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Phytotaxa 93 (1): 1–24 (2013)
www.mapress.com/ phytotaxa /
Copyright © 2013 Magnolia Press
ISSN 1179-3155 (print edition)
Article
PHYTOTAXA
ISSN 1179-3163 (online edition)
http://dx.doi.org/10.11646/phytotaxa.93.1.1
The relationship and different C4 Kranz anatomy of Bassia eriantha and Bassia
eriophora, two often confused Irano-Turanian and Saharo-Sindian species
HOSSEIN AKHANI1,* & ROXANA KHOSHRAVESH1
1
Department of Plant Sciences, School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Sciences,
University of Tehran, P. O. Box 14155-6455, Tehran, Iran
*
Corresponding author: akhani@khayam.ut.ac.ir
Abstract
The circumscription and generic status of Bassia eriantha (≡ Londesia eriantha) and B. eriophora have often been
confused in the literature. The reason is their extreme superficial similarity and phenology. In a multidisciplinary
approach, we investigated both in the field, by cultivation in the laboratory, and performed anatomical, ultra-structural
and molecular studies to clarify their taxonomy and relationships. Both species are not only geographically and
morphologically distinct by reliable and constant characters, but surprisingly also have different anatomical C 4 Kranz
types and occur in different clades using ITS nrDNA sequence analysis. Using the recent broad circumscription of the
genus Bassia they belong to Bassia but in different clades. In spite of their rather well distinct geography, the two species
are sympatric in the south-eastern Iran and south Afghanistan. Bassia eriantha as an Irano-Turanian species occurs
disjunctly as Irano-Turanian enclave in south Sinai, Jordan and W Saudi Arabia as a second sympatric range cooccurring with B. eriophora.
Key words: Amaranthaceae, bundle sheath, C4 photosynthesis, Camphorosmeae, Chenopodiaceae, halophyte, phylogeny
Introduction
The increasing interest in the evolution of C4 photosynthesis pathway requires taxonomic studies within C4
taxa and their C 3 relatives. Chenopodiaceae represents one of the major lineage of C 4 diversity among
Eudicots having a multiple origin of C4 photosynthesis and a high morpho-anatomical variability (Akhani et
al. 1997, Kadereit et al. 2003, Sage et al. 2011). In Eurasia this family is diversified extensively in the Middle
East, Central (uplands) and especially Middle Asia (lowland around the Aral sea and Turan), and to some
extent also in North and South African deserts, with a great success in formation of vegetation under harsh,
dry and saline conditions and during very hot growing seasons. Camphorosmeae Endlicher (1837: 294), that
is alternatively considered as subfamily Camphorosmioideae Scott (1978: 102), is a species-rich group which
classification of this lineage has always been controversial in the literature of this family (Scott 1978, Kühn et
al. 1993). A recent molecular investigation of this tribe (Kadereit & Freitag 2011) proposed a new
classification in which Bassia Allioni (1766: 177) is widely circumscribed by including several mono- and
oligo-specific genera such as Kochia Roth (1801: 307), Londesia Fischer & Meyer (1835: 40), Panderia
Fischer & Meyer (1835: 46), Kirilowia Bunge (1843: 7) and Chenoleoides (Ulbrich 1934: 530) Botschantzev
(1976: 1408). One of the species listed is Bassia eriophora (Schrader 1809: 86) Ascherson (in Schweinfurth
1867: 187) which was broadly circumscribed more recently (see below) and includes L. eriantha Fischer &
Meyer (1835: 40) or B. eriantha (Fisch. & C. A. Mey.) Kuntze (1891: 546).
Bassia eriophora was first described based on a cultivated plant under the genus Kochia (Schrader 1809).
The origin of the seeds was doubtfully mentioned as Spain which, considering its known range, is unlikely.
The illustration and description are fully informative and cannot be confused with any other plant. Kochia
Accepted by Duilio Iamonico: 12 Mar. 2013; published online in PDF: 11 Apr. 2013
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latifolia Fresenius (1834: 179) was described from Sinai “Thall Hebran” and distinguished from K. eriophora
by broader and shorter leaves, and longer woolly hairs covering the flowers. Londesia eriantha was described
from east of the Caspian Sea as a monotypic genus by Fischer & Meyer (1835). The range of the species
according to Iljin (1936) is mostly in the Aralo-Caspian parts of Central Asia.
FIGURE 1. Bassia eriantha (A–C) and B. eriophora (D–F) in natural condition and in cultivation. A) Habit in nature (50 km E of
Esfahan towards Naein, Esfahan Province, Iran), B) seedling and C) vegetative plant of B. eriantha; D) Habit in nature (east of
Mahshahr towards Hendijan, Khuzestan Province, Iran), E) seedling and F) vegetative plant of B. eriophora. Note that B and E, and C
and F are the same age cultivated under laboratory conditions. Scale bar=1 cm (photos A, D by H. Akhani, others by R. Khoshravesh).
Both species appear very similar from the macro-morphological point of view, including life form
(annual), paniculate inflorescence and connate tepals hidden by long white lanate hairs (Fig. 1 A & D).
Moreover, both plants employ C 4 photosynthetic pathways (Akhani et al. 1997), and have a more or less
similar ecology in the arid and semi-arid deserts and salines of Central and SW Asia from Sinai to Mongolia
(Post 1883, Iljin 1936, Zohary 1966, Pyankov & Vakhrusheva 1989, Heller & Heyn 1994, Boulos 1996,
Hedge 1997, Pyankov et al. 2000, Zhu et al. 2003, Czerepanov 2007). These close morphological similarities
of B. eriophora and L. eriantha resulted in their confusion in earlier literature. For instance, Boissier (1879)
reduced K. eriophora and L. eriantha under one species as varieties [K. latifolia var. latifolia Fresenius (1834:
2 •
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179) and var. inermis Boissier (1879: 927), respectively]. Scott (1978) suggested both as distinct species
belonging to different sections in a broadly defined Bassia. Hedge (1997) unified all the names under a broad
B. eriophora, a view which was not accepted by the Iranian authors working on Chenopodiaceae (Akhani et
al. 1997, Assadi 2000, 2001) but followed in the Flora of Pakistan (Freitag et al. 2001) and the Flora of the
Arabian Peninsula (Boulos 1996).
Bassia eriophora was first sequenced (Internal Transcribed Spacer, ITS) by Kadereit et al. (2005) from
Kuwait (as L. eriantha that was considered synonym of Bassia eriophora). Akhani et al. (2007) published ITS
and PsbB-PsbH sequences of B. eriophora from a population in SW Iran (Ilam Province). Recently, Kadereit
& Freitag (2011) analysed ITS sequences of Kuwait population plus that of Akhani et al. (2007) under B.
eriophora. The occurrence of these two sequences in the same clade with 100% bootstrap value (BP) misled
Kadereit & Freitag (2011) to conclude that B. eriophora and L. eriantha were likely synonyms.
In an ongoing research project on the taxonomic and photosynthetic diversification of Iranian C4 species, we
have studied this species complex in a biosystematic approach. The aims of this study are: (1) using
multidisciplinary approach to show the specific distinctiveness of L. eriantha and B. eriophora; (2) providing
detailed data on the morpho-anatomical features of the two species including cotyledons, leaves and
perianths, (3) comparing the chorotype of both species and discussing main climatic factors determining their
range, and finally (4) concluding how different approaches could help to address difficult taxonomic questions
in chenopod taxonomy.
Materials and Methods
Taxonomy and morphology
Field studies were conducted in natural populations of both species in Iran (Khuzestan, Semnan, Esfahan,
Yazd, Kerman, and Sistan and Baluchestan provinces) over many years by the first author. Herbarium
specimens have been studied in various Iranian and European herbaria: B, E, FR, FUMH, GOET, IRAN,
KAS, M, MSB, TARI (acronyms according to Thiers 2011) and own collections in the herbarium of the
“Halophytes and C4 Plants Research Laboratory” of the School of Biology, University of Tehran (Herb.
Akhani).
Seeds of L. eriantha originated from Yazd province (Akhani & Dehghani 18275) and B. eriophora from
Khuzestan province (Akhani & Pahlevani 20885) have been cultivated in the laboratory. They were grown in
a mix of sand and commercial peat 1:1 under natural condition of Tehran during April–June 2011. Information
on the germination, morphology and phenology of cultivated plants was recorded or photographed either by a
commercial digital Camera (Canon PowerShot S5 IS) or studied using a SZX12 Olympus Stereo microscope
coupled by a DP12 Olympus digital camera.
