沙漠研究 22-1, 73 -76 (2012 )"ICAL 1 / DT X"

Journal of Arid Land Studies－Refereed Paper－

Adaptive Fruit Structural Mechanisms of Asiatic Salsola Species and Its
Germplasm Conservation and Utilization
K.N. TODERICH*1), E.V SHUYSKAYA2), Faisal TAHA1), Shoaib ISMAIL1), L.G. GISMATULLINA3) and E.V. LI3)
Abstract: We summarize the predicted effects of flower and fruit adaptive traits on the genetic structure of some annual andperennial species of Asiatic Salsola populations in harsh desert environments. Results show that the Asiatic Salsola complex is an
example of evolutionary convergence of ecological, structural, and physiological mechanisms, which are determined genetically.
Phenotypic plasticity in the sexual expression of flower organs affects interspecies and intrapopulation genetic structure both for annual
and perennial species. Fruit diversity in the form and color of wings, structure of columns, presence, shape and spatial arrangementof the papillous protuberances, numbers of collenchymatous layers, degree of sclerification and parenchymatization determine seeddispersal and plant survival. Availability of pigments, tracheid-like moisture holding cells, and abundance of crystals in the perianth
tissues also promote the protection of the embryo from unfavorable desert environments. Wings or fruit tepals determine
anemochorous seed dispersion into open pastures spaces. Micro-morphology of epicuticular secretion and presence of crystals in the
pericarp may play a role in changing soil pH, and providing more favorable conditions for plant survival. Salt gland secretion
products on the surface of fruit tepals and perianth might protect reproductive organs and provide a strategy for germplasm
conservation. Small and isolated populations of the majority of the annual species with a predominantly wind-crossed mode of
reproduction exhibit low levels of genetic variation and in return the ability of plants to adapt to frequent droughts and climatechanging conditions. Appropriate conservation and sustainable utilization measures are suggested to protect natural habitats of
Salsola species.
Key Words: Adaptive traits, Chenopodiaceae, Flower dimorphism, Genetic polymorphism, Germplasm conservation

1. IntroductionMore than 140 species of the genus Salsola(Chenopodiaceae), which includes shrubs, semishrubs,
perennial and annuals herbs, have been described in Central
Asia (Botschantsev, 1969; Freitag, 1997). These species havea greater tolerance to water, heat, and salt stresses. Theycolonize marginal and desert lands and constitute up to 45% of
all Chenopodiaceae species in Central Asian Flora. They havedeveloped adaptive features that give them more competitive
advantage over sensitive glycophyte species. Perennial
species represent valuable germplasm resources for applications
such as fixation of shifting sands and improvement of degradedrangelands and salt affected marginal lands, and serve as an
excellent component for the creation of multiple-use protectedareas. Stems, fruits, and leaves can be used as a year-roundfeed for camels, and as summer feed for sheep and goats.
Annual Salsola species may be used as partial substitute forfeed concentrates, especially in autumn and winter. S. richteri,
has medicinal, industrial and commercial uses (Gintzburger etal., 2003). Currently, there is a gradual but serious decrease in

the size and the number of natural populations of many Salsola
species, which ultimately lowers their surviving rates undercurrent conditions of climate change.
Successful establishment of wild Salsola species appears to
be exclusively dependent on sexual reproduction. Plant
reproductive strategies, based on structural features and genetic
diversity in different ecological Salsola groups within Central
Asia are not well documented in literature (Butnik, 1981, Wolfe,
1998, Toderich et al., 2009). Traditionally, descriptive fruit
morphology studies were done mainly on the family or genus
level. Several key findings, however, are unreliable since
polymorphism within taxa often exceeds interspecificboundaries. The extent of vulnerability and the degree ofadaptability of Salsola taxa are difficult to evaluate, and theroles of different species in providing ecosystem services is notknown. It is impossible to define appropriate conservation
measures and sustainable use of Asiatic Salsola species without
knowledge of genetic information at all taxonomic levels(Lewontin, 1991).
Natural populations serve as repositories of genetic diversity,
which can be useful for ecosystem rehabilitation and/or
restoration, after a loss of species has occurred. Populations of* Corresponding Author: ktoderich@yahoo.com

PFU-CGIAR at ICARDA sub-office in Tashkent, 6a, Osie str., P.O. Box 4564, Tashkent 100000, Uzbekistan
1)

International Center for Biosaline Agriculture (ICBA)

2)

3)

Department of Desert Ecology and Water Resources Research, Samarkand Division of the Academy of Sciences of Uzbekistan. Uzbekistan

K.A. Timiryazev Institute of Plant Physiology RAS, Russia

wild Central Asian Salsola species may become extinct due toongoing climate change and increasing anthropogenic pressure.
Annual species, usually represented by small, geographicallyisolated populations are evidently sensitive to changing
environments and are under threat of habitat destruction.
Under current conditions of rapid climate change a catastrophic
loss of genetic diversity, is likely to occur (Safriel, 1994).
This paper considers the adaptive features of flower andfruit morphology of annual and perennial Asiatic Salsola taxa,
and interspecies genetic variation in order to identify adaptive
potential, and considers conservation.

