Int. J. Plant Sci. 168(6):931–956. 2007.
Ó 2007 by The University of Chicago. All rights reserved.
1058-5893/2007/16806-0011$15.00
DIVERSIFICATION OF THE OLD WORLD SALSOLEAE s.l. (CHENOPODIACEAE):
MOLECULAR PHYLOGENETIC ANALYSIS OF NUCLEAR AND CHLOROPLAST
DATA SETS AND A REVISED CLASSIFICATION
Hossein Akhani,1 ,* Gerald Edwards,y and Eric H. Roalson2 ,y
*School of Biology, University College of Science, University of Tehran, P.O. Box 14155-6455, Tehran, Iran; and ySchool of Biological
Sciences and Center for Integrated Biotechnology, Washington State University, Pullman, Washington 99164-4236, U.S.A.
A first comprehensive phylogenetic analysis of tribe Salsoleae s.l. (Salsoloideae: Chenopodiaceae) is
presented based on maximum parsimony and maximum likelihood analysis of nuclear ribosomal internal
transcribed spacer and chloroplast psbB-psbH DNA sequences. Our data strongly support (1) the sister
relationship of Camphorosmeae to the Salsoleae s.l.; (2) splitting of Salsoleae s.l. into two monophyletic tribes,
Salsoleae s.s. and Caroxyloneae tribus nova; (3) the current status of most monotypic or oligotypic genera in
Salsoleae; and (4) polyphyly of the Botschantzev and Freitag (among others) circumscriptions of Salsola, which
falls into 10 (on average) monophyletic genera/lineages. Three well-supported genera are described as new
(Pyankovia, Kaviria, and Turania), and four previously described genera are resurrected (Caroxylon, Climacoptera, Kali, and Xylosalsola). Salsola s.s. include a group of central and southwest Asian and north African
species that consists of Salsola sect. Salsola s.s., Salsola sect. Caroxylon subsect. Coccosalsola, Salsola sect.
Obpyrifolia, Fadenia, Hypocylix, Seidlitzia, and Darniella. All species of tribe Caroxyloneae investigated so
far have C4 photosynthesis of the NAD-malic enzyme subtype, while the majority of the species of Salsoleae
s.s. are known to be of the NADP-malic enzyme subtype.
Keywords: Caroxyloneae, Chenopodiaceae, classification, molecular phylogeny, Salsoleae, Salsoloideae.
Introduction
number of researchers using morphological and molecular
markers (Scott 1977a, 1977b, 1978; Cuénoud et al. 2002;
Kadereit et al. 2003, 2006; Pratt 2003; Schütze et al. 2003;
Müller and Borsch 2005; Shepherd et al. 2005; Kapralov
et al. 2006). The Salsoloideae subfamily has been circumscribed variously, but in recent years it has either included
tribes Sarcobateae, Suaedeae, and Salsoleae (Kühn et al.
1993) or been restricted to the tribes Camphorosmeae, Sclerolaeneae, and Salsoleae (Kadereit et al. 2003). The Salsoloideae,
here defined as including the Salsoleae s.l. and Camphorosmeae (including Sclerolaeneae) clades (Kadereit et al. 2003;
Pratt 2003; Kapralov et al. 2006), has been demonstrated to
be monophyletic (Kapralov et al. 2006). The monophyly of
the two Salsoleae clades in relation to the Camphorosmeae,
however, has been both questioned and poorly supported
in past studies (Pyankov et al. 2001a; Kadereit et al. 2003;
Kapralov et al. 2006).
Tribe Salsoleae includes one-third of all known genera currently recognized in the family Chenopodiaceae (32 of 98 genera; sensu Kühn et al. 1993), but it is a poorly understood
lineage. Species concepts in the tribe have varied widely
among researchers, with some recognizing a large number of
species separated by relatively minor morphological differences (the Russian ‘‘splitters’’; Botschantzev 1970, 1972, 1974a,
1975b, 1976, 1977, 1981a, 1982, among others; Pratov 1986)
and others circumscribing fewer ‘‘metaspecies’’ (the European
‘‘lumpers’’; Freitag 1997), resulting in between 300 and 400
species accepted in the tribe (Botschantzev 1969a, 1969b,
1969c, 1970, 1971, 1972, 1974a, 1974b, 1975a, 1975b,
1975c, 1975d, 1976, 1977, 1980, 1981a, 1981b, 1982,
1986, 1989; Kühn et al. 1993; Freitag 1997). It is unclear
Chenopodiaceae is a cosmopolitan, eudicot lineage especially
diverse in arid, semiarid, saline, and hypersaline ecosystems
(Kühn et al. 1993; Hedge et al. 1997). The family is extremely
variable in its ecomorphological and anatomical types and
modes of photosynthesis (Carolin et al. 1975, 1978; Gamaley
and Voznesenskaya 1986; Pyankov et al. 1992, 1997, 2001b,
2002; Akhani et al. 1997, 2005; Jacobs 2001; Voznesenskaya
et al. 2001b, 2002; Kadereit et al. 2003; Schütze et al. 2003;
Edwards et al. 2004; Akhani and Ghasemkhani 2007). Many
members of this family are succulent and late flowering and
fruiting, which has historically made collections difficult to
identify, with many specimens lacking the necessary characters for species identification. Additionally, the high levels of
diversity in the deserts of central Asia and the Middle East
have created a limitation on investigation and collection activities because of poor representation in Western herbaria.
The diversity of photosynthetic types and leaf anatomies in
this family, particularly the discovery of two anatomical
types that perform C4 photosynthesis without Kranz anatomy in one species of Suaeda (Borszczowia) and two species
of Bienertia (Freitag and Stichler 2000, 2002; Voznesenskaya
et al. 2001b, 2002; Akhani et al. 2003, 2005), has attracted
considerable interest in this intriguing group.
The classification of Chenopodiaceae and its phylogenetic
relationships with other families have been explored by a
1
2
Author for correspondence; e-mail akhani@khayam.ut.ac.ir.
Author for correspondence; e-mail roalson@mail.wsu.edu.
Manuscript received August 2006; revised manuscript received February 2007.
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
which school might better reflect phylogenetic relationships
and monophyletic lineages, but we here test several of these
concepts by sampling multiple individuals/populations within
some of these species groups. However, several of these groups
will require more detailed population genetic and morphological studies for an understanding of species boundaries.
This tribe is Old World in distribution, with its main center
of diversity in central Asian and Middle Eastern deserts and
subdeserts, with radiations into the Mediterranean, north
and south Africa, and Australia. Some species have also been
introduced into the New World. They are mostly leaf- and
stem-succulent halophytic, xerohalophytic, xerophytic, and ruderal plants with diverse traits, particularly in photosynthetic
pathways and concurrent anatomical structures (Butnik et al.
1991, 2001; Akhani et al. 1997; Pyankov et al. 1997, 2001b,
2002; Voznesenskaya et al. 1999, 2001a, 2001b; Akhani and
Ghasemkhani 2007). The potential synapomorphies for the
tribe are the presence of scarious winged perianth segments
in fruit, with possible loss in some species, and utricule with
a spiral embryo. Apparently, the winged fruiting perianth is a
most successful device for wind dispersal in desert areas.
However, the presence of a wing does not occur in all genera
and may be replaced by small protuberances or may be completely absent. In this latter group, zoochory and hydrochory
dispersal mechanisms seem likely.
Generic boundaries in Salsoleae have been the subject of a
long-standing controversy (Meyer 1829; Moquin-Tandon 1840,
1849; Bunge 1862; Bentham and Hooker 1880; Volkens
1893; Iljin 1936; Kühn et al. 1993; Hedge et al. 1997). Salsola
has had a controversial subgeneric classification, and its monophyly has been questioned, as has the recognition of such genera
as Climacoptera (Botschantzev 1956, 1969b; Pratov 1986),
Halothamnus (¼Aellenia) (Iljin 1936; Botschantzev 1981b),
Darniella (Brullo 1984), Fadenia (Aellen and Townsend 1972),
and Xylosalsola, Nitrosalsola, and Newcaspia (Tzvelev 1993).
Tables 1 and 2 summarize the complicated historical nomenclature of Salsoleae and the genus Salsola, at least for those
species included here. In the first phylogenetic analysis of
Salsoleae using internal transcribed spacer (ITS) sequences,
Pyankov et al. (2001a) revealed that Salsola is likely to be
polyphyletic, and similar results were found using rbcL sequences (Kadereit et al. 2003). The limited sampling of Salsoleae in both of these studies, however, leaves many questions
regarding phylogenetic relationships and generic circumscription in the tribe unanswered.
We use maximum parsimony and maximum likelihood
analyses of nrDNA ITS and cpDNA psbB-psbH spacer sequences to elucidate phylogenetic relationships in Salsoleae
to test generic monophyly. Further, we suggest a new generic
classification of the Salsoleae to more closely reflect phylogenetic relationships.
Material and Methods
Sampling
Most of the studied plants were collected by H. Akhani
during intensive collections since 1988 from Iran, Turkmenistan, Turkey, and the United Arab Emirates. Some collections
were dried in silica gel during field studies, and additional
specimens were obtained from the herbaria GAZ (Gazy
Herbarium, Ankara, Turkey) K, LE, M, and MSB (LudwigMaximilians-Universität, München, Germany) (table B1). Other
sources of samples included cultivated species in the greenhouse
of Washington State University (table B1) and nine ITS sequences previously published (Pyankov et al. 2001a; Kadereit
et al. 2003). Outgroups were chosen from representatives of
major lineages of the Suaedoideae and Salicornioideae (six
species in total); these lineages together have been demonstrated to be the sister group to the Salsoloideae s.l. (Kadereit
et al. 2003; Kapralov et al. 2006). Because of amplification
failure or lack of material, we could not include the following
monotypic Salsoleae s.l. genera: Sevada Moq. (MoquinTandon 1849), Iljinia Korovin ex V. Komarov (Iljin 1936),
Halarchon Bunge (1862), Physandra Botsch. (Botschantzev
1956), Traganopsis Maire et Wilczek, Nucularia Battand, and
Lagenantha Chiov. We also could not include the ditypic genus Choriptera Botsch. (¼Gyroptera). Further studies will be
necessary to resolve the phylogenetic position of these genera.
New sequences have been deposited in GenBank (accessions EF453380–EF453632). The data matrix and resultant
trees have been deposited in TreeBase (accession S1737).
DNA Sequencing
DNA was isolated using a modified 23 CTAB buffer
method (Doyle and Doyle 1987). Templates of the nrDNA
ITS region were prepared using the primers ITS5HP (59-AGG
TGA CCT GCG GAA GGA TCA TT-39; Suh et al. 1993) and
ITS4 (59-TCC TCC GCT TAT TGA TAT GC-39; White et al.
1990). Polymerase chain reaction (PCR) amplifications followed the procedures described by Roalson et al. (2001). The
chloroplast psbB-psbH spacer region was amplified using
the primers psbB-psbH-f (59-AGA TGT TTT TGC TGG TAT
TGA-39) and psbB-psbH-r (59-TTC AAC AGT TTG TGT
AGC CA-39; Xu et al. 2000). PCR amplifications followed
the procedures described by Schütze et al. (2003).
The PCR products were electrophoresed using a 0.8% agarose
gel in a 0.53 TBE (pH 8.3) buffer, stained with ethidium bromide to confirm a single product, and purified using the PEG
precipitation procedure (Johnson and Soltis 1995). Sequencing
was performed using an ABI Prism 3730 genetic analyzer. Directcycle sequencing of purified template DNAs followed manufacturer’s specifications, using the ABI Prism BigDye Terminator
Cycle Sequencing Ready Reaction Kit (PE Biosystems).
The two ITS sequencing primers provide sequences for
overlapping fragments that collectively cover the entire spacer
and 5.8S rDNA regions along both strands. The two psbBpsbH sequencing primers provide near-complete overlap
along both strands. Sequencing of ITS and psbB-psbH used
the same primers that were used for amplification.
Automated DNA sequencing chromatograms were proofed
and edited and contigs were assembled using Sequencher 4.0
(Gene Codes). The ITS sequences were truncated to include
only ITS1, 5.8S, and ITS2. The psbB-psbH sequences were truncated to include the 39 end of the psbB coding region, the psbBpsbT intergenic spacer, the psbT coding region, the psbT-psbN
intergenic spacer, the psbN coding region, and the psbN-psbH
intergenic spacer. Identification of the terminal ends and
spacer boundaries of ITS1, 5.8S, ITS2, and the psbB-psbH
Table 1
Historical Classifications of Salsoleae s.l. from 1829 to Present
Meyer 1829
Moquin-Tandon
1840, 1849
Bunge 1862a
Bentham and
Hooker 1880
Volkens
1893
Boissier 1879
Ulbrich 1934
Iljin 1936
Kühn et al.
1993
This article
Anabaseae
1840
Anabaseae
Salsoleae
Salsoleae
Salsoleae
Nucularieae
Salsoleae
Salsoleae
Salsoleae
Brachylepis
Salsoleae
Ofaiston
(A) Horizontal
Sodinae
Sodeae
Traganum
Salsola
Haloxylon
Anabasis
Anabasis
Halimocnemides
Noaea
seeds
Traganum
Traganum
Nucularia
Noaea
Sympegma
Arthrophytum?
Salsoleae
Salsola
Girgensohnia
Traganum
Arthrophytum
Horaninowia Salsoleae
Aellenia
Noaea
‘‘Canarosalsola’’
Halogeton
Traganum
Anabasis
Cornulaca
Horaninowia
Arthrophyton
Sodinae
Rhaphidophyton Salsola
‘‘Collinosalsola’’
Halimocnemis
Halimocnemis
Brachylepis
Seidlitzia
Seidlitzia
Haloxylon
Horaninovia
Horaninowia
Halothamnus
Cornulaca
Salsola
Halogeton
Nanophyton
Arthrophytum
Salsola
Seidlitzia
Seidlitzia
Seidlitzia
Cyathobasis
Cyatobasis
Schanginia
Anabaseae
Petrosimonia
Horaninovia
Haloxylon
Salsola
Salsola
Ofaiston
Anabasis
Girgensohnia
Schoberia
Cornulaca
Halocharis
Haloxylon
Helicilla
Anabaseae
Aellenia
Girgensohnia
Halogeton
Halogeton
Anabasis
Halimocnemis
Salsola
Anabasinae
Noea
Lagenantha
Anabasis
Seidlitzia
Halothamnus
Brachylepis
Halotis
Helicilla
Ofaiston
[Noaea]
Arthrophytum
Arthrophytum
Arthrophytum
Haloxylon
1849
Halarchon
(B) Vertical seeds
Noaea
Girgensohnia
Haloxylon
Iljinia
Iljinia
Hammada? p.p.
Salsoleae
Halanthium
Ofaiston
Girgensohnia
Anabasis
Anabasinae
Haloxylon
Nanophyton
Hammada
Sodeae
Gamanthus
Noaea
Anabasis
Brachylepis
Anabasideae
Nanophyton
Girgensohnia
salicornica
Helicilla
Cornulaca
Girgensohnia
Nanophytum
Petrosimonia
Ofaiston
Petrosimonia
Halocharis
Horaninowia
Horaninovia
Agathophora
Anabasis
Petrosimonia
Halocharis
Noaea
Halocharis
Halanthium
Iljinia?
Traganum
Halogeton
Nanophyton
Halocharis
Halimocnemis
Girgensohnia
Halimocnemis
Fadenia
Kali
Caroxylon
Petrosimonia
Halimocnemis
Halotis
Anabasis
Halotis
Sevada
Lagenantha?
Salsola
Halocharis
Noaea
Piptoptera
Piptoptera
Fredolia
Piptoptera
Choriptera
Halimocnemis
Anabaseae
Halanthium
Halarchon
Brachylepis
Halanthium
Rhaphidophyton Nucularia?
Halimocnemis
Halanthium
Halarchon
Gamanthus
Halimocnemideae Gamanthus
Ofaiston
‘‘Oreosalsola’’
Nanophyton
Halarchon
Cornulaca
Halanthium
Nanophytum
Cornulaca
Cornulaca
Rhaphidophyton
Halocharis
Piptoptera
Agathophora
Cornulaca
Petrosimonia
Halogeton
Traganum
Salsola s.s.
Physogeton
Halogeton
Halogeton
Halogeton
Halocharis
Sympegma
Traganopsis
Sympegma
Ofaiston
Sympegma
Sympegma
Sevada
Halimocnemis
Nucularia
Traganum
Halanthium
Suaedeae
Piptoptera
Horaninovia
Traganopsis?
Halogeton
Hypocylix
Halanthium
Piptoptera
Turania
Noaea
Gamanthus
Gamanthus
Xylosalsola
Anabasis
Halarchon
Halarchon
Caroxyloneae
Brachylepis
Cornulaca
Petrosimonia
Caroxylon
Cornulaca
Agathophora
Halimocnemis
Climacoptera
Halogeton
Halotis
Halarchon?
