Article

Chorological differentiation of endemo-relic species Ramonda serbica Panc. and R. nathaliae Panc. et Petrov. (Gesneriaceae) on the Balkan peninsula

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  • Faculty of Biology, University of Belgrade, Serbia
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... Among the rare angiosperm resurrection plants of the northern hemisphere are two endemic and preglacial relict species of the genus Ramonda-R. serbica and R. nathaliae (Košanin 1921, Stevanović et al. 1991. They grow on the shallow soil in crevices of the northern rocky slopes of gorges and canyons of the Balkan Peninsula, from the foothills to the upper alpine belts. ...
... These plants need effective protection against the free radical attack experienced either during dehydration or immediately upon rehydration. Although phylogenetically closely related, these plants differ in their ecological requirements (Stevanović et al. 1991) and ploidy levels (Š iljak-Yakovlev et al. 2008). Protective systems involved in the response to dehydration/ rehydration, such as changes of membrane lipids (Quartacci et al. 2002), ascorbate and glutathione contents (Sgherri et al. 2004), antioxidative enzyme activities (Veljović-Jovanović et al. 2006;Veljović-Jovanović et al. 2008), have been investigated in R. serbica but not in R. nathaliae. ...
... The polyploid R. serbica has until now received more attention. The diploid R. nathaliae, probably the evolutionary older species (Š iljak-Yakovlev et al. 2008), is restricted to habitats with least competition and consequently exposed to even harsher environmental conditions where the drought is prolonged and more severe (Stevanović et al. 1991). ...
Article
In order to investigate changes of oxidative status in relation to the activity of the various protective mechanisms in resurrection plant Ramonda nathaliae, we have analysed time and relative water content (RWC) related changes in lipid peroxidation and ion leakage, hydrogen peroxide accumulation, changes of pigment content and antioxidative enzyme activity, together with expression of dehydrins. The results indicate that enhanced oxidative status during dehydration, not previously reported for resurrection plants, could play an active role in inducing the desiccation adaptive response in R. nathaliae. A critical phase is shown to exist during dehydration (in the range of RWC between 50 and 70%) during which a significant increase in hydrogen peroxide accumulation, lipid peroxidation and ion leakage, accompanied by a general decline in antioxidative enzyme activity, takes place. This phase is designated as a transition characterized by change in the type of stress response. The initial response, relying mainly on the enzymatic antioxidative system, is suspended but more effective, desiccation specific protective mechanisms, such as expression of dehydrins, are then switched on. The expression of dehydrins in R. nathaliae could be inducible as well as constitutive. In order to cope with the oxidative stress associated with rapid rewatering, R. nathaliae reactivated antioxidative enzymes. We propose that controlled elevation of reactive oxygen species, such as hydrogen peroxide, could be an important mechanism enabling resurrection plants to sense dehydration and to trigger an adaptive programme at an appropriate stage during the dehydration/rehydration cycle. KeywordsResurrection plants– Ramonda nathaliae –Dehydration/rehydration–Antioxidative systems
... As it prefers more open habitats and higher altitudes it is considered to be more tolerant than R. serbica. (Stevanović et al. 1991). ...
... Since their discovery in the 19 th century (Pančić 1874, Petrović 1885, the Balkan Ramonda species were continuously studied from different biological and ecological aspects and have awakened the curiosity of researchers. The studied features include taxonomy, phytogeography, ecology, embryology and ecophysiology (Košanin 1921, 1939, Stefanoff & Georgiev 1937, Micevski 1956, Quezel 1968, Meyer 1970, Janković & Stevanovic 1981, Stevanović & Stevanović 1985, Stevanović et al. 1986a, 1986b, 1987, 1991, Stevanović, 1986, 1989 Peninsula. In Macedonia it forms three plant associations: AsplenioRamondetum nathaliae and ScorzoneroRamonde tum nathaliae on serpentine bedrock and AchilleoRamon detum nathaliae on limestone bedrock . ...
