ArticlePDF Available

Abstract and Figures

This study presents the preliminary results on sexual reproduction of Haberlea rhodopensis, Gesneriaceae – a Tertiary relict and endemic species to the Balkan Peninsula. Our experiments have shown that H. rhodopensis is self-compatible, but not autogamous. Phenology of the populations, herkogamy and weak protrandry are mechanisms which favour the outcrossing in natural populations. Pollination success is characterized by high seed production. Seeds germinate readily, but grow extremely slowly and few of them survive to adult plants in culture and in natural populations.
Content may be subject to copyright.
PHYTOLOGIA BALCANICA 19 (2): 201 – 208, Sofia, 2013
Breeding systems of Haberlea rhodopensis (Gesneriaceae), a
Tertiary relict endemic to the Balkan Peninsula
Katerina Bogacheva-Milkoteva1, Ekaterina Kozuharova1, Regine Claßen-Bockhoff 2
1 Department of Pharmacognosy, Faculty of Pharmacy, Medical University of Sofia,
2 Dunav Str. 1000 Sofia, Bulgaria, e-mail:, e-mail: ina_ (corresponding author)
2 Johannes Gutenberg-University, Institut für Spezielle Botanik, 55099 Mainz, Germany,
Received: May 26, 2013 ▷ Accepted: July 28, 2013
Abstract. This study presents the preliminary results on sexual reproduction of Haberlea rhodopensis, Gesneriaceae – a
Tertiary relict and endemic species to the Balkan Peninsula. Our experiments have shown that H. rhodopensis
is self-compatible, but not autogamous. Phenology of the populations, herkogamy and weak protrandry are
mechanisms which favour the outcrossing in natural populations. Pollination success is characterized by
high seed production. Seeds germinate readily, but grow extremely slowly and few of them survive to adult
plants in culture and in natural populations.
Key words: breeding systems, floral mechanism, Haberlea rhodopensis, phenology, seed set
Haberlea rhodopensis Friv. (Gesneriaceae) is a Ter-
tiary relict and Balkan endemic. In Europe, there
are only three genera in the family: Haberlea (in
Bulgaria and Greece), Ramonda (Balkans and Ibe-
rian Peninsula) and the monotypical Jankaea (in
Greece) (Ganchev 1950).
Haberlea rhodopensis is a medicinal plant, list-
ed in the Bulgarian Medicinal Plants Act (2000).
It is also an amazing resurrection plant; therefore,
recently most investigations have focussed on its
desiccation tolerance mechanisms and potential
for multipurpose usage. Efforts at conservation of
Haberlea rhodopensis are based mainly on in vitro
cultures, ex situ collections and habitat exploring
(Djiljanov & al. 2009). The plant propagates vege-
tatively and it is possible to cultivate it from seeds
(Ganchev 1950; Djiljanov & al. 2005), but there are
no studies on its breeding system.
The aim of our study was to throw light on the
breeding systems of Haberlea rhodopensis: 1) to test
outcrossing of the species and its mechanism; 2) to
test seed germination and early stages of ontogen-
esis; 3) to compare native populations and plants
grown ex situ.
Material and methods
Material and methods
We have used plant material collected from five
natural localities in Central and Eastern Rhodopi
Mts, Bulgaria and an ex situ collection from the Bo-
tanical Garden at Johannes-Gutenberg University
of Mainz, Germany. Observations were conducted
in 2008–2010 and 2012, during the flowering pe-
202 Bogacheva-Milkoteva, K. & al. • Breeding systems of Haberlea rhodopensis
riod from April to July. For laboratory works, we
used the Leitz Diaplan light microscope with flu-
orescence equipment, Binokular Leica MZ 16A,
Fuchs-Rosenthal counting chamber, Philips XL 30
scanning electron microscope (SEM), and Leica
Application Suite software and Image Tool MT 3.00
for photographs, pollen and ovule counting. The
authors have followed the manufacturers’ instruc-
tions and standard protocols.
Phenology. In the flowering period (April–July) of
2008–2010 and 2012, in situ (natural populations)
and ex situ observations have been carried out at
different altitudes and slope exposures. Life du-
ration of free and bagged-flower plants was com-
pared. For the purpose, two sites were chosen with
different sun exposure, so as to trace out any dif-
ferences in phenology, according to the autecolog-
ical factors.