2. Materials and Methods
Flowers and fruits were collected from different
populations of annual (S.aperta, S.pestifer, S.paulesenii) andperennial (S.orientalis, S. gemmascens, S. arbuscula and S.
richteri) species during several field expeditions (2005-2010)
across the Aral Sea Basin and Kyzylkum desert. Morphology
of fruit and seeds was investigated according to Kaden and
Smirnova (1971) and Dudik (1971). Samples for anatomical
studies of fruit covers were fixed in alcohol: glycerine : water(1:1:1). Sections were stained with methylene blue. Two
methods of sample preparation were used for ScanningElectron Microscopy (SEM) as described by Bozolla andRussell (1998).
For isoenzyme determination withelectrophoresis, seeds were randomly collected from 10-25
plants from each population. After a 12-hour germination ofseeds on wet paper, proteins were extracted by homogenisationof single embryos in 80 µl of extraction buffer (EDTA, KCl,
MgCl2, TRITON, PVP, TRIS-HCl). Isoenzymes wereseparated on 10% starch gel using two buffer systems systems
I and II (Muona and Szmidt, 1985).
Eight enzymatic
systems were studied: 6-phosphogluconate dehydrogenase(6PGD, E.C. 1.1.1.44), superoxide dismutase (SOD, 1.15.1.1),
glutamate dehydrogenase (GDH, E.C. 1.4.1.2), glucose-6-phosphate dehydrogenase (G6PD, E.C. 1.1.1.49), glutamate
oxaloacetate transaminase (GOT, E.C. 2.6.1.1), malate
dehydrogenase (MDH, Е.С. 1.1.1.37), malic-enzymes (Me,Е.С. 1.1.1.40) and NADH diaphorase (DIA, E.C. 1.6.99).
Staining of the enzymes as well as the genetic interpretation of
the results followed standard techniques (Soltis and Soltis,
1990; Goncharenko et al., 1989). Loci were numberedsequentially with the most anodally migrating enzyme
designated “1”.
Alleles at a locus were designatedaccordingly to the mobility of allozymes where the maximum
difference in migration of individual allozymes was set at100%. Based on electrophoretic data, the percent ofpolymorphic loci (P99p and P99s) were determined as describedby Nei and Roychoudhury (1978).

3. Results and Discussion
3.1. Flower morphology adaptive traits related toreproduction
Flowers of all investigated species are bisexual, single,
sepaloid (5-lobed perianth), alternate or assembled in a spike
inflorescence.
Anthers are tetrathecae, elongated withdifferent forms of appendage; stigma is thick and short forperennials; long papilliform and deeply bifurcate for annuals(Fig. 1.1).
Distinct sexual dimorphism of flowers(co-existence of functionally androecious/protandrous andprotogynous types), and temporal heterogeneity during
flowering period supports a high plasticity of the modes andmechanisms of pollination, pollen dispersal, and timing of
reproduction. Self-fertilization, including autogamy (within
one flower), geitenogamy (within-plant pollen transfer by wind)and cleistogamy (in closed flowers) was described mainly forannual species.
Perennial Salsola species have bothanamophylous and enthomophylous cross-pollination mode of
reproduction, which include different development times anddifferentiation of male and female flower organs, and varying
duration of pollen grain viability and embryo sac maturation.
A somewhat unusual feature was described for S. orientalis, S.
arbuscula and S. gemmascens in which large, colorful (brightyellow) anthers that protrude from an inconspicuous perianth
might serve as additional pollinator attractants. Additionally,
flowers of S. orientalis and S. arbuscula have a pronounced
hypogynous disk and a surprising amount of nectar that might
be considered as an apparent mode of insect cross-pollination.
Formation of viable seeds as a result of sexual and apomictic(development of embryo from somatic reproductive organs)mode of reproduction was found in S. orientalis and S. richteri.
3.2. Fruit morphology and germination ecology
Comparison of fruit morphology showed that in all studied
species fruit is dry, monospermous, lyzicarpous, indehiscent,with well-developed wings. The embryo is large, peripheral,spirally coiled; usually two cotyledons present with apical cleftor deeply divided; without perisperm. A full development ofembryo organs and tissue differentiation indicates germination
readiness (Fig. 1.2). Embryo development and organ
differentiation takes 4.5-5.5 months for perennials and 2.0-2.5
months for annual species. The weight of 1000 seeds varies
from 2.4 to 6.98 g. Fruits measured on the horizontal axis
ranges between 1.5-3.0 mm in diameter. Fruits are variable insize, shape and color (from light yellow to reddish - S. richteri;pale yellow to grayish S. gemmascens, S.orientalis, S.
paulsenii). Comparative analysis of fruit morphology bymeans of SEM revealed that taxonomic diagnostic features are
expressed in the upper leaflets (above the wings) and verticalFig. 1.1. Bisexual flower withbilobed long style, S. pestifer,adapted to anemophylous type ofpollination.

Fig. 1.3. Widely fan-shaped
wings of S. richteri strongly
pressed to the surface and almost
accreted, in the basis fruit tepals.