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In Europe, the genus Ramonda is represented with three species: Ramonda nathaliae, Ramonda serbica and Ramonda myconi. The first two are endemic Balkan species that are distributed also in Kosovo. These species grow in limestone as well as serpentine substrates, forming chasmophytic vegetation. The species Ramonda nathaliae is found in Macedonia, Greece, Serbia and in two localities in Kosovo, in the Sharri Mountains (Luboten and Gotovushë). R. nathaliae forms the following plant associations in the serpentines of Macedonia: Asplenio-Ramondetum nathaliae and Scorzonero-Ramondetum nathaliae, and the Achilleo-Ramondetum nathaliae in limestone substrates. Ostrya carpinifolia is charateristic species in Querco pubescentis-Ostryetum carpinifoliae, Ostryo-Fagetum, Querco-Ostryetum carpinifoliae and Corylo colurnae-Ostryetum carpinifoliae. This paper presents plant communities of Ramonda nathaliae and Ostrya carpinifolia in a limestone habitat, where the proposed new plant association named Ramondo-Ostryetum carpinifoliae ass. nova. is described. This plant community belongs to the class Quercetea pubescentis, order Quercetalia pubescenti-petraeae and alliance Fraxino orni-Ostryion. It was found and described on the limestone substrate on Mt. Luboteni (at 960‒982 m a.s.l.).
... They live in the close proximity to mosses and ferns, such as the poikilohydric moss Tortella tortuosa and fern Asplenium ceterach, as well as the drought tolerant ferns A. ruta-muraria and A. trichomanes. Their chorological differentiation is based on the fine differences in their ecological preferences ( Košanin, 1921;Stevanoví c et al., 1986;Stevanoví c et al., 1991). Thus, R. serbica inhabits rather cool and humid places in shadow, mostly on steep, north exposed, calcareous rocks, often well sheltered by a forest canopy. ...
... However, it has also been found to grow successfully alongside R. serbica in two sympatric populations in SE Serbia, within which they hybridize ( Siljak-Yakovlev et al., 2008;Lazareví c et al., 2013). Moreover, R. nathaliae is also found in harsh serpentine areas where it is subjected to metal overload and to drought conditions that are often more severe than in its usual limestone habitats ( Stevanoví c, 1989Stevanoví c,-1991Lazareví c et al., 2013;Rakí c et al., 2013). As desiccation tolerant plants (DT), both Ramonda species undergo dehydration of their vegetative tissues in the dry periods of the year. ...
... R. nathaliae is found in more restricted and rather compact area situated mostly in Macedonia and partially in Greece and in Kosovo. Its altitudinal range is somewhat wider, from 100 to 2200 m asl, and its habitats belong to the Aegean river system (Meyer, 1970;Stevanović et al., 1991). Within this distribution area in only two localities (Pčinja and Raduša gorges) R. nathaliae thrives on serpentine soil (Košanin, 1921;Stevanović and Stevanović, 1985). ...
... Therefore, the type and the traits of the soil are the prerequisites for the protection of these species survival in extreme habitat conditions. Clear differences exist between R. serbica and R. nathaliae with regard to their respective ecoanatomical and ecophysiological characters (Stevanović 1986(Stevanović , 1989(Stevanović -1991Stevanović et al., /1998. R. serbica performs as mesophyte: it grows in fairly humid and warm habitats, situated in rocky outcrops sheltered by surrounding shrubs and small trees, or in the forest understory. ...
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Paleoendemic species of the monophyletic genus Ramonda (R. myconi, R. serbica and R. nathaliae) are the remnants of the Tertiary tropical and subtropical flora in Europe. They are the rare resurrection plants of Northern Hemisphere temperate zone. Ramonda serbica and R. nathaliae are chorologically differentiated in the Balkan Peninsula and occupy similar habitats in calcareous, northward slopes in canyons and mountainsides. They remain well-hydrated during spring, late autumn and even in winter. In summer and early autumn when plants are subjected to drought and thermal stress, their desiccation tolerance comes into operation and they fall into anabiosis. Investigations revealed the permanent presence of ubiquitine and its conjugates, high amounts of oxalic acid and proline. Both species are homoiochlorophyllous. It enables them to rapidly resume photosynthesis upon rehydration, but also makes them susceptible to ROS formation. Dehydration induces activation of antioxidative enzymes (APX, GR, PPO), increase in amounts of AsA and GSH, phenolic acids, dehydrins, sucrose and inorganic ions. Plasma membranes, characterized by high amount of cholesterol, are subjected to decrease in membrane fluidity mostly on account of increased level of lipid saturation.Cytogenetic analysis revealed that R. nathaliae is a diploid (2n=48) and probably evolutionary older species, while R. serbica is a hexaploid (2n=144). Two species live together in only two localities forming hybrid individuals (2n=96). Polyploidization is the major evolutionary mechanism in the genus Ramonda that together with hybridization ability indicates that these relict species which have preserved an ancient survival strategy are not the evolutionary „dead end“.The species of the genus Ramonda are promising sources of data important for understanding the complex strategy of resurrection plants’ survival, appraised through a prism of their evolutionary and adaptive potential for multiple environmental str
... Numbers of localities corresponded to those listed in Table 1. range in SE Serbia (Kosanin, 1921;Meyer, 1970;Stevanovic et al., 1986aStevanovic et al., ,b, 1991 (Fig. 1). ...