Breeding systems. In order to test autogamy, the
protocols of Dafni (1992) were considered and con-
sequently were bagged: a) a total of 123 flowers of
29 plants for spontaneous self pollination, b) 38
hand-selfed flowers from six plants, c) four hand-
crossed flowers from four plants, and d) 10 untreat-
ed control flowers from three plants. Plant rosettes
were transferred to the experimental plot of the
Faculty of Pharmacy at different time of the year. To
test ability of propagation by leaves, 10 leaves were
put into a light soil mix. Ovaries and anthers were
sampled from three different sampling sites: Beden
village in 2008 (Central Rhodopi), river Borovitsa
in 2010 (Eastern Rhodopi), Ustovo district in 2010
(Central Rhodopi), and the Botanical Garden of
Mainz University, Germany in 2012. Pollen grains
and ovules were counted and calculations were per-
formed according to the standard methodology
(Cruden 1977; Daphni 1992).
Floral mechanism. To investigate dichogamy
and/or herkogamy, we have dissected and photo-
graphed flowers in different stages.
Stigma receptivity. To evaluate changes on the stig-
ma surface indicating receptivity, we have collected
stigmas from flowers in different phases of develop-
ment, and photographed them with SEM.
Pollen tube growth. Six flowers in bud stage were
bagged and hand-selfed. We sampled the stigmas 3,
4 and 20 hours after pollination and have observed
the pollen tube growth under a fluorescence micro-
Pollination success. Seed set per fruit of a random
sample in plants from different sampling sites was
Seed germination and mycorrhiza. Fifty fresh
seeds from the Ustovo district and the Botanical
Garden of Mainz and 50 two-year old seeds from
Yagodina and Mugla villages were placed in Petri
dishes on wet filter paper, or directly in soil, with-
out additional treatment. Three weeks later the
two-year old seeds were scarificated. Squash micro-
scopic preparations of roots were made following
the standard method, so as to test the plant for my-
Results and discussion
Results and discussion
Phenology. Anthesis is most prolonged in the natu-
ral populations (22 days) and the shortest in the shady
population from the Botanical Garden (12 days). The
exposed to sunshine ex situ population had an 18-days
anthesis. In spite of the same altitude, the anthesis in
the shady population of the Botanical Garden began
a week later, but ended at the same time. Compared
with the natural habitat at 800 m, anthesis in the ex si-
tu population had begun a month earlier at about 100
m. A comparison of the results in the natural habitat
for the years 2010 and 2012 has shown that in 2010
anthesis began on 15th May, and in 2012, after a very
long and cold winter, it began on 24th May (Fig. 1).
Life duration of a flower was prolonged between 7–10
days and no difference was traced out between free
and bagged flowers. Observation also showed that the
flowers in inflorescence of one individual were in dif-
ferent phases of flowering, as well as the individuals in
a population.
On 24th August 2008, secondary flowering was ob-
served in the area of Chudnite Mostove (Central Rho-
dopi, at 1500 m). The flowering buds were laid in au-
tumn and were preserved in winter time.
203Phytol. Balcan. 19(2) • Sofia • 2013
Fig. 1. Comparative phenology of three sites: a) population exposed to sunshine from the Botanical Garden of Mainz University, 100 m a.s.l.;
b) population in shadow from the Botanical Garden of Mainz University; c) natural population in Ustovo district, Central Rhodopi , 800 m a.s.l.
youn g flowers
204 Bogacheva-Milkoteva, K. & al. • Breeding systems of Haberlea rhodopensis
Breeding system. Haberlea rhodopensis is a long-
living perennial (Plate 1, Fig. 1). Plants of the white
variety ('Virginalis') are grown in the UK since
1938, and still grow strongly in the course of 75
years. This corresponds to the reports concerning
the age of plants from the sister species Ramonda
myconi. Data on the accumulated individual growth
in size (number of leaves and rosette diameter) sug-
gest that under the current environmental condi-
tions the time from germination to attainment of
the minimum size for reproduction is ca. 70 years.
Similarly, the estimated age of a plant with 11 leaves
and rosette diameter of 12 cm (the median size of
plants in all the regions) is 200–250 years (Dubreuil
& al. 2008).
Haberlea rhodopensis has good ability for vege-
tative propagation (Plate 1, Fig. 1, Plate 2, Fig. 1).
