Abstract
Morphological, anatomical and physiological traits of Rhamnus alaternus during leaf expansion were analysed. Bud break occurred when mean air temperature was 14.1 ± 1.2°C, and it was immediately followed by the increase of leaf area and leaf dry mass. The highest leaf expansion rates happened during the first 22 days of the process. Leaf area and leaf dry mass reached the steady-state value 46 and 62 days after bud break, respectively. Net photosynthesis increased from bud break to full leaf expansion, and total chlorophyll content had the same trend, confirmed by the correlation between the two variables. Leaf dark respiration peaked during the first 11 days of leaf expansion, then decreased and reached a steady-state value 34 days after bud break. R. alaternus completed cell division and cell enlargement of the epidermal tissue 28 days after bud break, and the ones of the mesophyll tissue at full leaf expansion. The results underline that morphological, anatomical and physiological leaf traits in R. alaternus are indicative of a less sclerophyllous species (i.e. higher specific leaf area) compared with other Mediterranean evergreen species. Moreover, the higher fraction of mesophyll volume occupied by the intercellular air spaces, and the ability to end the leaf expansion process before air temperature might be a limiting factor, makes R. alaternus closer to the mesophyte species.
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Armstrong AF, Logan DC, Atkin OK (2006) On the developmental dependence of leaf respiration: responses to short- and long-term changes in growth temperature. Am J Bot 93:1633–1639
Atkin OK, Evans JR, Ball MC, Siebke K (1998a) Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment. Aust J Plant Physiol 25:437–443
Atkin OK, Evan JR, Ball MC, Siebke K, Pons TL, Lambers H (1998b) Light inhibition of leaf respiration: the role of irradiance and temperature. In: Moller IM, Gardestrom P, Gliminius K, Glaser E (eds) Plant mitochondria: from gene to function. Backhuys Publishers, Leiden, pp 567–574
Atkins OK, Cummins WR (1994) The effect of nitrogen source on growth, nitrogen economy and respiration of 2 high arctic plant species differing in relative growth rate. Funct Ecol 8:389–399
Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, New York
Bolhàr-Nordenkampf HR, Draxler G (1993) Functional anatomy. In: Hall DO, Scurlock JMO, Bolhàr-Nordenkampf HR, Leegood RC, Lang SP (eds) Photosynthesis and production in a changing environment A field and laboratory manual. Chapman and Hall, London, pp 91–112
Bolmgren KB, Oxelman B (2004) Generic limits in Rhamnus L. s.l. (Rhamnaceae) inferred from nuclear and chloroplast DNA sequence phylogenies. Taxon 53:383–390
Cai ZQ, Slot M, Fan ZX (2005) Leaf development and photosynthetic properties of three tropical tree species with delayed greening. Photosynthetica 43:91–98
Cappelletti C (1954) Water content in plants and equations used to determine it. Ann Bot Roma 24:408–430
Castro-Díez P, Montserrat-Martí G (1998) Phenological pattern of fifteen Mediterranean phanaerophytes from Quercus ilex communities of NE-Spain. Plant Ecol 139:103–112
Castro-Díez P, Puyravaud JP, Cornelissen JHC (2000) Leaf structure and anatomy as related to leaf mass per area variation in seedlings of a wide range of woody plant species and types. Oecologia 124:476–486
Cookson SJ, Van Lijsebettens M, Granier C (2005) Correlation between leaf growth variables suggest intrinsic and early controls of leaf size in Arabidopsis thaliana. Plant Cell Environ 28:1355–1366
Evans JR, Loreto F (2000) Acquisition and diffusion of CO2 in higher plant leaves. In: Leegood RC, Sharkey TD, von Caemmerer S (eds) Photosynthesis: physiology and metabolism. Kluwer, Dordrecht, pp 312–351
Evans JR, Schortemeyer M, Mc Farlane N, Atkin OK (2000) Photosynthetic characteristics of 10 Acacia species grown under ambient and elevated atmospheric CO2. Aust J Plant Physiol 27:13–25
Galmés J, Cifre J, Medrano H, Flexas J (2005) Modulation of relative growth rate and its components by water stress in Mediterranean species with different growth forms. Oecologia 145:21–31
Granier C, Tardieu F (1998) Spatial and temporal analyses of expansion and cell cycle in sunflower leaves. A common pattern of development for all zones of a leaf and different leaves of a plant. Plant Physiol 116:991–1001
Gratani L, Bombelli A (1999) Leaf anatomy, inclination, and gas exchange relationships in evergreen sclerophyllous and drought semideciduous shrub species. Photosynthetica 37:573–585
Gratani L, Bombelli A (2001) Differences in leaf traits among Mediterranean broad-leaved evergreen shrubs. Ann Bot Fenn 38:15–24
Gratani L, Bonito A (2009) Leaf traits variation during leaf expansion in Querus ilex L. Photosynthetica 47:323–330
Gratani L, Ghia E (2002) Changes in morphological and physiological traits during leaf expansion of Arbutus unedo. Environ Exp Bot 48:51–60
Gratani L, Varone L (2004) Adaptive photosynthetic strategies of the Mediterranean maquis species according to their origin. Photosynthetica 42:551–558
Gratani L, Pesoli P, Crescente MF, Aichner K, Larcher W (2000) Photosynthesis as a temperature indicator in Quercus ilex L. Glob Planet Change 24:153–163