Micropeplis
Lagenantha
Halimocnemis
Sympegma
Halocharis
Suaedoideae-Suaedeae
Kaviria
Hypocylix
Nanophyton
Sevada
Ofaiston
Piptoptera
Petrosimonia
Physandra?
Pyankovia
Note. Classification of Salsola and its segregates is given separately in table 2. Other tribes are mentioned only when a member of Salsoleae was classified under that tribe. Genera
marked with a question mark are genera of questionable status, as dealt with in this article. Several other infratribal units are not listed here. Other authors: Botschantzev (1967, 1975a,
1975b, 1975c, 1975d: Salsoleae, subtrib. Sevadinae [Sevada, Lagenantha, Fadenia, Choriptera, Gyroptera], 1977: Agathophora [=Halogeton subgen. Agathophora]).
a The monograph dealt only with Anabaseae.
Table 2
Historical Classification of Salsola and Segregate Genera
Iljin 1936
Sect. Kali
S. kali6
S. paulsenii 6
S. soda10
S. aperta6
S. deserticola11
Sect. Physurus
S. lanata3
S. crassa3
S. turcomanica3
Sect. Heterotricha9
S. brachiata9
Sect. Anchophyllum
S. arbuscula12
S. arbusculiformis4
S. montana8
S. chiwensis12
S. richteri12
Sect. Sphragidanthus
S. subaphylla5
S. glauca5
Sect. Caroxylon2
S. laricina2
S. nitraria2
S. dendroides2
S. dzhungarica2
Sect. Aleuranthus2
S. sclerantha2
Sect. Belanthera
S. gemmascens2
S. aucheri7
S. vvdenskyi7
S. forcipitata2
S. gossypina7
Sect. Cocosalsola
S. foliosa10
Aellenia5
A. auricula5
Botschantzev (various articles)a
Climacoptera (1956)3
Halothamnus (1981b)5
Sect. Caroxylon subsect.
Caroxylon2 (1974a, 1974b)
S. zeyheri2
S. araneosa2
S. dendroides2
S. glabrescens2
S. cyclophylla2
Sect. Caroxylonsubsect.
Vermiculatae2 (1975a,
1975b, 1975c, 1975d)
S. nitraria2
S. vermiculata2
S. laricina2
S. orientalis2
S. dzhungarica2
Sect. Caroxylon subsect.
Coccosalsola (1976, 1989)
S. divaricata1
S. kerneri10
S. drummondii
(sub S. schweinfurthii)10
S. foliosa10
S. zygophylla10
Sect. Caroxylon subsect.
Arbusculae (1976)
S. arbusculiformis4
S. montana8
S. masenderanica8
S. arbuscula12
S. richteri12
Sect. Caroxylon subsect.
Tetragona (1972)2
(No species included
in our analysis)
Sect. Caroxylon subsect.
Genistoides (1976)
(No species included
in our analysis)
Sect. Belanthera
(1968, 1980)
S. canescens
(as S. boissieri)9
S. carpatha2
S. rubescens7
S. aucheri7
S. tomentosa7
S. vvdenskyi7
S. gossypina7
Sect. Malpigipila2
(1969a, 1969b, 1969c)
S. gemmascens2
Sect. Cardiandra
(1969a, 1969b, 1969c)
S. inermis2
S. forcipitata2
S. chorassanica2
S. jordanicola2
S. turkestanica2
Sect. Obpyrifolia10
(Botschantzev and
Akhani 1989)
S. drummondii10
(sub S. obpyrifolia)
Sect. Irania (1986)
S. abarghuensis2
Subtribe Sevadinae (1975c)
Fadenia zygophylloides10
Tzvelev 1993
Freitag 1997;
Hedge 1997; Rilke 1999
Salsola
Freitag 1997
Sect. Belanthera
Sect. Coccosalsola10
S. gossypina7
Sect. Kali (Mill.)
S. drummondii10
Dumort.6
S. brachiata9
S. vvdenskyi7
Sect. Salsola
S. kerneri10
Climacoptera
Sect. Arbuscula
S. canescens2
Sect. Heterotricha
S. richteri12
S. aucheri7
Iljin ex Pratov9
S. montana8
S. rubescens7
3
12
Sect. Climacoptera
S. lachnantha7
S. arbuscula
Sect. Brachyphylla
S. arbusculiformis4
S. tomentosa7
3
Iljin ex Pratov
Sect. Salsola
Sect. Physurus3
Nitrosalsola2 (=Salsola
S. soda10
S. lanata3
11
sect. Nitraria Ulbr.)
S. aperta
S. crassa3
Caroxylon2
S. paulsenii6
Hedge 1997
Sect. Belanthera
S. kali6
Seidlitzia10
(Iljin) Tzvel.
S. griffithii6
Rilke 1999
Sect. Caroxylon2
Sect. Caroxylon2
Sect. Salsola10
Sect. Malpigipila
S. nitraria2
S. soda10
2
2
S. dendroides
Sect. Sogdiana
(Botsch.) Tzvel.
S. cyclophylla2
Xylosalsola12
S. sogdiana11
2
S. abarghuensis
S. aperta11
S. vermiculata2
Sect. Androssowia
S. orientalis2
S. androssowi s.l.11
Sect. Malpighipila2
Sect. Kali6
S. gemmascens2
S. griffithii6
S. yazdiana2
S. tragus6
2
Sect. Cardiandra
S. kali6
S. chorassanica2
S. paulsenii6
2
S. forcipitata
S. jordanicola2
S. turkestanica2
S. inermis2
This article
1 ‘‘Canarosalsola’’
2 Caroxylon
3 Climacoptera
4 ‘‘Collinosalsola’’
5 Halothamnus
6 Kali
7 Kaviria gen. nov.
8 ‘‘Oreosalsola’’
9 Pyankovia gen. nov.
10 Salsola s.s.
11 Turania gen. nov.
12 Xylosalsola
Note. Only those taxa that were used in our phylogeny are listed. For a full checklist, see appendix A and references. Superscript numbers correspond to the numbers of the accepted
genera in this article (right column). Other classifications not listed included Brullo (1984): Darniella;10 Galushko (1976): Caspia; and Woloszczak (1885): Hypocylix.10
a References are given by section. Publication years of the relevant Botschantzev articles are given in parentheses.
AKHANI ET AL.—PHYLOGENY AND CLASSIFICATION OF SALSOLEAE s.l.
gene regions was based on comparisons with other species
of Chenopodiaceae (Kapralov et al. 2006). Sequences were
aligned using Clustal X (Thompson et al. 1997) with gap opening penalty of 10.00 and gap extension penalty of 1.00 for
both pairwise and multiple comparisons. The resultant alignment was then checked by eye for necessary minor corrections.
Alternate alignment parameters did not result in significantly
different topologies (data not shown). Gaps were not coded as
binary characters because of the complex nature of the gaps
in these data sets and the additional problem that they cannot be integrated into the maximum likelihood analyses.
Phylogenetic Analyses
ITS and psb-psbH regions were analyzed separately and
in combination with both maximum parsimony (MP) and
maximum likelihood (ML) analyses. All analyses were performed using PAUP* 4.0b10 (Swofford 2001). MP analyses of
the individual and combined data sets used heuristic searches
(ACCTRAN; 1000 random addition cycles, tree-bisectionreconnection [TBR] branch swapping, limit of 10,000 rearrangements per addition sequence replicate). Swapping was
run to completion for all random addition replicates. Clade
support was estimated using 1000 heuristic bootstrap replicates (100 random addition cycles per replicate, TBR branch
swapping, limit of 10,000 rearrangements per addition sequence replicate; Felsenstein 1985; Hillis and Bull 1993).
ML analyses employed heuristic searches (TBR branch
swapping). Clade support was estimated using 100 heuristic
bootstrap replicates (10 random addition cycles and 100 total rearrangements per replicate, TBR branch swapping;
Felsenstein 1985; Hillis and Bull 1993). ML analysis of the
ITS data set employed the general time-reversible model with
proportion of invariant sites (I) and gamma shape (G) parameters and empirical base frequencies (six substitution types:
A=C ¼ 1:4064, A=G ¼ 2:5332, A=T ¼ 1:7413, C=G ¼ 0:7280,
C=T ¼ 3:5703, G=T ¼ 1:0000; I ¼ 0:2193; G ¼ 0:9803; A ¼
0:2084, C ¼ 0:2519, G ¼ 0:2849, T ¼ 0:2548). ML analysis
of the psbB-psbH genetic region employed a five–rate class
transversion model with I and G parameters and empirical base
frequencies (five substitution types: A=C ¼ 0:9657, A=G ¼
1:3422, A=T ¼ 0:2773, C=G ¼ 0:7521, C=T ¼ 1:3422, G=T ¼
1:0000; I ¼ 0:2417; G ¼ 0:9036; A ¼ 0:2982, C ¼ 0:1616,
G ¼ 0:1794, T ¼ 0:3608). ML analysis of the combined data
set employed a four–rate class transition model with I and G
parameters and empirical base frequencies (four substitution
types: A=C ¼ 1:0000, A=G ¼ 1:9407, A=T ¼ 0:8031, C=G ¼
0:8031, C=T ¼ 2:5593, G=T ¼ 1:0000; I ¼ 0:2700; G ¼
0:7111; A ¼ 0:2613, C ¼ 0:2239, G ¼ 0:2239, T ¼ 0:2909).
These models were chosen based on the results of analysis using DT_ModSel (Minin et al. 2003). The DT_ModSel analysis uses a Bayesian information criterion to select a model
using branch-length error as a performance measure in a decision theory framework that also includes a penalty for
model overfitting.
Results
New ITS and psbB-psbH sequences were obtained for 132
species/accessions belonging to tribe Salsoleae s.l. and six
935
species of Salicornieae and Suaedeae as outgroups. The
aligned ITS data matrix was 743 base pairs (bp) long with
511 variable sites (68.8%), of which 400 (53.8%) were parsimony informative. Because of poor sequencing reads of some
regions, three sequences are missing a portion (104–182 bp)
of the 59 end of the ITS 1 spacer, eight sequences are missing
a portion (92 bp) of the 59 end of the ITS 2 spacer, and 14 sequences are missing a portion (4–82 bp) of the 39 end of the
ITS 2 spacer. The aligned psbB-psbH data matrix was 741 bp
long with 270 variable sites (36.4%), of which 144 (19.4%)
were parsimony informative. Because of poor sequencing reads
of some regions, nine sequences are missing a portion (1–113 bp)
of the 59 end of the psbB-psbH spacer region, and 21 sequences
are missing a portion (1–121 bp) of the 39 end of the psbB-psbH
spacer region.
MP analysis of the ITS Salsoleae data set resulted in 1451
most parsimonious trees (length ¼ 3445 steps, consistency index ½CI ¼ 0:303, retention index ½RI ¼ 0:741, rescaled consistency index ½RC ¼ 0:224). The ITS ML analysis resulted in
a single tree (ln L ¼ 17800:03435, where L ¼ likelihood).
MP analysis of the psbB-psbH data set resulted in 11,122
most parsimonious trees (length ¼ 600 steps, CI ¼ 0:595,
RI ¼ 0:766, RC ¼ 0:456). The psbB-psbH ML analysis resulted in two tied trees (ln L ¼ 4783:22431). Strict consensus trees of the MP individual data set analyses and the ML
trees of individual data set analyses are available from the
corresponding authors. MP analysis of the combined data set
resulted in 231 most parsimonious trees (length ¼ 4067 steps,
CI ¼ 0:343, RI ¼ 0:740, RC ¼ 0:254; fig. 1). The combined
ML analysis resulted in a single tree (ln L ¼ 23216:90496;
fig. 2).
Analyses of individual data sets resulted in congruent estimates of relationships, with slight differences associated with
unresolved branches and short branches with low bootstrap
support, particularly in the psbB-psbH analysis. Combined
analyses reflect the well-resolved portions of individual data
set analyses, and all branches are better supported in the
combined analysis than in either of the individual data set
analyses (trees from individual analyses in TreeBase). Given
our results that multiple alignments of individual data sets
produced congruent topologies and that there were no wellsupported conflicting branches, as well as the fact that the
clades we found are generally supported by morphological
characters, we do not consider the high levels of ITS variability or alignment issues to reduce the ability of our analyses to
reconstruct robust phylogenetic hypotheses. MP and ML
analyses of the combined data result in congruent inferences
of relationships, with differences in resolution resulting in
slightly different placement of some species (figs. 1, 2). These
differences, however, are associated with branches with low
bootstrap support in one or both analysis types. In all analyses, Salsola s.l. is clearly polyphyletic, with Salsola species
present in seven to 13 lineages or different clades, depending
on the resolution of the phylogenetic hypotheses (figs. 1, 2).
Several other genera are not monophyletic as currently circumscribed, namely, Anabasis, Halanthium, Halimocnemis,
Hammada, Gamanthus, and Climacoptera (figs. 1, 2). In
some cases, this is due to the misclassification of one or a
small number of species (e.g., Climacoptera brachiata; figs.
1B, 2B), whereas other cases, such as the polyphyly and
Fig. 1 Maximum parsimony combined data analysis strict consensus tree of 231 shortest trees (length ¼ 4067; consistency index ¼ 0:343;
retention index ¼ 0:740; rescaled consistency index ¼ 0:254). A, Outgroups and clades of Camphorosmeae and Salsoleae s.s. tribes. B,
Caroxyloneae tribe clade. Numbers above branches reflect maximum parsimony bootstrap numbers. Shaded boxes refer to species traditionally
placed in the genus Salsola. Generic abbreviations are as follows: A: ¼ Anabasis, B: ¼ Bassia, Bi: ¼ Bienertia, C: ¼ Climacoptera, Ca: ¼
936
Camphorosma, Ch: ¼ Chenoleoides, Co: ¼ Cornulaca, Cy: ¼ Cyatobasis, F: ¼ Fadenia, G: ¼ Gamanthus, Gi: ¼ Girgensohnia, H: ¼ Halotis,
Ha: ¼ Halimocnemis, Hal: ¼ Halocharis, Hala: ¼ Halanthium, Halo: ¼ Halogeton, Halot: ¼ Halothamnus, Halox: ¼ Haloxylon, Ham: ¼
Hammada, Ho: ¼ Horaninowia, K: ¼ Kochia, Ka: ¼ Kalidium, Ki: ¼ Kirilowia, L: ¼ Londesia, M: ¼ Maireana, Mi: ¼ Microcnemum, N: ¼
Nanophyton, No: ¼ Noaea, O: ¼ Ofaiston, P: ¼ Panderia, Pe: ¼ Petrosimonia, R: ¼ Rhaphydophyton, S: ¼ Salsola, Sa: ¼ Salicornia, Se: ¼ Seidlitzia,
Su: ¼ Suaeda, Sy: ¼ Sympegma, T: ¼ Traganum.
937
Fig. 2 Maximum likelihood combined data analysis tree (ln L ¼ 23216:90496). A, Outgroups and clades of Camphorosmeae and Salsoleae
s.s. tribes. B, Caroxyloneae tribe clade. Numbers above branches reflect maximum likelihood bootstrap numbers. Shaded boxes refer to species
traditionally placed in the genus Salsola. Generic abbreviations follow those in fig. 1.
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
interdigitation of Halanthium and Halimocnemis, are more
difficult (figs. 1B, 2B).
Discussion
Tribal Classification
Because individual analyses were congruent with, although
less resolved than, the combined analyses, we will generally
refer to the combined MP and ML results in our discussion.
It seems clear from the analyses presented here that the Salsoloideae is a monophyletic group with the Camphorosmeae
tribe the sister clade to Salsoleae s.l. (figs. 1, 2) and is well
supported by maximum parsimony bootstrap (mpbs ¼ 92%)
and maximum likelihood bootstrap (mlbs ¼ 75%). This relationship has been previously found (Kadereit et al. 2003;
Kapralov et al. 2006), although this branch was weakly supported by rbcL, and the multigene analysis of Kapralov et al.
(2006), while providing strong support (mlbs ¼ 86%), did
not have sufficiently extensive sampling to allow confidence
in this relationship. One previous study placed the Camphorosmeae as sister to a portion of the Salsoleae s.l. (our Caroxyloneae), creating a paraphyletic Salsoleae s.l., but this result
was weakly supported (mpbs < 50%; Pyankov et al. 2001a).
Furthermore, the traditional Salsoleae is clearly composed of
two strongly supported clades, here referred to as the Salsoleae s.s. (mpbs ¼ 100%; mlbs ¼ 100%) and the Caroxyloneae (mpbs ¼ 98%; mlbs ¼ 98%; figs. 1, 2; see taxonomic
revision in app. A). The occurrence of two well-supported
clades in Salsoleae s.l. has been found with analyses of ITS
sequences from 34 species (Pyankov et al. 2001a) and 12 species in rbcL analysis (Kadereit et al. 2003). The latter authors
referred to these two clades as Salsoleae I and Salsoleae II.