In situ the big plants shoot thin pale-yellow hori-
zontal rhizomes, running under the moss around
the plants, and bear small rosettes. Such rhizomes
have never been seen in cultivated plants, however,
it was certainly easy to divide the large plants and
grow up many of the divisions ex situ. Even some ex
situ propagation by leaf was possible: three of the
leaves produced daughter rosettes, although they
remained extremely small and did not develop in-
to big plants. Plants transferred in spring and early
summer, especially if taken with the moss cushion,
were doing very well ex situ (Plate 1, Fig. 4, On the
other hand, if the plants were transferred in the au-
tumn they had zero ability to survive.
The flowers bear features of bee pollination syn-
drome (Plate 1, Fig. 2, Plate 2, Fig. 2,). The tested
flowers did not self-pollinate spontaneously. None
of the 123 bagged flowers tested for spontaneous
self-pollination set seeds. There was no self incom-
patibility, as 16 flowers (50 %) of the hand-selfed
ones produced seeds. The control hand-crossed
four flowers (100 %) produced seeds, which have
proved that bagging does not effect the process of
pollination and fertilization. Eight of the ten un-
treated flowers set seeds (80 %).
An alternative method for testing the breed-
ing system by calculation of P/O ratio correspond-
ed partially to the field tests. Interestingly, differ-
ent values of pollen-to-ovule ratio were recorded
for the different sampling sites: Beden village 308:1,
river Borovitsa 94:1, Ustovo district 141:1, and
Mainz Botanical Garden 141:1. Following Cruden`s
classification of the breeding system P/O ratio, var-
ying in the populations between 94:1 and 308:1, in-
dicates an obligate to facultative autogamy (Cruden
1977). If taken into account that pollination success
is not dependent solely on pollen limitation, but is
due to sex allocation, it could be maintained that
the increased number of ovules is not just an auto-
gamy indicator, but an attempt at ensuring a maxi-
mum seed set (Etcheverry & al. 2012).
Pollen tube growth. Our results show that self pol-
len germinates on the stigma of the same individu-
al. Three hours after pollination, pollen germina-
tion is at its very beginning. After four hours the
pollen tubes can be clearly distinguished and twen-
ty hours after pollination the pollen tubes reach
about 2–3 mm in the pistil (Plate 1, Fig. 6).
Floral mechanism. In our opinion, outcrossing was
favoured under natural conditions: weak protandry
was observed and strong herkogamy, as mecha-
nisms which support outcrossing. In the bud stage,
the anther length exceeded the length of the pistil
and they were situated above the stigma (Plate 1,
Figs 3, 5). In many cases, the extrorse pollen-shed-
ding anthers opened in the bud stage, thus self pol-
len deposition on the stigma was possible, but at
that time the stigma was not receptive.
Stigma receptivity. Changes in the stigma area in-
dicating receptivity are visible on the microscopic
pictures 2–3 days after the flower opening (Plate 2,
Figs 5, 6). During bud development the pistil grows
and, when the flower opens, the pistil length ex-
ceeds the length of anthers. Anthers remain fas-
tened in pairs about 3 mm under the stigma level
on the pistil.
Pollination success. Eighty percent of the random-
ly collected fruits for estimation of the free pollina-
tion success had seeds. Sixteen percent of the flow-
ers had not been pollinated and four percent were
predated. Seed set in a fruit of a random sample
showed that on the average 70 % of the ovules per
fruit have matured to seeds (Fig. 2).
Obviously, when self pollen reaches the receptive
stigma, pollination starts and seeds are formed, but
a pollen-transporting agent is needed. The relative-
ly high fruiting success of the control flowers shows
205Phytol. Balcan. 19(2) • Sofia • 2013
Seed set per fruit
129,6 147
174,8 0
428,2 632,8 507,5
ovules damaged seeds
Fig. 2. Seed set per capsule of random
samples from four di erent natural popu-
lations in the Central Rhodopi Mountains.
that pollination is efficient, but bagging experiments
reveal that Haberlea is self-compatible, though not
generally autogamous. Our results correspond to the
data obtained for the related species Jankaea heldre-
ichii (Vokou & al. 1990) in Greece, which also pro-
duces a high number of seeds per capsule and is not
autogamous, as well as for Ramonda myconi on the
Iberian Peninsula (Pico & Riba 2002).
Seed germination and mycorrhiza. The seeds
of H. rhodopensis readily germinate after 7–12
days. Seedlings grow extremely slowly, reaching a
length of less than 4 mm in five months as shown
in Plate 2 Fig. 6. After five months, less than 1 %
of the seeds survived. Two-year old seeds did not
germinate, even after being scarificated for a week.
