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Photosynthesis and Photoprotection Responses to Water Stress in The Environmental and Experimental Botany 60 (2007) 308–317 Photosynthesis and photoprotection responses to water stress in the wild-extinct plant Lysimachia minoricensis Jeroni Galmes´ a,∗, Anunciacion´ Abad´ıa b, Hipolito´ Medrano a, Jaume Flexas a a Grup de Recerca en Biologia de les Plantes en Condicions Mediterr`anies, Edifici Guillem Colom i Casasnovas, Area` de Fisiologia Vegetal, Universitat de les Illes Balears, Carretera de Valldemossa Km.7.5, 07122 Palma de Mallorca, Spain b Estaci´on Experimental Aula Dei, CSIC, Zaragoza, Spain Received 30 January 2006; received in revised form 11 September 2006; accepted 27 December 2006 Abstract Lysimachia minoricensis is an endemic species of the Balearic Islands that has become extinct in the wild, but persists in botanical gardens. Attempts of re-introducing the species into its natural habitat, which consisted in temporary dry streams, have failed. Low genetic variability has been reported for the garden individuals, suggesting that a reduced potential to adapt to environmental changes could be among the reasons for its extinction. In the present study, we particularly test whether photosynthesis and photoprotection responses of this species to water stress could help explaining the lack of success of this species in its natural habitat. Plants of L. minoricensis were grown in pots in a growth chamber. Soil water depletion was imposed over 20 days by stopping irrigation. Early stomata closure was observed in response to soil water depletion while leaves desiccated progressively. Although net photosynthesis was low in irrigated plants, due to a remarkably low mesophyll conductance to CO2, substantial photosynthetic activity was kept at severe drought, where leaf relative water content was as low as 50%, suggesting that L. minoricensis is a very drought-tolerant species. In parallel with decreased photosynthesis, thermal dissipation of the excess light and photorespiration progressively increased. The former was linearly related to increased de-epoxidation of the xanthophylls cycle. Photoprotection was effective, as pre-dawn maximum photochemical efficiency was maintained higher than 0.75 through the entire experiment. Moreover, photosynthetic capacity was largely (80%) recovered only 24 h after re-watering. These results show that stomatal regulation, photosynthetic metabolism and photoprotection in L. minoricensis are well adapted to water stress, suggesting that additional factors may be responsible for its status as a wild-extinct plant. © 2007 Elsevier B.V. All rights reserved. Keywords: Balearic Islands; Mediterranean; Endemism; Drought 1. Introduction oran Islet) and Dianthus multinervis Vis. (Jakuba islet), one of the three Mediterranean island endemic species that has gone The Balearic Islands, located within the Mediterranean basin, extinct in the wild but that is still preserved in botanic gardens. are characterized by the richness of its endemic flora (Cardona L. minoricensis was described from a single population located and Contandriopoulous, 1979), which contributes to the main- in the south of the island of Minorca (Rodriguez, 1868), and tenance of a high biodiversity in the area. However, a high probably disappeared in the field in the first half of the last cen- proportion of the endemic species is confined to a few geo- tury (Iba´nez˜ et al., 1999). Fortunately, few individuals were kept graphically restricted populations, being partially responsible in the botanical garden of Barcelona and seeds distributed to for the high fragility of the island ecosystems (Carlquist, 1974). several European botanical gardens (Bolos,´ 1962). Therefore, This involves a higher risk of extinction for island species as according to conservation categories developed by the IUCN compared to those growing in continental areas (Alcover et al., (1994) this species has been classified as extinct in the wild. 1999; Hylton-Taylor, 2000). Lysimachia minoricensis J.J. Rodr. Attempts to re-introduce L. minoricensis to its original habi- (Primulaceae) is, along with Diplotaxis siettiana Maire (Alb- tat, which consisted in the vicinity of temporary drying water streams, have failed (Iba´nez˜ et al., 1999). The shortage of sample propagules originally recovered in the field before its extinction ∗ Corresponding author. Tel.: +34 971 259556; fax: +34 971 173168. is probably the cause of the extremely low genetic variability E-mail address: [email protected] (J. Galmes).