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Plant function and evolutionary biology
RESEARCH ARTICLE

Seasonal changes in optically assessed epidermal phenolic compounds and chlorophyll contents in leaves of sessile oak (Quercus petraea): towards signatures of phenological stage

Juliette Louis A , Sylvie Meyer A D , Florence Maunoury-Danger A B , Chantal Fresneau A , Emmanuelle Meudec C and Zoran G. Cerovic A
+ Author Affiliations
- Author Affiliations

A Université Paris-Sud, Laboratoire Ecologie, Systématique et Evolution, UMR 8079, Orsay Cedex, F-91405; CNRS, Orsay Cedex, F-91405; AgroParisTech, Paris, F-75231, France.

B UMR 7618 – Université Paris-Diderot – Laboratoire Bioemco (Biogéochimie et écologie des milieux continentaux). Ecole Normale Supérieure, 46 rue d’Ulm, F-75230 Paris Cedex 05, France.

C UMR 1083 Sciences pour l’œnologie, Plate-forme Polyphénols, INRA, Université Montpellier 1, F-34000 Montpellier, France.

D Corresponding author. Email: sylvie.meyer@u-psud.fr

Functional Plant Biology 36(8) 732-741 https://doi.org/10.1071/FP09010
Submitted: 10 January 2009  Accepted: 22 June 2009   Published: 23 July 2009

Abstract

Seasonal patterns of dry mass invested in chlorophyll and epidermal phenolic compounds (EPhen) were investigated in vivo using optical methods, in leaves of 2-year-old oaks (Quercus petraea Matt. (Liebl.)) grown under semi-controlled conditions. The plasticity of the seasonal pattern was investigated by applying stem girdling treatment. In control young expanding leaves, leaf dry mass per area, dry mass investment in chlorophyll and abaxial EPhen content increased. In late May, at leaf maturity, these variables reached a plateau, and adaxial and abaxial EPhen contents became similar. Thereafter, as leaves aged, dry mass investment in chlorophyll gradually decreased, whereas it remained steady for EPhen. Girdling treatment impacted this seasonal pattern differently depending on the phenological stage. Treatment effects and their reversion revealed in vivo EPhen turnover. Finally, optical signatures of immature and mature leaf phenological stages with contrasting nitrogen and carbon economy were proposed, based on the relationship between the chlorophyll to EPhen ratio and the leaf nitrogen to carbon ratio.

Additional keywords: Dualex, girdling, leaf age, LMA, nitrogen, polyphenols, SPAD, UV absorption.


Acknowledgements

This work was supported by the CNRS, the company FORCE-A, and the Essonne country through the project ASTRE. We thank Claire Bouchut (laboratory ‘Science pour l’oenologie’, Montpellier, France) for technical assistance in HPLC analysis. We are grateful to Dr Gérard Lacroix (Laboratoire Bioemco, ENS, France), Dr Michael Danger (Laboratoire Bioemco, ENS, France), Marine Le Moigne (Force-A, Université Paris Sud, France) and Dr Erwin Dreyer (Ecologie et Ecophysiologie forestières, INRA-UHP1137, France) for very helpful comments on the manuscript. American Journal Experts (Durham, USA) reviewed the paper for English usage.


References


Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytologist 164, 157–164.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bacilieri R, Ducousso A, Petit RJ, Kremer A (1996) Mating system and asymmetric hybridization in a mixed stand of European oaks. Evolution 50, 900–908.
Crossref | GoogleScholarGoogle Scholar | open url image1

Barthod S, Cerovic Z, Epron D (2007) Can dual chlorophyll fluorescence excitation be used to assess the variation in the content of UV-absorbing phenolic compounds in leaves of temperate tree species along a light gradient? Journal of Experimental Botany 58, 1753–1760.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Barz W , Köster J (1981) Turnover and degradation of secondary (natural) products. In ‘The biochemistry of plant’. (Eds PK Stumpf, EE Conn), pp. 35–85. (Academic Press Inc.: London)

Bidel LPR, Meyer S, Goulas Y, Cadot Y, Cerovic ZG (2007) Responses of epidermal phenolic compounds to light acclimation: in vivo qualitative and quantitative assessment using chlorophyll fluorescence excitation spectra in leaves of three woody species. Journal of Photochemistry and Photobiology. B, Biology 88, 163–179.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Bilger W, Veit M, Schreiber L, Schreiber U (1997) Measurement of leaf epidermal transmittance of UV radiation by chlorophyll fluorescence. Physiologia Plantarum 101, 754–763.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Bilger W, Johnsen T, Schreiber U (2001) UV-excited chlorophyll fluorescence as a tool for the assessment of UV-protection by the epidermis of plants. Journal of Experimental Botany 52, 2007–2014.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Cartelat A, Cerovic ZG, Goulas Y, Meyer S, Lelarge C , et al . (2005) Optically assessed contents of leaf polyphenolics and chlorophyll as indicators of nitrogen deficiency in wheat (Triticum aestivum L.). Field Crops Research 91, 35–49.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cerovic ZG, Ounis A, Cartelat A, Latouche G, Goulas Y, Meyer S, Moya I (2002) The use of chlorophyll fluorescence excitation spectra for the non-destructive in situ assessment of UV-absorbing compounds in leaves. Plant, Cell & Environment 25, 1663–1676.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Cerovic ZG, Moise N, Agati G, Latouche G, Ben Ghozlen N, Meyer S (2008) New portable sensors for the assessment of winegrape phenolic maturity based on berry fluorescence. Journal of Food Composition and Analysis 21, 650–654.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Corp LA, McMurtrey JE, Middleton EM, Mulchi CM, Chappelle EW, Daughtry CST (2003) Fluorescence sensing systems: in vivo detection of biophysical variations in field corn due to nitrogen supply. Remote Sensing of Environment 86, 470–479.
Crossref | GoogleScholarGoogle Scholar | open url image1