The root microscope preparations clearly show the
structures, which indicate the mycorrhiza (Plate 2,
Fig. 4). Mycorrhizas have been observed also in the
related species R. serbica (Rakic & al. 2009).
Observations of the natural populations have
shown that they are dominated by adult plants.
Young plants were very few and no seedlings could
be found. Demographic studies of the sister species
Ramonda myconi are in concordance with the pre-
sent study: populations of this species exist due to
the adult, well-adapted plants (Pico & Riba 2002).
Young plants of H. rhodopensis seldom survive, so
vegetative reproduction and preservation of the ex-
isting plants is of extreme importance for conserva-
tion of the species. In spite of the desiccation toler-
ance of adult plants, it is not certain that seedlings
are desiccation tolerant. Thus drought may be a
limiting factor in nature. Another possible explana-
tion is the lack of suitable surfaces, where the seed-
lings can get established, supposedly as in the case
of R. myconi (Pico & Riba 2002) – the steep, rocky
slopes are often flooded. Taking into account that
the species is self compatible, other possible expla-
nation of its low survival rate can be potential in-
breeding depression. This could be regarded as a di-
rection for future studies. The low survival rate of
the seedlings in culture could be explained by the
lack of symbiotic fungi.
Although the populations are not endangered pres-
ently and the species is categorized as Least Concern
(Petrova & Vladimirov 2009), picking of adult plants
is the main hazard factor for the balance in the popu-
lations. Ex situ collections and in vitro cultures are ex-
tremely important for investigation, but future stud-
ies should also include aut- and sinecological factors,
such as pollinating agents, symbiotic or antagonistic
relationships, demographic structure of the popula-
tions, possible genetic sequences of self-compatibility,
and effectiveness of the mechanisms preventing auto-
gamy. The protection status of Haberlea rhodopensis
should also correspond to the tendencies in the devel-
opment of natural populations.
206 Bogacheva-Milkoteva, K. & al. • Breeding systems of Haberlea rhodopensis
Plate I. Fig. 1. Typical microhabitat of Haberlea rhodopensis; Fig. 2. e owers bear features of bee pollination syndrome; Figs 3 and
5. Floral mechanism – weak protandry and strong herkogamy; Fig. 4. Plants transferred in spring and early summer, especially if taken
with the moss cushion, were doing very well ex situ; Fig. 6. Pollen tube growth.
Plate I
207Phytol. Balcan. 19(2) • Sofia • 2013
Plate II. Fig. 1. Haberlea rhodopensis has good ability for vegetative propagation; Fig. 2.  e owers bear features of bee pollination
syndrome; Fig. 3. Seedling of age about four  ve months; Fig. 4. Root microscope preparations clearly show the structures, which indi-
cate the mycorrhiza; Figs 5 and 6. Changes in the stigma area indicating receptivity are visible on the microscopic pictures.
Plate II
5 6
208 Bogacheva-Milkoteva, K. & al. • Breeding systems of Haberlea rhodopensis
Acknowledgements. The study was conducted with the fi-
nancial support of the Deutsche Bundesstiftung Umwelt project,
Medical University of Sofia and Johannes Guthenberg University
of Mainz. The authors extend special thanks to Prof. A.J. Richards
for the interest in their work and his valuable comments.
Bulgarian Medicinal Plants Act 2000. Promulgated, SG
No. 29/7.04.2000, Amended, SG No. 23/1.03.2002, 91/25.09.2002
(in Bulgarian).
Cruden, W. 1977. Pollen-ovule ratios: a conservative indicator of
breeding systems in flowering plants. – Evolution, 31(1): 32-46.
Dafni, A. 1992. Pollination Ecology : A Practical Approach. Oxford
Univ. Press.
Djiljanov, D., Genova, G., Parvanova, D., Zapryanova, N.,
Konstan tinova, T. & Atanassov, A. 2005. In vitro culture of the
resurrection plant Haberlea rhodopensis. – Pl. Cell Tissue Organ
Cult., 80(1): 115-118.
Djiljanov, D., Ivanov, S., Georgieva, T., Monyakova, D., Berkov, S.,
Petrova, G., Mladenov, P., Christov, N., Hristozova, N., Peshev,
D., Tchorbadjieva, M., Alexieva, V., Tosheva, A., Nikolova,
M., Ionkova, I. & van den Ende, W. 2009. A holistic approach
to resurrection plants. Haberlea rhodopensis – a case study. –
Biotechnology & Biotechnological Equipment, 23(4):1414-1416.