DNA sequencing and phylogenetic analysis
The Internal Transcribed Spacer (ITS) sequences of six samples belonging to B. eriantha, B. eriophora and B.
scoparia have been newly generated after the methods described in detail in Khoshravesh et al. (2012). 28
additional sequences from two B. eriophora accessions (Kadereit et al. 2005, Akhani et al. 2007) and 26 other
species and genera of Camphorosmeae have been taken from GenBank (Table 1). The ITS matrix was aligned
firstly by Muscle and then edited manually. The matrix was analysed by Maximum Likelihood method using
MEGA 5 (Tamura et al. 2011). After finding the best fitting model (K2 + G), a tree showing highest
likelihood was generated after 1000 replicate analyses.
BASSIA ERIANTHA AND BASSIA ERIOPHORA
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TABLE 1. Genbank accession numbers of ITS sequences used in phylogenetic analysis. The detailed localities of new
sequences are given in additional specimen examined. Newly generated sequences are indicated by an asterisk.
Taxon
Voucher, location (herb.) or reference
GenBank accession
number
Bassia angustifolia (Turcz.) Freitag & G. Kadereit (≡ Kochia angustifolia (Turcz.) Peschkova)
Kadereit & Freitag (2011)
HM630024
Bassia eriantha (Fisch. & C.A. Mey.). Kuntze
H. Akhani et al. 22225 (Hb. Akhani); Iran
KC149997*
H. Akhani & M. Dehghani 18275 (Hb. Akhani ); Iran
KC149996*
S. Collenette 2417 (E); Saudi Arabia
KC149994*
W. Frey & H. Kürschner 5428; Jordan
KC149995*
Bassia eriophora (Schrad.) Asch.
Kadereit et al. (2005)
AY489220
H. Akhani 8381 (Hb. Akhani); Iran
EF453391
H. Akhani et al. 22067 (Hb. Akhani); Iran
KC149993*
S. Rilke 1415 (B); Israel
KC149992*
Bassia hyssopifolia Kuntze
Kapralov et al. (2005)
DQ499333
H. Akhani 18064 (Hb. Akhani); Iran
EF453390
Bassia indica (Wight) A.J.Scott
Kadereit & Freitag (2011)
HM630026
Bassia laniflora (S.G. Gmel.) A.J. Scott
Kadereit et al. (2005); Russia
AY489214
Bassia cf. laniflora (S.G.Gmel.) A.J.Scott
Fuentes et al. (2012); Germany
HE577336
Bassia lasiantha Freitag & G. Kadereit (≡ Kirilowia eriantha Bunge)
Kadereit et al. (2005)
AY489209
Bassia muricata (L.) Asch.
Kadereit et al. (2005)
AY489198
Bassia stellaris (Moq.) Bornm. s.l. [incl. B. odontoptera (Schrenk) Freitag & G. Kadereit]
Kadereit et al. (2005)
AY489219
Bassia pilosa (Fisch. & C.A. Mey.) Freitag & G. Kadereit s.l. ( ≡ Panderia pilosa Fisch. & C.A. Mey., including P. turkestanica Iljin)
H. Akhani 1451 (Hb. Akhani); Iran
DQ499335
Bassia prostrata (L.) A.J. Scott (≡ Kochia prostrata (L.) Schrad.)
Kadereit et al. (2005)
AY489216
Bassia salsoloides (Fenzl) A.J. Scott (≡ Kochia salsoloides Fenzl)
Kadereit & Freitag (2011)
HM630030
Bassia scoparia (L.) A.J. Scott (≡ Kochia scoparia (L.) Schrad.)
Akhani & Dehghani 18248 (Hb. Akhani); Iran
KC149998*
Kadereit et al. (2005)
AY489212
Bassia tianschanica (Pavlov) Freitag & G. Kadereit (≡ Kochia tianschanica Pavlov)
Kadereit & Freitag (2011)
HM630033
Bassia tomentosa (Lowe) Maire & Weiller (≡ Chenoleoides tomentosa (Lowe) Botsch.)
Kadereit et al. (2005)
AY489204
Bassia villosissima (Bong. & C.A. Mey.) Freitag & G. Kadereit (≡ K. villosissima (Bong. & C.A. Mey.) Serg.)
Kadereit & Freitag (2011)
HM630034
Camphorosma annua Pall.
Kadereit & Freitag (2011)
HM630019
Camphorosma lessingii Litw.
Pyankov s.n. (no voucher); Uzbekistan
DQ499334
Camphorosma monspeliaca L.
Kadereit et al. (2005)
AY489200
Camphorosma songorica Pall.
Kadereit et al. (2005)
AY489201
Dissocarpus biflorus F. Muell.
Kadereit et al. (2005)
AY489205
Grubovia dasyphylla (Fisch. & C.A. Mey.) Freitag & G. Kadereit (≡ Bassia dasyphylla (Fisch. & C.A. Mey.) Kuntze)
Kadereit et al. (2005)
AY489195
Grubovia melanoptera (Bunge) Freitag & G. Kadereit ( ≡ Kochia melanoptera Bunge)
Kadereit et al. (2005)
AY489215
Maireana erioclada (Benth.) Paul G. Wilson
Kadereit et al. (2005)
AY489222
Sclerolaena diacantha (Nees) Benth.
Kadereit et al. (2005)
AY489231
Sedobassia sedoides (Pall.) Freitag & G. Kadereit (≡ Bassia sedoides (Pall.) Asch.)
Kadereit et al. (2005)
AY489199
4 •
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Anatomy
Small sections of leaves and cotyledon leaves were fixed in 1.5% w/v glutaraldehyde and 0.05 M % Sodium
Cacodylate buffer pH 6.9 overnight in room temperature, post fixed in 1% Osmium Tetroxide another
overnight, then rinsed in buffer twice and dehydrated in a gradient of Ethanol and embedded in Araldite resin
using propylene oxide as transitional solvent (Millonig 1976). Sections were cut by ultra-microtome (Leica
Ultracut UCT, College of Science, University of Tehran), dried on Gelatin coated slides and stained with 0.5%
(w/v) Toluidine blue in 1% (w/v) Na2CO3 in double distilled water. Sections were observed by a BX51
Olympus microscope and photographed by a DP12 Olympus digital camera. Several samples from natural
habitats and/or from different herbaria were hand- sectioned to ensure that the samples of the same region had
the same anatomy.
For ultrastructral studies, ultra thin silver sections were collected on copper grids and stained by uranyl
acetate and lead citrate. Sections were observed by a Philips EM 208 transmission electron microscope (TEM)
(Freie University of Berlin). Granal index was calculated following Voznesenskaya et al. (2007).
SEM and pollen grains studies
Non-acetolysed pollen grains were divided into two parts, first part were gold coated and observed by a Zeiss
DSM 960 SEM microscope (Electron Microscopy Laboratory, College of Science, University of Tehran). For
light microscopy the second part of pollen grains were directly transferred to the regular slides and mounted
by glycerin jelly. Then examined and photographed by the same microscope and digital camera (see above).
Pollen diameter, exine thickness, pore diameter and pore density were measured following Dehghani &
Akhani (2009). All the measurements were done using image processing software Image J (Rasband 1997–
2012) . The data obtained from quantitative measurements were analyzed by SPSS 11.0 Windows compatible.
The data set was tested for normality using normal Kolmogrov-Smirnove fit test. T test was employed for
normally distributed data (P > 0.050) and the parameters lacking normality (including pollen diameter, pore
diameter and exine thickness), were analyzed by non-parametric test for two independent samples. The haires
of dried fruits were gold coated and observed by SEM using the same method.
Biogeographical and ecological studies
All distribution data on both species based on own observations and reliable references have been converted
into geographical co-ordinates. The distribution map for both species was generated by DIVA-GIS 7.5 (http://
www.diva-gis.org). Climatic data was extracted from DIVA-GIS climate data set (http://www.diva-gis.org/
climate) with 2–5 m spatial resolution and applied for 60 own observations for each species.
Results
Morphology and micromorphology
Observations on developing live plants in both field studies and laboratory conditions provided unequivocal
tools to distinguish the two species (Table 2). They are very distinct even in early vegetative developing
phases (Figs.1 B & E, Table 2).
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TABLE 2: Comparison of characters in Bassia eriantha and B. eriophora. Mean and standard deviations (± SD) are presented
for quantitative characters. N=10 for morphological and ultrastructural measurements and 100 for pollen grains. Sigma two
tailed for independent two samples test (in the case of normal distributed data) and Mann-Whitney U test (for the nonparametric
data including pollen diameter, pore diameter and exine thickness) statistical tests are applied. ND= Not determined.