... The Balkan Ramonda species were discovered at the beginning of 19th century by Serbian botanists Pancic and Petrovic. Their taxonomy, phytogeography, ecology, embryology and ecophysiology have since been studied (Pancic, 1874;Petrovic, 1885;Kosanin, 1921Kosanin, , 1939Glisic, 1924;Stefanoff and Georgiev, 1937;Micevski, 1956;Quezel, 1968;Meyer, 1970;Jankovic and Stevanovic, 1981;Stevanovic and Stevanovic, 1985;Stevanovic et al., 1986aStevanovic et al., ,b, 1987Stevanovic et al., , 1991Stevanovic, 1986Stevanovic, , 1989Stevanovic et al., 1992;Stevanovic and Glisic, 1997). However, cytogenetic data on the genus are still very scarce. ...
Article
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The genus Ramonda includes three preglacial paleoendemic species surviving as the rare resurrection angiosperms of the Northern hemisphere in refugia habitats in the Balkan (Ramonda nathaliae and Ramonda serbica) and Iberian Peninsulas (Ramonda myconi). This study focuses on: assessing genome size and base composition, determining chromosome number and ploidy level in several populations, evaluating inter- and intra-specific variations in DNA content and chromosome number as well as looking for the possible hybridization in the sympatric zones of Balkan species. R. nathaliae and R. myconi are diploid species (2n=2x=48) while R. serbica is hexaploid (2n=6x=144). The mean 2C DNA values ranged from 2.30pg for R. nathaliae to 2.59pg for R. myconi compared to 7.91pg for R. serbica. The base composition for R. nathaliae was 42.1% GC, for R. myconi 39.9% and for R. serbica 41.2%. In one population of R. serbica the DNA content ranged from 2C=7.65 to 11.82pg, revealing different ploidy levels among its individuals. In sympatric populations genome size was intermediary (∼5pg) between the diploid and hexaploid classes which indicates the hybridization ability between R. serbica and R. nathaliae. It appears that polyploidization is the major evolutionary mechanism in the genus Ramonda.
... We presume that these plant species have preserved the natural and molecular mechanisms of adaptation to their environment. R. serbica usually grows in more favorable habitats with mosses, which preserve the soil humidity, often sheltered by forest canopy, whereas R nathaliae thrives under open, drier, and warmer habitats (Stevanovic et al., 1991). Mosses are efficient in absorbing moisture and simultaneously they play the role of an insulating buffer that prevents rapid evaporation from the shallow soil (Rakic et al., 2009). ...
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Introduction: Ramonda nathaliae and Ramonda serbica are resurrection plants belonging to homoiochlorophyllous desiccation-tolerant angiosperms. Chlorophyll biosynthesis is one of the most important metabolic pathways to tolerate desiccation in these plant species. Materials and methods: To better understand the early pathway steps of chlorophyll biosynthesis, we have analyzed the enzyme δ-aminolevulinic acid dehydratase (ALA-D) and contents of δ-aminolevulinic acid (ALA) and total chlorophyll as a final product during dehydration and rehydration stages for these plant species. Results: Our results showed that the activity of ALA-D in R. nathaliae and R. serbica plants rapidly decreased during dehydration and in the final stage of desiccation the activity of this enzyme was decreased by 79% and 86%, respectively. After rehydration of plants, the ALA-D activity was fully restored. In contrast, the ALA content of both plant species significantly increased during desiccation and decreased after 48 hr of rewatering. In each stage of dehydration or rehydration, a significant negative correlation was established between ALA-D activity and ALA content in both plant species. Conclusions: Total chlorophyll content was preserved more in R. nathaliae than in R. serbica during desiccation. Moreover, ALA-D activity was decreased to a minimal level but preserved its function during desiccation, and this suggests one possible mechanism of desiccation tolerance to retain the chlorophyll of these plant species.
