum yield

IC50 :

Free radical scavenging activity

NPQ:

Non-photochemical quenching

qP:

Coefficient of photochemical quenching

References

  • Ackerly DD (1999) Self-shading, carbon gain and leaf dynamics: a test of alternative optimality models. Oecologia 119:300–310

    Article  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Archetti M (2009) Classification of hypotheses on the evolution of autumn colours. Oikos 118:328–333

    Article  Google Scholar 

  • Björkman O, Demmig B (1987) Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta 170:489–504

    Article  PubMed  Google Scholar 

  • Chapin FS, Kedrowski RA (1983) Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology 64:376–391

    Article  CAS  Google Scholar 

  • Chapin FS, Moilanen L (1991) Nutritional controls over nitrogen and phosphorus resorption from Alaskan birch leaves. Ecology 72:709–715

    Article  Google Scholar 

  • Esteban R, Fernández-Marín B, Becerril JM, García-Plazaola JI (2008) Photoprotective implications of leaf variegation in E. dens-canis L. and P. officinalis L. J Plant Physiol 165:1255–1263

    Article  PubMed  CAS  Google Scholar 

  • Feild TS, Lee DW, Holbrook NM (2001) Why leaves turn red in autumn. The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiol 127:566–574

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Feng YL, Lei YB, Wang RF, Callaway RM, Valiente-Banuet A et al (2009) Evolutionary tradeoffs for nitrogen allocation to photosynthesis versus cell walls in an invasive plant. PNAS USA 106:1853–1856

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Field C (1983) Allocating leaf nitrogen for the maximization of carbon gain: leaf age as a control on the allocation program. Oecologia 56:341–347

    Article  Google Scholar 

  • Fujiki T, Suzue T, Kimoto H, Saino T (2007) Photosynthetic electron transport in Dunaliella tertiolecta (Chlorophyceae) measured by fast repetition rate fluorometry: relation to carbon assimilation. J Plankton Res 29:199–208

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gielen B, Löw M, Deckmyn G, Metzger U, Franck F et al (2007) Chronic ozone exposure affects leaf senescence of adult beech trees: a chlorophyll fluorescence approach. J Exp Bot 58:785–795

    Article  PubMed  CAS  Google Scholar 

  • Gould KS, Vogelmann TC, Han T, Clearwater MJ (2002) Profiles of photosynthesis within red and green leaves of Quintinia serrata A. Cunn Physi Plant 116:127–133

    Article  CAS  Google Scholar 

  • Grizzard T, Henderson GS, Clebsch EEC, Reichle DE (1976) Seasonal nutrient dynamics of foliage and litterfall on Walker Branch, a deciduous forest ecosystem. ORNL/TM-5254, Oak Ridge National Laboratory, Oak Ridge

  • Hoch WA, Singsaas EL, McCown BH (2003) Resorption protection. Anthocyanins facilitate nutrient recovery in autumn by shielding leaves from potentially damaging light levels. Plant Physiol 133:1296–1305

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hoch WA, Zeldin EL, McCown BH (2001) Physiological significance of anthocyanins during autumnal leaf senescence. Tree Physiol 21:1–8

    Article  PubMed  CAS  Google Scholar 

  • Hughes NM, Neufeld HS, Burkey KO (2005) Functional role of anthocyanins in high-light winter leaves of the evergreen herb Galax urceolata. New Phytol 168:575–587

    Article  PubMed  CAS  Google Scholar 

  • Ishikura N (1973) The changes in anthocyanin and chlorophyll content during the autumnal reddening of leaves. Kumamoto J Sci Biol 11:43–50

    CAS  Google Scholar 

  • Kolb TE, McCormick LH (1993) Etiology of sugar maple decline in four Pennsylvania stands. Can J For Res 23:2395–2402

    Article  Google Scholar 

  • Kozlowski TT, Pallardy SD (1997) Physiology of woody plants. Academic Press, New York