Both clades are well distinguished by a number of characters
(table 3). A particularly distinguishing characteristic of the
Caroxyloneae clade is the vesicular and disjunct anther appendage, which seems to occur in most groups and may be
involved in attracting insect pollinators, which have been observed frequently in nature (H. Akhani, personal observation). These connectives are absent or very small in members
of Salsoleae and have been noted as a minute appendage in
Halothamnus, Noaea, and Halogeton (Kothe-Heinrich 1993;
Hedge 1997); they are rarely large as those found in Raphydophytum (Iljin 1936). The two clades are also distinguishable based on C4 photosynthesis subtypes: all known species
of Caroxyloneae are of the NAD-malic enzyme subtype (table 3), and except for one doubtful case (H. Akhani, unpublished data), all Salsoleae are known to be of the NADP-malic
enzyme subtype (see also Pyankov et al. 2001a, 2001b).
Classification and Relationships in Clade Salsoleae
The Salsoleae s.s. tribe is more diverse than Caroxyloneae,
both morphologically and physiologically. In this tribe, C4,
C3, and C3-C4 intermediate species occur, with strong morphological features separating the tribe from Caroxyloneae
(table 3). Four primary lineages or clades in Salsoleae s.s. can
be distinguished: Sympegma, the Halothamnus clade, the
Kali clade, and the Salsola clade (figs. 1A, 2A). The monotypic Sympegma is sister to a clade composed of the rest of
the lineages of the Salsoleae s.s., although its separation is
only weakly supported (mpbs ¼ 62%; mlbs < 50%). The ordering of the other three clades is not strongly supported
(mpbs < 50%; mlbs < 50%), but both analyses suggest that
the Kali clade is sister to a clade composed of the Halothamnus and Salsola clades.
The monotypic Sympegma is restricted to central Asia
and is unique in the family in having terminal glomerate
Table 3
Comparison of the Characters of the Two Major Clades of Salsoleae s.l.
Character
Caroxyloneae
Life form
Mostly annual, with some hemicryptophytes and subshrubs
Branches and leaves
Alternate (except Pyankovia and one species of Petrosimonia)
Assimilation organs
Spines at leaf apex
Cotyledon leaves
Leaves and sometimes stems by age, never articulated
Mostly obtuse, rarely with spine or mucro at apex
Flat, linear, oblong, ovate
Indumentum
Stem, leaves, and perianths with long multicellular hairs,
at least when young
Hairs various; mostly articulate, spinulose, flattened,
bladderlike, basifixed, or medifixed
Present and mostly separated from theca and vesiculose,
discolor with anthers
Type of indumentum
Anther appendage
Wing on fruiting
perianths
Photosynthetic type
C4 subtype
Ecology
Geography
Wings mostly present; absent in some genera
Exclusively C4
NAD-malic enzyme
Plants with concentration in temperate deserts on
nitrified soil and ruderalized habitats
Mostly central and southwest Asia,
northern and southern Africa
Salsoleae s.s.
Mostly shrubby, subshrubby and even tree;
rarely annual
Alternate in basal genera, opposite in most
advanced lineages
Leaves and stems, often articulated
Mostly with mucro or spine at apex, rarely obtuse
Mostly terete and filiform
(flat in Anabasis and Halothamnus)
Plants mostly glabrous, with a tuft of flexuose hairs
in nodes or axil of leaves and flowers
Hairs papillose, unicellular; axial hairs flexuous and
multicellular, always basifixed
Mostly absent; if present, small and nonvesiculose,
color usually concolor with anthers
Wings always present
C4 with a few C3 and C3-C4 intermediates
NADP-malic enzyme (with few exceptions)
Plants concentrated mostly in hot deserts rich in sand,
gravel, and gypsum
As for Caroxyloneae but absent in southern Africa
AKHANI ET AL.—PHYLOGENY AND CLASSIFICATION OF SALSOLEAE s.l.
inflorescence consisting of several flowers surrounded by two
or more bracts. This species is most likely to be C3, as suggested by its Kranz-less sympegmoid leaf anatomy (Carolin
et al. 1975) and a 21.6& carbon isotope ratio. However,
the carbon isotope ratio is more positive than is typical for
C3 species, which suggests that more studies on living plants
are necessary to exclude the possibility of it functioning as a
C3-C4 intermediate.
The monophyletic Halothamnus clade probably includes
21–23 species, although only four taxa are included here.
Most species are concentrated in southwest Asia (Iran and
Afghanistan) but also occur widely in central Asia, and one
species is found in east Africa (Somalia, Ethiopia, and Djibouti) (Kothe-Heinrich 1993). The monophyly of this genus is
well supported (figs. 1A, 2A; mpbs ¼ 100%; mlbs ¼ 100%).
This genus can be defined by green annual branches, speciform inflorescence, indurated fruiting perianths that are pitted in the abscission zone, presence of a hypogenous disk,
horizontal seeds, absence of Kranz anatomy in cotyledon
leaves, and presence of a short anther appendage clearly not
separated from the theca. All known species are C4 with a
leaf anatomy lacking a hypodermis layer (Pyankov and Vakhrusheva 1989; Kothe-Heinrich 1993; Akhani et al. 1997).
The Kali clade is strongly supported in all analyses (mpbs ¼
97%; mlbs ¼ 90%). This clade assembles four previously
separate taxa in Salsoleae: the genus Traganum, Salsola sect.
Kali, Salsola sect. Sogdiana (sensu Rilke 1999), and Salsola
sect. Caroxylon subsect. Arbusculae p.p. (sensu Botschantzev
1976) or Salsola sect. Arbuscula p.p. (sensu Freitag 1997).
Besides sharing similar habitats in sandy deserts or coastal
sands, members of this clade can be defined by the combination
of morphological characteristics including succulent leaves,
nonjointed stems, apiculate to spiny leaf and bract apices,
winged fruiting perianths in most species (except Traganum),
and a cupulate or cylindrical corona above the wings of
fruiting perianths. The clade is divided into two wellsupported subclades (figs. 1A, 2A). The first of these is the
Kali subclade, previously classified as Salsola sect. Kali (sensu
Rilke 1999) or Salsola sect. Salsola s.l. p.p. (Iljin 1936), and
is strongly supported (mpbs ¼ 99%; mlbs ¼ 99%). Included
here are annual or perennial species with spiny leaf tips that
lack a leaf hypodermis. The most important feature characterizing this clade is the green cortex of annual shoots, which
are associated with longitudinal striae. The striate lines are
chlorenchymotous tissue interrupted by cholenchyma tissue
(Rilke 1999). Because the genus Kali Miller is validly published (Miller 1754), it is here used for this subclade. We
here designate Kali soda Moench (Methodus 331, 1794) as
the lectotype of Kali (see app. A) against two other possibilities: Kali tragus (L.) Scop., Fl. Carniol. 1: 775, 1772 (¼Salsola
tragus L., Cent. Pl. 2: 13, 1756) and Kali rosacea (L.)
Moench, suppl. Meth. Plant. 115, 1804 (¼S. rosacea L., Sp.
Pl. 222, 1753). Kali soda was validly described under Salsola
kali L., Sp. Pl.: 222, 1753, 1 yr earlier than the description of
the genus Kali in 1754 (Rilke 1999), and it is among the oldest
names of species in this genus (1753).
The second subclade of the Kali clade is a heterogeneous
assemblage of small trees, shrubs, subshrubs, and annual species distributed in extreme deserts of central Asia and north
Africa, primarily as components of sandy ecosystems. Its
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monophyly is well supported (mpbs ¼ 89%; mlbs ¼ 80%); it
is composed of species previously placed in Salsola sect.
Sogdiana (Iljin) Rilke, Salsola sect. Androssowia Rilke (sensu
Rilke 1999), Salsola sect. Caroxylon subsect. Arbusculae p.p.
(sensu Botschantzev 1976), and the monotypic genus Traganum. Based on the topology of the tree and distribution of
morphological features in the group, three well-supported
genera are here distinguished: Xylosalsola, Traganum, and
Turania. Xylosalsola Tzvelev includes C4 species of Salsola
sect. Caroxylon subsect. Arbuscula p.p. (Botschantzev 1976)
or Salsola sect. Arbuscula p.p. (sensu Freitag 1997). These
are shrubby species of central Asia characterized by long terete linear leaves, solitary flowers, milky white and shining
young stems, overlapping fruiting perianths that form a
corona-like structure above the winged fruiting perianths,
and presence of a minute anther appendage (Botschantzev
1976; Freitag 1997).
The small genus Traganum includes two north African/
eastern Mediterranean species, one of which is sampled here.
These are small shrubs with woolly nodes and semiterete
leaves. The fruiting perianths are indurated throughout, have
two hornlike teeth, and lack a wing. The leaves reportedly
lack a hypodermis layer (Carolin et al. 1975), which separates this genus from other lineages in this subclade of the
Kali clade.
The third lineage of this subclade includes species previously classified in Salsola sect. Salsola (Iljin 1936) or Salsola
sect. Sogdiana (Iljin) Rilke and Salsola sect. Androssowia
Rilke (Rilke 1999). These central Asian annual species have
succulent flat or semiterete leaves with a short (0.5 mm) or
long (5 mm) spine at the apex, a leaf hypodermis layer, and
cupulate fruiting perianths that are somewhat connate at the
base and give the ovary a false-inferior appearance. Furthermore, they have filiform stigmas that are very long, up to
three to five times as long as the style. Given the clear morphological circumscription of these species, we are here recognizing this clade as the genus Turania (see app. A).
The Salsola clade is a complex assemblage of genera in Salsoleae but is moderately supported in the phylogenetic hypotheses presented here (mpbs ¼ 72%; mlbs ¼ 65%). This
lineage includes taxa occurring from central and southwest
Asia to the north African and Mediterranean areas. The
monophyly of the clade is supported by several morphological features including presence of a spine or mucro on
leaf tips that sometimes appears as a caducous bristle and
most species being completely glabrous or having papillose
or tubercle-like hairs. Many groups are represented by opposite leaves or branches, and stamens have no or very short
anther appendages. Many genera have been previously described in this clade, and most of them are supported by the
phylogenetic hypotheses (figs. 1A, 2A).
The genus Salsola was typified by Salsola soda (Jarvis et al.
1993; see Rilke 1999 for details), which is nested within a
homogenous group of species that have been variously placed
in several genera in previous classifications. The monophyly
of this clade is well supported (mpbs ¼ 84%; mlbs ¼ 79%).
In spite of the morphological synapomorphies that strongly
support this clade, species of this clade have been placed
by various authors in several sections of Salsola, including
sect. Salsola (Rilke 1999), sect. Obpyrifolia (Botschantzev
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
and Akhani 1989), sect. Caroxylon subsect. Coccosalsola
(Botschantzev 1976, 1989), and sect. Coccosalsola (Freitag
1997), or have been classified into other genera, including
Seidlitzia Bunge ex Boiss. (Iljin 1954), Hypocylix Woloszczak
(Woloszczak 1885), Darniella Maire & Weiller (Brullo 1984),
Neocaspia Tzvelev (Tzvelev 1993), Caspia (Galushko 1976),
Fadenia (Aellen and Townsend 1972), and Anabasis p.p. The
most obvious synapomorphy of Salsola s.s. as treated here is
the presence of clusters of two to six flowers (or, rarely, one)
in the axil of each floral leaf. Further characters include absence or presence of a very minute anther appendage, presence of a hypogynous disk or staminode (much reduced in
S. soda), presence of a leaf hypodermis, cylindrical and obtuse leaves (more often obpyriform, at least in the juvenile
state or in bracts) that are opposite in most species, and fruiting perianths with well-developed wings (reduced in S. soda).
A surprising result is the inclusion of the tropical African
monotypic genus Fadenia in Salsola (Aellen and Townsend
1972). Fadenia zygophylloides is known from Kenya, Ethiopia, and Somalia and was previously separated from all other
species of Salsoloideae by the fruiting perianths having longitudinal membranous crests. This species has been previously
classified in subtribe Sevadinae (Botschantzev 1967, 1975c;
Boulos et al. 1991). Although we have not sampled all species of the complex, there is little doubt that all species
treated under the genus Darniella by Brullo (1984) and the
genus Seidlitzia by Iljin (1954) belong to Salsola s.s.
With the exclusion of Anabasis setifera, the rest of the genus Anabasis forms a well-supported monophyletic group
(mpbs ¼ 99%; mlbs ¼ 96%). The monophyly of this clade is
supported by the combination of several morphological features, including a perennial and shrubby habit, a thick basal
caudex (mostly woolly), opposite leaves and branches, vertical seeds, fleshy utricle that resembles a berrylike fruit in several species, articulated branches, vestigial leaves in most
species (in Anabasis eugeniae, the leaves are developed), and
the presence of a multilayered epidermis and sunken stomata
(Bokhari and Wendelbo 1978). Ecologically, most species are
extreme xerohalophytic species and frequently grow on halogypsum soils. The genus Anabasis is distributed from southwest Europe and north Africa to the Red Sea coast (Ethiopia)
and southwest and central Asia.
The monophyly of the genus Halogeton is strongly supported by all analyses (mpbs ¼ 100%; mlbs ¼ 100%). This
is a small genus of approximately five species, including both
annual (in temperate salines and ruderal places) and perennial species (in warm and hot deserts). The genus is well
defined by the combination of fleshy cylindrical leaves terminating in a persistent or caducous bristle, presence of three to
several flowers in the axil of each floral leaf, presence of a
papillose staminodial disk, presence of five wings on fruiting
perianths, and membranous perianth segments. Some authors
have removed the perennial species to the genus Agathophora
(Botschantzev 1977; Hedge 1997). Our results support a monophyletic clade including both annual and perennial species;
however, because only one of each is sampled here, future
studies will be necessary to explore whether the two growth
forms form monophyletic sister lineages.
Girgensohnia, Cyatobasis, and two species of Hammada
form a clade in the analyses presented here, although it is
weakly supported. The central Asian and Persian genus Girgensohnia includes approximately four or five species, three
sampled in this study, and forms a monophyletic wellsupported group (mpbs ¼ 96%; mlbs ¼ 86%). Morphologically,
the genus is well defined by an annual life form, opposite
leaves and branches, presence of an indumentum of scabrid
papillae, semiamplexicaule leaves with a scarious base and
spine-tipped apex, and vertical seeds. The species of Girgensohnia are ruderal and sometimes weedy species on low salty
soils in the deserts of central Asia and Iran. The monotypic
central Anatolian genus Cyatobasis was described by Aellen
(1949), who distinguished it from Girgensohnia by characters
such as elongate styles, a noncapitate stigma, and connate leaf
base. Our analyses suggest that this species, together with
Hammada articulata and Hammada griffithii, forms a grade
leading to Girgensohnia s.s. These results and shared morphological characters suggest that a wider circumscription of
the genus Girgensohnia, including Cyatobasis and Hammada
p.p. and probably the other species of Arthrophytum, is appropriate.
Analysis of two of the approximately six species of Cornulaca reveals a strongly monophyletic group (mpbs ¼ 100%;
mlbs ¼ 100%). The genus is characterized by a sturdy habit,
alternate branches, decurrent strongly spiny leaves and
bracts, presence of a dense white tuft of hairs among and at
the base of flowers, membranous perianth segments that become indurated and coalescent in fruit, one (sometimes two)
terminal perianth spine, filaments connating into a tube, and
vertical seeds. Cornulaca species occur in central and southwest Asia and northern Africa on sandy or dry soils and can
tolerate long periods of drought (H. Akhani, personal observation). The genus is sister to Horaninowia, another spiny
genus, but is clearly separated by other morphological characteristics (see next paragraph).
Horaninowia is a well-supported monophyletic genus in
our analyses (mpbs ¼ 88%; mlbs ¼ 73%). There are approximately seven spiny annual species that are characterized by
a green cortex, the presence of unicellular papillae, spinytipped leaves and bracts, solitary flowers in hairy leaf axils,
exappendiculate anthers, perianths in fruit becoming hardened in the upper middle, capitate or clavate stigmas, and
horizontal seeds (Carolin et al. 1975). Species of Horaninowia are restricted in their range to central Asia and Iran,
growing on sandy dunes or gravelly deserts. The phylogenetic
analyses and morphological features clearly support a close
relationship with Cornulaca (figs. 1A, 2A).
