Carla AMARAL, Berta GONÇALVES, Filipa MARTINS, Ivo OLIVEIRA, Ana BARROS, Sílvia AFONSO, Helena FERREIRA, José MOUTINHO PEREIRA

Leaf morpho-physiological dynamics in Salvia officinalis L. var. purpurascens

Salvia officinalis L. var. purpurascens is one of the most insufficiently studied varieties of the genus Salvia. Hence, the study and characterization of this plant, as well as the monitoring of changes occurring during leaf ontogeny, are of great importance and interest. For this purpose, young and adult leaves of Salvia officinalis L. var. purpurascens collected in two different seasons and in two different years were analyzed, considering morpho-anatomical traits but also leaf gas exchange and chlorophyll a fluorescence parameters. Leaf age was found to have significant effects on several of the analyzed parameters, including the parenchyma, mesophyll, xylem, and phloem thickness, as well as transpiration rate (E) and maximum photochemical efficiency of PSII (Fv /Fm). On the other hand, considerable differences were found for several characteristics of Salvia officinalis caused by season, e.g., leaf area, vessel dimensions, stomatal conductance (gs ), waxes, E, and intrinsic water-use efficiency (A/gs ). The year of harvest also resulted in significant variations in several parameters, such as leaf area and leaf mass per area (LMA), and palisade and spongy parenchyma thickness. These results show the dynamics of Salvia officinalis leaf traits, presently poorly known, and are further helpful when aiming towards optimization of characteristics of cultivated sage.