B. eriantha
Seedling
Cotyledon leaf shape
Cotyledon leaf size (cm): Length
Width
Cotyledon cross section shape
Average of hypocotyls length (cm)
Cotyledon anatomy
Mature plant
Leaf arrangements
Caulin leaf shape
Cauline leaf apex
Floral leaf shape
Leaf size (cm): Length
Width
Length/width ratio
Leaf anatomy
Stem color: in fresh plant
in dried plant
Pollen grains
Average of pollen diameter (µm)
Exine thickness (µm)
Average of pore diameter (µm)
Chord length* (mm)
Maximum and minimum and average of
pore numbers
Average of pore density per 100 µm 2
Ultrastructure
Granal index (% )
(MC)
(BSC)
Thylakoids per granum (MC)
(BSC)
Oblong to broad elliptic,
spreading
0.50 (±0.1)
0.17 (±0.02)
Almost half the size of the
first seedling leaves or shorter
Elliptic
0.13 (±0.04)
C4-Atriplicoid
Alternate
Oblanceolate, narrowly
obtrullate to spatulate
Acute
Broadly lanceolate, subsessile
to petiolate
1.5 (±0.2 )
0.21 (±0.3)
7.7 (±1)
C4-Atriplicoid
Pinkish white to pale green
Reddish brown, dark pink to
purple
B. eriophora
Statistical
test
Linear, recurved
1.00 (±0.1)
0.15(±0.03)
More than half as long as the
primary seedling leaves
Bean shape with narrowed
ends
1.40 (±0.2)
C4-Atriplicoid
<0.001
0.6
<0.001
Alternate
Linear to narrowly spatulate
Acute, obtuse to rounded
Linear, sessile
2.80 (±0.6)
0.30 (±0.04)
9.8 (±2)
C4-Kochioid
Pale green to greenish white
White, brownish white to pale
brown
<0.001
<0.001
0.02
27.7 (±3)
2.40 (±0.5)
2.8 (±0.4)
6.8 (±0.2)
33–85(–60) (±3)
31.00 (±4)
2.20 (±0.4)
1.50 (±0.5)
5.6 (±0.1)
73–149(–112) (±5)
<0.001
0.9
<0.001
<0.001
<0.001
2.5 (±0.1)
3.8 (±0.2)
<0.001
47.00 (±5)
30.34 (±4)
(3) 6–10 (–12)
2–5 (–6)
ND
ND
ND
ND
-
* Chord length measured based on distance between two adjacent pores.
In maturity, the two species look superficially very similar in their growth form, alternate leaves,
secondary branching and paniculate inflorescence, and the flowers hidden by long woolly articulated whitish
hairs (Figs. 1 A & D). However, cauline and floral leaf shape, size and length/width ratio are distinctive
characters (Table 2; Figs. 1 C & F, 2 A & B). Stem colour is a further character that is consistently different in
almost all specimens (Table 2).
The most peculiar difference between the two species is the spine-like horizontal outgrowth on the back of
each mature perianth in B. eriophora and the absence of it in B. eriantha (Figs. 2 E & F). Furthermore, in B.
eriantha, perianths are connate at 2/3 to 3/4 of their length. The dentate upper parts and fused parts are hyaline
and remain as a membranous cover on fruit (Figs. 2 E, 5 A). The tepals in B. eriophora are fused for almost ½
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to 2/3 of their length, with a dentate upper dark green part and a pale connate part (Fig. 5 D); both parts
become indurated in fruit.
SEM micrographs of fruiting hairs were compared and showed that the hairs in B. eriantha are distinctly
spinulose (Fig. 4 A), whereas the fruiting hairs of B. eriophora are smooth to minutely spinulose (Fig. 4 B).
Both species have the general characters of pollen grains of Chenopods: spherical with several pores—
pantoporate, with the exine surface covered with numerous spinules (Dehghani & Akhani 2009). Quantitative
study of pollen revealed that except for exine thickness that is almost equal in two species (Table 2), the other
parameters present significant differences between them. In B. eriantha, the pollen size is smaller, pore
diameter and chord length is higher; pore number and consequently pore density is significantly lower
compared to B. eriophora (Table 2).
Anatomy and ultrastructure
Cotyledon anatomy: Cotyledon cross sections of both species showed a similar pattern of C4-atriplicoid Kranz
anatomy (Carolin et al. 1975), in which there is one layer of hypodermis below the adaxial epidermis that in
B. eriantha is more or less rounded and sometimes contain chloroplasts and 2–5 layers of water storage cell on
the abaxial side connecting epidermis and mesophyll cells (Figs. 3 A and C).
Mature leaf anatomy and vein pattern: C4 Kranz anatomy is developed in both species: B. eriantha leaf
cross section presents C4-atriplicoid type of Kranz anatomy with a layer of large hypodermis cells below the
epidermis (Fig. 3 B). In contrast, in B. eriophora bundle sheath cells surround the vascular bundles partially,
typical of kochioid type of Kranz anatomy (Fig. 3 D). Hand sections from several herbarium samples revealed
the same result for both species (Figs. 2 C and D).
FIGURE 2. A & B) Venation in floral leaves of Bassia eriantha (A) and B. eriophora (B), arrow shows freely ending veinlets; C & D)
hand section of the fresh leaves collected from natural habitat shows atriplicoid type for B. eriantha, Akhani et al. 22225 (C) and
kochioid type for B. eriophora, Akhani et al. 22048 (D); E & F) fruits in B. eriantha Akhani et al. 22225 (E) and B. eriophora Akhani
et al. 20885 (F) after removal of hairs.
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The vein pattern in leaves of both species is reticulate (see Fig. 2 A and B). However, the veinlets in B.
eriophora are longitudinally oriented along the length of the leaves, giving a false parallel venation in which
the ends of tertiary veinlets are not distinguishable (see Nelson & Dengler 1997) (Fig. 2 B). In contrast, the
tertiary veins in B. eriantha are well-developed and the end point of veinlets is visible, even in herbarium
specimens (Fig 2 A).
FIGURE 3. Cotyledon and leaf cross sections of Bassia eriantha (A, B) and B. eriophora (C, D). Cotyledon leaf cross sections in B.
eriantha (A) and B. eriophora (C), both present atriplicoid like C4 anatomy. Leaf anatomy with atriplicoid type of C4 anatomy in B.
eriantha (B) and kochioid type of C4 anatomy in B. eriophora (D). Scale bar=100 µm.
FIGURE 4. SEM image of fruiting perianth hairs in Bassia eriantha (A) and B. eriophora (B). SEM view of pollen grains of B.
eriantha, Akhani et al. 22225 (C), and of B. eriophora, Akhani et al. 22118 (D). Scale bar= 200 µm for A–B, 5 µm for C–D.
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Floral anatomy: Tepals in B. eriantha flowers are pale and very thin throughout (Fig. 5 A). The anatomy
of upper dentate and lower connate parts are very similar (Figs. 5 B and C). The tubular section consists of an
outer and inner epidermis, a few (1–2) layers of simple parenchyma cells, and a few vascular bundles. The
cells lack any chloroplast. The adaxial epidermis underneath by a layer of more or less U shaped thickened
and non-lignified cells (horse-shoe like in section, Fig. 5 C). In the dentate upper part, only this layer exists
between two layers of outer and inner epidermis (Fig. 5 B). Tepals in B. eriophora are clearly divided into two
distinct colours. The upper dentate part is dark green, fleshy and thick (Fig. 5 D). Sectioning the green part
revealed kochioid like C4 anatomy in the sun-exposed abaxial side beneath the outer epidermis (Fig. 5 E).
From the adaxial to abaxial side, the section contains one layer of inner epidermis followed by a layer of
crystalliferous cells [terminology adopted from Sukhorukov (2008)] with thickened and lignified U-shaped
adaxial walls (horse-shoe like in section) (Fig. 5 F), then 2–3 rows of subepidermal parenchyma which may
play the role of water storage cells and are responsible for the fleshiness of the tepals. Around this fleshy
tissue, vascular bundles are partly enclosed by two layers of chloroplast-containing cells, inner layer rounded
and similar to the BS cells with inward clustered chloroplasts and the outer one, slightly elongated and contain
centrifugally arranged chloroplasts similar to M cells. A layer of outer epidermis covers the adaxial side. The
lower tubular part of tepals is hyaline and lacks chloroplast-bearing structures while subepidermal
parenchyma, outer and inner epidermis and crystalliferous layer exist as well as vascular bundles that occur in
smaller numbers and further apart (Fig. 5 G).
FIGURE 5. Perianth shape and floral anatomy in Bassia eriantha (A–C) and. B. eriophora (D–G). Dissected tepal (A), anatomy of hyaline
tepal and upper dentate segments (B) and cross section of lower tubular portion of connate tepal (C) of B. eraintha. Dissected tepal (D),
anatomy of upper green part of perianths showing kochioid-like type of C4 anatomy (E), close up of crystaliferous cells in which the arrows
show the lignified “U-shape” side of the cell wall (F) and lower hyaline part lacking photosynthetic structures (G) in B. eriophora.
Ultrastructure: Organelles in BS cells of B. eriophora are centripetally arranged, BS cells possess few
mitochondria in contact with the chloroplasts (Fig. 6 A); chloroplasts in MC are granal rich and contain (3–
)6–10(–12) thylakoids per granum; conversely in BS cells chloroplasts, thylakoids reduced to 2–5(–6) per
granum (Figs. 6 B and C), all indicative of NADP-ME biochemical subtype (Kanai & Edwards 1999).