The traditional circumscription of Haloxylon (Iljin 1936)
includes only tall shrub to small tree species and is well supported in these analyses (mpbs ¼ 100%; mlbs ¼ 100%). The
two species, Haloxylon ammodendron and Haloxylon persicum, are found in central and southwest Asia and occur on
sandy dunes or dry salty habitats close to the margins of playas,
where their long roots have access to underground salty water
(Léonard 1991; Akhani et al. 2003; Akhani 2004). The combination of unique tree life form with articulated branches,
horizontal seeds, occurrence of an arista at the scalelike leaf
apex, presence of a hypodermis layer in assimilating shoots,
and the isopalisade cotyledon leaves without Kranz anatomy
(Pyankov et al. 1999), characterizes the genus. Bunge (1879)
and Hedge (1997) proposed a broader circumscription of this
AKHANI ET AL.—PHYLOGENY AND CLASSIFICATION OF SALSOLEAE s.l.
genus, including species from other genera such as Arthrophytum and Hammada, but this is not supported by the phylogenetic hypotheses presented here (figs. 1A, 2A).
The genera Hammada and Arthrophytum have been interpreted differently by different authors. Hedge (1997) and
Boulos (1996) considered them congeneric with Haloxylon.
The three species we have analyzed (Hammada salicornica,
Hammada articulata, and Hammada griffithii) are not closely
associated with Haloxylon and may form early lineages of
the Girgensohnia/Cornulaca/Horaninowia clade (fig. 2A), although these relationships are not well supported and are
placed differently by the MP strict consensus (fig. 1A) but,
again, with little support.
The phylogenetic hypotheses presented suggest a possible
clade including the C3 Salsola montana complex, Salsola arbusculiformis, Raphydophytum regelii, and the genus Noaea
(fig. 2A). This clade, however, is not strongly supported
and is not present in the MP strict consensus (fig. 1A). The
placement of the C3-C4 intermediate Salsola arbusculiformis
(Voznesenskaya et al. 2001a) between Salsola montana and
Noaea, a C4 genus, might demonstrate an interesting case of
transition in photosynthetic pathway across a clade. Given
the weak phylogenetic placement of S. arbusculiformis in the
phylogenetic hypotheses presented here, we are only informally recognizing this species as ‘‘Collinosalsola’’ and will
await further evidence of its phylogenetic position before formally placing the species. The small subshrub Raphydophytum is characterized by stiff and spinescent leaves that are
acicular and three-angular in cross section, with scabrid margins and a dilated base. The perianths bear wings near the
base, and the filaments produce a staminal tube with welldeveloped semiorbicular lobes on the hypogynous disk.
All known species of Noaea are included in our phylogenetic analyses, and its monophyly is well supported (mpbs ¼
100%; mlbs ¼ 100%). This genus is characterized by alternate branches, leaves spiny tipped or cuspidate at the base
with broad white membranous margins, and vertical seeds.
All three species grow in temperate and cold-temperate deserts or montane and submontane steppe vegetation, which is
not typical for C4 species.
The S. montana complex was classified in Salsola sect. Anchophyllum by Iljin (1936), sect. Caroxylon subsect. Arbusculae by Botschantzev (1976), and sect. Arbuscula by Freitag
(1997). The complex includes subshrubby species that differ
from species of previously mentioned Salsola s.l. groups in having not only green young stems but also a sympegmoid leaf
anatomy (Akhani and Ghasemkhani 2007), filaments attached
to the disk without staminodes, and anthers divided only to
two-thirds of their length. The precise phylogenetic position of
this strongly supported clade (mpbs ¼ 100%; mlbs ¼ 100%) is
not clear, and we are therefore here treating this complex as the
informal taxonomic entity ‘‘Oreosalsola’’ (see app. A).
The S. montana species complex represents an assemblage
of microspecies (Salsola maracandica Iljin, Salsola oreophila
Botsch., Salsola masenderanica Botsch., Salsola botschantzevii Kurbanov, Salsola flexuosa Botsch., Salsola tianschanica
Botsch., Salsola lipschitzii Botsch., Salsola junatovii Botsch.,
and S. montana Litw.), which are collectively included in a
broadly defined S. montana by Freitag (1997). We have here
examined three populations in this complex, one from Golestan
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National Park (S. montana), one from the Alborz mountains
(S. masenderanica), and ‘‘Salsola touranica,’’ an undescribed
but likely distinct entity from the Touran Protected Area of
Iran. Members of this species complex need to be studied further in order for us to understand where species boundaries lie
and whether one or eight or more species should be recognized.
Salsola divaricata was included in Salsola sect. Caroxylon
subsect. Coccosalsola by Botschantzev (1976, 1989). This
shrubby species is endemic to the Canary Islands and is distinctive in having opposite leaves, mature leaves that are triangular
in cross section, and leaves with one layer of hypodermis, two
layers of palisade parenchyma, scattered peripheral vascular
bundles, and a central aqueous tissue. Morphologically, it is
very similar to species of Salsola s.s., but this species does not
strongly group with Salsola s.s. Given its unclear phylogenetic
position and the need to sample the similar C3 Mediterranean/
north African/central Asian species Salsola genistoides, Salsola
webbii, and Salsola pachyphylla, no nomenclatural changes are
here proposed.
Classification and Relationships in Clade Caroxyloneae
Three major clades can be distinguished in Caroxyloneae,
which are here labeled as the Caroxylon clade (mpbs ¼ 88%;
mlbs ¼ 93%), the Kaviria clade (mpbs ¼ 86%; mlbs ¼ 87%),
and the Climacoptera clade (mpbs ¼ 77%; mlbs ¼ 83%). Two
of the three clades can be divided further into two or more
monophyletic lineages, which in most cases correspond with
traditional classifications of Salsoleae genera. However, the relationship and generic circumscription of several closely related
annual genera in this clade, including Halanthium, Halimocnemis, Halotis, Gamanthus, Climacoptera, Piptoptera, Halocharis,
Halarchon, Petrosimonia, and Physandra, has been controversial (Pratov 1986; Akhani 1996; Hedge 1997; Assadi 2001; Ghobadnejhad et al. 2004). These euhalophytic and xerohalophytic
species are endemic to the Irano-Turanian area, primarily in temperate deserts of central Asia, Afghanistan, and Iran. Except Petrosimonia, with connate cagelike anther appendages, all species
are characterized by large, often showy and colorful (white, yellow, or purple) vesciculate anther appendages, which apparently
act as an attractor for insect pollinators and may also contribute
as a wind-dispersal device for anthers and pollen grains, depending on the species.
The Caroxylon clade includes a large group of species traditionally classified as Salsola sects. Caroxylon p.p. (subsect.
Caroxylon, subsect. Vermiculatae), Cardiandra, Irania, and
Malpigipila and two species of sect. Belanthera (Salsola canescens and Salsola carpatha). The monophyly of this clade is
well supported (figs. 1B, 2B). This is the most widespread
lineage of Salsoleae s.l., with ca. 140 described species, being
found in central Asia, Arabia, and northern and southern
Africa (Botschantzev 1968, 1969a, 1969c, 1970, 1972, 1974a,
1974b, 1975b, 1975d, 1980, 1986; Freitag 1997). Our phylogeny includes 19 species covering most known lineages and
geographic areas. The clade is morphologically heterogeneous,
although the presence of an acute anther appendage, winged
perianth segments, a gibbous leaf base, and a staminal disk provides a combination of characters that distinguishes the clade.
The oldest generic name for species in this clade is Caroxylon
Thunb. It was reduced to a section of Salsola by several
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
subsequent authors (Fenzl 1851; Iljin 1936) but recognized at
the generic level by Tzvelev (1993), which is supported by our
data. Relationships within Caroxylon are generally weakly supported (figs. 1B, 2B) and will require further study to clarify.
The Kaviria clade includes species traditionally classified in
Salsola sect. Belanthera (excluding S. canescens, S. carpatha, and
other microspecies classified in subsect. Kochioides by Botschantzev [1968, 1980]), the oligotypic genus Halocharis, and the
monotypic genus Nanophyton (figs. 1B, 2B). The combination
of the C3 cotyledon leaves, the absence of a leaf hypodermis, and
the presence of an acute triangular anther appendage that is separated from the thecae circumscribes this clade well, and morphological and ecological features clearly separate each of these
three lineages from each other (table 4). Salsola sect. Belanthera
is here named Kaviria (see app. A) after the Persian term ‘‘Kavir,’’
a name used to refer to the Iranian Great Desert.
The Climacoptera clade is composed of a lineage including
Petrosimonia and Ofaiston, which is sister to the remainder
of the clade (figs. 1B, 2B). This is an exclusively Irano-Turanian
species group that predominantly occurs in annual halophytic
and xerohalophytic communities of central and southwest
Asia. Petrosimonia and Ofaiston are quite distinct morphologically, and Petrosimonia is supported as monophyletic in
all analyses. Ofaiston is characterized by having only one or
two stamens and three to five perianth parts (tepals), strongly
keeled bracteoles, and small wings on two tepals (Iljin 1936).
In Petrosimonia, the anther appendages are connate at the
apex, creating a cagelike structure, and wings are completely
absent from the membranous tepals.
The remainder of the Climacoptera clade is strongly supported (mpbs ¼ 100%; mlbs ¼ 100%). All of the genera
within this clade are para- or polyphyletic, including Climacoptera, Gamanthus, Halanthium, and Halimocnemis (figs.
1B, 2B). The majority of the members of several genera form
strongly supported clades, and clear lineages can be defined
in several cases. If Climacoptera brachiata is excluded from
the rest of the genus, Climacoptera forms a strongly supported monophyletic genus (mpbs ¼ 100%; mlbs ¼ 100%).
Climacoptera was segregated from Salsola by Botschantzev
(1956); however, it was considered as Salsola sect. Physurus
by Freitag (1997). The presence of five winged perianths in
fruit, strongly fleshy, glaucous, and mostly decurrent floral
leaves, a main central erect stem, and an interrupted Kranz
layer on the adaxial leaf surface define the genus. The number of species in this lineage is unclear, as different authors
have recognized from as many as 42 species (Pratov 1986) to
as few as six (Freitag 1997). Preliminary evidence from Iran
(H. Akhani, unpublished data) suggests that approximately
eight to 10 species are distinguishable, as opposed to only
two species recognized in Flora Iranica by Freitag (1997).
Climacoptera brachiata has been variously treated as a member of Salsola sect. Heterotricha Iljin (Iljin 1936), Climacoptera
(Botschantzev 1956), Climacoptera sect. Heterotricha Iljin ex
Pratov (Pratov 1986), and Salsola sect. Belanthera (Freitag 1997).
Based on the characteristic opposite leaves (except uppermost
floral leaves), small obtuse anther appendage, and presence of a
spinulose indumentum with long smooth articulate hairs, it is
well separated from the other genera of the Climacoptera
Table 4
Morphological and Anatomical Comparison of Genera in the Kaviria Clade
Character
Habit
Inflorescence
(flowers in each
floral leaf axis)
Indumentum
Kaviria
Annual, prostrate
Pulvinate undershrub, with
stout woody base, erect
Solitary
Spinulose, branched, scabrid,
articulated
Solitary to several
Articulated, scabrid hairs,
multicellular flexuous hairs
on axil of flowers
Terete, strongly succulent,
with one or a few bristlelike
hairs at apex
Gibbous
Absent
Solitary
Multicelluar, smooth flexuous
hairs in leaf and flower axils
Terete to semiterete, succulent,
hairy or glabrous throughout
Leaf base
Hypodermis
Central vascular
bundle (VB)
Slightly gibbous
Absent
Seeds
Hypogynous disc
Nanophyton
Undershrub, rarely annual,
erect to ascending
Leaf shape
Fruiting perianth
Halocharis
VB associated with
sclerenchymatous tissue
Winged or with small
transversal line
Horizontal, rarely vertical
Hypogynous disk present, without
or with short interstaminal lobes
Anther
Triangular, appendage scabrous
Stigma
Ecology
Flat, shortly dentate
Dry gravelly and slightly salty soils
VB lacking sclerenchymatous
tissue
Scarious, wingless
Vertical
Filaments not narrowed to base,
hypgynous disk absent
Appendage divided to the base,
appendage vesiculous or
triangular, papillose
Terete, not dentate
High salty clay soils
Semiterete to triangular in
section, spiny tipped
Not gibbous
Present
VB associated with
sclerenchymatous tissue
Enlarged and inflated in
fruit but without wing
Vertical
Filament not narrowed to base,
located at hypogynous disk
with staminode lobes
Anthers divided to the apex,
appendage triangular, smooth
Terete, not dentate
Xerophytic communities
AKHANI ET AL.—PHYLOGENY AND CLASSIFICATION OF SALSOLEAE s.l.
clade. Given the isolated phylogenetic position of this species
and its distinctive combination of characteristics, we feel it is
best treated as a monotypic genus, here named Pyankovia
(see app. A) in honor of the late professor Vladimir Pyankov.
The remainder of the species in the Climacoptera clade belong to four genera: Gamanthus, Halanthium, Halotis, and
Halimocnemis. The relationships and generic boundaries of
these genera have been debated (Akhani 1996; Hedge 1997;
Assadi 2001; Ghobadnejhad et al. 2004). The phylogenetic
results presented here suggest the possibility of four lineages,
although the relationships among these lineages and clade
membership are generally poorly supported (figs. 1B, 2B),
and whether there are consistent morphological characters
by which to define these clades is unclear. Further, there are
entanglements of the types of some genera (e.g., Gamanthus
pilosus nested within the Halanthium clade, separate from
the rest of Gamanthus). While a case could be made for either rejecting the current lectotype of Gamanthus or renaming the rest of the Gamanthus clade under a new name
(given its strong support), we consider the recognition of all
of these species within Halimocnemis to be the best option at
this time, at least until the generic boundaries and nomenclatural problems can be untangled. While this group is not
present in the MP strict consensus, it is present in the most
likely tree, albeit with low support (58%). Because Halimocnemis and Halotis are very similar morphologically and were
previously merged by Hedge (1997), and the phylogenetic
hypotheses places Halimocnemis purpureum and Halotis pedunculata among Halanthium species (see Akhani 1996;
Hedge 1997), we feel the combination of these genera to be
a reasonable compromise, despite the low branch support.
945
The monotypic genus Piptoptera was amplified only for
psbB-psbH, confirming that it is not a well-supported member of any of the clades described above, which corresponds
with its morphological isolation. It is weakly placed among
Halanthium and Gamanthus species. This might suggest its
inclusion in the more broadly circumscribed Halimocnemis,
but formal inclusion in that genus will require further data,
particularly given the peculiar features of this genus of sturdy
habit with adpressed indumentum and development of two
large, circular perianthal wings.
Acknowledgments
This article is the result of a sabbatical leave of H. Akhani
supported by a grant of the University of Tehran. The fieldwork was partly supported by the Geobotanical Studies in
Different Parts of Iran I–III research project, and portions of
this project were also supported by Civilian Research and
Development Foundation grant RB1-2502-ST-03. Five of the
sequenced species in this study were provided during a research visit to Royal Botanical Gardens, Kew (Jodrell Laboratory). H. Akhani acknowledges the financial support of
the Royal Society and the help of Mark Chase and other
staff members. We acknowledge Maraym Ghasemkhani for
her help; Ehsan Akhani, A. Beck, R. Khoshravesh, M. Djamali, T. Eftekhari, C. Deigele, and H. Ziegler for providing
material from collections in Munich and Iran; C. M. WilmotDear (Kew) for correcting the Latin diagnoses; and Larry
Hufford and two anonymous reviewers for comments on a
previous version of the manuscript.
Appendix A
A Revised Classification of Salsoleae s.l.
Here we present a synopsis of generic circumscriptions and new combinations resulting from this study, where both strong
molecular and morphological support necessitate changes. To save space, we have included only the most necessary nomenclatural data. Therefore, most synonyms and citations are not included in this article. A detailed morphological, taxonomical, and
anatomical assessment of tribes Camphorosmeae, Caroxyloneae, and Salsoleae awaits future publication.
Tribe Salsoleae s.s.
Anabasis L., Sp. Pl. 223, 1753. Type: Anabasis aphylla L.
Includes Anabasis aphylla L., A. aretioides Moq. & Coss., A. articulata (Forssk.) Moq., A. brevifolia C. A. Mey., A. brachiata Fisch. & C. A.
Mey., A. calcarea (Charif & Aellen) Bokhari & Wendelbo, A. cretacea Pall., A. ebracteolata Korov. ex Botsch., A. ehrenbergii Schweinf. ex
Boiss., A. elatior (C. A. Mey.) Schrenk, A. eriopoda (Schrenk) Benth. ex Volkens, A. eugeniae Iljin, A. ferganica Drob., A. gypsicola Iljin, A.
haussknechtii Bunge ex Boiss., A. iranica Iljin, A. jaxartica (Bunge) Benth. ex Volkens, A. lachnantha Aellen & Rech. f., A. paucifolia M.
Pop. ex Iljin, A. pelliotii Danguy, A. macroptera Moq., A. prostrata Pomel., A. oropediorum Maire, A. salsa (C. A. Mey.) Benth. ex
Volkens, A. syriaca Iljin, A. tianschanica Botsch., A. truncata (Schrenk) Bunge, A. turkestanica Iljin & Korov., and A. turgaica Iljin &
Krasch.