... and Jankaea Boiss.) and five species (Ramonda serbica, Ramonda nathaliae, Ramonda myconi, Haberlea rhodopensis and Jankaea heldreichii). Four of these species occur in Balkan Peninsula, and the only representative in Iberian Peninsula is R. myconi (Tutin et al. 1972;Stevanovic et al. 1991). R. serbica and R. nathaliae are endemic and relict species of the Balkan Peninsula. ...
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Ramonda serbica and Ramonda nathaliae are rare and endemo relict plant species from Balkan Peninsula. An efficient micro propagation and in vitro conservation method via direct and indirect organogenesis from seed and leaf explants, respectively, was established in this study. The seed of both Ramonda species were collected from different populations in Kosovo, and were germinated in nutrient media JG-B without any phytohormone. The highest number of shoots and multiplication rate was observed on JG-B medium supplemented with BAP and IAA (0.5 mg l−1 each), whereas the highest number of leaves per plantlets was found on WPM and RA medium supplemented with BAP and IAA (0.1 mg l−1 each). During this stage of micro propagation some significant differences were observed in plantlets from different populations. The indirect organogenesis from parts of leaves of natural plants was not successful due to unavailability of established protocol for disinfections of the plant material. On other hand, parts of leaves from micro propagated plantlets, cultured on MS medium supplemented with different ratio of BAP and NAA, resulted in the highest efficiency for shoot regeneration. In vitro conservation of micro propagated plants at the lower temperature (4 °C) had a significantly positive effect for storage of more than 12 months.
... Macedonia), except in E. Serbia, where both species grow in syntopy and/or sympatry (Stevanović et al. 1986a(Stevanović et al. , 1986b. Namely, the major part of the range of R. nathaliae is restricted to the Aegean river system in R. Macedonia (Vardar and its tributaries), while the range of R. serbica covers gorges, canyons and ravines of the Adriatic river system in Montenegro, S.W. Serbia (Kosovo and Metohija province) and Albania (Košanin 1921;Stevanović et al. 1991). ...
Article
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Chasmophytic communities of endemic and relict species Ramonda nathaliae on ophiolithic (serpentine) substrate are very rare phenomenon in the whole range of the species considering that it grows mainly on limestone. The paper presents the two communities of R. nathaliae on serpentine habitats: Asplenio-Ramondaetum nathaliae previously described near the village Raduša and new community Scorzonero-Ramondaetum nathaliae from the gorge of the river Pcinja. Floristic composition, chorological and life form spectra of these two communities are compared. The syntaxonomical position of these communities in relation to the alliance of chasmophytic vegetation on limestone Ramondion nathaliae and alliance of serpentine rocky grasslands of alliance Centaureo-Bromion fibrosi is discussed. Due to significant floristic differences between communities of R. nathaliae on serpentine and those growing on limestone, a new sub-alliance Ramondion nathaliae serpentinicum is proposed. © 2014 Institute of Botany and Botanical Garden Jevremovac, Belgrade.
... Additional shared feature is the abundant presence of mycorrhizal fungi that colonize the roots of R. nathaliae individuals. Taken together, the area of the serpentine habitat, the dominant status of R. nathaliae within it, and the plant's long persistence on the site make it evident that the plant's serpentine population is as well established and stable as the population growing on limestone (Košanin, 1921;Stevanović et al., 1991). ...
... The distribution of Ramonda serbica today extends from NE, SW, and SE Serbia and NW Bulgaria, through SE Montenegro and Albania, to W Macedonia and NW Greece. Ramonda nathaliae is restricted to Central Macedonia and North Greece with several localities in SE Serbia (Košanin, 1921;Stevanović et al., 1986aStevanović et al., , 1986bStevanović et al., , 1991. The 2 species cooccur only in SE Serbia, establishing a sympatric zone with mixed syntopic populations (Stevanović et al., 1986b). ...