Additionally, calculation of granal index (GI) for B. eriophora (Table 2) disclosed an average GI of 47.00%
which is 1.5 times greater than in bundle sheath cells (30.34%). Bassia eriantha presents similar
characteristics in TEM images (data not shown).
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FIGURE 6. The scanning electron microscopy images of C4 structures in Bassia eriophora. A) Overall view of BS cells; chloroplasts
are arranged close to the vascular bundles, BS cells contain few numbers of mitochondria; B) close view of granal poor BSC
chloroplasts; C) close view of granal rich chloroplasts of M cells. VB: Vascular Bundles, Chl: Chloroplast, Mt: Mitochondria.
Bassia (Kochia) scoparia
Bassia (Kochia) scoparia_18248
Bassia (Kochia) angustifolia
Bassia indica
Bassia hyssopifolia
Bassia hyssopifolia
Bassia (Kochia) cf. laniflora_Germany
Bassia (Kochia) prostrata
Bassia (Kochia) villosissima
Bassia (Kochia) tianschanica
Bassia eriantha_Iran_22225
Bassia eriantha_Iran_18275
Bassia eriantha_Saudi Arabia_2417
B. eriantha (Londesia): Atriplicoid leaf anatomy
Bassia eriantha_Jordan_5428
Bassia lasiantha (Kirilowia eriantha)
Bassia (Panderia) pilosa
Bassia (Chenoleoides) tomentosa
Bassia muricata
Bassia (Kochia) salsoloides
Bassia (Kochia) odontoptera
Bassia (Kochia) laniflora
Bassia eriophora_Iran_22067
Bassia eriophora_Kuwait
Bassia eriophora_Iran
B. eriophora: Kochioid leaf anatomy
Bassia eriophora_Palestina_ 1415
Camphorosma lessingii
Camphorosma monspeliaca
Camphorosma annua
Camphorosma songorica
Sedobassia (Bassia) sedoides
Grubovia (Bassia) dasyphylla
Grubovia (Kochia) melanoptera
Dissocarpus biflorus
Maireana erioclada
Sclerolaena diacantha
FIGURE 7. Maximum likelihood tree obtained from nuclear ITS sequences of Bassia eriantha, B. eriophora and other members of
tribe Camphorosmeae. Bootstrap supports above 50% are given.
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Molecular phylogeny
The aligned ITS matrix including 660 characters, having 175 variable, 107 parsimony informative and 474
constant characters. The nucleotide frequencies are: T=22.8%, C=26.6%, A=21.6% and G=28.9%. Among
620–621 compared nucleotide sequences, 23 changes were detected between the two species with a similarity
percentage of 96.2%. The maximum-likelihood tree (n= -2859.90) is shown in Fig. 7. Both species forms
strongly supported clades (99 and 96% BP) but occurring in different subclades of Bassia clade (Kadereit &
Freitag 2011). The two Bassia eriantha samples from Saudi Arabia and Jordan form a clade with 92% BP. The
inclusion of new sequences of L. eriantha did not change the unresolved internal topology of ITS
phylogenetic tree among several species of Bassia clade.
Distribution
A list of studied specimens is provided in taxonomic parts of this paper. The general distribution of B.
eriophora and B. eriantha is given in Figs. 8 A–C. B. eriantha occurs in a latitudinal range of 25° to 43°N and
elevational range of 0–2500 m. The range of B. eriantha is mostly in the central and eastern parts of the IranoTuranian phytogeographical region. It occurs in Iran, Afghanistan, Pakistan, Turkmenistan, Kazakhstan,
Uzbekistan, Mongolia and N Xinjiang in China (the two latter not shown in the map and data from Pyankov et
al. 2000 and Zhu et al. 2003). It occurs disjunctly in the southern Sinai in Wadi Hebron and Wadi el Isla
(vouchers: Schimper 133, Kneuker 19 & 159), South Jordanian desert (voucher: Frey & Kürschner 5428) and
in the central part of Saudi Arabia (voucher: Collenette 2417). On the basis of the Euro-Med Checklist B.
eriantha was reported as casual alien species in Estonia (Laasimer et al. 1993), which considering the very
different climate of Estonia needs critical checking. Bassia eriophora occurs from Sinai, around the Dead Sea
and Syrian desert, north and east of Saudi Arabia and Kuwait, east, south east and central parts of Iraq,
southern part of Iran along the Persian Gulf and Gulf of Oman, penetrating to Sistan around the Lut desert in
southeast of Iran, western parts of Pakistan and southern Afghanistan (Fig. 8 A). This matches well with the
Saharo-Sindian zone (SS2 and SS3) according to the phytogeographical concept of White & Léonard (1991).
B. eriophora occurs between 24° to 35° northern latitude where the elevations vary from much below sea
level (-300 m, near the Dead Sea shore) to 1500 m near the Bakhtegan Lake in Fars Province, Iran (Fig. 8 A).
The distribution of the species was compared with annual mean temperature (AMT), mean temperature of
warmest quarter and temperature of growing season (Figs. 8 B, 9 A and B). More than 40% of observed B.
eriantha samples occur in areas with AMT of 13–18°C, while 90% of observed samples of B. eriophora
distributed in the area with AMT ranging from 18–28°C (Fig. 8 B, 9 A). Mean temperature of warmest quarter
revealed that both species are most frequent in mean temperature of 28–33°C, but the frequency in B. eriantha
shows a sudden decrease in mean temperature of warmest quarter more than 33°C, conversely, a large number
of B. eriophora (42%) occur under this conditions (Fig. 9 B). Otherwise, approximately 34% of observed B.
eriantha distribute in habitats with mean summer temperature of 23–28°C. In southern and south eastern parts
of Iran, south Afghanistan and the west of Pakistan, both species are sympatric and even occur in mixed
populations [voucher: Iranshahr & Ershad 49791-1 (B. eriantha) and 49791-2 (B. eriophora) and Freitag
2441]. This interfacing has been observed in the border that annual mean temperature shifts from 8–18°C to
18–28°C (Fig. 8 B).
The distribution of the species related to the mean temperature of growing season (March to May/June)
disclosed that there is a temperature dependent border separating the range of both species. This separation
and a north to south transition from B. eriantha to B. eriophora happens when mean temperature shifts upper
than 18°C in March, 20°C in April, 25°C in May and 28°C in June (Fig. 8 C).
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FIGURE 8. Geographical distribution of Bassia eriantha (dots) and B. eriophora (triangles) based on verified herbarium specimens.
Empty dots represent literature records of B. eriantha and stars represent those of B. eriophora, respectively. A. Distribution of both
species on a relief map; B) Distribution of species on an annual mean temperature map and C) Distribution of species on a map
showing mean temperature of April.
Discussion
Taxonomy, morphology and anatomy
The combination of differences described for leaf and floral anatomy, morphology, pollen morphology, DNA
sequence data, geographical distribution, and co-cultivation experiments evidently reject synonymizing L.
eriantha and B. eriophora as suggested by Boisser (1879), Zohary (1966), Hedge (1997) and Kadereit &
Freitag (2011) (Table 2). This study showed that relying only on limited taxonomic characters of herbarium
specimens in the family Chenopodiaceae is misleading. The very small flowers and succulent structure of
many parts loose, on drying, important taxonomic characters, especially in succulent subfamilies Salsoloideae
Ulbrich (1934: 561), Suaedoideae Ulbrich (1934: 554), Salicornioideae Ulbrich (1934: 543) and
Camphorosmioideae.
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Frequency (%)
A
50
45
40
35
30
25
20
15
10
5
0
B. eriantha
B. eriophora
8-13
13-18
18-23
23-28
Annual Mean Temperature (°C)
B
40
35
Frequency
30
25
20
B. eriantha
15
B. eriophora
10
5
0
18-23
23-28
28-33
33-38
Mean temperature of warmest quarter (°C)
FIGURE 9. Frequency of the species Bassia eriantha and B. eriophora in relation to annual mean temperature (A) and mean
temperature of warmest quarte (B).
This study and two similar studies carried out in Bienertia Bunge ex Boissier (1879: 945) belonging to
Suaedoideae (Akhani et al. 2012, Akhani et al. 2005) showed that seedling characters including cotyledon and
hypocotyl are useful specific characters in the family. The larger seedling and longer hypocotyls in Bassia
eriophora, Bienertia sinuspersici Akhani (2005: 291) and Bienertia kavirense Akhani (2012: 552) may reflect
functional advantage and reduce seedling vulnerability of species growing in hot and dry climatic conditions.
At maturity, possibly, B. eriophora has adjusted to harsh situations by becoming anatomically fleshier with
the ability of preserving water inside water storage cells (Figs. 3 C–D).