Arthrophytum Schrenk, Bull. Phys. Math. Acad. Petrop. 3: 211, 1845. Type: A. subulifolium Schrenk.
Includes Arthrophytum gracile Aellen, A. iliense Iljin, A. balchaschense (Iljin) Botsch., A. lehmannianum Bunge, A. pulvinatum Litv., A.
subulifolium Schrenk, A. longibracteatum Korov., A. korovinii Botsch., and A. betpakdalense Korov. (Korovin and Mironov 1935).
Cornulaca Delile, Flore d’Egypte—explic. des planches 72, 1813. Type: Cornulaca monacantha Delile.
Includes Cornulaca alaschanica C. P. Tsien & G. L. Chu, C. aucheri Moq., C. ehrenbergii Asch., C. korshinskyi Litv., C. monacantha Delile,
and C. setifera (DC.) Moq. (Aellen 1950; Boulos 1992).
Girgensohnia Bunge ex Fenzl in Ledeb., Fl. Ross. 3: 835, 1851. Type: Girgensohnia oppositiflora (Pall.) Fenzl.
Includes Girgensohnia diptera Bunge, G. imbricata Bunge, G. minima E. Korov., and G. oppositiflora (Pall.) Fenzl.
Halogeton C. A. Mey. in Ledeb., Icon. Pl. Fl. Ross. 1: 10, 1829. Type: Halogeton glomeratus (M. Bieb.) C. A. Mey. Synonyms: Agathophora
(Fenzl) Bunge, Micropeplis Bunge.
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INTERNATIONAL JOURNAL OF PLANT SCIENCES
Includes Halogeton alopecuroides (Delile) Moq., H. arachnoideus Moq., H. glomeratus (M. Bieb.) C. A. Mey., H. sativus (L.) Moq., and H.
tibeticus Bunge (Bunge 1862; Botschantzev 1977).
Halothamnus Jaub. & Spach, Illustr. Pl. Or. 2: 50, tab. 136, 1845. Type: Halothamnus bottae Jaub. & Spach. Synonym: Aellenia Ulbr.
Includes Halothamnus beckettii Botsch., H. somalensis (N. E. Br.) Botsch., H. bottae Jaub. & Spach, H. iranicus Botsch., H. hierochunticus
(Bornm.) Botsch., H. iliensis (Lipsky) Botsch., H. auriculus (Moq.) Botsch., H. kermanensis Kothe-H., H. afghanicus Kothe-H., H.
lancifolius (Boiss.) Kothe-H., H. cinerascens (Moq.) Kothe-H., H. glaucus (M.Bieb.) Botsch., H. bamianicus (Gilli) Botsch., H. shurabi Botsch.,
H. turcomanicus Botsch., H. ferganensis Botsch., H. sistanicus (De Marco & Dinelli) Kothe-H., H. oxianus Botsch., H. seravschanicus Botsch.,
H. iraqensis Botsch., and H. subaphyllus (C. A. Mey.) Botsch. (Aellen 1950; Botschantzev 1981b; Kothe-Heinrich 1993).
Haloxylon Bunge, Rel. Lehm. in Mém. Sav. Etrang. Petersb. 7: 468, 1851. Type: Haloxylon ammodendron (C. A. Mey.) Bunge ex Fenzl.
Includes Haloxylon ammodendron (C. A. Mey.) Bunge and H. persicum Bunge ex Boiss.
Hammada Iljin, Bot. Zhurn. 33: 582, 1948. Type: Hammada leptoclada (M. Popov) Iljin.
Includes Hammada articulata (Moq.) O. Bolós & Vigo, H. eigii Iljin, H. griffithii (Moq.) Iljin, H. multiflora (Moq.) Iljin, H. negevensis Iljin
& Zoh., H. ramosissima (Boiss.) Iljin, H. salicornica (Moq.) Iljin, H. schmittiana (Pomel) Botsch., H. scoparia (Pomel) Iljin, H. thomsoni
(Bunge) Iljin, and H. tamariscifolia (L.) Iljin, and H. wakhanica (Paulsen) Iljin (Iljin 1948).
Horaninowia Fisch. & C. A. Mey., Enum. Pl. Nov. Schrenk 1: 10, 1841. Type: Horaninowia ulicina Fisch. & C. A. Mey.
Includes Horaninowia anomala (C. A. Mey.) Moq., H. excellens Iljin, H. minor Fisch. & C. A. Mey., H. platyptera Charif & Aellen, H.
pungens (Gilli) Botsch., and H. ulicina Fisch. & C. A. Mey. (Aellen 1950).
Kali Mill., Gard. Dict. Abridg. Ed. 4, 1754. (¼Salsola sect. Kali Dumort; Rilke 1999). Type (lectotype selected here): Kali soda Moench,
Method 331, 1794. [ Salsola kali L., Sp. Pl.: 222, 1753.
Kali australis (R. Br.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola kali R. Br. Prodr. 411, 1810.
Kali griffithii (Bunge) Akhani & E. H. Roalson, comb. nov. Basionym: Noaea griffithii Bunge, Mém. Acad. Imp. Sci. St. Pétersb., Sér. 7, 4, 11:
22–23, 1862.
Kali tamariscina (Pall.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola tamariscina Pall., Illustr. Pl. 33, 1803.
Kali collina (Pall.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola collina Pall., Illustr. Pl.: 34, 1803.
Kali zaidamica (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola zaidamica Iljin, Bot. Mater. Gerb. Bot. Inst. Komarova Akad.
Nauk SSSR 17: 122–124, 1955.
Kali tamamschjanae (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola tamamschjanae Iljin, Trudy Bot. Inst. Akad. Nauk. SSSR,
ser. 1: 161, 1936.
Kali jacquemontii (Moq.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola jacquemontii Moq. in DC. Prodr. 13, 2: 188, 1849.
Kali komarovii (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola komarovii Iljin, Bot. Zhurn. SSSR 18, 2: 276, 1933.
Kali ikonnikovii (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola ikonnikovii Iljin, Izv. Glavn. Bot. Sada Akad. Nauk SSSR 30:
748, 1931.
Kali paulsenii (Litv.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola paulsenii Litv., Izv. Turkestansk. Otd. Imp. Russk. Geogr.
Obshch. 4, 5: 28, 1905 and in Sched. Herb. Fl. Ross. 5: 29, No. 1431, 1905.
Other species recognized include Kali soda Moench (¼Salsola kali L.), K. tragus (L.) Scop., and K. rosasea (L.) Moench.
Noaea Moq. in DC., Prodr. 13, 2: 207 (1849). Type: Noaea mucronata (Forssk.) Aschers. & Schweinf.
Includes Noaea major Bunge, N. minuta Boiss. & Bal., and N. mucronata (Forssk.) Aschers. & Schweinf.
Rhaphidophyton Iljin, Tr. Bot. Inst. Akad. Nauk SSSR I, Fl. Sist. Vyss. Rast. 3: 157, 1936. Type: Rhaphidophyton regelii (Bunge) Iljin.
Includes Rhaphidophyton regelii (Bunge) Iljin.
Salsola L., Sp. Pl. ed. 1: 222, 1753. Type: Salsola soda L. Synonyms: Darneilla Maire & Weiller, Fadenia Aellen & Townsend, Neocaspia
Tzvelev, Hypocylix Wol., Seidlitzia Bunge ex Boiss., Salsola sect. Coccosalsola Fenzl subsect. Coccosalsola, and S. sect. Obpyrifolia Botsch.
& Akhani (Woloszczak 1885; Iljin 1954; Aellen and Townsend 1972; Botschantzev 1976; Brullo 1984; Botschantzev 1989; Botschantzev
and Akhani 1989; Tzvelev 1993; Rilke 1999).
Salsola setifera (Moq.) Akhani, comb. nov. Basionym: Anabasis setifera Moq., Chenopod. Monogr. 164, 1840.
Salsola rosmarinus (Ehrenb. ex Boiss.) Akhani, comb. nov. Basionym: Seidlitzia rosmarinus Ehrenb. ex Boiss., Fl. Or. 4: 951, 1879.
Salsola zygophylloides (Aellen & Townsend) Akhani, comb. nov. Basionym: Fadenia zygophylloides Aellen & Townsend, Kew Bull. 27: 501,
1972.
Other species recognized include Salsola acutifolia (Bunge.) Botsch., S. cruciata Chevall. ex Batt. & Traubut, S. cyrenaica (Maire & Weiller)
Brullo, S. drummondii Ulbr., S. florida (M. Bieb.) Poir, S. foliosa (L.) Schrad., S. grandis Freitag, Vural & N. Adigüzel, S. glomerata (Maire)
Brullo, S. gymnomaschala Maire, S. kerneri (Wol.) Botcsh., S. longifolia Forssk., S. makranica Freitag, S. melitensis Botsch., S. oppositifolia
Desf., S. papillosa Willk., S. schweinfurthii Solms-Laub., S. sinaica Brullo, S. soda L., S. stocksii Boiss., S. tunetana Brullo, S. verticillata
Schousboe, and S. zygophylla Batt. & Traub.
Sympegma Bunge, Bull. Acad. St. Pétersb. 25: 351, 371, 1879. Type: Sympegma regelii Bunge.
Includes Sympegma regelii Bunge.
Traganum Del., Fl. Égypte: 204, 113–1814. Type: Traganum nudatum Del.
Includes Traganum nudatum Del. and T. moquini Webb.
Traganopsis Maire et Wilczek, Bull. Soc. Hist. Nat. Afr. N. 27: 67, 1936. Type: Traganopsis glomerata Maire & Wilczek.
Includes Traganopsis glomerata Maire & Wilczek.
Turania Akhani & E. H. Roalson, gen. nov. Type: Turania sogdiana (Bunge) Akhani; basionym: Salsola sogdiana Bunge, Mém. Acad. Imp. Sci.
St. Pétersb. Divers Savans 7: 473, 1852. Synonyms: Salsola sect. Sogdiana (Iljin) Rilke, Rev. Sekt. Salsola Gatt. Salsola 69, 1999; S. sect.
Androssowia Rilke, Rev. Sekt. Salsola Gatt. Salsola 77, 1999.
Plantae annuae. Foliae, bracteae bracteolaeque spina terminatae. Antherae per 3/4 vel 4/5 longitudinem incisae, minute appendiculatae.
Stigmata 2 quam stylus multo (3–4 x) longioria. Flores in axilibus singulae. Tepala fructificantia alata; tubus patelliformis, induratus;
semina valde complanata. A Kali caule non striato, antheris per 3/4 vel 4/5 longitudinem (nec usque medium tantum) incisis differt.
Turania sogdiana (Bunge) Akhani, comb. nov. Basionym: Salsola sogdiana Bunge, Mém. Acad. Imp. Sci. St. Pétersb. Divers Savans 7: 473,
1852.
AKHANI ET AL.—PHYLOGENY AND CLASSIFICATION OF SALSOLEAE s.l.
947
Turania aperta (Paulsen) Akhani, comb. nov. Basionym: Salsola aperta Paulsen, Vidensk. Meddel. Dansk Naturhist. Foren. Kjøbenhavn. 6, 5:
197, 1903.
Turania androssowii (Litw.) Akhani, comb. nov. Basionym: Salsola androssowii Litv., Sched. Herb. Fl. Ross. 6: 111, No. 1890, 1908.
Turania deserticola (Iljin) Akhani, comb. nov. Basionym: Salsola deserticola Iljin, Bot. Zhurn. SSSR 18: 277, 1933.
Xylosalsola Tzvelev in Ukr. Bot. Zhurn., 50 (1): 81, 1993. Type: Salsola arbuscula Pall. Synonym: Salsola section Coccosalsola Fenzl subsection
Arbuscula (Ulbrich) Botsch. p.p.
Xylosalsola richteri (Moq.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola arborescens L. fil. var. richteri Moq. in DC., Prodr. 13, 2:
185, 1849; S. richteri (Moq.) Karel. ex Litw.
Xylosalsola paletzkiana (Litw.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola paletzkiana Litw., Sched. Herb. Fl. Ross. 50: no.
2569, 1914.
Xylosalsola chiwensis (M. Pop.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola chiwensis M. Pop. in Pochv. Issl. V Bass. R. SyrDar’i i Amu-Dar’i, 1, 1915; 49; in O. et B. Fedtsch. Consp. Fl. Turk. 7: 355, 1916.
Other species recognized include Xylosalsola arbuscula (Pall.) Tzvelev.
Tribe Salsoleae incertae sedis
‘‘Canarosalsola’’: Salsola divaricata Masson ex Link.
‘‘Collinosalsola’’: Salsola arbusculiformis Drob. and S. laricifolia Turcz. ex Litw.
‘‘Oreosalsola’’: Salsola abrotanoides Bunge, S. botschantzevii Kurbanov, S. flexuosa Botsch., S. junatovii Botsch., S. lipschitzii Botsch., S.
maracandica Iljin, S. masenderanica Botsch., S. montana Litw., S. oreophila Botsch., and S. tianschanica Botsch.
Others: Salsola genistoides Juss. ex Poir., S. pachyphylla Botsch., and S. webbii Moq.
Tribe Caroxyloneae Akhani & E. H. Roalson, tribus nov. Type: Caroxylon Thunb.
A tribu Salsoleae planta plerumque tota pilosa, caulibus et foliis pilos articulatos atque interdum etiam pilos medifixos ferentibus differt. Antherae
vario modo appendiculatae, disjunctae, plerumque vesiculosae. Caules numquam articulati. Folia alterna (rarissime opposita).
For details of the differences between Salsoleae s.s. and Caroxyloneae, see table 3.
Caroxylon Thunb. Nov. Gen. ii. 37, 1782. Type: Caroxylon aphyllum (L. f.) Tzvelev (¼Salsola aphylla L.). Synonyms: Salsola sect. Caroxylon
(Thunb.) Fenzl, Salsola sect. Irania Botsch., Salsola sect. Malpighipila Botsch., Salsola sect. Cardiandra Aellen, and Nitrosalsola Tzvelev
(Botschantzev 1970, 1974a, 1974b, 1975b, 1975d, 1981a, 1986; Freitag 1997).
Caroxylon abarghuense (Assadi) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola abarghuensis Assadi, Iranian J. Bot. 2: 136,
1984.
Caroxylon aegeum (Rech. f.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola aegaea Rech. f., Denksch. Akad. Wiss. Wien, Math.Nat. 105, 2, Abt. 1: 67, 1943.
Caroxylon arabicum (Botsch.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola arabica Botsch. in Bot. Zhurn. 60(4): 499, 1975.
Caroxylon araneosum (Botsch.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola araneosa Botsch. in Bot. Zhurn. 58(6) 818,
1973.
Caroxylon canescens (Moq.) Akhani & E. H. Roalson, comb. nov. Basionym: Noaea canescens Moq. in DC., Prodr. 13, 2: 208, 1849.
Caroxylon carpathum (P. H. Davis) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola carpatha P. H. Davis, Notes Roy. Bot. Gard.
Edinb. 21: 139, 1953.
Caroxylon chorassanicum (Botsch.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola chorassnica Botsch., Bot. Mat. Gerb. Inst. Bot.
Akad. Nauk Uzbek. SSR 18: 6, 1969.
Caroxylon cyclophyllum (Baker) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola cyclophylla Baker in Bull. Misc. Inform. (Kew Bull.)
1894: 340, 1894.
Caroxylon dzhungaricum (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola dzhuncarica Iljin in Trudy Bot. Inst. Akad. Nauk
SSSR, ser 1, 2: 129, 1936.
Caroxylon ericoides (M. Bieb.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola ericoides M. Bieb., Mém. Soc. Imp. Naturalites
Moscou 1: 141, 1806.
Caroxylon forcipitatum (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola forcipitata Ljin, Bot. Zhurn. 18: 275, 1933.
Caroxylon gaetulum (Maire) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola foetida Delile var. gaetula Maire, Bull. Soc. Hist. Nat.
Afriq. Nord, 27, 7: 257, 1936.
Caroxylon glabrescens (B. Davy) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola glabrescens B. Davy, in Man. Fl. Pl. & Ferns Pt. 1.
50: 177, 1926.
Caroxylon imbricatum (Forssk.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola imbricata Forssk., Fl. Egypt.-Arab.: 57, 1775.
Caroxylon incanescens (C. A. Mey.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola incanescens C. A. Mey. in Eichw., Pl. Casp.Cauc. 2: 35, 1833.
Caroxylon inermis (Forssk.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola inermis Forssk., Fl. Aegypt.-Arab. 57, 1775.
Caroxylon implicatum (Botsch.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola implicata Botsch., in Bot. Mater. Gerb. Bot. Inst.
Akad. Nauk Uzbeksk. SSR, 13: 6, 1952.