Dubreuil, M., Riba, M. & Mayol, M. 2008. Genetic structure and
diversity in Ramonda myconi (Gesneriaceae): effects of historical
climate change on a pre-Glacial relict species. – Amer. J. Bot.,
95(5): 577-587.
Etcheverry, A., Aleman, M., Figueroa-Fleming, T., Lopez-Spahr,
D., Gomez, C., Yanez, C., Figueroa-Castro, D. & Ortega-Baes, P.
2012. Pollen:ovule ratio and its relationship with other floral traits
in Papilionoideae (Leguminosae): an evaluation with Argentine
species. – Pl. Biol, 14(1): 171-178.
Ganchev, I. 1950. Anabiotic desiccation resistance and other
biological traits of Haberlea rhodopensis Friv. – Izv. Bot. Inst.
(Sofia), 1(1): 191-214.
Petrova, A.& Vladimirov, V. (eds) 2009. Red list of Buglarian
vascular plants. – Phytol. Balcan., 15(1): 63-94.
Pico, F. & Riba, M. 2002. Regional-scale demography of Ramonda
myconi: Remnant population dynamics in a pre-Glacial relict
species. – Pl. Ecol., 161(1): 1-13.
Rakic, T., Quartacci, M F., Cardelli, P., Navari-Izzo, F. & Ste-
fa no vic, B. 2009. Soil properties and their effect on water and
mineral status of resurrection plant Ramonda serbica. – Pl. Ecol.,
208(1): 13-21.
Vokou, D., Petanidou, Th. & Bellos, D. 1990. Pollination ecology
and reproductive potential of Jankaea heldreichii (Gesneriaceae):
a tertiary relict on Mt Olympus, Greece. – Biol. Conservation,
52(2): 125-133.
... Borderea is an obligate outcrossed genus, for it is dioecious (García et al. 1995(García et al. , 2012. The three Gesneriaceae genera Haberlea, Ramonda and Jankea, are hermaphrodite, but incapable of spontaneous self-pollination (Bogacheva-Milkoteva et al. 2013a;Dubreuil et al. 2008;Vokou et al. 1990) even if the selfcompatibility has been recorded only in H. rhodopensis (Bogacheva-Milkoteva et al. 2013a) and R. myconii (Dubreuil et al. 2008). In Berardia subacaulis differently to the two Gesneriaceae species, the long pollen viability, the incomplete protandry of the florets and the secondary pollen presentation may allow for spontaneous self-pollination. ...
... Borderea is an obligate outcrossed genus, for it is dioecious (García et al. 1995(García et al. , 2012. The three Gesneriaceae genera Haberlea, Ramonda and Jankea, are hermaphrodite, but incapable of spontaneous self-pollination (Bogacheva-Milkoteva et al. 2013a;Dubreuil et al. 2008;Vokou et al. 1990) even if the selfcompatibility has been recorded only in H. rhodopensis (Bogacheva-Milkoteva et al. 2013a) and R. myconii (Dubreuil et al. 2008). In Berardia subacaulis differently to the two Gesneriaceae species, the long pollen viability, the incomplete protandry of the florets and the secondary pollen presentation may allow for spontaneous self-pollination. ...
... In paleo-endemic species considered in this study, climate change during the Quaternary presumably caused cycles of range contraction and expansion, reproductive isolation and genetic drift (Dubreuil et al. 2008;Segarra-Moragues et al. 2005, 2007Dubreuil et al. 2008). Most of these paleoendemics suffer from low pollinator service (Bogacheva-Milkoteva et al. 2013a;Dubreuil et al. 2008;García et al. 2012;Vokou et al. 1990), probably due to changes in pollinator network (H. rhodopensis and J. heldreichii) or to a very uncommon pollination system (Borderea genus). ...