    Google Scholar 

  • Lee DW, O’ Keefe J, Holbrook NM, Feild TS (2003) Pigment dynamics and autumn leaf senescence in a New England deciduous forest, eastern USA. Ecol Res 18:677–694

    Article  CAS  Google Scholar 

  • Lepeduš H, Gaća V, Viljevac M, Kovač S, Fulgosi H, Simić D, Jurković V, Cesar V (2011) Changes in photosynthetic performance and antioxidative strategies during maturation of Norway maple (Acer platanoides L.) leaves. Plant Physiol Bioch 49:368–376

    Article  Google Scholar 

  • Lev-Yadun S, Holopainen JK (2009) Why red-dominated autumn leaves in America and yellow-dominated autumn leaves in Northern Europe? New Phytol 183:497–501

    Article  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current protocols in food analytical chemistry. Wiley, New York, pp 431–438

    Google Scholar 

  • Lu C, Zhang J (1998) Modifications in photosystem II photochemistry in senescent leaves of maize plants. J Exp Bot 49:1671–1679

    Article  CAS  Google Scholar 

  • Matile P, Hörtensteiner S, Thomas H (1999) Chlorophyll degradation. Annu Rev Plant Physiol Plant Mol Biol 50:67–95

    Article  PubMed  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–668

    Article  PubMed  CAS  Google Scholar 

  • May JD, Killingbeck KT (1992) Effects of preventing nutrient resorption on plant fitness and foliar nutrient dynamics. Ecology 73:1868–1878

    Article  Google Scholar 

  • McGrath R (1972) Protein measurement by ninhydrin determination of amino acids released by alkaline hydrolysis. Anal Chem 49:95–102

    CAS  Google Scholar 

  • Mitchell AK (1998) Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–757

    Article  PubMed  Google Scholar 

  • Miyazawa Y, Yahata H (2006) Is the parameter electron transport rate useful as a predictor of photosynthetic carbon assimilation rate? Bull Inst Trop Agr Kyushu Univ 29:39–53

    Google Scholar 

  • Murray JR, Hackett WP (1991) Dihydroflavonol reductase activity in relation to differential anthocyanin accumulation in juvenile and mature phase Hedera helix L. Plant Physiol 97:343–351

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Paquette A, Fontaine B, Berninger F, Dubois K, Lechowicz MJ, Messier C, Posada JM, Valladares F, Brisson J (2012) Norway maple displays greater seasonal growth and phenotypic plasticity to light than native sugar maple. Tree Physiol 32:1339–1347

    Article  PubMed  CAS  Google Scholar 

  • Paquette A, Fontaine B, Messier C, Brisson J (2010) Homogeneous light regime in shade-house experiment overestimates carbon gains in Norway maple seedlings. J Hortic For 2:117–121

    Google Scholar 

  • Park YI, Chow WS, Osmond CB, Anderson JM (1996) Electron transport to oxygen mitigates against the photoinactivation of Photosystem II in vivo. Photosynth Res 50:23–32

    Article  PubMed  CAS  Google Scholar 

  • Perron MC, Juneau P (2011) Effect of endocrine disrupters on photosystem II energy fluxes of green algae and cyanobacteria. Environ Res 111:520–529

    Article  PubMed  CAS  Google Scholar 

  • Pietrini F, Iannelli MA, Massacci A (2002) Anthocyanin accumulation in the illuminated surface of maize leaves enhances protection from photo-inhibitory risks at low temperature, without further limitation to photosynthesis. Plant, Cell Environ 25:1251–1259

    Article  CAS  Google Scholar 

  • Sanz-Pérez V, Pilar Castro-Díez P, Millard P (2009) Effects of drought and shade on nitrogen cycling in the leaves and canopy of Mediterranean Quercus seedlings. Plant Soil 316:45–56