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Albano S, Miguel M (2011). Biological activities of extracts of plants grown in Portugal. Ind Crop Prod 33: 338-343.
Alizadeh A, Shaabani M (2012). Essential oil composition, phenolic content, antioxidant and antimicrobial activity in Salvia officinalis L. cultivated in Iran. Adv Environ Biol 6: 221-226.
Baker N (2008). Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59: 89-113.
Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B (2011). Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiol Plant 33: 1103-1111.
Bilger W, Schreiber U (1986). Energy-dependent quenching of darklevel chlorophyll fluorescence in intact leaves. Photosynth Res 10: 303-308.
Björkman O, Demmig B (1987). Photon yield for O2 evolution and chlorophyll fluorescence characteristics at 77K among vascular plants of diverse origins. Planta 170: 489-504.
Bringe K, Schumacher C, Schmitz-Eiberger M, Steiner U, Oerke E (2006). Ontogenetic variation in chemical and physical characteristics of adaxial apple leaf surfaces. Phytochemistry 67: 161-170.
Centritto M (2002). The effects of elevated [CO2 ] and water availability on growth and physiology of peach (Prunus persica) plants. Plant Biosyst 136: 177-188.
Chabot B, Chabot J (1977). Effects of light and temperature on leaf anatomy and photosynthesis in Fragaria vesca. Oecologia 26: 363-377.
Chaves M, Maroco J, Pereira J (2003). Understanding plant responses to drought - from genes to the whole plant. Funct Plant Biol 30: 239-264.
Cohu C, Muller O, Adams W, Demming‐Adams B (2014). Leaf anatomical and photosynthetic acclimation to cool temperature and high light in two winter versus two summer annuals. Physiol Plantarum 152: 164-173.
Damour G, Simonneau T, Cochard H, Urban L (2010). An overview of models of stomatal conductance at the leaf level. Plant Cell Environ 33: 1419-1438.
Gan R, Xu X, Song F, Kuang L, Li H (2010). Antioxidant activity and total phenolic content of medicinal plants associated with prevention and treatment of cardiovascular and cerebrovascular diseases. J Med Plants Res 4: 2438-2444.
Genty B, Briantais J, Baker N (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990: 87-92.
Gonçalves B, Silva A, Bacelar E, Correia C, Santos A, Ferreira H, Moutinho-Pereira J (2009). Effect of training system on hazelnut (Corylus avellana) physiology. Acta Hortic 845: 239- 244.
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: 141-153.
Guerfel M, Baccouri O, Boujnah D, Chaïbi W, Zarrouk M (2009). Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. Sci Hortic - Amsterdam 119: 257-263.
IPMA (2015). http://www.ipma.pt/pt/index.html. Kahmen A, Dawson T, Vieth A, Sachse D (2011). Leaf wax n‐alkane δD values are determined early in the ontogeny of Populus trichocarpa leaves when grown under controlled environmental conditions. Plant Cell Environ 34: 1639-1651.
Karabacak E, Uysal I, Doğan M (2009). Cultivated Salvia species in Turkey. Biological Diversity and Conservation 2: 71-77.
Kofidis G, Bosabalidis A, Moustakas M (2007). Combined effects of altitude and season on leaf characteristics of Clinopodium vulgare L. (Labiatae). Environ Exp Bot 60: 69-76.
Kofidis G, Kokkini S, Bosabalidis A (2011). Seasonal variations in leaf structure, morphometry and essential oils of two Mentha spicata populations grown at altitudinal extremes. J Biol ResThessalon 16: 255-265.
Kouhila M, Belghit A, Daguenet M, Boutaleb B (2001). Experimental determination of the sorption isotherms of mint (Mentha viridis), sage (Salvia officinalis) and verbena (Lippia citriodora). J Food Eng 47: 281-287.
Kowalczuk A, Raman V, Galal A, Khan I, Siebert D, Zjawiony J (2014). Vegetative anatomy and micromorphology of Salvia divinorum (Lamiaceae) from Mexico, combined with chromatographic analysis of salvinorin A. J Nat Med 68: 63-73.
Lambrecht S, Santiago L, DeVan C, Cervera J, Stripe C, Buckingham L, Pasquini S (2011). Plant water status and hydraulic conductance during flowering in the southern California coastal sage shrub Salvia mellifera (Lamiaceae). Am J Bot 98: 1286-1292.
Larcher W (1995). Physiological Plant Ecology, 3rd ed. Berlin, Germany: Springer.
Letts M, Rodríguez-Calcerrada J, Rolo V, Rambal S (2012). Longterm physiological and morphological acclimation by the evergreen shrub Buxus sempervirens L. to understory and canopy gap light intensities. Trees 26: 479-491.
Mapes C, Xu Y (2014). Photosynthesis, vegetative habit and culinary properties of sage (Salvia officinalis) in response to low-light conditions. Can J Plant Sci 94: 881-889.
Maxwell K, Johnson G (2000). Chlorophyll fluorescencea practical guide. J Exp Bot 51: 659-668.
Meier I, Leuschner C (2008). Leaf size and leaf area index in Fagus sylvatica forests: competing effects of precipitation, temperature, and nitrogen availability. Ecosystems 11: 655-669.
Nasta O, Akoumianaki-Ioannidou A, Liakopoulos G, Nikolopoulou A (2014). Effects of salinity in the form of simulated sea-spray (NaCl or NaCl+ H3 BO3 solution) on growth and photosynthetic performance of sage (Salvia officinalis). Australian Journal of Crop Science 8: 1186-1194.
Niinemets Ü (1999). Components of leaf dry mass per area thickness and densityalter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144: 35-47.
Niinemets Ü, Portsmuth A, Truus L (2002). Leaf structural and photosynthetic characteristics, and biomass allocation to foliage in relation to foliar nitrogen content and tree size in three Betula species. Ann Bot-London 89: 191-204.
Pellegrini E, Francini A, Lorenzini G, Nali C (2015). Ecophysiological and antioxidant traits of Salvia officinalis under ozone stress. Environ Sci Pollut R 22: 13083-13093.
Poorter H, Niinemets Ü, Poorter L, Wright I, Villar R (2009). Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis. New Phytol 182: 565-588.
Rogiers S, Greer D, Hutton R, Clarke S (2011). Transpiration efficiency of the grapevine cv. Semillon is tied to VPD in warm climates. Ann Appl Biol 158: 106-114.
Sánchez-Díaz M, Aguirreolea J (2000). Movimientos estomáticos y transpiración. In: Azcon-Bieto, J, Talon M, editors. Fundamentos de Fisiología Vegetal. 1ª ed. Madrid, Spain: McGraw-Hill/Interamericana de España, pp. 31-43.
Sangwan N, Farooqi A, Shabih F, Sangwan R (2001). Regulation of essential oil production in plants. Plant Growth Regul 34: 3-21.
Scalbert A, Manach C, Morand C, Remesy C, Jimenez L (2005). Dietary polyphenols and the prevention of diseases. Crit Rev Food Sci 45: 287-306.
Schippmann U, Leaman D, Cunningham A (2006). A comparison of cultivation and wild collection of medicinal and aromatic plants under sustainability aspects. In: Bogers R, Craker L, Lange D, editors. Medicinal and Aromatic Plants. Dordrecht, the Netherlands: Springer, pp. 75-95
Seidler-Łożykowska K, Mordalski R, Król D, Bocianowski J, Karpińska E (2015). Yield and quality of sage herb (Salvia officinalis L.) from organic cultivation. Biol Agric Hortic 31: 53-60.
Taârit M, Msaada K, Hosni K, Marzouk B (2012). Physiological changes, phenolic content and antioxidant activity of Salvia officinalis L. grown under saline conditions. J Sci Food Agr 92: 1614-1619.
Tanko H, Carrier D, Duan L, Clausen E (2005). Pre- and post-harvest processing of medicinal plants. Plant Genetic Resources 3: 304- 313.
Vile D, Pervent M, Belluau M, Vasseur F, Bresson J, Muller B, Granier C, Simonneau T (2012). Arabidopsis growth under prolonged high temperature and water deficit: independent or interactive effects? Plant Cell Environ 35: 702-718.
von Caemmerer S, Farquhar G (1981). Some relationships between the biochemistry of photosynthesis and gas exchange of leaves. Planta 153: 376-387.
Wang R, Chang J, Li K, Lin T, Chang L (2014). Leaf age and light intensity affect gas exchange parameters and photosynthesis within the developing canopy of field net-house-grown papaya trees. Sci Hortic-Amsterdam 165: 365-373.
Witkowski E, Lamont B (1991). Leaf specific mass confounds leaf density and thickness. Oecologia 88: 486-493.
World Health Organization (2003). WHO guidelines on good agricultural and collection practices (GACP) for medicinal plants. Geneva, Switzerland: World Health Organization.
Yi W, Wetzstein H (2010). Biochemical, biological and histological evaluation of some culinary and medicinal herbs grown under greenhouse and field conditions. J Sci Food Agr 90: 1063-1070.
Zimmermann M (1983). Xylem Structure and the Ascent of Sap. Berlin, Germany: Springer-Verlag.