´ of the individuals nowadays kept in botanical gardens (Iba´nez˜ 0098-8472/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.envexpbot.2006.12.016 J. Galm´es et al. / Environmental and Experimental Botany 60 (2007) 308–317 309 et al., 1999; Calero et al., 1999). The lack of genetic vari- 2. Materials and methods ability to counteract unfavourable environmental changes has been considered the most decisive factor for the survival of 2.1. Plant material and treatments plant species restricted to small areas with low population size (Ellstrand and Elam, 1993; O’Brien, 1994). Therefore, this rea- Seeds of L. minoricensis J.J. Rodr. (Primulaceae) were son may be argued to explain the unsuccessful re-introduction obtained from a botanical garden (Jard´ı Botanic` de Soller,´ Spain) attempts. and germinated on filter paper moistened with de-ionized water According to Lambers et al. (1998), a given species would in a controlled environment (germination chamber, at 18 ◦Cin inhabit a given site if it successfully passes three filters: a darkness). After germination and emergence of one true leaf, historical filter (‘does it arrive?’), a physiological filter (‘can seedlings were transplanted to large pots (25 L volume, 40 cm it germinate, grow, survive and reproduce?’) and a biotic fil- height) containing a 40:40:20 mixture of clay–calcareous soil, ter (‘does it successfully compete and defend itself?’). The horticultural substrate and perlite. Plants were grown under natu- attempts of re-introduction of L. minoricensis ensure passing ral conditions at the University of the Balearic Islands (Mallorca, the historical filter. Then the next cause of its lack of success- Spain). Four weeks before starting the experiment, 1-year-old fulness of this species in the field should be searched among plants were placed in a controlled growth chamber with a 12 h physiological characters of the species that possibly limit over- photoperiod (26 ◦C day/20 ◦C night) and a photon flux density passing of the physiological filter. In this sense, a previous study at the top of the leaves of about 600 ␮mol m−2 s−1 (halogen by Rossello´ and Mayol (2002) clearly established that fertil- lamps). ity and seed viability were not the major causes of extinction Plants were once abundantly supplied with 50% Hoagland’s and lack of viability after re-introduction. Nevertheless, there solution, and then irrigated daily prior to the onset of the exper- could be many other negative traits underlying the ecophysio- iment. Measurements corresponding to control treatments were logical performance that could limit the grow and survival of made during the first day of the experiment, when all the plants in their native habitat. The habitat of L. minoricensis has plants were well watered. Thereafter, irrigation was stopped on a Mediterranean-type climate, characterized by hot, dry sum- five plants and measurements made when soil water content mers alternating with cool, wet winters (Nahal, 1981). From reached 65% (mild drought treatment), 58% (moderate drought an ecophysiological point of view, the variability and unpre- treatment) and 50% (severe drought treatment) with respect to dictability of precipitation in such environment imposes strong control. Re-watering was measured 1 day after re-filling pots. constraints on plants that could be extremely important for the Pots were weighted daily to determine soil water content. Five survival of individuals (Joffre et al., 1999). The seasonal fluctu- control plants were watered daily throughout the experiment to ations in soil moisture, particularly during summer drought, are ensure that they maintained constant values of each parameter considered a limiting factor for the growth and productivity of during the experiment. The experiment lasted 21 days. Mediterranean perennial species (Mitrakos, 1980). Indeed, the severity of this stress in Mediterranean areas has increased over 2.2. Plant water status the last Century, providing more frequent and longer drought periods (Osborne et al., 2000). These changing climatic and Pre-dawn (Ψ MD) and midday leaf water potential (Ψ MD)was environmental conditions may add even more dramatism to the determined with a Scholander chamber (Soil Moisture Equip- unsuccessfulness of the low genetically diverse populations of ment Corp., USA) in four replicates per treatment. L. minoricensis. Relative leaf water content at pre-dawn (RWCPD) and mid In addition to the possible existence of physiologically related morning (RWCMD) was determined as follows: RWC = (fresh negative traits, in many cases the extinction of species derives weight − dry weight)/(turgid weight − dry weight) × 100. The from a combination of other diverse factors. Among these, habi- turgid leaf weight was determined after keeping the leaf in dis- tat disturbance, fluctuating environments, niche competition, tilled water in darkness at 4 ◦C to minimise respiration losses, pests, predation, introgression and hybridization with relatives, until they reached a constant weight (full turgor, typically after and extensive recollection
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