Gratani L, Crescente MF, Fabrini G, Varone L (2008a) Growth pattern of Bidens cernua L.: relationships between relative growth rate and its physiological and morphological components. Photosynthetica 46:179–184
Gratani L, Varone L, Catoni R (2008b) Relationship between net photosynthesis and leaf respiration in Mediterranean evergreen species. Photosynthetica 46:567–573
Gulías J, Traveset A, Riera N, Mus M (2004) Critical stages in the recruitment process of Rhamnus alaternus L. Ann Bot 93:723–731
Gunn S, Farrar F (1999) Effects of a 4°C increase in temperature on partitioning of leaf area and dry mass, root respiration and carbohydrates. Funct Ecol 13:12–20
Hegazy AK, Fahmy GM, Ali MI, Gomaa NH (2005) Growth and phenology of eight common weed species. J Arid Environ 61:171–183
Hsiao TC, Frensch J, Rojas-Lara BA (1998) The pressure-jump technique shows maize leaf growth to be enhanced by increases in turgor only when status is not too high. Plant Cell Environ 21:33–42
Johnson IR, Thornley JHM (1983) Vegetative crop growth model incorporating leaf area expansion and senescence, and applied to grass. Plant Cell Environ 6:721–729
Lambers H, Poorter H (1992) Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequences. Adv Ecol Res 23:187–261
Larcher W (2003) Physiological plant ecology. Springer, Berlin, Heidelberg
Marchi S, Tognetti R, Minnocci A, Borghi M, Sebastiani L (2008) Variation in mesophyll anatomy and photosynthetic capacity during leaf development in a deciduous mesophyte fruit tree (Prunus persica) and an evergreen sclerophyllous Mediterranean shrub (Olea europaea). Trees 22:559–571
Miyazawa SI, Terashima I (2001) Slow development of leaf photosynthesis in an evergreen broad-leaves tree, Castanopsis sieboldii: relationships between leaf anatomical characteristics and photosynthetic rate. Plant Cell Environ 24:279–291
Miyazawa SI, Satomi S, Terashima I (1998) Slow leaf development of evergreen broad-leaved tree species in Japanese warm temperate forests. Ann Bot 82:859–869
Miyazawa SI, Makino A, Terashima I (2003) Changes in mesophyll anatomy and sink–source relationships during leaf development in Quercus glauca, an evergreen tree showing delayed leaf greening. Plant Cell Environ 26:745–755
Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505–512
Parkhurst DF (1994) Diffusion of CO2 and other gases inside leaves. New Phytol 126:449–479
Rhizopoulou S, Psaras GK (2003) Development and structure of drought-tolerant leaves of the Mediterranean shrub Capparis spinosa L. Ann Bot 92:377–383
Shirke PA (2001) Leaf photosynthesis, dark respiration and fluorescence as influenced by leaf age in an evergreen tree, Prosopis juliflora. Photosynthetica 39:305–311
Sobrado MA (2008) Leaf and photosynthetic characteristics of pioneer and forest species in tropical montane habitats. Photosynthetica 46:604–610
Stessman D, Miller A, Spalding M, Rodermel S (2002) Regulation of photosynthesis during Arabidopsis leaf development in continuous light. Photosynth Res 72:27–37
Stewart JR, Graves W (2006) Photosynthesis, growth, carbon allocation, and fruit load of Fragula caroliniana and Rhamnus cathartica. Int J Plant Sci 167:1161–1168
Suc JP (1984) Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature 307:429–432
Sugiyama S (2005) Developmental basis of interspecific differences in leaf size and specific leaf area among C3 grass species. Funct Ecol 19:916–924
Sun SC, Jin D, Li R (2006) Leaf emergence in relation to leaf traits in temperate woody species in East-Chinese Quercus fabri forests. Acta Oecol 30:212–222
Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ 18:149–157
Taiz L, Zeiger E (2002) Plant physiology, 3rd edn. Sinauer, Sunderland
Tardieu F, Granier C, Muller B (1999) Modelling leaf expansion in a fluctuating environment: are changes in specific leaf area a consequence of changes in expansion rate? New Phytol 143:33–43
Terashima I, Miyazawa SI, Hanba YT (2001) Why are sun leaves thicker than shade leaves? Consideration based on analysis of CO2 diffusion in the leaf. J Plant Res 114:93–105
Turgeon R (1989) The sink-source transition in leaves. Annu Rev Plant Physiol Plant Mol Biol 40:119–138
Van Volkenburgh E (1999) Leaf expansion—an integrating plant behaviour. Plant Cell Environ 22:1463–1473
Wotherspoon SH, Wotherspoon JA (2002) The evolution and execution of a plan for invasive weed eradication and control, Rangitoto Island, Hauraki Gulf, New Zealand. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN SSC Invasive Species Specialist Group, IUCN, Gland, Cambridge, pp 381–388
Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827
Yu MML, Konorov SO, Schulze HG, Blades MW, Turner RFB, Jetter R (2008) In situ analysis by microspectroscopy reveals triterpenoid compositional patterns within leaf cuticles of Prunus laurocerasus. Planta 227:823–834
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Communicated by M. Zwienieki.
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Varone, L., Gratani, L. Leaf expansion in Rhamnus alaternus L. by leaf morphological, anatomical and physiological analysis. Trees 23, 1255–1262 (2009). https://doi.org/10.1007/s00468-009-0365-5
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DOI: https://doi.org/10.1007/s00468-009-0365-5