Caroxylon jordanicola (Eig) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola jordanicola Eig, Palest. Journ. Bot., Jerusalem Ser. 3, 3:
130, 1945.
Caroxylon littoralis (Moq.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola littoralis Moq., in DC. Prodr. 13, 2: 180, 1849.
Caroxylon nitrarium (Pall.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola nitraria Pall., Illustr. Pl.: 25, 1803. Synonym:
Nitrosalsola nitraria (Pall.) Tzvelev, in Ukr. Bot. Zhurn. 50(1): 80, 1993.
Caroxylon passerinum (Bunge) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola passerina Bunge, Linnaea 17: 4, 1843.
Caroxylon persicum (Bunge ex Boiss.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola persica Bunge ex Boiss., Fl. Or. 4: 964, 1879.
Caroxylon pulvinatum (Botsch.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola pulvinata Botsch., Bot. Mat. Gerb. Bot. Inst. Akad.
Nauk SSSR 22: 96, 1963.
Caroxylon scleranthum (C. A. Mey.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola sclerantha C. A. Mey., in Eichw., Pl. Nov.
Casp.-Cauc. 2: 35, 1835.
948
INTERNATIONAL JOURNAL OF PLANT SCIENCES
Caroxylon spinescens (Moq.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola spinescens Moq., in DC., Prodr. 13(2): 179, 1849.
Caroxylon stenopterum (Wagenitz) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola stenoptera Wagenitz, in Ber. Deutsch. Bot. Ges.
72: 155, 1959.
Caroxylon tetrandrum (Forssk.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola tetrandra Forssk., Fl. Aegypt..-Arab. 58, 1775.
Caroxylon turkestanicum (Litw.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola tukestanica Litw., Trudy Bot. Muz. Akad. Nauk, 7:
78, 1910.
Caroxylon vermiculatum (L.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola vermiculata L., Sp. Pl. 223, 1753.
Caroxylon villosum (Schult.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola villosa Schult., Syst. Veg. 6: 232, 1820.
Caroxylon volkensii (Aschers & Schweinf.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola volkensii Aschers & Schweinf., in Ill. Fl.
Égypte 130, 1887.
Caroxylon yazdianum (Assadi) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola yazdiana Assadi, Iranian J. Bot. 2, 2: 140,
1984.
Caroxylon roshevitzii (Iljin) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola roshevitzii Iljin, in Journ. Bot. URSS, 18: 277, 1933.
Other species include Caroxylon aphyllum (L.f.) Tzvelev, C. dendroides (Pall.) Tzvelev, C. foetidum Moq., C. gemmascens (Pall.) Tzvelev, C.
imbricatum Moq., C. laricinum (Pall.) Tzvelev, C. orientale (S. G. Gmel.) Tzvelev, C. tetragonum (Delile) Moq., C. verrucosum Moq., and
C. zeyheri Moq.
Climacoptera Botsch., Sborn. Posv. Akad. Sukachevu: 111, 1956. Type: Climacoptera lanata (Pall.) Botsch.
Climacoptera maimanica (Freitag) Akhani, comb. nov. Basionym: Salsola maimanica Freitag, in Fl. Iranica 172: 254, 1997.
Includes Climacoptera affinis (C. A. Mey.) Botsch., C. afghanica Botsch., C. amblyostegia Botsch., C. aralensis (Iljin) Botsch., C.
botschantzevii Pratov, C. bucharica (Iljin) Botsch., C. chorassanica Pratov, C. crassa (M. Bieb.) Botsch., C. czelekenica Pratov, C. ferganica
(Drob.) Botsch., C. glaberrima Botsch., C. intricata (Iljin) Botsch., C. iranica Pratov, C. iraqensis Botsch., C. kasakorum (Iljin) Botsch., C.
khalisica Botsch., C. korshinskyi (Drob.) Botsch., C. lachnophylla (Iljin) Botsch., C. lanata (Pall.) Botsch., C. longipistillata Botsch., C.
longistylosa (Iljin) Botsch., C. malyginii (Korov. ex Botsch.) Botsch., C. merkulowitschii (Zakir.) Botsch., C. minkwitzae (Korov.) Botsch.,
C. narynensis Pratov, C. obtusifolia (Schrenk) Botsch., C. olgae (Iljin) Botsch., C. oxyphylla Pratov, C. pjataevae Pratov, C. ptiloptera
Pratov, C. roborowskii (Iljin) Grub., C. subcrassa (M. Pop.) Botsch., C. sukaczevii Botsch., C. susamyrica Pratov, C. tyshchenkoi Pratov, C.
transoxana (Iljin) Botsch., C. turcomanica (Litv.) Botsch., C. turgaica (Iljin) Botsch., C. ustjurtensis Pratov, and C. vachschi Kinz. & Pratov
(Botschantzev 1982; Pratov 1986).
Halarchon Bunge, Mém. Acad. Imp. Sc. Pétersb. 7. sér., 4, 11: 75, 1862. Type: Halarchon vesiculosum (Moq.) Bunge.
Includes Halarchon vesiculosum (Moq.) Bunge.
Halimocnemis C. A. Mey. in Ledeb., Fl. Alt. 1: 381, 1829. Type (lectotype selected here): Halimocnemis sclerosperma (Pall.) C. A. Mey., Fl. Alt.
1: 387, 1829; basionym: Polycnemum sclerospermum Pall., Reise Versch. Prov. Russ. Reich 3: 725, Tab. M, Fig. 2E, e. 1776. Synonyms:
Gamanthus Bunge, Mém. Acad. Imp. Sci. Saint Pétersbourg 7. sér., 4, 11: 76, 1862; Halanthium C. Koch, Linnaea 17: 313, 1843; Halotis
Bunge, Mém. Acad. Imp. Sc. Pétersb. 7. sér., 4, 11: 73, 1862.
Halimocnemis alaeflava (Assadi) Akhani, comb. nov. Basionym: Halanthium alaeflavum Assadi, Iranian J. Bot. 5, 2: 58, 1992.
Halimocnemis commixtus (Bunge) Akhani, comb. nov. Basionym: Gamanthus commixtus Bunge, Mém. Acad. Imp. Sc. Pétersb. 7. Sér., 4, 11:
76, 1862.
Halimocnemis ferganica (Iljin) Akhani, comb. nov. Basionym: Gamanthus ferganicus Iljin, in Acta Inst. Bot. Acad. Sc. URSS, sér. 1, 2. 1936.
Halimocnemis leucophysa (Botsch.) Akhani, comb. nov. Basionym: Gamanthus leucophysus Botsch., Not. Syst. Herb. Inst. Bot. Acad. Sci.
URSS 12: 97, 1963.
Halimocnemis pedunculata (Assadi) Akhani, comb. nov. Basionym: Halotis pedunculatus Assadi, Iranian J. Bot. 5, 2: 60, 1992.
Halimocnemis pilosa (Pall.) Akhani, comb. nov. Basionym: Salsola pilosa Pall., Illustr. Pl. 28, tab. 20, 1803.
Halimocnemis rarifolia (C. Koch) Akhani, comb. nov. Basionym: Halanthium rarifolium C. Koch, Linnaea 17: 314, 1844.
Halimocnemis rosea (Trautv.) Akhani, comb. nov. Basionym: Halanthium kulpianum var. roseum Trautv., in Trudy Imp. S.-Petersburgsk. Bot.
Sada 4: 1, 1876.
Includes Halimocnemis aequipila Iljin, H. beresinii Iljin, H. gamocarpus Moq., H. glaberrima Iljin, H. karelinii Moq., H. kulpiana C. Koch,
H. lasiantha Iljin, H. latifolia Iljin, H. longifolia Bunge, H. macrantha Bunge, H. mamamensis (Bunge) Assadi, H. mironovii Botsch., H.
mollissima Bunge, H. occulta (Bunge) Hedge, H. pilifera Moq., H. purpurea Moq., H. sclerosperma (Pall.) C. A. Mey., H. smirnovii Bunge,
and H. villosa Kar. & Kir. (Botschantzev 1971; Ghobadnejhad et al. 2004).
Halocharis Moq. in DC., Prodr. 13, 2: 201, 1849. Type: Halocharis sulphurea Moq.
Includes Halocharis clavata Bunge, H. gossypina Korov. & Kinz., H. lachnantha E.Korov., H. hispida (Schrenk) Bunge, H. sulphurea (Moq.)
Moq., H. turcomanica Iljin, and H. violacea Bunge (Iljin 1949).
Kaviria Akhani & E. H. Roalson, gen. nov. Type: Kaviria tomentosa (Moq.) Akhani; basionym: Halimocnemis tomentosa Moq. Synonym:
Salsola section Belanthera Iljin, Trudy Bot. Inst. Nauk SSSR 1, 3: 158, 1937, p.p. (Revised by Botschantzev 1968, 1980).
Genus novum ad Halocharem approximatum, sed seminibus saepius horizontalibus (nec verticalibus), stigmatibus planis (nec teretibus) 6
denticulatis, perianthio non scarioso, appendice antherarum non vesiculosa, peranthio fructicanti plerumque alato, flore solitari (nec
floribus saepe pluris) differt. Planta plerumque fruticosa raro tantum annua pilis articulatis spinulossimis vel ramosis immixtis ornata.
Kaviria aucheri (Moq.) Akhani, comb. nov. Basionym: Noaea aucheri Moq. in DC., Prodr. 13, 2: 207, 1849.
Kaviria cana (C. Koch) Akhani, comb. nov. Basionym: Salsola cana C. Koch, Linnaea 22: 190, 1849.
Kaviria futilis (Iljin) Akhani, comb. nov. Basionym: Salsola futilis Iljin, Bot. Mat. Gerb. Bot. Inst. Akad. Nauk SSSR, 7: 210, 1938.
Kaviria gossypina (Bunge) Akhani, comb. nov. Basionym: Salsola gossypina Bunge in Boiss. Fl. Or. 4: 956, 1879.
Kaviria lachnantha (Botsch.) Akhani, comb. nov. Basionym: Salsola tomentosa (Moq.) Spach subsp. lachnantha Botsch., Bot. Zhurn. 53:
1448, 1968.
Kaviria pycnophylla (Brenan) Akhani, comb. nov. Basionym: Salsola pycnophylla Brenan, Kew Bull. 3: 433, 1953.
Kaviria rubescens (Franch.) Akhani, comb. nov. Basionym: Salsola rubescens Franch., in Révoil, Faune Fl. Çomalis: 60, 1882.
Kaviria tomentosa (Moq.) Akhani, comb. nov. Basionym: Halimocnemis tomentosa Moq., Hist. Mém. Acad. Sci. Toulouse 5: 180, 1839.
Kaviria vvdenskyi (Iljin & M. Pop.) Akhani, comb. nov. Basionym: Salsola vvedenskyi Iljin & M. Pop. in Fl. URSS 6: 876, 1936.
AKHANI ET AL.—PHYLOGENY AND CLASSIFICATION OF SALSOLEAE s.l.
949
Kaviria zehzadii (Akhani) Akhani, comb. nov. Basionym: Salsola zehzadii Akhani, Sendtnera 3: 6, 1996.
Nanophyton Less., Linnaea 9: 197, 1834–1835. Type: Nanophyton erinaceum (Pall.) Bunge.
Includes Nanophyton erinaceum (Pall.) Bunge.
The identities of nine additional taxa described by Botschantzev (1975a) and Pratov (1975, 1982, 1985) need to be clarified. They include N.
botschantzevii Pratov, N. erinaceum (Pall.) Bunge subsp. karataviense Pratov, N. erinaceum (Pall.) Bunge subsp. subulifolium Pratov, N.
grubovii Pratov, N. iliense Pratov, N. mongolicum Pratov, N. narynense Pratov, N. pulvinatum Pratov, and N. saxatile Botsch.
Ofaiston Raf., Fl. Tell. 3: 46, 1837. Type: Ofaiston monandrum (Pall.) Moq.
Includes Ofaiston monandrum (Pall.) Moq.
Petrosimonia Bunge, Mém. Acad. Imp. Sci. St. Pétersb. 7. sér., 4, 11: 19, 52, 1862. Type: Petrosimonia monandra (Pall.) Bunge.
Includes Petrosimonia brachiata (Pall.) Bunge, P. brachyphylla (Bunge) Iljin, P. glauca (Pall.) Bunge, P. glaucescens (Bunge) Iljin, P.
hirsutissima (Bunge) Iljin, P. litwinowii Korsh., P. nigdeensis Aellen, P. monandra (Pall.) Bunge, P. oppositifolia (Pall.) Litv., P. sibirica
(Pall.) Bunge, P. squarrosa (Schrenk) Bunge, and P. triandra (Pall.) Simonk.
Piptoptera Bunge Trudy Glavn. Bot. Sada 5: 644, 1877. Type: Piptoptera turkestana Bunge.
Includes Piptoptera turkestana Bunge.
Physandra Botsch., Sborn. Posv. Akad. Sukachevu: 114, 1956. Type: Physandra halimocnemis (Botsch.) Botsch.
Includes Physandra halimocnemis (Botsch.) Botsch.
Pyankovia Akhani & E. H. Roalson, gen. nov. Type: Pyankovia brachiata (Pall.) Akhani & E. H. Roalson; basionym: Salsola brachiata Pall.
Synonym: Climacoptera section Heterotricha Iljin ex Pratov, in Rod Climacoptera 24, 1986.
Planta annua, erecta, pilos longos articulatos atque pilos breviores spinulissimos immixtos ferentes; folia superiora floralibus exceptis opposita,
ad apicem cuspidata. Stylus brevis, ad maturitatem conicus, stigma subulata. Stamina 5; antherae lineares, per 1/3 vel 2/5 longitudinem
partitae appendicibus sessilibus albis obtusis ornatae. Perianthia fructificantia horizontalia omnia alata. Semina verticalia. Genus novum a
Climacoptera foliis oppositis, pilis spinulissimis, seminibus verticalibus differt.
Pyankovia brachiata (Pall.) Akhani & E. H. Roalson, comb. nov. Basionym: Salsola brachiata Pall., Illustr. 30, tab. 22, 1803.
Lectotype (Pratov 1986): In siccis squalidis salsis deserti australoris Volgum frequens, P. S. Pallas (LE).
Appendix B
Table B1
List of Sampled Taxa with Their Respective Vouchers and GenBank Accession Numbers
GenBank no.
Subfamily, tribe, and species
Salsoloideae:
Camphorosmeae:
Bassia hyssopifolia (Pall.) O. Kuntze
Bassia eriophora (Schrad.) Aschers.
Bassia sedoides Aschers.
Camphorosma monspeliaca L.
Camphorosma monspeliaca L.
Chenoleoides tomentosa (Lowe)
Botsch.
Kirilowia eriantha Bunge
Kochia scoparia (L.) Schrad.
Kochia stellaris Moq.
Londesia eriantha Fisch. & C. A. Mey.
Maireana coronata (J. M. Black) P. G.
Wilson
Panderia pilosa Fisch. & C. A. Mey.
Panderia pilosa Fisch. & C. A. Mey.
Salsoleae s.l.:
Anabasis aphylla L.
Anabasis calcarea (Charif & Aellen)
Bokhari & Wendelbo
Voucher of DNA source
ITS
psbB-psbH
H. Akhani 18064. Iran: Golestan, Alagol Lake, 37°21980N, 54°349130E, 10 m,
8.10.2004.
H. Akhani 8381. Iran: Ilam, Mehran, 3.5.1992.
Kadereit et al. 2005.
H. Akhani & M. Ghobadnejhad 15585. Iran, E Azerbaijan: 55 km NE of Tabriz toward
Ahar, 38°159390N, 46°529530E, 1571 m, 4.9.2001.
Akhani et al. 17960. Turkey: Aksaray: S of Tuz Gölü Lake, 17 km from Yenikent
toward Sultanhani, 38°159560N, 33°389510E, 938 m, 27.8.2004.
EF453390
EF453527
EF453391
AY489199
EF453392
EF453528
...
EF453529
EF453393
EF453530
EF453394
EF453531
EF453445
EF453574
EF453446
AY489219
AY489220
...
...
...
Based on cultivated plant from Royal Botanical Gardens, Kew (origin Australia).
H. Akhani 14513. Iran, Tehran: 35 km E of Eshtahard, ca. 8 km
W of Mardabad, Rude Shur, 35°429440N, 50°44926E, 1163 m, 8.12.2000.
H. Akhani et al. 17948. Turkey: Ankara, eastern side of Tuz Gölü Lake, 62 km S of
Sereflikochisar, 5–7 km W of Ulukisla, 38°29910N, 33°449170E, 921 m, 27.8.2004.
EF453447
EF453454
EF453575
EF453582
EF453455
EF453583
H. Akhani 18072. Iran: Khorassan, easternmost parts of Golestan National Park,
near Mirzabaylu Protection Station, 37°199590N, 56°149200E, 1756 m, 9.10.2004.