The C4 anatomy in leaves of B. eriantha and B. eriophora vary in the arrangement of chloroplast
containing M and BS cells and location of water storage cells. The leaf anatomy in B. eriantha corresponds
well with a variant of atriplicoid anatomy with hypodermis cells (Kadereit et al. 2003, Pyankov et al. 2000).
The morphology and anatomical differences in perianths may have both a fundamental and functional
significance. All the examined mature fruits of B. eriophora (except early stages of development) bear five
erect spine-like outgrowths on the middle of tepals. Tepals in B. eriophora possess chloroplast containing
cells, but flowers in Bassia eriantha lack these structures. Floral photosynthesis is proposed as an
evolutionary benefit when plant reduces the transpiration rate by partial defoliation in response to harsh
environments. Such examples happens in perianths of two C4 Chenopods Bienertia cycloptera Bunge ex
Boissier (1879: 945) and Suaeda aralocaspica (Bunge 1878: 643) Freitag & Schütze (in Schütze et al. 2003:
283) (Boyd et al. 2007), as well as in fruiting perianths of Halimocnemis gamocarpus Moquin-Tandon (1840:
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155) (Pyankov & Vakhrusheva 1989) by employing the C4 structures. In this study a new example of C 4
photosynthesis in flowers of another member of family Chenopodiaceae, B. eriophora is presented.
Bassia eriantha is a psammo-halophyte plant that frequently grows under Haloxylon Bunge ex E. Fenzl
(1851: 819) trees and shrubs in stabilized sand dunes. Diaspores consist of few numbers of aggregated seeds
enclosed by woolly hairs moving in desert and rolling on sands by wind until being stopped by larger plants or
physical barriers. Probably, the thinner seed coat and scarified photosynthetic abilities helps the seeds to move
lightly and the spinulose hairs of perianths (Fig. 4 A) tie them together to travel in groups. Conversely, spiny
projections of perianths in B. eriophora could increase the chance of dispersal of seeds by epizoochory (Howe
& Smallwood 1982). Thus, the anatomy and morphology of these flowers may be a combination of seed
dispersal strategies and a response to the climatic conditions of their habitats.
The ultrastructural features of BS chloroplasts and the amounts of measured granal index are comparable
to former reports for some other NADP-ME dicots (reviewed by Edwards & Voznesenskaya 2010, see also
Voznesenskaya et al. 1999). The reports with reference to the biochemical subtype of these species relates to
the works on Central Asian C4 plants (Pyankov & Vakhrusheva 1989, Pyankov et al. 2000) that indicated B.
eriantha as a NADP-ME C4 species. Given that we suppose the Central Asian species as B. eriantha, possibly,
both species could be regarded as NADP-ME species based on ultra-structural evidences, although, additional
biochemical examinations are needed to support this finding.
Chorology and Biogeography
The chorology of B. eriantha and B. eriophora matches, respectively, regions classically named as IranoTuranian and Saharo-Sindian. This supports the previous idea that the distribution of halophytes is not only
determined by edaphic factors, but are good phytogeographical and macroclimatic markers (Djamali et al.
2011, Freitag 1991). Presence of B. eriantha in Sinai, southern Jordan and western Saudi Arabia emphasizes
the proportion of Irano-Turanian elements in this area, what has been discussed previously by presence of
several Irano-Turanian species (Danin & Plitmann 1987, Davis & Hedge 1971). However, the slight
differences in ITS sequences and monophyly of two studied samples from Jordan and Saudi Arabia (Fig 7)
show evidences that the populations of B. eriantha occurring in the western parts of SW Asia might represent
another taxon, preferably in subspecific level. This can be verified by co-cultivation experiments and
additional molecular markers. The floristic connection of Sinai with Irano-Turanian region is proposed as a
migration of species during and after the glacial periods in early Miocene via SW Asia. Realizing the Central
Asian deserts as the centre of evolution of C4 members of Camphorosmeae and derivation of this lineage in
the early Miocene (Sage 2004; Kadereit & Freitag 2011), would suggest that both species might have been
originated from Central Asia and extended to the warmer parts of SW and S Asia. Knowledge of historical
ecology will disclose when B. eriantha missed its favorable habitat in the Arabian, Syrian and Iraq deserts and
isolated in Sinai, south Jordan and west of Saudi Arabia.
Although the analyses were based on own observations and exclude literature data from many Central
Asian and Arabian localities, the results gives a pattern of distribution mainly correlated with annual mean
temperature as a limiting factor. Distribution maps (Figs. 8 A–C) demonstrate that B. eriophora is a low
elevation arid adapted species experiencing very hot summers corresponding to tropical deserts and semideserts. B. eriantha prefers habitats with lower AMT in higher elevation characterized temperate deserts and
semi-deserts. Such conditions exist as a small area in Sinai and Southern Jordan with the preferential AMT
favoured by B. eriantha (Fig. 8 B), and the eastern sides of Dead Sea valley where B. eriantha is reported
from Jordan (Al-Eisawi 1982). The single observation from west of Saudi Arabia has been collected almost
from the same elevation. According to climatic maps (Fig. 8 B) we would expect finding B. eriantha in
suitable habitats in Syrian and north western Iraqi deserts. We suggest that the several unchecked samples
from North East Pakistan, north Afghanistan and Turkmenistan could refer to B. eriantha and the unchecked
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sample from the border of Pakistan and India as B. eriophora. All the unchecked specimens from northern
Saudi Arabia should be B. eriophora, but those from the western and southern parts must be checked for
correct identification.
It is well known that in general, aridity and high temperatures are of the most remarkable pre-conditions
in evolution and establishment of C 4 species in natural habitats (Osborne & Sack 2012), however, in
particular, microclimatic conditions including soil nutrient, salinity, competition, growing aspect and some
biological factors like biochemial subtype and leaf anatomy, life cycle and fast establishment ability of
seedling play important roles in adaptation of C4 species to their habitat (Ehleringer et al. 1997, Long 1999,
Sage 2004, Akhani & Ghasemkhani 2007). To better understand further limitation of two species in this study,
microclimatic factors of their special habitat, distribution of seasonal rain and species biological features must
be studied in detail. One important feature could be related to seedling morphology and adaptation strategies.
Conclusion
In conclusion, the extreme superficial similarities of two species of Bassia yet which show much difference in
anatomical, developmental and molecular level demonstrate that conventional taxonomic practices using only
morphological characters cannot always give a reliable taxonomic image of complex groups in the family
Chenopodiaceae. The morphological homoplasy resulted from selective pressure in harsh environment,
plasticity, and scarified constant morphological characters are challenges faced by Chenopod students which
can only be satisfactorily understood by multidisciplinary approaches.
Taxonomy and nomenclature
Here an updated identification key for species of Bassia s.l. in Iran (largely modified from Hedge, 1997) and
the nomenclatural synopsis and description of B. eriantha and B. eriophora are presented.
Key to the Bassia species growing in Iran
1.
2.
3.
4.
5.
6.
-
Subshrubs, with woody rootstock; leaves linear, semi-fleshy, fruiting perianth segments with five well developed
wings ............................................................................................................................................................B. prostrata
Plants annual without woody rootstock; leaves herbaceous to fleshy, linear to broadly elliptic; fruiting perianth segments wingless or with wings or spine-like outgrowth ............................................................................................... 2
Inflorescence covered by white woolly long cotton-like hairs; mostly small-sized herbs with short life cycle during
spring and early summer .............................................................................................................................................. 3
Inflorescence not covered by woolly long hairs; usually tall herbs with life cycle mostly extending to late summer
and autumn.................................................................................................................................................................... 4
Fruiting perianth segments with five erect to slightly curved spine-like projections; leaves linear to narrowly oblong,
slightly fleshy; fruiting hairs smooth (need high magnification), veinlets dense, longitudinally oriented along the
length of the leaves, giving a false parallel venation .................................................................................B. eriophora
Fruiting perianths without spine-like outgrowth; leaves not or slightly fleshy, elliptic to ovate; fruiting hairs spinulose, veinlets not dense, reticulate, with visible end points ......................................................................... B. eriantha
Fruiting perianths with five spine-like projections on the back.................................................................................... 5
Fruiting perianths with five wings on the back............................................................................................................. 6
Spines on fruiting perianths uncinate...................................................................................................... B. hyssopifolia
Spines on fruiting perianths straight-spreading .......................................................................................... B. muricata
Leaves green, herbaceous, glabrous or glabrescent on upper surface; bush-like plants up to 150 cm tall growing as
road side and garden weed in disturbed habitats ..........................................................................................B. scoparia
Leaves green to whitish, semi-fleshy, variously hairy on upper surface; lower size plants up to 80 cm tall, mostly
xerohalophyte species occurring in desert habitats and high salty river banks ........................................................... 7
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7.