Climate change is known to have a profound influence on plant reproduction, mainly because it affects plant/pollinator interactions, sometimes driving plants to extinction. Starting from the Neogene, the European climate was subjected to severe alterations. Nevertheless, several genera, including Berardia, survived these climatic changes. Despite the numerous studies performed about the relationship between climate change and plant reproductive biology, equivalent studies on ancient species are lacking, even though they may furnish crucial information on the strategies that allowed them to survive drastic climatic fluctuations. We investigated floral and reproductive features in Berardia subacaulis (Asteraceae), describing pollen vectors, capitulum and florets phenology, evaluating reproductive efficiency and defining the reproductive mode of the plant with bagging experiments and test of apomixis. B. subacaulis grows in habitats with low pollination services; it is self-compatible, but many typical features favouring cross-pollination are still present: florets are characterized by incomplete protandry, capitulum protogyny and high pollen-ovule ratio. The plant is not apomictic and self-fertilization is allowed within each capitulum. Similarly to other European Alpine endemics supposed to belong to the Mediterranean ancient tropical flora, the reproductive mode observed in the monospecific genus Berardia assured reproduction also under a pollinator decline. Differently from the other endemics, it took advantage of its spontaneous self-pollination and compatibility and its generalist pollination service, common both among high altitude plants and in the Asteraceae.
... Proteome, transcriptome and genomic approaches have identified protective mechanisms related to photosynthesis, cell wall folding and genome stability ( Jiang et al. 2007, L. , Zhao et al. 2014). Boea hygrometrica is propagated mainly via seeds, which is rare among other resurrection plant species within the Gesneriaceae, such as Haberlea rhodopensis and Ramonda myconi (Xavier Pico and Riba 2002, Bogacheva-Milkoteva et al. 2013). Unlike H. rhodopensis and R. myconi, both young and perennial B. hygrometrica plants are found in nature during the wet season ( Supplementary Fig. S1). ...
... Immature B. hygrometrica plants are uncommon in natural populations during winter, although tolerant accessions have been isolated in summer. Similarly, immature plants seldom survive in natural populations of two European Gesneriaceae resurrection plants, H. rhodopensis and R. myconi (Xavier Pico and Riba 2002, Bogacheva-Milkoteva et al. 2013). In this study, we demonstrate how pre-exposure to gradual water loss may alter subsequent responses to rapid water loss, implying the existence of so-called acclimation or training. ...
Full-text available
Boea hygrometrica resurrection plants require a period of acclimation by slow soil-drying in order to survive a subsequent period of rapid desiccation. The molecular basis of this observation was investigated by comparing gene expression profiles under different degrees of water deprivation. Transcripts were clustered according to the expression profiles in plants that were air-dried (rapid desiccation), soil-dried (gradual desiccation), rehydrated (acclimated), and air-dried after acclimation. Although phenotypically indistinguishable, acclimated plants were shown by principal component analysis that the gene expression profiles in rehydrated, acclimated plants resemble those of desiccated plants more closely than those of hydrated. Enrichment analysis based on gene ontology was performed to deconvolute the processes that accompanied desiccation tolerance. Transcripts associated with autophagy and α-tocopherol accumulation were found to be activated in both air-dried, acclimated plants and soil-dried non-acclimated plants. Furthermore transcripts associated with biosynthesis of ascorbic acid, cell wall catabolism, chaperone-assisted protein folding, respiration and macromolecule catabolism were activated and maintained during soil-drying and rehydration. Based on these findings, we hypothesize that activation of these processes leads to the establishment of an optimal physiological and cellular state that enables tolerance during rapid air-drying. Our study provides a novel insight into the transcriptional regulation of critical priming responses to enable survival following rapid dehydration in B. hygrometrica. © The Author 2015. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For Permissions, please e-mail:
... These two species have been shown to be bumblebee flowers and, accordingly, bumblebees pollinate them. Bogacheva-Milkoteva & al. (2013) reported that H. rhodopensis is self-compatible, but not autogamous. Phenology, herkogamy and weak protandry favour outcrossing in natural populations. ...
Full-text available
Sida acuta, S. cordata and S. cordifolia (Malvaceae) exhibit almost the same flowering phenology, floral morphology, floral biology, sexual, breeding and pollination systems, fruiting behavior, and seed dispersal. They complete vegetative and reproductive events in quick succession during rainy season and disperse seeds at the onset of dry season. Their simultaneous flowering, anthesis schedules, anther dehiscence schedules, and similar floral structural and functional characteristics attract the same bees, wasps and butterflies to their flowers. Bees use these plants as principal pollen source, while wasps and butterflies use them as a nectar source and thus contact the anthers and stigmas and pollinate the flowers. The plants display functional autogamy and allogamy, and produce the highest natural fruit set and seed set. Fruits mature quickly, split apart and disperse seeds into the air early in the dry season. The seeds are dispersed by wind, humans, animals, and rain water. Sida species are suitable for initial restoration of degraded, disturbed and mined habitats. As annual weeds, they have a unique role to play in plant community restoration, bloom quickly and sustain diverse insect pollinators, as well as herbivore communities.