EF453380
EF453517
H. Akhani 14372. Iran: Tehran, Kavir Protected Area, near Qasre Bahram, 34°449N,
52°109E, 1200 m, 27.10.2000.
EF453381
EF453518
H. Akhani 16440. Canary Islands: Gran Canaria, southeastern coasts,
Faro de Arinaga, sea level, 22.9.2002.
D. Podlech 18952 (M). Afghanistan: Ghorat, Panjao to La’l,
Asgharat to Khargol, 3120 m, 29.7.1970.
H. Akhani & Zangui 10114. Iran: Khorassan, 17.8.1994.
Kadereit et al. 2005.
Kadereit et al. 2005.
Table B1
(Continued )
GenBank no.
Subfamily, tribe, and species
Anabasis eriopoda (C. A. Mey.) Benth.
Anabasis eugeniae Iljin
Anabasis hausskenchtii Bunge ex Boiss.
Anabasis hausskenchtii Bunge ex Boiss.
Anabasis aff. hausskenchtii Bunge
Anabasis iranica Iljin
Anabasis jaxartica (Bunge) Benth.
ex Volkens
Anabasis setifera Moq.
Climacoptera brachiata (Pall.) Botsch.
Climacoptera crassa (M. Bieb.) Botsch.
Climacoptera glaberrima Botsch.
Climacoptera glaberrima Botsch.
Climacoptera iranica Pratov
Climacoptera ‘‘khalijefarsica’’
Climacoptera lanata (Pall.) Botsch.
Climacoptera lanata (Pall.) Botsch.
Climacoptera longipistillata Botsch.
Climacoptera turcomanica (Litv.)
Botsch.
Cornulaca aucheri Moq.
Cornulaca monacantha Delile
Cyatobasis fruticulosa (Bunge) Aellen
Fadenia zygophylloides Aellen &
Townsend
Gamanthus commixtus Bunge
Gamanthus gamocarpus (Moq.) Bunge
Gamanthus gamocarpus (Moq.) Bunge
Gamanthus ‘‘khorassanicus’’
Gamanthus pilosus (Pall.) Bunge
Girgensohnia imbricata Bunge
Girgensohnia minima K. Korov.
Girgensohnia oppositiflora (Pall.)
Fenzl
Voucher of DNA source
ITS
psbB-psbH
H. Akhani & M. Ghobadnejhad 15812. Iran: Semnan, Touran Biosphere Reserve,
19 km SW of Biarjmand toward Daqe Biar, 35°569280N, 55°429480E, 1260 m,
4.10.2001.
T. Eftekhari 10219. Iran: Semnan, ca. 28 km NW of Semnan, W of Aftar,
Khonar Forbidden Hunting, 1980 m, 11.10.1999.
H. Akhani & M. Salimian 15339. Iran: Semnan, 19 km NW of Damghan toward
Cheshmeh Ali, 1420 m, 36°149580N, 54°99570E, 14.7.2001.
H. Akhani & M. Ghobadnejhad 15699. Iran: Yazd: ca. 10 km W of
Taft toward Abarkuh, 31°569280N, 54°159230E, 1233 m, 18.9.2001.
H. Akhani & M. R. Joharchi 17306. Khorassan: 65 km SE of Birjand, near Sarbisheh,
at the beginning of the road toward Doroh, 32°349260N, 59°489350E, 2.9.2003.
H. Akhani & M. Ghobadnejhad 15700. Iran: Yazd: ca. 10 km W of Taft toward
Abarkuh, 31°569280N, 54°159230E, 1233 m, 18.9.2001.
EF453383
EF453520
EF453384
EF453521
EF453386
EF453523
EF453387
EF453524
EF453388
EF453525
EF453382
EF453519
EF453385
EF453522
EF453389
EF453526
EF453403
EF453536
EF453401
EF453534
EF453396
EF453532
EF453400
EF453533
EF453395
...
EF453402
EF453535
EF453404
EF453537
EF453398
...
EF453397
...
H. Akhani 17207. Iran: Tehran, ca. 60 km W of Tehran, Mardabad, salt flats near Rude
Shur, 35°439N, 50°449E, 1164 m, 8.8.2003.
H. Akhani 7964. Iran: Bushehr, 13 km after Cheghadak toward Delvar, near Gar Gur
village, sea level, 20.11.1991.
H. Akhani & M. R. Joharchi 17297. Iran: Khorassan, ca. 50 km S of Birjand,
Mokhtaran, 32°289250N, 59°23980E, 1506 m, 1.9.2003.
Turkey, M. Vural, H. Duman, Z. Aytaç 8012 (GAZ). Kayseri: Dortyol-Develi,
Tuzlu Topraklar, 1080 m, 19.9.1997.
EF453399
...
EF453405
EF453538
EF453406
EF453539
EF453516
...
I. Friis, K. Vollesen & A. S. Hassan 4768 (K). Somalia: Gedo Region, ca. 36 km S of
Lung, 3°339N, 42°429E, ca. 200 m, 25.5.1987.
V. Botschantzev 15 (LE). Uzbekistan, Surkhandarja province, between Shirabad and
Zarabag, 8.10.1970.
H. Akhani 14086. Iran: Golestan, southern border of Golestan National Park, NW of
Dasht village toward Yelaq, 37°189410N, 55°589430E, 1200 m, 5.6.2000.
Cultivated based on H. Akhani 18053. Iran: Golestan, between Aghghala and
Dashliborun, 38 km N of Aghghala, 37°209430N, 54°339E, 16 m, 8.10.2004.
H. Akhani & M. R. Joharchi 17237. Khorassan: between Torbate-Heydarieh and
Gonabad, 55 km N of Gonabad, 34°509260N, 58°519180E, 908 m, 31.8.2003.
Akhani & Ghobadnejhad 15551. Iran: E Azerbaijan, 52 km S of Aslanduz in the road
toward Ardabil, 39°99N, 47°389370E, 1200 m, 3.9.2001.
H. Akhani & M. R. Joharchi 17291. Iran: Khorassan, ca. 40 km S of Birjand, 13 km
E of Majhan toward Giv, 32°339250N, 59°79540E, 1492 m, 1.9.2003.
H. Akhani & Zangooei 10109. Iran: Khorassan, 10–11 km E of Chahchaheh along
Turkmenistan border, 700–850 m, 17.8.1994.
EF453513
...
EF453410
EF453543
EF453407
EF453540
EF453408
EF453541
EF453411
EF453544
EF453409
EF453542
EF453412
EF453545
EF453413
EF453546
EF453414
EF453547
H. Akhani 14078. Iran, Golestan: Southern border of Golestan National Park,
37°179500N, 55°559360E, 1240 m, 4.6.2000.
H. Akhani 14519. Iran, Tehran: Tehran-Qom highway, Heuze Soltan Lake,
34°59920N, 50°519220E, 840 m, 22.12.2000.
Akhani 17356. Iran: Golestan: Golestan National Park, 2 km S of Dasht,
37°199260N, 55°579240E, 1403 m, 13.10.2003.
H. Akhani & al. 18005. Turkey: Aksaray, 10 km E of Eskil toward southern
saline shores of Tuz Gölü Lake, 38°25950N, 33°299520E, 914 m, 28.8.2004.
H. Akhani 18087. Golestan: 5 km E of Maraveh Tappeh, along Atrak river,
37°549230N, 56°009360E, 230 m, 11.10.2004.
Based on cultivated plant originated from the same population as above Akhani
18087.
Voucher lost. Iran: Golestan, 5 km E of Maraveh Tappeh, along Atrak river,
37°549230N, 56°009360E, 230 m, 11.10.2004.
H. Akhani et al. 18118. Iran: Khuzestan, Persian Gulf coasts near Bandare Imam,
30°349520N, 49°19590E, 10.12.2004.
H. Akhani & M. R. Joharchi 17241. Khorassan: between Torbate-Heydarieh and
Gonabad, ca. 35 km N of Gonabad, Kal Shur River, 34°409210N, 58°479100E, 856 m,
31.8.2003.
H. Akhani & M. R. Joharchi 16510. Iran: Khorassan, ca. 35 km E of Torbat-e Jam near
Malu, 35°129190N, 61°19170E, 820 m, 20.11.2002.
H. Akhani 18092. Golestan: 28 km W of Maraveh Tappeh, near Ghara-Gol,
37°549560N, 55°399430E, 140 m, 11.10.2004.
H. Akhani & M. Ghobadnejhad 15701. Iran: Yazd, ca. 27 km W of Taft toward
Abarkuh, 31°419540N, 53°559190E, 2179 m, 18.9.2001.
950
Table B1
(Continued )
GenBank no.
Subfamily, tribe, and species
Halanthium alaeflavum Assadi
Halanthium mamamense Bunge
Halanthium rarifolium C. Koch
Halanthium rarifolium C. Koch
Halanthium rarifolium C. Koch
Halimocnemis azarbaijanensis Assadi
Halimocnemis longifolia Bunge
Halimocnemis mollissima Bunge
Halimocnemis purpurea Moq.
Halocharis hispida (Schrenk) Bunge
Halocharis sulphurea (Moq.) Moq.
Halocharis violacea Bunge
Halogeton alopecuroides (Delile) Moq.
Halogeton glomeratus (M. Bieb.)
C. A. Mey.
Halothamnus auriculus (Moq.) Botsch.
Halothamnus auriculus (Moq.) Botsch.
subsp. acutifolius (Moq.)
Kothe-Heinr.
Halothamnus glaucus (M. Bieb.)
Botsch.
Halothamnus subaphyllus (C. A. Mey.)
Botsch.
Halotis occulta Bunge
Halotis pedunculata Assadi
Halotis pilifera (Moq.) Botsch.
Haloxylon ammodendron
(C. A. Mey.) Bunge ex Fenzl
Haloxylon persicum Bunge ex
Boiss. & Buhe
Haloxylon stocksii (Boiss.)
Benth. & Hook.
Hammada articulata (Moq.)
O. Bolòs & Vigo
Hammada griffithii (Moq.) Iljin
Hammada salicornica (Moq.) Iljin
Horaninowia platyptera
Charif & Aellen
Horaninowia pungens (Gilli) Botsch.
Voucher of DNA source
ITS
psbB-psbH
H. Akhani & M. Ghobadnejhad 15610. Iran: E Azerbaijan, 1 km W of Maraqeh toward
Bonab, 37°219110N, 46°89580E, 1383 m, 7.9.2001.
H. Akhani & M. Ghobadnejhad 15531. Iran: E Azerbaijan, 10 km E of Mianeh, near
Maman, 37°279180N, 47°52930E, 1095 m, 2.9.2001.
H. Akhani 16491. Iran: Semnan, SW of Touran Protected Area, ca. 15 km from Razeh
toward Torud, 35°249290N, 55°159510E, 1320 m, 14.11.2002.
H. Akhani 17206. Iran: Tehran, ca. 60 km W of Tehran, Mardabad, salt flats near Rude
Shur, 35°439N, 50°449E, 1164 m, 8.8.2003.
H. Akhani 17208. Iran: Tehran: ca. 60 km W of Tehran, Mardabad, salt flats near Rude
Shur, 35°439N, 50°449E, 1164 m, 29.8.2003.
H. Akhani & M. Ghobadnejhad 15550. Iran: E Azerbaijan, 52 km S of Aslanduz in the
road toward Ardabil, 39°99N, 47°389370E, 1200 m, 3.9.2001.
H. Akhani & M. R. Joharchi 17245. Iran: Khorassan, between Torbate-Heydarieh and
Gonabad, ca. 33 km N of Gonabad, 34°399510N, 58°459530E, 871 m, 31.8.2003.
H. Akhani 17208. Iran: Tehran, ca. 60 km W of Tehran, Mardabad, salt flats near Rude
Shur, 35°439N, 50°449E, 1164 m, 8.8.2003.
H. Akhani 9036. Iran: Ilam, ca. 25–28 km N of Mehran, Konjancham river margin,
300 m, 16.10.1993.
H. Akhani 10179-T. Turkmenistan, 2 km N of Ashghabad, 16.9.1994.
H. Akhani & M. Ghobadnejhad 15841. Iran: Semnan, 47 km W of Shahrud toward
Damghan, 36°15951N, 54°399400E, ca. 1140 m, 6.10.2001.
H. Akhani & M. R. Joharchi 17288. Khorassan: 143 km E of Qaen toward Afghanistan
border, W of Daqe Petergan, 33°319290N, 60°399120E, 644 m, 31.8.2003.
Originated from Arabia, cultivated in WSU.
EF453416
EF453548
EF453417
...
EF453419
EF453550
EF453418
EF453549
EF453415
...
EF453420
EF453551
EF453421
EF453552
EF453422
EF453553
EF453426
EF453557
EF453429
EF453427
EF453560
EF453558
EF453428
EF453559
EF453430
EF453561
Voucher unknown, the same specimen used in Pyankov et al. 2001a.
H. Akhani 15164. Iran: Qom, at the beginning of Qom-Tehran highway, 34°419150N,
50°539200E, 962 m, 24.5.2001.
EF453431
EF453433
EF453562
EF453564
Akhani & Salimian 15444. Iran: Semnan, 28 km E of Shahrud toward Sabzevar,
36°269420N, 55°149210E, 1375 m, 20.7.2001.
EF453432
EF453563
A. Ghorbani 56. Iran: Golestan, N of Golestan National Park, between Lohondor and
Soolegerd, 8.7.2002.
EF453434
EF453565
H. Akhani & M. Salimian 15445. Iran: Semnan, 28 km E of Shahrud toward Sabzevar,
36°269420N, 55°149210E, 1375 m, 20.7.2001.
H. Akhani & M. R. Joharchi 17202. Khorassan: ca. 42 km SE of Birjand, 3 km NE of
Mokhtaran toward Razgh, 32°289420N, 59°24970E, 1558 m, 1.9.2003.
H. Akhani 17217. Iran: Hormozgan, 9 km SW of Goshoon toward Tadroyeh,
27°219250N, 54°499100E, 584 m, 21.8.2003.
H. Akhani et al. 17692. Iran: Esfahan, 12 km E of Golpayegan in the Muteh road, near
Vedagh, 33°309230N, 50°26910E, 1819 m, 9.6.2004.
EF453435
EF453566
EF453423
EF453554
EF453424
EF453555
EF453425
EF453556
H. Akhani 17398. Iran: Khorassan, eastern parts of Golestan National Park, 6 km W of
Mirzabaylu toward Almeh, 37°219N, 56°119E, 1384 m, 15.10.2003.
EF453436
EF453567
H. Akhani & M. Ghobadnejhad 15832. Iran: Semnan, Touran Biosphere Reserve,
4 km E of Ahmadabad, 35°479N, 56°399E, ca. 1000 m, 5.10.2001.
EF453438
EF453569
H. Akhani s.n. Sistan va Baluchestan, 5 km S of Negur, 25°229150N, 61°109310E,
140 m, 28.11.2005.
EF453512
...
Based on cultivated plant from Royal Botanical Gardens, Kew.
D. Podlech 32707 (MSB). Afghanistan: Samangan, Tang-I Tashqurghan, 7 km S of
Tashqurghan, 520 m, 11.11.1978.
H. Akhani 16004. Iran: Hormozgan, northern parts of Mehregan saline, 26°459490N,
54°469460E, 30 m, 21.12.2001.
EF453440
EF453437
EF453571
EF453568
EF453439
EF453570
H. Akhani & M. Salimian 15442. Iran, Semnan, 28 km E of Shahrud toward Sabzevar,
36°269420N, 55°149210E, 1375 m, 20.7.2001.
D. Podelch 19662 (MSB). Afghanistan: Kandahar, Banks of Helmand river at Girishk,
840 m, 18.09.1970.
EF453441
EF453572
EF453442
...
951
Table B1
(Continued )
GenBank no.
Subfamily, tribe, and species
Horaninowia ulicina Fisch. &
C. A. Mey.
Nanophyton erinaceum (Pall.) Bunge
Noaea major Bunge
Noaea minuta Boiss. & Ball
Noaea mucronata (Forssk.)
Asch. & Schweinf.
Ofaiston monandrum (Pall.) Moq.
Petrosimonia brachiata (Pall.) Bunge
Petrosimonia glauca (Pall.) Bunge
Petrosimonia nigdeensis Aellen
Piptoptera turkestana Bunge
Rhaphidophyton regelii (Bunge) Iljin
Salsola abarghuensis Assadi
Salsola aperta Paulsen
Salsola arbuscula Pall.
Salsola arbusculiformis Drob.
Salsola araneosa Botsch.
Salsola aucheri (Moq.) Bunge
Salsola canescens (Moq.) Boiss.
Salsola carpatha P. H. Davis
Salsola chivensis M. Pop.
Salsola chorassanica Botsch.