-
Seed embryo horizontal, fruiting segments winged in the middle; leaves whitish or grey, fleshy, with prominent
indumentum on upper surface, plant occurs mostly in desert habitats on gravelly soils and road side .........................
................................................................................................................................................................. B. stellaris s.l.
Seed embryo vertical, fruiting segments with a small wing-like apical appendage, plant often growing on highly
salty soils .................................................................................................................................................... B. pilosa s.l.
Bassia eriantha (Fisch. & C. A. Mey.) Kuntze (1891: 546).
Londesia eriantha Fischer & Meyer (1835: 40). Type:—KAZAKHSTAN: Novo Alexandrovsk, G. Karelin s.n. (lectotype
LE, photo! here designated by V. P. Botschantzev) (Fig. 10).—Bassia eriantha (Fisch. & C. A. Mey.) Pavlov (1935:
28). Latter homotypic synonym according to Art. 11. 5 ICN (McNeill et al. 2012).
―
Seedling: Cotyledon leaves oblong to broad elliptic, spreading and slightly fleshy, up to half the length of
the first true leaves, 0.1–0.2 × 0.4–0.6 cm, hypocotyls (0–)0.10–0.17 cm.
Mature plant: Annual, stem erect to ascending, branched from or near the base, up to 20 cm, villous,
pale to pinkish in young stems and red to purplish in age and/or in dried plants. Leaves alternate, slightly
fleshy or not, villous on both surfaces, spreading or slightly curved at apex in living plants, with prominent
reticulate veins; cauline leaves oblong, oblanceolate to spathulate, 1.6–2.5 × 1.25–1.80 cm, acute at apex,
sessile, attenuate at the base; floral leaves smaller, broadly lanceolate to broadly ovate, subsessile to shortly
petiolate. Inflorescence paniculate; flowers hermaphroditic, sometimes pistillate in upper parts of the
branches, 1(–2) flowers at the base of floral leaves, hidden in long white woolly hairs; perianths connate to 4/
5 of the length, hyaline, scarious; anthers exserted; style absent; stigmas 2–3, filiform, papillose; perianths in
fruiting stage attached to the seed coat, without outgrowth, densely covered with white woolly hairs, hairs
spinulose (very high magnification needed); fruits hidden by dense woolly hairs; seeds rounded, ovoid to
orbicular, 0.5–0.8 × 1–1.5 mm, embryo horizontal, horse-shoe shaped.
Phenology: Flowering and friuting is from May to June.
Additional specimens examined: AFGHANISTAN. Bamian: Bamian, Kash Rud, 96 km SW Dilaram,
Kuh-i-Khwaja Alta, 17 March 1968, Freitag 2441 pp (KAS); 15 km E Red Town, 2350 m, 27 October 1968,
Freitag 3963 (KAS); Farah: Farah to Dilaram, 2500–4000 ft, 24 March 1964, Furse 5529 (M). EGYPT:
Sinai Peninsula: lower Wadi el Isla, 30 April 1902, Kneucker 19 (B); in rocky and sandy places of Wadi
Hebran, 24 March 1835, Schimper 133 (B, GOET, M); Wadi esh-Sheikh, to Feiran, 7 March 1902, Kneucker
159 (B). IRAN. Esfahan: Qamishlu Protected Area, between Shah Mahur and Allahabad, 2000 m, 18 June
1996, Assadi & Khatamsaz 76399 (TARI); ibid, Godar Khakestar, 2200 m, 29 May 1996, Yusefi 1264 (TARI);
on road towards Jandagh, 950 m, 7 May 1978, Dini & Bazargan 33011 (TARI); Khur, Arusan, Khanj to
Dadkin, 950–1100 m, 24 March 1984, Nowroozi 3336 (TARI); West of Gavkhooni Wetland, 32º 18' 45'' N, 52º
39' 58'' E, 1483 m, 7 June 2010, Akhani 21384 (Hb. Akhani); Fars: Abadeh towards Shahreza (Dasht), 2 June
1969, Termeh & Izadyar 6386 (IRAN); Hormozgan: Bandar-Abbas, Gahkom, 27 March 1955, Alexandrov
6329 (IRAN); between Haji-Abad and Bandar Abbas, near Tarom and Saadatabad, Rechinger, Aellen &
Esfandiari 3288 (IRAN); Kerman: West of the Jaz Murian, 22 March 1972, 370m, J. Léonard 5742 (KAS); 25
km S Golbaf, 2000 m, 5 October 1988, Assadi & Amirabadi 66510 (TARI); 50 km W Ravar, mountain above
Hamkar coal mine, 2350–2700 m, 1 June 1986, Assadi & Bazgosha 56260 (TARI); in the south-west ridge of
the Nosratabad, Rechinger 54670 (B); Qariat-ol-Arab to Kuh-e Hezar, 2350 m, 15 June 1975, Foroughi &
Assadi 16202 (TARI); Khorassan: Ferdows to Tabas, 1100 m, 4 June 1987, Rejamand & Bazargan 31965
(TARI); Sabzevar, April 1976, Ferdowsi University Staff 20 (TARI); Eastern parts of Golestan National Park,
ca. 2–7 km road from Mirza-Baylu towards Almeh, 1250–1300 m, 10 March 1989, Akhani 6218 (Hb. Akh);
West of Tabas, South of Dasht-e Kavir, 33° 09' N 55° 49' E, 7 March 1972, Léonard 5887 (IRAN); Boshruyeh,
between Espak and Deh-Mohammad, 1220 m, 12 May 1975, Iranshahr 6606 (IRAN); Semnan: 10 km
Chahjam to Razeh, 1320 m, 25 March 1978, Freitag & Mozaffarian 28508 (TARI); Chahjam, 800m, Gabriel
& Gabriel 158b (B); 18 km SE Delbar towards Ahmadabad, 820 m, 28 March 1975, Rechinger 50547
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(TARI); 48 km ESE Delbar towards Ahmad-Abad, 1000 m, 28 March 1975, Iranshahr 6607 (IRAN); Delbar,
near rivulet just above the gardens, 1200 m, 8 May 1978, Freitag 15211 (KAS); just W of Touran Protected
Area, 500 m E of Chahjam, 1090 m, 25 May 1978, Freitag 14782 (KAS); ibid, 9 km SW Chahjam, 1150 m,
24 March 1978, Freitag 14725 (KAS); Garmab, ca. 8 km S at road to Kavir, 1150 m, 15 May 1978, Freitag
15418 (KAS); Garmab towards Kavir, 15 May 1978, Freitag & Jadidi 29058 (TARI); 35 km S of Shahrud
towards Torud, 1000–1100m, 23 March 1978, H. Freitag 14675 (KAS); 50 km Semnan to Damghan, 1630 m,
28 June 1972, Foroughi 7789 (TARI); 66 km SE Semnan, Anjirab, 1500 m, 2 May 1974, Iranshahr & Riedl
6562 (IRAN); 67 km from Garmsar to Semnan, 860 m, 7 June 1972, Amin & Mousavi 2858 (TARI); Between
Asb-Keshan and Bough, 1100 m, 2 May 1975, Iranshahr 6609 (IRAN); Damghan to Semnan, 1500 m, 26
June 1976, Rejamand & Bazargan 32156 (TARI); Torud, 800 m, 28 March 1978, Freitag & Mozaffarian
28658 (TARI); Sistan and Baluchestan: Khash, 16 March 1965, Safavi & Dezfulian 6327 (IRAN); 10 km from
Khash towards Iranshahr, 1450 m, 28 March 1977, Rechinger 54866 (B); Khash towards Iranshahr, 16 May
1948, Rechinger, Aellen & Esfandiari 6353 (IRAN); Khash, Karvandar, 1 March 1949, Mirzayan 9786
(IRAN); 40–50 km Iranshahr to Khash, 900–1000 m, Runemark, Assadi & Sardabi 22245 (TARI); 25 km
Bazman to Bam, 1200–1400 m, Runemark, Assadi & Sardabi 22598 (TARI); 35 km WSW of Nosratabad in
the road towards Bam, gravelly and sandy desert, 29º 41' 23'' N, 59º 47' 37'' E, 947 m, 1 March 2011, Akhani,
Noormohammadi & Samadi 22225 (Hb. Akhani); 120 km from Zahedan to Bam, pass after Nosratabad, 1200
m, 24 March 1977, Assadi 22763 (TARI); 41 km SW Khash, 1410 m, Babakhanlu 19780; 19766 (TARI);
Esfandak, 13 April 1974, Iranshahr & Ershad 49791-1 (IRAN); 30–40 km E of Zahedan towards Mirjawa, 28
April 1965, Lamond 124 (E); Tehran: 25 km Shah Abbasi Carvanserai towards Varamin, 850 m, 26 May 1975,
Assadi & Varnecke 17149 (TARI); Kavir Protected Region, Siah Kuh, 1000–1301 m, 26 March 1974,
Wendelbo, An Ala & Gobham 10892; 10882 (TARI); ibid., 19 May 1974, Amin & Bazargan 18317 ; 18318
(TARI); ibid., 23 May 1975, Rechinger 46209 (TARI); ibid., 19 May 1974, Amin & Bazargan 18277 (TARI);
ibid., 2 May 1974, Babakhanlu, Dini, Amin & Bazargan 17838 (TARI); near Shah Abbas Carvanserai, N of
Siah Kuh, 980 m, 2 August 1976, Freitag 13.998 (KAS); 40 km S Varamin, Mobarakiyeh, 900 m, Rechinger
46087 (TARI); 12–30 km Mobarakiyeh towards Siah-Kuh, 22 May 1974, Iranshahr 6281 (IRAN); Qom: ca.