... Phenology of the populations, herkogamy and weak protrandry are mechanisms which favour the outcrossing in natural populations. Pollination success is characterised by high seed production: the seeds germinate readily, grow extremely slowly and few of them survive to adult plants in culture and in natural populations (Bogacheva-Milkoteva et al. 2013). Picking of adult plants is the main hazard factor for the populations balance and for the protection status of H. rhodopensis. ...
This review discusses the potential of Haberlea rhodopensis as a food additive. The following are described: plant distribution, reproduction, cultivation, propagation and resurrection properties; extraction, isolation and screening of biologically active compounds; metabolite changes during dehydration; phytotherapy-related properties such as antioxidant potential and free radical-scavenging activities, antioxidant skin effect, antibacterial activity, cytotoxic activity and cancer-modulating effect, radioprotective effect, chemoprotective effect, immunologic effect; present use in homoeopathy and cosmetics, pharmacological and economical importance; perspectives based on the ethnobotanical data for medicinal, cosmetic or ritual attributes. H. rhodopensis showed unique medical and pharmaceutical potential, related to antioxidant, antimicrobial, antimutagenic, anticancer, radioprotective, chemoprotective and immunological properties. H. rhodopensis extracts lack any cytotoxic activity and could be used in phytotherapy. The metabolic profiling of H. rhodopensis extracts revealed the presence of biologically active compounds, possessing antiradical and other physiological activities, useful for design of in vitro synthesised analogues and drugs.
Most people are aware that pollinators are in trouble, and with them agricultural products worth more than $200 billion annually (FAO. Pollinators vital to our food supply under threat., 2017). Pollinators are fundamental to maintaining both biodiversity and agricultural productivity, but habitat destruction, loss of flower resources, and increased use of pesticides (particularly neonicotinoids) are causing declines in their abundance and diversity.
Full-text available
The national threat status of 898 species of vascular plants from the Bulgarian flora has been evaluated using Version 3.1 of the IUCN Red List Categories and Criteria. The resulting Red List of the Bulgarian vascular plants (threat categories) comprises 801 species (20.5 % of the total flora), of which one Extinct (EX), 12 Regionally Extinct (RE), 208 Critically Endangered (CR), 297 Endangered (EN), 204 Vulnerable (VU), and 79 Near Threatened (NT). The list of other evaluated species comprises 96 taxa, of which, 53 Data Deficient (DD) and 43 Least Concern (LC).
Full-text available
The small group of resurrection plants is a unique model which could help us in further understanding of abiotic stress tolerance. The most frequently used approach for investigations on gene functions in plant systems is genetic transformation. In this respect, the establishment of in vitro systems for regeneration and micro propagation is necessary. On the other hand, in vitro cultures of such rare plants could preserve their natural populations. Here, we present our procedure for in vitro regeneration and propagation of Haberlea rhodopensis – a resurrection plant species, endemic for the Balkan region.
Full-text available
Recent environmental changes challenge world agriculture and reconfirm the importance of wild flora as useful source of valuable traits. Due to their extreme desiccation tolerance, the so called "Resurrection plants" are extensively studied and characterized The Bulgarian endemic species Haberlea rhodopensis, apart from its typical resurrection capacity is very interesting also as a potential source of bioactive compounds with putative application in pharmacology, veterinary medicine and cosmetics. Here we discuss our approaches to Haberlea in the frames of the NSF funded project DO02-105 "Centre for sustainable development of plant and animal genomics".
Pollen-ovule ratios (P/O's) of flowering plants, including grasses, reflect their breeding system and these can be divided into five classes: xenogamy, facultative xenogamy, facultative autogamy, obligate autogamy and cleistogamy. The evolutionary shift from class to class is accompanied by a significant decrease in the mean P/O. This pattern is found in anemophilous plants and their relatives as well as zoophilous plants and their relatives. Plants in Asclepiadaceae and Mimosaceae are exceptions in the xenogamous group. These plants invest minimal energy in pollen production and their fecundity is low, but when pollination is successful the reproductive return is relatively high. A comparison of P/O's with successional stage shows that P/O's increase significantly from disturbed habitats to late successional seres. In addition to suggesting that autogamy is adaptive in disturbed habitats and xenogamy in advanced successional stages, the data show that in intermediate habitats P/O's, hence breeding systems, also are intermediate, and display a balance between autogamy and xenogamy. P/O's may be minimal and if P/O's fall below a certain minimum, fecundity decreases. This is probably a consequence of insufficient pollen grains reaching the stigmas. Several examples are discussed showing that P/O's are a better indicator of a plant's breeding system than floral size and morphology.