Article
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The pollen and seeds of 3 paleoendemic resurrection species, Ramonda myconi (L.) Rchb. (Iberian Peninsula), R. nathaliae Pančić & Petrović, and R. serbica Pančić (Balkan Peninsula), as well as of natural hybrids between the 2 last species, have been analyzed using light and scanning electron microscopy. Their general structural differences, taxonomic and phylogenetic significance, pollen viability, and seed germination capacity, as well as the correlation of pollen and seed characteristics and plant ploidy levels, have been studied. The pollen grains are small (R. myconi, R. nathaliae) to medium (R. serbica) in size, ranging from 10 to 28 μm, and 3-colporate, isopolar monads with microreticulate-perforate exine. Seeds are small, 309 to 1000 μm long and 80 to 425 μm wide, elongated, with a reticulate surface and auriculate ornamentation. Micromorphologies of the pollen exine ornamentation and seed surface revealed significant differences among the 3 species. Pollen from hybrid individuals was heterogeneous in size and morphology, and the germination of their tiny seeds was very low. A strong correlation was found between pollen size, DNA content, and chromosome number. The environmental influence on pollen and seeds of 3 species and especially of the R. nathaliae population growing on serpentine is also discussed.
... The aim of this paper is to lectotypify the name Ramonda serbica. It was described from Serbia (Pančić 1874) and also occurs in Albania, Bulgaria, Greece, Kosovo, Macedonia and Montenegro (Stevanović et al. 1986aStevanović et al. , 1991 Stevanović and Bulić 1992). Ramonda serbica has been the subject of many studies concerning its distribution, ecology and syntaxonomy (Janković and Stevanović 1981, Stevanović and Stevanović 1985; Hill 1986; Stevanović 1986; Stevanović et al. 1986b Stevanović et al. , 1987), but has not been typified to date (cf. ...
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A lectotype of the name Ramonda serbica Panč, is designated from Pančic's specimens held in the Hungarian Natural History Museum in Budapest (BP) and illustrated.
... R. serbica inhabits in more humid and cooler habitats, primarily sheltered by forest canopy, while R. nathaliae is found in more open, drier and warmer habitats. These ecological differences showed that R. nathaliae is a more xerophiluos species than R. serbica (Stevanovic et al. 1991). Therefore, the preservation of the RWC in R. serbica more than in R. nathaliae, in first stage of dehydration (D1), could be as a result of these conditions. ...
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The desiccation-tolerant plants of the R. serbica and R. nathaliae are resurrection plants which are able to fully recover their physiological function after anabiosis. A comparison of chlorophyll fluorescence imaging and photosynthetic pigment contents responses of R. serbica and, for the first time, R. nathaliae to dehydration and rehydration were investigated. For this purpose, plants after collection from their natural habitats were kept fully watered for 14 days at natural condition. The experiment was conducted with mature leaves of both species. R. serbica and R. nathaliae plants were dehydrated to 5.88 % and 7.87 % relative water content (RWC) by withholding water for 15 days, afterwards the plants were rehydrated for 72 hours to 94.67 % and 97.02 % RWC. During desiccation, R. serbica plants preserved the chlorophyll content about 84 %, while R. nathaliae about 90 %. During dehydration when RWC were more than 40 %, photochemical efficiency of PSII for photochemistry, the Fv/Fm ratio, decreased about 40 % in R. nathaliae plants, but a strong reduction with 60 % was recorded for R. serbica. Following rehydration, the Fv/Fm ratio recovered more rapidly in R. nathaliae. The higher photosynthetic rates could also be detected via imaging the chlorophyll fluorescence decrease ratio Rfd, which possessed higher values after rehydration leaves of R. nathaliae as compared to R. serbica. The results showed that the photosynthetic activity and chlorophyll contents after rehydration are recovered more rapidly in R. nathaliae in comparison to R. serbica.