72 km NE Qom towards Varamin, Deyre Gachin Carvansarai, 35° 31' 19"N, 51° 24' 43" E, 855 m, 22 March
2011, Akhani & Samadi 22349 (Hb. Akhani); Yazd: 63 km Bafq from Yazd, 1400 m, Assadi & Bazgosha
55979 (TARI); Kushke mine near Bafgh, c. 135 km ESE of Yazd, edge of Lut desert, limestone and river
gravel, c. 1830 m, 12 May 1967, Berens 3 (E); 7 km N of Zavareh towards Karimabad, 33° 29' 19'' N, 52° 32'
38'' E, 974 m, 28 October 2005. Akhani & Dehghani 18275 (Hb. Akhani). JORDAN. 25 km S of Ma’an,
1300 m, 14 March 1980, Frey & Kürschner, VO 5428 (E). KAZAKHSTAN. Mangyschlak peninsula: Aktau,
between the Karaschek Mountains, NW-part of the Karünjarük sand dunes, 50 m, 43° 10' 37'' N, 54° 11' 23'' E,
10 May 1995, Schnittler 6105 (KAS); Jugum Alatau Dshungaricum, montes Uljkun Kalkan, prope fontem
Kokbastau in arenis stabilis, 16 June 1971, Goloskokov 5757 (E). PAKISTAN. E2: Chagai distr. Koh-e
Sultan, 39 km N of Nokkundi, near to sulphur mines, 1800 m, 14 October 1986, 18.699/698, Freitag & Kothe
(KAS). SAUDI ARABIA. Near Uglat Asuugur off the road Medina-Qasim road, 853 m altitude, salt flat
near village, 18 March 1981, Collenette 2417 (E). TURKMENISTAN. In sandy deserts of Repetek, 5 May
1898, Litwinow 355 (B); Transcaspian region, Ashgabat, in salty desert, 3 July 1900, Sintenis s.n. (FR).
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Bassia eriophora (Schrad.) Asch. (in Schweinfurth 1867: 187).
Kochia eriophora Schrader (1809: 86). Type:—ORIGIN UNKNOWN. Herb. Fischer (lectotype GOET! here
designated); Fig. 11.—Echinopsilon eriophorus (Schrad.) Moquin-Tandon (1840: 127).—Chenolea eriophora
(Schrad.) Aitchison & Hemsley (in Aitchison 1888: 102).
Kochia latifolia Fresenius (1834: 179). Type:—EGYPT: Sinai, Thal Hebran, 2500’, Mai 1831, Rüppel, s.n. (lectotype
FR!, designated here).
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Seedling: Cotyledon leaves linear, recurved, semi fleshy, more than half to equal to the primary true leaves,
0.12–0.22 × 0.7–1.1 cm, hypocotyl elongated, up to 1.6 cm.
Mature plant: Annual, stem erect to ascending, branching from the base, up to 40 cm, densely villous,
pale to greenish white in the young vegetative state, white, pale to lightly pinkish in flower, and sometimes
reddish brown. Leaves alternate, ± fleshy, recurved in living plant, villous on both sides, reticulate veins
slightly visible; cauline leaves linear to narrowly spatulate, 0.25–0.38 × 2.10–3.75 cm, apex acute, obtuse to
rounded, sessile, leaves in branch junction smaller; floral leaves oblong to broadly elliptic, apex ± rounded;
venation densely reticulate, with few space between two adjacent/parallel veins, tertiary veinlets not clearly
visible. Inflorescence paniculate; flowers hermaphrodite, 1-2 (3) flowers in the base of floral leaves, enclosed
in long white and woolly hairs; hairs smooth or with scattered, very tiny spine like projections (under high
magnification); perianth connate to 1/2 to 2/3 of the length, with five dark green acute lobes, covered by long
woolly hairs; style short with two long filiform papillose stigma; anthers exserted; perianth at fruiting time
indurate, with five erect or slightly curved spiny outgrowths, (0.5–)1–1.5(–2) mm long; fruits hidden by
woolly hairs; seeds rounded, symetrical, 1-1.6 mm, embryo horizontal, horse-shoe shaped. Fl.- Fr.: April-June.
Typification:—The type specimen of K. eriophora was not indicated in the protologue and in subsequent
references (e.g. Hedge 1997). The description of K. eriophora was based on a cultivated plant of unknown
origin. In the herbarium of Göttingen (GOET), there is a specimen from the Fischer Herbarium annotated as
K. eriophora. The hand-writing of its label is similar to that of A. H. Schrader (see Wagenitz 1982) and
therefore can be chosen as the lectotype (Fig. 11). According to a personal communication by G. Wagenitz,
cultivated specimens of Schrader are in the Fischer herbarium. Lobin (1999) reported that the type specimen
of Bassia latifolia was probably lost; however, it was later found by A. N. Becker in Senckenberg (FR).
Additional specimens examined: AFGHANISTAN. Bamian: Kash Rud, 96 km SW Dilaram, Kuh-iKhwaja Alta, 17 April 1968, Freitag 2441 pp (KAS!); Kandahar: 20 km E of Kandahar, 1040 m, 6 May 1969,
Hedge, Wendelbo & Ekberg W 7617 (E); 60 km W of Kandahar, 900 m, 17 May 1967, Freitag 640 (KAS); 13
km E Keshkenakhud at the road to Kandahar, 980 m, semi-desert, 31° 36' N, 65° 10' E, 17 April 1978,
Podlech 30667 (M); ibid. Podlech & Jarmal 28918 (MSB); 4 km E Keshkenakhud at the road to Kandahar,
1000 m, 16 April 1972, Anders 8407 (M); 16 km NE Qala Bist, 31°28’N, 64°21’E, 900m, 21 May 1967,
Rechinger 34749 (B); Helmand: Shor Ab, on the road Dilaram–Girishk, 980 m; 32° 02' N, 63° 50' E, 20 April
1972, Anders 8611 (MSB); East Mohamad Rahi Kalay, Jabbar Oza Dasht, S Darweshan, 710 m, 30° 41' N,
64° 07' E, 17 April 1972, Anders 8479 (MSB); 25 km SE Läse Jowayn, Eastern bank of the lake Jehile Puzak,
475 m, 31° 33' N, 61° 49'E, April 1978, Moh. Rahim 12 (MSB); Farah: Farah Rud, 32° 48' N, 62° 40' to the
north, the road between Shindand and Dilaram, 1150, 24 April 1967, Rechinger 33393 (M); ca. 100 km SE of
Farahrod [Farah Rud] on the road from Herat to Kandahar, 850m, 7 July 1972, Uotila 16453 (E). IRAQ.
