Abstract
In the field, leaves may face very different light intensities within the tree canopy. Leaves usually respond with light-induced morphological and photosynthetic changes, in a phenomenon known as phenotypic plasticity. Canopy light distribution, leaf anatomy, gas exchange, chlorophyll fluorescence, and pigment composition were investigated in an olive (Olea europaea, cvs. Arbequina and Arbosana) orchard planted with a high-density system (1,250 trees ha−1). Sampling was made from three canopy zones: a lower canopy (<1 m), a central one (1–2 m), and an upper one (>2 m). Light interception decreased significantly in the lower canopy when compared to the central and top ones. Leaf angle increased and photosynthetic rates and non-photochemical quenching (NPQ) decreased significantly and progressively from the upper canopy to the central and the lower canopies. The largest leaf areas were found in the lower canopy, especially in the cultivar Arbequina. The palisade and spongy parenchyma were reduced in thickness in the lower canopy when compared to the upper one, in the former due to a decrease in the number of cell layers from three to two (clearly distinguishable in the light and fluorescence microscopy images). In both cultivars, the concentration of violaxanthin-cycle pigments and β-carotene was higher in the upper than in the lower canopy. Furthermore, the de-epoxidized forms zeaxanthin and antheraxanthin increased significantly in those leaves from the upper canopy, in parallel to the NPQ increases. In conclusion, olive leaves react with morphological and photosynthetic changes to within-crown light gradients. These results strengthen the idea of olive trees as “modular organisms” that adjust the modules morphology and physiology in response to light intensity.
Similar content being viewed by others
References
Acebedo MM, Cañete ML, Cuevas J (2002) Processes affecting fruit distribution and its quality in the canopy of olive trees. Adv Hortic Sci 14:169–175
Agromillora Catalana SA (2007) Evolución de la superficie plantada de olivos en sistema superintensivo o en seto en el mundo. Olint 12:24–27
Belkhodja R, Morales F, Quílez R, López-Millán AF, Abadía A, Abadía J (1998) Iron deficiency causes changes in chlorophyll fluorescence due to the reduction in the dark of the photosystem II acceptor side. Photosynth Res 56:265–276
Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185
Boardman NK (1977) Comparative photosynthesis of sun and shade plants. Annu Rev Plant Physiol 28:355–377
Bongi G, Mencuccini M, Fontanazza G (1987) Photosynthesis of olive leaves: effect of light flux density, leaf age, temperature, peltates and H2O vapor pressure deficit on gas exchange. J Am Soc Hortic Sci 112:143–148
Boughalleb F, Hajlaoui H (2011) Physiological and anatomical changes induced by drought in two olive cultivars (cv Zalmati and Chemlali). Acta Physiol Plant 33:53–65
Cerovic ZG, Morales F, Moya I (1994) Time-resolved spectral studies of blue-green fluorescence of leaves, mesophyll and chloroplasts of sugar beet (Beta vulgaris L.). Biochim Biophys Acta 1188:58–68
Cerovic ZG, Langrand E, Latouche G, Morales F, Moya I (1998) Spectral characterization of NAD(P)H fluorescence in intact isolated chloroplasts and leaves: effect of chlorophyll concentration on reabsorption of blue-green fluorescence. Photosynth Res 56:291–301
Cerovic ZG, Samson G, Morales F, Tremblay N, Moya I (1999) Ultraviolet-induced fluorescence for plant monitoring: present state and prospects. Agronomie 19:543–578
Ceulemans RJ, Saugier B (1991) Photosynthesis. In: Raghavendra AS (ed) Physiology of trees. Wiley, New York, pp 21–50
Cherbiy-Hoffmann SU, Searles PS, Hall AJ, Rousseaux MC (2012) Influence of light environment on yield determinants and components in large olive hedgerows following mechanical pruning in the subtropics of the Southern Hemisphere. Sci Hortic 137:36–42
Cherbiy-Hoffmann SU, Hall AJ, Rousseaux MC (2013) Fruit, yield, and vegetative growth responses to photosynthetically active radiation during oil synthesis in olive trees. Sci Hortic 150:110–116
Connor DJ (2006) Towards optimal designs for hedgerow olive orchards. Aust J Agric Res 57:1067–1072
Connor DJ, Fereres E (2005) The physiology of adaptation and yield expression in olive. Hortic Rev 31:157–231
Connor DJ, Centeno A, Gómez-del-Campo M (2009) Yield determination in olive hedgerow orchards. II. Analysis of radiation and fruiting profiles. Crop Pasture Sci 60:443–452
Connor DJ, Gómez-del-Campo M, Comas J (2012) Yield characteristics of N–S oriented olive hedgerow orchards, cv. Arbequina. Sci Hortic 133:31–36
Connor DJ, Gómez-del-Campo M, Rousseaux MC, Searles PS (2014) Structure, management and productivity of hedgerow olive orchards: a review. Sci Hortic 169:71–93