Salsola cyclophylla Baker
Salsola dendroides Pallas
Salsola deserticola Iljin (S. androssowii
Litv. subsp. deserticola [Iljin] Rilke)
Salsola divaricata Masson ex Link
Salsola drummondii Ulbr.
Salsola dzhungarica Iljin
Salsola foliosa (L.) Schrad.
Salsola forcipitata Iljin
Salsola gemmascens Pall.
Salsola glabrescens B. Davy
Salsola gossypina Bunge
Salsola gossypina Bunge
Voucher of DNA source
ITS
psbB-psbH
H. Akhani & M. Ghobadnejhad 15833. Iran: Semnan, Touran Biosphere Reserve,
sand dunes 4 km E of Ahmadabad, 35°479N, 56°399E, ca. 1000 m, 5.10.2001.
(LE). Central Asia: southwest Kyzylkum, 2.11.96. Data on collector unavailable.
Neubauer 4768 (M). Afghanistan: Kabul, Bande Kargha, 2000 m.
Cultivated specimen based on H. Akhani 18095. Iran: Hamadan, 9 km NE of Hamadan
in the road toward Noubaran, 1729 m, 34°549260N, 48°3970E, 8.12.2004.
EF453443
EF453573
EF453449
EF453450
EF453451
EF453577
EF453578
EF453579
EF453452
EF453580
EF453453
EF453581
EF453457
EF453585
EF453456
EF453584
EF453458
EF453586
...
EF453631
EF453459
EF453587
EF453464
EF453591
EF453466
...
EF453467
EF453592
EF453468
EF453593
EF453461
EF453588
EF453469
EF453594
EF453503
EF453623
EF453514
AF318642
EF453487
...
...
EF453609
EF453471
EF453596
EF453472
EF453597
EF453473
EF453598
EF453474
EF453599
EF453475
EF453600
EF453476
AF318652
EF453477
EF453601
...
...
EF453478
...
EF453479
EF453602
EF453480
EF453481
EF453603
EF453604
H. Akhani 13761. Iran: Mazandaran, ca. 5 km E of Doab (Chalus road) toward Kojur,
36° 289280N, 51°259130E, 657 m, 12.9.1999.
V. I. Vasilevich et al. 3008 (LE). Kazakhstan: Semipalatinsk, 90 km W of Ajaguza, by the
road to village Chubartau, 26.7.1965.
H. Akhani & M. Salimian 14238. Iran: E Azerbaijan, northern side of Orumiyeh Lake,
W of Bandar-e Sharafkhaneh, 38°119230N, 45°279410E, 1300 m, 3.9.2000.
H. Akhani & M. Ghobadnejhad 15535. Iran: E Azerbaijan, 13 km E of Maman,
near salt mine, 37°259280N, 47°559580E, 1378 m, 2.9.2001.
H. Akhani et al. 17925. Turkey: Ankara, 28 km N of Sereflikochisar toward Ankara,
N of Tuz Gölü Lake, Mogan Gol Lake, 39°89500N, 33°19940E, 895 m, 27.8.2004.
H. Akhani 5775. Iran: Esfahan, ca. 30 km ESE of Kashan, 2 km N of Abu-Zeid abad,
9.9.1989, ca. 900 m.
V. Botschantzev & Litvinova N. P. 477 (LE). Kazakhstan: Chimkent province, Karatau
mountain range, 2 km NE of village Leontjevka, valley of river Ulkan- Burul,
17.7.1980.
H. Akhani 16492. Iran: Semnan, SW of Touran Protected Area, 8 km after Razeh
toward Sahl, around Cheshmeh Morra, 35°359380N, 55°20910E, 1227 m,
14.11.2002.
Chopanov & Sejfulin 27.8.1976. Turkmenistan: Kunya-Urgench Region, on sand dunes
between Daryalyk and Butentau.
H. Akhani & M. Ghobadnejhad 15826. Iran: Semnan, Touran Biosphere Reserve,
85 km SW of Biarjmand toward Torud, river bed 6 km S of Sahl, 35°359400N,
55°20940E, 1230–1240 m, 4.10.2001.
H. Akhani 17397. Iran: Khorassan, eastern parts of Golestan National Park, 5–6 km W
of Mirzabaylu toward Almeh, 37°219160N, 56°12960E, 1350 m, 15.10.2003.
Merxmüller and Giess 28372 (M). Namibia: S Lüderitz, 23 km S of Grillental,
12.09.1972.
H. Akhani 17190. Iran: Golestan, southern parts of Golestan National Park,
between Sharlegh and Cheshmeh Khan, 37°189130N, 56°5910E, 1154 m, 3.8.2003.
H. Akhani 13185. Iran: Tehran, N Tehran, Golabdareh, 35°509100N,
51°269230–480E, 3.9.1998.
W. Greuter 7835 (K). Greece, Dragonára Island, 31.10.1966.
Pyankov et al. 2001a.
H. Akhani & M. R. Joharchi 17281. Iran: Khorassan, 143 km E of Qaen toward
Afghanistan border, W of Daqe Petergan, 33°319290N, 60°399120E, 644 m,
31.8.2003.
H. Akhani 15998. Iran: Hormozgan, 10 km W of Bandar Khamir, 26°, 26°569400N
55°29950E, 50 m, 20.12.2001.
H. Akhani 18090. Iran: Golestan, 5 km E of Maraveh Tappeh, along Atrak river,
37°549230N, 56°009360E, 230 m, 11.10.2004.
Chopanov & Sejfulin 1.9.1976. Turkmenistan: Dargan-Ata region, on the hills
nearby southern lake Soltansardzhar.
Based on cultivated plant originated from H. Akhani 16469. Canary Islands:
Gran Canaria, western coasts, near Agaete, 23.9.2002.
H. Akhani 17234. Iran: Hormozgan, 36 km W of Bandar Abbas, at the beginning of
Gachin village, 27°49320N, 55°549450E, 22.8.2003.
The same herbarium material cited in Pyankov et al. 2001a (no voucher available).
Pyankov et al. 2001a.
D. Podlech 17012 (MSB). Afghanistan: Baghlan, 8 km E of Kotal-i-Mirza Atbili,
between Aybak and Pul-i-Khumri, 1100 m, 08.10.1969.
D. Podlech 32697 (MSB). Afghanistan: Samangan, 8 km N of road Mazar-i-Sharif to
Tashkurghan, at road to Termez, 320 m, 11.11.1978.
R. Story 2083 (M). South Africa: Cape, Aliwal North, banks of
Orange River, 1300 m, 10.03.47.
Herbarium material from Pyankov et al. 2001a.
H. Akhani & Zangooi 10088. Iran: Khorasan, 24 km from Chahchaheh toward
Kalat-e Naderi, 700–720 m, 17.8.1994.
952
Table B1
(Continued )
GenBank no.
Subfamily, tribe, and species
Salsola griffithii (Bunge)
Freitag & Khani
Salsola inermis Forssk.
Salsola inermis Forssk.
Salsola jordanicola Eig
Salsola jordanicola Eig
Salsola kali L.
Salsola kerneri (Wol.) Botsch.
Salsola lachnantha (Botsch.) Botsch.
Salsola laricina Pallas
Salsola masenderanica Botsch.
Salsola montana Litw.
Salsola montana Litw.
Salsola nitraria Pallas
Salsola orientalis S. G. Gmelin
Salsola
Salsola
Salsola
Salsola
orientalis S. G. Gmlein
paulsenii Litw.
richteri (Moq.) Karel. ex Litw.
rubescens Franch.
Salsola soda L.
Salsola soda L.
Salsola tomentosa (Moq.) Spach
Salsola tomentosa (Moq.) Spach
Salsola ‘‘touranica’’
Salsola tragus L. (published under
S. australis R. Br.)
Salsola turkestanica Litw.
Salsola vermiculata L.
Salsola vvdenskyi Iljin & M. Popov
Salsola yazdiana Assadi
Salsola zehzadii Akhani
Salsola zehzadii Akhani
Salsola zeyheri (Moq.) Bunge
Salsola zygophylla Batt. et Trab.
Seidlitzia florida (M. Bieb.)
Bunge ex Boiss.
Seidlitzia rosmarinus Ehrenb. ex Boiss.
Sympegma regelii Bunge
Voucher of DNA source
ITS
psbB-psbH
H. Akhani et al. 17823. Iran: Kerman, ca. 7 km N of Faryab, sandy dunes near
Hoore Olia village, 28°99180N, 57°16930E, 674 m, 14.6.2004.
H. Akhani 5561. Iran: Ilam, 5 km SW of Dehloran, 170 m, 6.8.1989.
H. Akhani et al. 17963. Turkey: Aksaray, salt flats S of Tuz Gölü Lake, 17 km from
Yenikent toward Sultanhani, 38°159560N, 33°389510E, 938 m, 27.8.2004.
H. Akhani 7947. Iran: Fars, 11 km in the road from Konartakhteh toward Borazjan,
300–400 m, 20.11.1991.
H. Akhani & M. R. Joharchi 17236. Iran: Khorassan, between Torbate-Heydarieh and
Gonabad, 55 km N of Gonabad, 34°509260N, 58°519180E, 908 m, 31.8.2003.
Pyankov et al. 2001a; Kapralov et al. 2006.
H. Akhani 15045. Iran: Tehran, 20 km S of Behesht-e Zahra toward Hasanabad,
35°249N, 51°199E, 1300 m, 3.5.2001.
H. Akhani 9022. Iran: Ilam, ca. 25 km from Salehabad in the road toward Mehran,
16.10.1993.
H. Akhani et al. 17966. Turkey: Aksaray, ruderal places near Sultanhani, 39°159400N,
33°329210E, 956 m, 28.8.2004.
H. Akhani 17403. Iran: Mazandaran, 169 km to Tehran, 5 km after Veresk toward
Amol, 35°569530N, 53°009200E, 1201 m, 16.10.2003.
H. Akhani 17391. Iran: Golestan, southern parts of Golestan National Park,
near Sharlegh, 15.10.2003.
Cultivated based on seeds originated from Iran: Golestan National Park.
H. Akhani et al. 17946. Turkey: Ankara, eastern side of Tuz Gölü Lake, 14 km S of
Sereflikochisar, 38°489130N, 33°369400E, 919 m, 27.8.2004.
H. Akhani 16498. Iran: Semnan, 38 km E of Khors toward Chajam, S of Kavire Haj Ali
Qoli, 35°489220N, 54°579100E, 1098 m, 14.11.2002.
Cultivated plant originated from central Asia.
Pyankov et al. 2001a.
Cultivated from a central Asian origin.
H. Akhani 9117. United Arab Emirates: ca. 23 km S of Al-Ain, near Jebel Hafit
(Hafit Mont), 350 m, 15.12.1990.
H. Akhani 15901. Iran: Tehran, Tehran-Saveh, Rude Shur, 9.11.2001.
H. Akhani 18045. Iran: Golestan, N Gomishan, 37°109140N, 54°3940E, 13 m,
8.10.2004.
H. Akhani & M. Ghobdnejhad 15632. Iran: E Azerbaijan, 10 km SW of Sarab in the
road toward Asbforoushan, 37°52970N, 47°309300E, 1700 m, 8.9.2001.
H. Akhani 18080. Iran: Golestan, 70 km S of Maraveh Tappeh, near Golidagh,
37°419430N, 56°49190E, 979 m, 11.10.2004.
H. Akhani & M. Ghobadnejhad 15808. Iran: Semnan, Touran Biosphere Reserve,
above Qaaleh Bala, 36°009150N, 56°009410E, 1350 m, 4.10.2001.
EF453482
EF453605
EF453465
EF453483
...
...
EF453484
EF453606
EF453485
EF453607
AF318646
EF453486
DQ499431
EF453608
EF453488
EF453610
EF453470
EF453595
EF453504
EF453624
EF453489
EF453611
EF453490
EF453491
EF453612
EF453613
EF453492
EF453614
EF453493
AF318647
EF453494
EF453495
EF453615
...
EF453616
...
EF453496
EF453497
EF453617
EF453618
EF453499
EF453620
EF453500
EF453621
EF453505
EF453625
AF318648
...
...
EF453632
EF453501
EF453622
EF453462
EF453589
EF453515
...
EF453463
EF453590
EF453498
EF453619
EF453502
...
AF318651
...
EF453507
EF453627
EF453506
EF453626
EF453510
EF453629
Pyankov et al. 2001a.
H. Akhani & M. Ghobadnejhad 15821. Iran: Semnan, Touran Biosphere Reserve,
80 km SW of Biarjmand toward Torud, river bed near Sahl, 35°39910N, 55°189240E,
1351 m, 4.10.2001.
H. Akhani 18102. Iran: Kermanshah, 35 km from Gilanegharb toward Sumar,
33°57960N, 45°569550E, 630 m, 9.12.2004. ITS based on cultivated plant
from the same collection.
D. Podlech 17001 (M). Afghanistan: Mazar-i Sharif, 2 km NW of Ghaznigak,
near the road to Haibak (Aybak), 700 m.
H. Akhani & M. Dehghani s.n. Esfahan: 32 km S of Jandagh toward Chupanan,
33°479120N, 54°259180E, 1004 m, 27.10.2005.
H. Akhani, 10029. Iran: Khorassan: ca. 35 km E of Torbat-e Jam near Malu,
35°129190N, 61°19170E, 15.8.1994.
H. Akhani & Zangui 10043. Khorasan: ca. 38 km E of Torbat-e Jam,
11 km after Mohammad-abad toward Maloo, gypsum hills, 720–740 m, 15.8.1994.
Giess, Volk & Bleissner 5349a (M). Namibia: S Luederitz; Farm Zebrafontein,
LU 87, 21.02.1963.
Pyankov et al. 2001a.
H. Akhani & M. Ghobadnejhad 15630. Iran: E Azerbaijan, 10 km SW of Sarab in the
road toward Asbforoushan, 37°52970N, 47°309300E, 1700 m, 8.9.2001.
H. Akhani, s.n. Iran: Tehran, between Tehran and Qom, W of Heuz-Soltan Lake,
35°2960N, 50°519470E, 861 m, 23.7.2003.
V. Bochantzev et al. 5229 (LE). Kyrgystan: Issykkulj province, Gionskij region,
Mountain range Terskej Alatoo, northern slopes around village Kadanisaj.
953
INTERNATIONAL JOURNAL OF PLANT SCIENCES
954
Table B1
(Continued )
GenBank no.
Subfamily, tribe, and species
Traganum nudatum Del.
Salicornioideae:
Salicornieae:
Kalidium caspicum (L.) Ungern-Sternb.
Microcnemum corraloides
(Loscos & Pardo) Buen
Salicornia persica Akhani
Suaedoideae:
Bienertieae:
Bienertia sinuspersici Akhani
Suaedeae:
Suaeda cuculata Aellen
Suaeda maritima (L.) Dum.
Voucher of DNA source
ITS
psbB-psbH
S. Chaudhary 8644 (LE). Saudi Arabia: Haayer, 16.4.1984.
EF453511
EF453630
H. Akhani 15329. Iran: Semnan, Alborz mountains, 67 km W of Damghan in the
road toward Cheshmeh Ali, 1822 m, 36°69190N, 53°479270E, 14.7.2001.
EF453444
...
H. Akhani & M. Ghobadnejhad 15491. Iran: Arak (Ostan-e Markazi), northwestern
parts of the Kavir-e Meyghan, near Deh-e Namak, 33°559N, 49°199E, 1688 m,
19.8.2001.
H. Akhan & M. Ghobadnejhad 15719. Iran: Fars, N of Tashk lake, high salty soils
near Gomban, 29°489N, 53°289E, 1590 m, 20.9.2001.
EF453448
EF453576
EF453460
...
H. Akhani 17433. Iran: Khuzestan, 17 km N of Bandare Mahshahr, 30°3995 N,
49°159510E, 28 m, 31.10.2003.
DQ499349
DQ499434
H. Akhani et al. 17920. Turkey: Ankara, 28 km N of Sereflikochisar toward Ankara,
N of Tzu Gölü Lake, 39°89500N, 33°19940E, 895 m, 27.8.2004.
H. Akhani & M. Ghobadnejhad 15492. Iran: Arak (Ostan-e Markazi), northwestern
parts of the Kavir-e Meyghan, near Deh-e Namak, 33°559N, 49°199E, 1688 m,
19.8.2001.
EF453509
...
EF453508
EF453628
Note. The vouchers, unless otherwise indicated, are deposited in TUH and the School of Biology, University of Tehran, Research Laborartory of Plant Systematics and Plant Geography (H. Akhani). Herbarium abbreviations: GAZ ¼ Gazy Herbarium, Ankara, Turkey; K ¼ Royal Botanic Gardens, Kew, United Kingdom;
LE ¼ V: L. Komarov Botanical Institute, St. Petersburg, Russia; M ¼ Botanische Staatssammlung München, München, Germany; MSB ¼ Ludwig-MaximiliansUniversität, München, Germany. ITS ¼ internal transcribed spacer.
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