desert land near Samarra, 19 May 1977, Hossain & Sofaji 92 (B); Basra, Southern desert, Zubair, 30° 20' N,
47° 40' E, 18 March 1957, Rechinger 8627 (B); 2–3 miles south of Zubair, Basra Liwa, Anonymous,
Department of Botany, University Herbarium 8494 (E); Ur, Nazirya Liwa, 23 April 1953, Regel 110 (B); Near
the border of Iran, between Mandali and Badra, ca 20 km S of Badra, 3 June 1957, Rechinger 9684 (E); Faluja
desert, 20 April 1955, Wheeler Haines 110 (E); Kut al-Imara, near the Iranian border, 16 km SE Badra, on
rocky sandy area, ca. 33º N, 46º E, 12.-13 April 1957, Rechinger 9216 (E); ca. 70 km South of Mosul along
Mosul Baghdad road, 21 September 1978, Mosharaf Hossain s.n. (E). KUWAIT. 3–4 km from ‘Jahra 7 km;
Qurain 9 km sign board along Kuwait City-Ahmadi road, 29°06’N, 48°04’E, 16 March 1995, Mathew 2512
(KAS); 11 km from Sulaibhikhat roundabout on Sulaibhikhat-Jahra road, 29° 18' N, 47° 46' E, 21 March
1996, Mathew 2794 (KAS); Khaldiah, University Sports Field, 40 m, 17 March 1982, Armer 11,007
(E). PAKISTAN. Baluchestan: 7 miles from Hushab, on way to Awaran, 23 4 1970, Waiser, Raza and Abrar
Hossein 823 (KAS); Makran, Panjgur to Surab 30-50 km from Panjgur, gravel plains, c. 1100 m, 21 April
1965, Lamond 635 (E); Hoshab to Panjgur, c. 20–30 km from Panjgur, 20 April 1965, Lamond 560
(E). EGYPT. Sinai Peninsula: Wadi Hebran: in rocky mountains, 24 April 1835, Schimper, s.n. (FR); Thal
Hebran, 2500 m, May 1831, Rüppell (Holotype of Kochia latifolia Fresen., FR). JORDAN/PALESTINE. In
dry salty places near Jordan, Jericho, -300 m, 31 March 1897, Bornmüller 1376 (B); Jordan tall, April 1900,
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Warburg s.n. (B); Kaser el Yahud, 11 March 1930, Amsel s.n. (B); Dead sea valley, near Mizpe Dragot, 15 km
N of Ein Gedi, slopes and small cliffs of dolomite and wadis, 350 m, 22 March 1989, A. Danin et al. 06.065
(B); in the mountain slopes near Dead Sea, 7 April 1873, Dingler (B); Dead Sea, 1855, Rothii s.n. (M); North
of Dead Sea (Maris Mortui), -394 m, 3 March 1909, Dinsmore 4522 (E); Wadi Araba, 5 km NW of Hatzeva,
Acacia tortilis pseudosavanna, 130 m, 17 May 1988, Rilke 1415 (B); lower Jordan valley, env. of Mar
Yohanan, broken land, slopes of hills, 18 March 1942, Zohary, Orshan and Grizi 611 (B, E). IRAN.
Bushehr: 14 km Deylam to Hendijan, 50 m, 18 April 1985, Massoumi and Abuhamze 51934 (TARI); On the
salt coasts of Buschir [Bushehr], May 1868, Haussknecht (B, FR, Gott, M); Mohammad Ameri (Med Mery),
1 April 1975, Iranshahr and Termeh 34373 (IRAN); 5–10 km N of Bashi (S. of Bushir), 10 m, saline flats, 11
March 1974, Davis & Bokhari 56553 (E); Fars: Neyriz, Bakhtegan lake, 1590 m, 2 May 1972, Foroughi 7831
(TARI); 13 km N Lar, 900 m, 1 May 1961, Pabot 6081 (IRAN); 18 km Lar to Bastak, 1000 m, 16 March
1983, Assadi and Sardabi 41767 (TARI); Darab, 125 km road to Bandar Abbas, 620 m, 27 March 1972, Riazi
7829 (TARI); Hormozgan: 100 km SE Lar, near Sartang village, 300 m, 19 March 1983, Assadi and Sardabi
41950 (TARI); 110 km Bandar Abbas to Hajiabad, after Tang Zaq Tunnel, 27 June 1995, Assadi 73703
(TARI); ibid, above the tunnel Tang-e Zagh, 1100–1400 m, 16 May 1983, Mozaffarian 44915 (TARI); 22 km
N Qotbabad, N tunnel, 1000 m, 10 March 1975, Wendelbo and Foroughi 15829 (TARI); after Ghotbabad,
Sirman village, 1100 m, 16 March 2007, Pahlevani and Torabi 47702 (IRAN); 5 km Siahu, 500 m, 8 May
1982, Mozaffarian 39637 (TARI); Bastak, Dahang, 350 m, 25 March 1985, Mozaffarian 49710 (TARI);
Kerman: Kerman, in the sandy places, 2000m, 2 May 1892, Bornmüller 4223 (B); 22 km S Kahnuj, 450 m, 21
March 1972, Babakhanlu 22912 (TARI); Khuzestan: 14 km from Ahvaz to Khoramshahr, 20 m, 12 March
1983, Ruhipur 350 (TARI); Ahvaz, 20 km towards Hamidiyeh, 2 April 1985, Ghaffari 47164 (TARI);
Omidiyeh, 100 m, 14 May 1986, Mozaffarian 63344 (TARI); Shush-e Danial, 200 m, 10 April 1972,
Foroughi 3150 (TARI); 10 km Ahvaz to Susangerd, 20 m, 12 March 1985, Mozaffarian 53429 (TARI); 12 km
E Ahvaz, 8 April 1959, Pabot 6082 (IRAN); 20 km Ahvaz from Susangerd, 13 February 1972, Iranshahr and
Termeh 9788 (IRAN); Minoo Island, 14 March 2002, Eskandari 38003 (IRAN); 38 km east of Mahshahr in
the road towards Hendijan, saline soils around the road, 30° 30' N, 49° 36' E, 9 March 2010, Akhani and
Pahlevani 20885 (Hb. Akh.); Behbahan to Omidiye, 350–400 m, 21 April 1974, Davis & Bokhari 55794 (E);
Sistan and Baluchestan: ca. 48 km s of Zabol, 8 km S Ramshahr, 30° 38' 54" N, 61° 23' 33" E, 481–492 m,
along and around the salt playa and surrounding salty and gypsy hills, ca. 9 km N of Shahre Sookhte, 1 March
2011, Akhani, Noormohammadi and Samadi 22118 (Hb. Akh.); East of Dasht-e Lut, road from Neh towards
Zahedan, 31° 03' N 60° 27' E, 15 March 1972, Léonard 5888 (IRAN); Iranshahr, Bampur, 14 December 1974,
Achak 46908 (IRAN); 25 km Bazman to Bam, 1200–1400 m, 10 April 1977, Runemark, Assadi & Sardabi
22598 (TARI); 25 km Iranshahr to Khash, Baluchakan, 950 m, 4 June 1985, Mozaffarian 53373 (TARI); 40–
45 km Iranshahr to Khash, 900-1000 m, 6 April 1977, Runemark, Assadi & Sardabi 22245 (TARI); 60 km
Zabol to Zahedan, 760 m, 25 April 1985, Valizadeh & Maassoumi 1028 (TARI); Esfandak, 13 April 1974,
Iranshahr & Ershad 49791-2 (IRAN); between Iranshahr and Bam, Bazman, 1200 m, 28 March 1977, Assadi
23024 (TARI); Kuh-e Khajeh, 500–630 m, 19 February1984, Valizadeh and Maassoumi 1003 (TARI); Qasr-e
Qand, 16 km road to Rask, 450 m, 9 March 1974, Foroughi 10772 (E, TARI); Khorassan: Boshruyeh,
between Ali-Abad and Espak, 900m, 12 May 1975, Iranshahr 6608 (IRAN); 17 km after Nehbandan towards
Zabol, along dry river, 31° 37' 00" N, 60° 11' 21" E, 1227 m, 30 April 2011, Akhani, Noormohammadi and
Samadi 22067 (Hb. Akh.); 20 km W of Nehbandan towards Deh Salam, near Chahdashi, saline flat and
disturbed soils around the road, 31° 13' 23" N, 59° 46' 18" E, 1068 m, 30 February 2011, Akhani,
Noormohammadi and Samadi 22048 (Hb. Akh.). SAUDI ARABIA. Eastern Province: Jaww Dukha, 24º
48’N, 49º 5’E, 1 March 1983, Naylor 339 (E).
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FIGURE 10. Lectotype of Bassia eriantha (LE).
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FIGURE 11. Lectotype of Bassia eriophora (GOET).
Acknowledgments
This paper is part of the results of a research project supported by a grant from Iranian National Science
Foundation (INSF) under Project No. 842951, and in part from the PhD dissertation of the second author with
equal contribution of both authors. The molecular and transmission electron microscopy part and study of
specimens from European herbaria were done by the first author during his sabbatical stay in the Botanic
Garden and Botanical Museum Berlin-Dahlem (BGBM), supported by a grant from the Alexander von
Humboldt Foundation. Prof. Th. Borsch and Dr. R. Vogt, the director and curator of BGBM are particularly
acknowledged for invitation and providing facilities and working place during this study. The cooperation of
BASSIA ERIANTHA AND BASSIA ERIOPHORA
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the staff of Electron Microscopy Laboratory of the College of Science, University of Tehran (Mr S.M.H.
Hashemi) and Biological Institute of the Freie University of Berlin (Dr. R. Radek) was much appreciated. We
acknowledge the curators of E, FR, GOET, HAM, IRAN, M, MSB and KAS (in particular Prof. H. Freitag)
for lending herbarium specimens, Dr. V. Dorofeyev (St. Petersburg) for providing the picture of the type of
Londesia eriantha, Mr. I. C. Hedge for his linguistic improvements and critical suggestion on the earlier
version of this paper, Prof. G. Wagenitz for discussion on typification, Dr. A. Suchorukov for improving
suggestions and discussion on floral anatomy.
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