Demotes-Mainard S, Boumaza R, Meyer S, Cerovic ZG (2008) Indicators of nitrogen status for ornamental woody plants based on optical measurements of leaf epidermal polyphenol and chlorophyll contents. Scientia Horticulturae 115, 377–385.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Evans JP (1989) Partitioning of nitrogen between and within leaves grown under different irradiances. Australian Journal of Plant Physiology 16, 533–548.
Crossref | GoogleScholarGoogle Scholar | open url image1

Goldschmidt EE, Huber SC (1992) Regulation of photosynthesis by end-product accumulation in leaves of plants storing starch, sucrose, and hexose sugars. Plant Physiology 99, 1443–1448.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Goulas Y, Cerovic ZG, Cartelat A, Moya I (2004) Dualex: a new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence. Applied Optics 43, 4488–4496.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. The Quarterly Review of Biology 67, 283–335.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hughes NM, Morley CB, Smith WK (2007) Coordination of anthocyanin decline and photosynthetic maturation in juvenile leaves of three deciduous tree species. New Phytologist 175, 675–685.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Iglesias DJ, Lliso I, Tadeo FR, Talon M (2002) Regulation of photosynthesis through source: sink imbalance in Citrus is mediated by carbohydrate content in leaves. Physiologia Plantarum 116, 563–572.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Jones CG, Hartley SE (1999) A protein competition model of phenolic allocation. Oikos 86, 27–44.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Kleiner KW, Raffa KF, Dickson RE (1999) Partitioning of 14C-labeled photosynthate to allelochemicals and primary metabolites in source and sink leaves of aspen: evidence for secondary metabolite turnover. Oecologia 119, 408–418.
Crossref | GoogleScholarGoogle Scholar | open url image1

Krizek DT, Kramer GF, Upadhyaya A, Mirecki RM (1993) UV-B response of cucumber seedlings grown under metal halide and high pressure sodium/deluxe lamps. Physiologia Plantarum 88, 350–358.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Layne DR, Flore JA (1995) End-product inhibition of photosynthesis in Prunus cerasus L. in response to whole-plant source–sink manipulation. Journal of the American Society for Horticultural Science 120, 583–599. open url image1

le Maire G, François C, Dufrêne E (2004) Towards universal broad leaf chlorophyll indices using PROSPECT simulated database and hyperspectral reflectance measurements. Remote Sensing of Environment 89, 1–28.
Crossref | GoogleScholarGoogle Scholar | open url image1

Markwell J, Osterman JC, Mitchell JL (1995) Calibration of the Minolta SPAD-502 leaf chlorophyll meter. Photosynthesis Research 46, 467–472.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Maunoury-Danger F (2007) Etude de la signature isotopique du carbone (δ13C) du CO2 respiré et du cerne en relation avec le fonctionnement de l’arbre. Thèse de doctorat, Université Paris-Sud.

Meyer S, Cerovic ZG, Goulas Y, Montpied P, Demotes-Mainard S, Bidel LPR, Moya I, Dreyer E (2006) Relationships between optically assessed polyphenols and chlorophyll contents, and leaf mass per area ratio in woody plants: a signature of the carbon-nitrogen balance within leaves? Plant, Cell & Environment 29, 1338–1348.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Niinemets U, Kull O, Tenhunen JD (2004) Within-canopy variation in the rate of development of photosynthetic capacity is proportional to integrated quantum flux density in temperate deciduous trees. Plant, Cell & Environment 27, 293–313.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Paul MJ, Pellny TK (2003) Carbon metabolite feedback regulation of leaf photosynthesis and development. Journal of Experimental Botany 54, 539–547.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents – verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochimica et Biophysica Acta 975, 384–394.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Reich PB, Walters MB, Ellsworth DS (1991) Leaf age and season influence the relationships between leaf nitrogen, leaf mass per area and photosynthesis in maple and oak trees. Plant, Cell & Environment 14, 251–259.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salminen JP, Roslin T, Karonen M, Sinkkonen J, Pihlaja K, Pulkkinen P (2004) Seasonal variation in the content of hydrolyzable tannins, flavonoid glycosides, and proanthocyanidins in oak leaves. Journal of Chemical Ecology 30, 1693–1711.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Schultz JC, Nothnagle PJ, Baldwin IT (1982) Seasonal and individual variation in leaf quality of two northern hardwoods tree species. American Journal of Botany 69, 753–759.
Crossref | GoogleScholarGoogle Scholar | open url image1

Turgeon R (1989) The sink–source transition in leaves. Annual Review of Plant Physiology and Plant Molecular Biology 40, 119–138.
Crossref | GoogleScholarGoogle Scholar | open url image1

Urban L, Alphonsout L (2007) Girdling decreases photosynthetic electron fluxes and induces sustained photoprotection in mango leaves. Tree Physiology 27, 345–352.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wink M (1999) Function of plant secondary metabolites and their exploitation in biotechnology. In ‘Annual plant reviews’. (Ed. M Wink), pp. 1–15. (Academic Press: CRC Press Sheffield)

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z , et al . (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1