    Article  Google Scholar 

  • Schaberg PG, Murakami PF, Turner MR, Heitz HK, Hawley GJ (2008) Association of red coloration with senescence of sugar maple leaves in autumn. Trees 22:573–578

    Article  CAS  Google Scholar 

  • Schaberg PG, van den Berg AK, Murakami PF, Shane JB, Donnelly JR (2003) Factors influencing red expression in autumn foliage of sugar maple trees. Tree Physiol 23:325–333

    Article  PubMed  CAS  Google Scholar 

  • Takashima T, Hikosaka K, Hirose T (2004) Photosynthesis or persistence: nitrogen allocation in leaves of evergreen and deciduous Quercus species. Plant, Cell Environ 27:1047–1054

    Article  CAS  Google Scholar 

  • van den Berg AK, Perkins TD (2007) Contribution of anthocyanins to the antioxidant capacity of juvenile and senescing sugar maple (Acer saccharum) leaves. Funct Plant Biol 34:714–719

    Article  Google Scholar 

  • van den Berg AK, Vogelmann TC, Perkins TD (2009) Anthocyanin influence on light absorption within juvenile and senescing sugar maple leaves —do anthocyanins function as photoprotective visible light screens? Funct Plant Biol 36:793–800

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monographs 82:205–220

    Article  Google Scholar 

  • Walters MB, Reich PB (1997) Growth of Acer saccharum seedlings in deeply shaded understories of northern Wisconsin: effects of nitrogen and water availability. Can J Forest Res 27:237–247

    Article  Google Scholar 

  • Wingler A, Masclaux-Daubresse C, Fischer AM (2009) Sugars, senescence, and ageing in plants and heterotrophic organisms. J Exp Bot 60:1063–1066

    Article  PubMed  CAS  Google Scholar 

  • Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57:391–399

    Article  PubMed  CAS  Google Scholar 

  • Yasumura Y, Onoda Y, Hikosaka K, Hirose T (2005) Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species. Plant Ecol 178:29–37

    Article  Google Scholar 

  • Zeliou K, Manetas Y, Petropoulou Y (2009) Transient winter leaf reddening in Cistus creticus characterizes weak (stress-sensitive) individuals, yet anthocyanins cannot alleviate the adverse effects on photosynthesis. J Exp Bot 60:3031–3042

    Article  PubMed  CAS  PubMed Central  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge funding by the Fonds québécois de la recherche sur la nature et les technologies (FQRNT) and the Youth Talent Team Program of the Institute of Mountain Hazards and Environment, CAS (SDSQB-2012-01). We also thank the Montreal Botanical Garden for providing the space necessary for this experiment.

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Author notes

  1. Frank Berninger

    Present address: Department of Forest Sciences, University of Helsinki, PL 27, 00014, Helsinki, Finland

Authors and Affiliations

  1. Département des sciences biologiques, Université du Québec à Montréal, C.P. 8888 Succ. Centre-ville, Montréal, QC, H3C 3P8, Canada

    Baoli Duan, Philippe Juneau & Frank Berninger

  2. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, 610041, China

    Baoli Duan

  3. Center for Forest Research (CFR), Université du Québec à Montréal, C.P. 8888 Succ. Centre-ville, Montréal, QC, H3C 3P8, Canada

    Alain Paquette, Jacques Brisson & Frank Berninger

  4. Institut de recherche en biologie végétale, Département de sciences biologiques, Université de Montréal, 4101 East, Sherbrooke St, Montréal, QC, H1X 2B2, Canada

    Jacques Brisson & Bastien Fontaine

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  1. Baoli Duan
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Correspondence to Baoli Duan.

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Communicated by S. Renault.

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Duan, B., Paquette, A., Juneau, P. et al. Nitrogen resorption in Acer platanoides and Acer saccharum: influence of light exposure and leaf pigmentation. Acta Physiol Plant 36, 3039–3050 (2014). https://doi.org/10.1007/s11738-014-1674-x

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