Fig. 1.2. Micro-morphology ofmature embryo, S. pestifer ready togerminate.

Fig. 1.4. Mature fruit with fiveunequal and narrow horizontally
spreading , wings of S. pestifer.

Fig. 1.5. Specialized adaptive structure of fruit tepals: Salt excretingtrichomes and epicuticular wax at the epidermis; hydracitic cells, pigments
and tracheid-like cells; abundance of crystals; large celled parenchyma.
Fig. 1. Flower, embryo and fruit morphology and anatomy of annual
and perennial species; Source: Toderich , 2008

column (open funnel), and less so on the bottom leaflets (under
the wings). Among the species studied, fruit variation isdisplayed in the form and color of wings, structure of columns,
and the presence, shape and spatial arrangement of thepapillous protuberances (Figs 1.3 and 1.4). Fruit tepals
played an essential role in embryo protection due to high levelof sclerification. Fruit tepals ensure anemohorous seeddispersion into the extensive open pastures, providing selfpropagation of Salsola populations, which in turn ensure
ecosystem functioning and stability. Significant differences
between perennial and annual species were found. Perennial
species are characterized by presence of two rows ofchlorenchyma, which consist of palisade bundle sheath
cells and small vascular tissue. Also present is highparenchymatization of perianth segments during fruit
maturation, radially elongated cells of thin-walledparenchyma, absence of sclerenchyma in the upper tepals,cholenchymatous thickening of lower epidermis and 1-2
row parenchyma that closely adhere to the epidermis.
Annual species are characterized by a thick-walledparenchyma and large thin-walled epidermis cells;presence of a pronounced crystal-salt bearing cell and apigmented layer. Micromorphology of the epicutical, salt
gland/trichome secretion and presence of crystals in pericarp
may play a role in changing soil pH, thereby providing amore favorable condition for plant survival (Fig. 1.5).
Our experiments showed that perennial Salsola species has
a low rate (48-72%) of seed germination both under laboratory
and field conditions despite a high proportion of viable seeds(with fully a developed embryo), while annual species arecharacterized by a high rate (90-94%) of seed germination andseedling survival. A high degree of perianth sclerification is
one of the main reasons for lower seed germination rate inperennials (Toderich, 2008). Destruction of intact of seed coator removal of fruit covers resulted in increased germination rate.
Short-term dormancy occurs in woody Salsola species, lastingfrom 8-10 months, up to 1.5 years depending on storage conditions.
Dry storage conditions alternating with low temperatures usuallystimulate seed germination (Gintzburger et al., 2003).
3.3. Genetic variation and conservation measures
The significant genetic polymorphism detected in this study
indicates that perennial Salsola species possess an abundantsource of variation required for evolution in a changing
environment. Genetic variation of perennial species at
population level is lower than at species level, but significantly
higher than that of annual species (Table l). This evidence
indicates a high genetic differentiation of populations and,
consequently, a genetic isolation of populations.
Habitat fragmentation in annual Salsola species, resulting insmaller and more isolated populations, can pose a significant
threat to genetic diversity. For wind-pollinated species,
geographic isolation can increase in-breeding. Genetic
erosion can affect the ability of plants to adapt to changing

Table 1. Genetic intra-species (P99s) and population (P99p) variation.
Life
form
S. orientalisp*S.gemmascensp
S. arbusculap
S. richterip
S. apertaaS. paulseniia
S pestifera*p – perennial, a - annual

Number of
population
5
2
9
3
1
9
2

Sample
size
143
59
291
85
19
265
68

P99p

P99s

0.29
0.18
0.36
0.29
0.00
0.05
0.22

0.64
0.29
0.73
0.53
---0.130.31

conditions. This is likely to increase the potential impact of
threats, such as climate change, as plants are unable to adapt
quickly enough to change. The greater genetic heterozygosityof cross-pollinated perennials, at species and population levels,
may give them a selective advantage in unstable environments(Hamrick et al., 1992).
Appropriate measures forconservation of genetic diversity should be developed,
especially for locally adapted populations for majority of annual
Salsola species. Phenotypic plasticity in sexual expression,
diversity of mode and mechanism of pollination, and of pollen
and seed dispersal detected by these studies could also affectgenetic structure by altering the distribution of individuals inspace and time. Therefore, conservation of fragmented
populations is crucial to ensuring their survival in a changing
environment. Disappearance of this unique germplasm willlead to the loss of a significant proportion of the total genetic
diversity of genus Salsola within Central Asian Flora.
Surveys and seed collections show that Salsola has potential
uses in soil remediation affected by severe salinity and also in
improvement of arid fodder pasture production. Ex-situ andin-situ conservation of economically valuable salt-and droughttolerant Salsola species has been initiated by International
Center for Biosaline Agriculture (ICBA) at the Gulistan State
University, Uzbekistan. It is imperative to accurately assess
the threat status of individual species of these valuable arid andsemiarid fodder plant resources. Results will help in setting
priorities for conservation, and providing the guidance needed
to protect the diversity of desert hotspots from land degradationand intensive use.
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