de Casas RR, Vargas P, Pérez-Corona E, Manrique E, García-Verdugo C, Balaguer L (2011) Sun and shade leaves of Olea europaea respond differently to plant size, light availability and genetic variation. Funct Ecol 25:802–812
Del Río C, García-Fernández MD, Caballero JM (2002) Variability and classification of olive cultivars by their vigour. Acta Hortic 586:229–232
Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626
Demmig-Adams B, Adams WW III (1996) The role of xanthophylls cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26
Demmig-Adams B, Adams WW III, Logan BA, Verhoeven AS (1995) Xanthophyll cycle-dependent energy dissipation and flexible PSII efficiency in plants acclimated to light stress. Aust J Plant Physiol 22:249–261
Demmig-Adams B, Adams WW III, Barker DH, Logan BA, Bowling DR, Verhoeven AS (1996) Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. Physiol Plant 98:253–264
Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Gilmore AM, Yamamoto HY (1993) Linear models relating xanthophylls and lumen acidity to non-photochemical fluorescence quenching: evidence that antheraxanthin explains zeaxanthin independent quenching. Photosynth Res 35:67–78
Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92
Granado-Yela C, García-Verdugo C, Carrillo K, Rubio de Casas R, Kleczkowski LA, Balaguer L (2011) Temporal matching among diurnal photosynthetic patterns within the crown of the evergreen sclerophyll Olea europaea L. Plant Cell Environ 34:800–810
Gregoriou K, Pontikis K, Vemmos S (2007) Effects of reduced irradiance on leaf morphology, photosynthetic capacity, and fruit yield in olive (Olea europaea L.). Photosynthetica 45:172–181
Harbinson J, Genty B, Baker NR (1989) Relationship between the quantum efficiencies of photosystems I and II in pea leaves. Plant Physiol 90:1029–1034
He J, Chee CW, Goh CJ (1996) “Photoinhibition” of Heliconia under natural tropical conditions: the importance of leaf orientation for light interception and leaf temperature. Plant Cell Environ 19:1238–1248
Higgins SS, Larsen FE, Bendel RB, Radamaker GK, Bassman JH, Bidlake WR, Al Wir A (1992) Comparative gas exchange characteristics of potted, glasshouse-grown almond, apple, fig, grape, olive, peach and Asian pear. Sci Hortic 52:313–329
Huang D, Wu L, Chen JR, Dong L (2011) Morphological plasticity, photosynthesis and chlorophyll fluorescence of Athyrium pachyphlebium at different shade levels. Photosynthetica 49:611–618
Jackson JE (1980) Light interception and utilization by orchard systems. Hortic Rev 2:208–267
Kchaou H, Larbi A, Chaieb M, Sagardoy R, Msallem M, Morales F (2013) Genotypic differentiation in the stomatal response to salinity and contrasting photosynthetic and photoprotection responses in five olive (Olea europaea L.) cultivars. Sci Hortic 160:129–138
Larbi A, Abadía A, Morales F, Abadía J (2004) Fe resupply to Fe-deficient sugar beet plants leads to rapid changes in the violaxanthin cycle and other photosynthetic characteristics without significant de novo chlorophyll synthesis. Photosynth Res 79:59–69
Larbi A, Ayadi M, Dhiab AB, Msallem M, Caballero J (2011) Tunisian and foreign olive cultivars suitability to high density orchards. Span J Agric Res 9:1279–1286
Leon JM, Bukovak MJ (1978) Cuticle development and surface morphology of olive leaves with reference to penetration of foliar-applied chemicals. J Am Soc Hortic Sci 103:465–472
Leong TY, Anderson JM (1984a) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. I. Study on the distribution of chlorophyll–protein complexes. Photosynth Res 5:105–115
Leong TY, Anderson JM (1984b) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. II. Regulation of electron transport capacities, electron carriers, coupling factor (CF1) activity and rates of photosynthesis. Photosynth Res 5:117–128
Mariscal MJ, Ogaz F, Villalobos FJ (2000) Radiation use efficiency and dry matter partitioning of a young olive (Olea europaea) orchard. Tree Physiol 20:65–72
Marler TE, Schaffer B, Crane JH (1994) Developmental light level affects growth, morphology, and leaf physiology of young carambola trees. J Am Soc Hortic Sci 119:711–718
Melgar JC, Guidi L, Remorini D, Agati G, Degl’Innocenti E, Castelli S, Camilla Baratto M, Faraloni C, Tattini M (2009) Antioxidant defences and oxidative damage in salt-treated olive plants under contrasting sunlight irradiances. Tree Physiol 29:1187–1198
Monteith JL (1977) Climate and efficiency of crop production in Britain. Philos Trans R Soc Lond B Biol Sci 281:277–294
Morales F, Abadía A, Abadía J (1991) Chlorophyll fluorescence and photon yield of oxygen evolution in iron-deficient sugar beet (Beta vulgaris L.) leaves. Plant Physiol 97:886–893
Morales F, Cerovic ZG, Moya I (1994) Characterization of blue-green fluorescence in the mesophyll of sugar beet (Beta vulgaris L.) leaves affected by iron deficiency. Plant Physiol 106:127–133