The pollen:ovule ratio (P⁄O) has traditionally been used as a rough estimator of plant breeding systems. It has been shown that plant breeding systems are associ- ated with particular floral traits. In this study, we determined the P⁄O in 21 Legu- minosae species from Argentina and explored relationships between P ⁄ O and taxonomic position, flower size, floral rewards, pollen presentation and pollination mechanisms. According to the results, 15 out of the 21 species classified were obli- gate xenogamous, although some of them have been recorded as facultative xenoga- mous in previous studies. There was a significant effect of taxonomic position (genus), reward type and pollination mechanism on P ⁄ O. Species offering only nec- tar as a floral reward (which were species with a brush mechanism) had a signifi- cantly lower P ⁄ O than species offering pollen or pollen and nectar. Species with the brush pollination mechanism had the lowest P⁄O, while species with valvular and pump mechanism had the highest P⁄O. However, pollen presentation (primary and secondary) and flower size did not have a significant effect on P⁄O. Our results demonstrate that P⁄O variability is determined by taxonomic position and pollina- tion mechanism in this plant group.
Jankaea heldreichii, a monotypic species of the Gloxinia family and a Tertiary relict, is restricted only to Mt Olympus (Greece). Its phenology of flowering, breeding system, mode of pollination, and reproductive potential were studied. Results showed that, although confined to a small area, this important plant species is not at present seriously endangered. Its vulnerability depends mostly on tourist pressure and uncontrolled collection.
The resurrection flowering plant Ramonda serbica inhabits the shallow organo-mineral soil that develops in crevices on northern-facing carbonate rocks in the gorges in the Balkan Peninsula. This type of soil represents a complex substrate whose physical and chemical properties were found to be well suited to the most important requirements for the growth and development of R. serbica as well as for the plant’s survival in the state of anhydrobiosis in periods of drought stress. Considerable amount of organic matter (39.4%) in the soil resulted in the high field capacity (134ml/100g soil) as well as the slow changes in the amount of its available water. The suitable soil hydric status, based on the organic remains, supports the slow dehydration of this poikilohydric plant, which is extremely important in allowing the activation of the plant’s protective mechanisms. The pH of the soil solution was slighty alkaline (7.7) mostly due to carbonates in its crystallographic structure. The large amount of incompletely decomposed organic debris resulted in a marked difference between total and available nutrient concentration in the soil. Still, the adequate content of nutrients in the leaves points to efficient mineral consumption by the plant roots. The sufficient bioavailability of nutrients and water was also improved by vesicular–arbuscular mycorrhiza detected in R. serbica roots.
Remnant population dynamics permit many plant species to persist timespans extending from decades up to several millenia. The regional-scalepersistence of these plant species strictly depends on the persistence of localpopulations within the region. This type of dynamics can explain the existenceof preglacial relict species in the Mediterranean today. We studied thepopulation dynamics of the long-lived iteroparous herb Ramondamyconi, a preglacial relict species with a fragmented distributioninMediterranean mountains, to evaluate the regional-scale persistence of thespecies. Demographic data were collected from 5 populations placed at LaCerdanya Pyrenean region for up to 6 years. The main life-history features ofthis species are the great longevity of adult plants and the high mortality ofseedlings. Matrix population models were used to investigate its demography.Overall, the population growth rate () ranged from a low of 0.79 to ahigh of 1.06. However, did not differ significantly from theequilibrium point, as indicated by their confidence intervals, except for onepopulation in one year. Despite the small between-year variation in ,variation in climatic conditions at La Cerdanya from year to year explained animportant part of such variation. Elasticity analyses were performed toevaluatethe relative importance of demographic parameters for population growth. Stasistransitions made the greatest contribution to . Finally, the long-termdynamics of R. myconi populations were analysed byincorporating environmental stochasticity into the models. Projectionsindicatedthat local R. myconi populations tend to decline over timebut with a long time to extinction, so the persistence ofR. myconi all over La Cerdanya is determined by thepersistence of its remnant local populations.