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Ramonda serbica is a Balkan endemic and relict plant, included in the European list of rare plants. The aim of this study is to present the current natural condition and to elaborate the risk assessment for extinction, and in vitro conservation of R. serbica populations from Kosovo. We began a thorough exploration of the various habitats and ecological characteristics of R. serbica locations in the Sharri Mountains and Albanian Alps. The ecological responses of this species were more diverse than expected. We can explain the observed differences mostly as a response to the variations in the basic environmental conditions of the habitats. Almost all examined morphological characteristics, plant density and phenological traits were significantly different between the locations. In this case, locations with a small number of rosettes per m2 and a smaller regeneration were Radaci, The Rugova Canyon , Zhlebi Gorge , and The Sushica River Gorge , therefore, the risk for extinction is very high. According to the IUCN Red List Categories and Criteria, the conservation status of R. serbica populations in Kosovo should be estimated as Vulnerable (VU), B1ab(iii)+B2ab(iii). For the first time in Kosovo our research group began the in vitro micropropagation and conservation of the rare plant R. serbica. During the micropropagation some differences, but not significant, for the number of shoots per plantlets were recorded for the plantlets originating from the different locations. After micropropagation, plantlets from the different locations of R. serbica were transferred for in vitro conservation and preserved for 8-12 months without transfers.
Article
Ramonda serbica and R. nathaliae (Gesneriaceae) are endemo-relic species of the Balkan peninsula and the desiccation-tolerant homoiochlorophyllous flowering plants. In order to follow the pattern of chlorophyll metabolism during dehydration and after rewatering, the chlorophyll content was studied. Its change during the dehydration was monitored in intact plants and during the recovery in intact specimens as well as in cut off leaves. The regreening rate depended on previous hydration state of plants collected from their natural habitat. Eight to 12 h after the start of the rehydration of air-dried detached leaves the resynthesis of chlorophyll began. Rehydration and chlorophyll resynthesis were not light depended. Levulinic acid inhibited completely the chlorophyll resynthesis indicating that the regulatory site on the biosynthetic pathway was located before protoporphyrin formation. Chlorophyllase activity changed during the dehydration and rehydration, but the chlorophyll content was not in direct correlation with this enzyme activity.
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The "resurrection plant" Ramonda serbica is included in the Albanian and Bulgarian list of endangered plants as a rare, Balkanic-endemic species and tertiary relic species, while R. nathaliae is characteristic in the FYROM area. Our research groups have established national in vitro collections of R. serbica in Albania and Bulgaria and R. nathaliae in Macedonia. The aim of this joint study is (1) the choice of successful micropropagation methods as the basis for the in vitro collections and (2) the evaluation of polymorphism of some natural populations. In both collections, seeds were used as a convenient starting point for micropropagation in the nutrient medium JG-B. In the Bulgarian in vitro collection, a dry sterilization of seeds was applied for a first time for Gesneriaceae family. The micropropagation and conservation of Ramonda seeds and plantlets were similar in Albanian and Bulgarian collections. The plantlets in vitro as an explant material were developed in JG-B medium with different phytohormones. The direct organogenesis of two Ramonda species is very similar models. The method of conservation in vitro with minimal growth method (modification of nutrient medium) was used. Meiosis and mitosis examinations of the natural populations and plantlets cultivated in vitro were carried out by standard Squash method. Cytogenetical study of natural populations showed polyploid forms as a mixture (2n=72) and (2n=96). Mitosis preparations in plantlets in vitro showed a predominance of the most frequent form (2n=96). The biodiversity in interspecific level of the natural populations of Ramonda serbica of Central Albania, R. nathaliae from Macedonia and cultivated plantlets in vitro from Albania and Bulgaria was evaluated via molecular markers (RAPDs). The micropropagation method is a convenient way for the international exchange of germplasm of rare and endemic plants. From the data obtained in this study it can be concluded that RAPD markers provided a useful technique to study genetic diversity in Ramonda serbica and R. nathaliae populations. This technology allows the identification of different populations as well as the assessment of the genetic similarity among different populations.
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Comparative analysis of the electrolyte efflux, as a screening test of the membrane tolerance to water stress, was carried out in poikilohydric plants Ramonda serbica Panč. and Ramonda nathaliae Panč. & Petrov. and homoiohydric plant Saintpaulia ionantha Wendl. from the same family Gesneriaceae. Water stress was induced by PEG 600. The high degree of solute leakage in the East-African drought-intolerant Saintpaulia ionantha points to the loss of membrane integrity. In contrast, Balkan endemites Ramonda serbica and R. nathaliae show high resistance to water stress due to the specific constitutional drought tolerance mechanisms.
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