Morales F, Cerovic ZG, Moya I (1996) Time-resolved blue-green fluorescence of sugar beet (Beta vulgaris L.) leaves. Spectroscopic evidence for the presence of ferulic acid as the main fluorophore of the epidermis. Biochim Biophys Acta 1273:251–262
Msallem M (2002) Etude de la juvénilité chez l’olivier (Olea europaea L.). Aspects morphologiques, anatomiques et biochimiques. Thèse Doctorat d’Etat. Institut National Agronomique de Tunisie
Nii N, Kuriowa T (1988) Anatomical changes including chloroplast structure in peach leaves under different light conditions. J Hortic Sci 63:37–45
Pastor M, García-Vila M, Soriano MA, Vega V, Fereres E (2007) Productivity of olive orchards in response to tree density. J Hortic Sci Biotechnol 82:555–562
Peguero-Pina JJ, Gil-Pelegrín E, Morales F (2013) Three pools of zeaxanthin in Quercus coccifera during light transitions with different roles in rapidly reversible photoprotective energy dissipation and photoprotection. J Exp Bot 64:1649–1661
Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410
Proietti P (2000) Effect of fruiting on leaf gas exchange in olive (Olea europaea L.). Photosynthetica 38:397–402
Proietti P, Prezios P, Tombesi A (1988) Influence of shading on olive leaf photosynthesis. In: Proceedings of the 2nd international meeting on mediterranean tree crops, Chania, pp 334–342
Proietti P, Tombesi A, Boco M (1994) Influence of leaf shading and defoliation on oil synthesis and growth of olive fruit. Acta Hortic 356:272–277
Proietti P, Nasini L, Ilarioni L (2012) Photosynthetic behavior of Spanish Arbequina and Italian Maurino olive (Olea europaea L.) cultivars under super-intensive grove conditions. Photosynthetica 50:239–246
Roselli G, Benelli G, Morelli D (1989) Relationship between stomatal density and winter hardiness in olive (Olea europaea L.). J Hortic Sci 64:199–203
Sagardoy R, Vázquez S, Florez-Sarasa ID, Albacete A, Ribas-Carbó M, Flexas J, Abadía J, Morales F (2010) Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol 187:145–158
Salisbury FB, Ross C (1978) Photomorphogenesis. Plant physiology, 2nd edn. Wadsworth Publishing Company, Belmont, pp 438–463
Sofo A, Dichio B, Montanaro G, Xiloyannis C (2009) Photosynthetic performance and light response of two olive cultivars under different water and light regimes. Photosynthetica 47:602–608
Syvertsen JP, Smith ML (1984) Light acclimation in citrus leaves. I. Changes in physical characteristics, chlorophyll and nitrogen content. J Am Soc Hortic Sci 109:807–812
Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Fraquhar GD (1995) On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves. Plant Cell Environ 18:149–157
Tattini M, Gucci R, Coradeschi MA, Ponzio C, Everard JD (1995) Growth, gas-exchange and ion content in Olea europea plants during salinity stress and subsequent relief. Physiol Plant 95:203–210
Tombesi A (1992) Photosynthesis and interception of light energy by olive trees. Progetto Agricoltura. University of Perugia, Italy
Tombesi A, Cartechini A (1986) The effect of crown shading on the differentiation of flowering buds in olive. Riv Ortoflorofruitticolt Ital 70:277–285
Tombesi A, Boco M, Pilli M, Metzidakis IT, Voyiatzis DG (1999) Influence of light exposure on olive fruit growth and composition. Acta Hortic 474:255–259
Van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150
Villalobos FJ, Testi L, Hidalgo J, Pastor M, Orgaz F (2006) Modelling potential growth and yield of olive (Olea europaea L.) canopies. Eur J Agron 24:296–303
Vogelmann TC, Martin G (1993) The functional significance of palisade tissue: penetration of directional versus diffuse light. Plant Cell Environ 16:65–72
Yang S-J, Sun M, Zhang Y-J, Cochard H, Cao K-F (2014) Strong leaf morphological, anatomical, and physiological responses of a subtropical woody bamboo (Sinarundinaria nitida) to contrasting light environments. Plant Ecol 215:97–109
Yoshimura K (2010) Irradiance heterogeneity within crown affects photosynthetic capacity and nitrogen distribution of leaves in Cedrela sinensis. Plant Cell Environ 33:750–758
Zhang SB, Hu H, Xu K, Li ZR, Yang YP (2007) Flexible and reversible responses to different irradiance levels during photosynthetic acclimation of Cypripedium guttatum. J Plant Physiol 164:611–620
Acknowledgment
This work was supported by the Spanish Agency of International Cooperation for Development (AECID) Project AP/040397/11 and the Aragón Government (A03 Research Group).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Larbi, A., Vázquez, S., El-Jendoubi, H. et al. Canopy light heterogeneity drives leaf anatomical, eco-physiological, and photosynthetic changes in olive trees grown in a high-density plantation. Photosynth Res 123, 141–155 (2015). https://doi.org/10.1007/s11120-014-0052-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-014-0052-2