Phytotaxa 268 (1): 001–024
http://www.mapress.com/j/pt/
Copyright © 2016 Magnolia Press
ISSN 1179-3155 (print edition)
Article
PHYTOTAXA
ISSN 1179-3163 (online edition)
http://dx.doi.org/10.11646/phytotaxa.268.1.1
A broadly sampled 3-loci plastid phylogeny of Atraphaxis (Polygoneae,
Polygonoideae, Polygonaceae) reveals new taxa: I. Atraphaxis kamelinii spec. nov.
from Mongolia
OLGA V. YURTSEVA1*, OXANA I. KUZNETSOVA2 & EVGENY V. MAVRODIEV3
1
Department of Higher Plants, Faculty of Biology, M.V. Lomonosov Moscow State University, 1–12, Leninskie Gory, 119234, Moscow,
Russia; e-mail: olgayurtseva@yandex.ru
2
Tsitsin Main Botanical Garden of Russian Academy of Sciences, Moscow, Russia
3
Department of Botany, University of Florida, Gainesville, Florida 32611, U.S.A.; Florida Museum of Natural History, University of
Florida, Gainesville, Florida 32611, U.S.A.
Abstract
Maximum Likelihood (ML) and Bayesian analyses (BI) applied for 3-plastid loci (cpDNA trnL(UAA) intron, trnL–trnF IGS,
and rpl32–trnL(UAG) IGS regions) / 65 tips matrix resulted in preliminary phylogenetic reconstruction of the genus Atraphaxis. In combination with the morphological data the obtained phylogeny appears sufficient for recognition of challenging
taxonomic entities. We found that a collection of Atraphaxis from the Dzungarian Gobi, which appears to be phylogenetically related to A. pungens, is morphologically different from the latter by the predominantly dimerous perianth and gynoecium, shorter outer perianth segments, and the absence of the spiny shoots. It also differs from all other species of Atraphaxis
that occur in Mongolia and neighboring countries. As a result, we described the novel endemic species Atraphaxis kamelinii
O.V.Yurtseva sp. nov. More investigations are necessary to fully understand the origin of the newly described species.
Key words: Atraphaxis, molecular phylogeny, Mongolia, new species, taxonomy
Introduction
The genus Atraphaxis L. comprises ca. 35 species, which are distributed across North-Eastern Africa and Eurasia,
ranging from South-Eastern Europe to Eastern Siberia, China and Mongolia. The genus is most diverse in SouthWest Asia, Central Asia, and China (Bentham & Hooker 1880, Pavlov 1936, Webb 1964, Cullen 1967, Rechinger &
Schiman-Cheika 1968, Lovelius 1978, 1979, Borodina 1989, Brandbyge 1993, Czerepanov 1995, Gubanov 1996, Bao
& Grabovskaya-Borodina 2003, Nikiforova 2012).
Atraphaxis includes xeromorphic shrubs with pseudoterminal or lateral thyrses, nodes with ocreas, trigonous or
lenticular achenes, a perianth with 4–5 segments, and 6–8 stamens with dilatated filament bases (Bentham & Hooker
1880, Haraldson 1978, Ronse De Craene & Akeroyd 1988, Brandbyge 1993). These shrubs are distributed in stony
and desert steppes and mountain scrub communities, from plains and foothills to middle mountain belts. They grow on
gravelly and stony substrates such as gravel riverbeds, sand dunes, clay and chalky outcrops (Lovelius 1978).
The genus was recircumscribed by Jaubert & Spach (1844–46) by combining the genera Atraphaxis and Tragopyrum
M. Bieb. The intrageneric taxonomy of Atraphaxis was traditionally based on the flower merosity, the position of
thyrses, the shape and venation patterns of the leaf blade, and the presence of thorns. Jaubert & Spach (1844–46)
recognized the subgenera: 1) A. subgen. “Euatraphaxis” Jaub. & Spach with a tetramerous perianth, six stamens and a
dimerous gynoecium; 2) A. subgen. Tragopyrum (M. Bieb.) Jaub. & Spach with a pentamerous perianth, 8–9 stamens
and a trimerous gynoecium; 3) A. subgen. Tragatraphaxis Jaub. & Spach with a single species Atraphaxis variabilis
Jaub. & Spach demonstrating a variable flower merosity. The majority of later systematic treatments of Atraphaxis
was based solely on morphology (Ledebour 1847–1849, Meisner 1857, Boissier 1879, Pavlov 1936, Rechinger &
Schiman-Czeika 1968) and supported the two first as subgenera or sections.
Krasnov (1888) proposed the first classification of Atraphaxis, which included 21 species classified in five sections,
and Lovelius (1979) proposed a treatment including 27 species of Atraphaxis split into three sections. In addition to
Accepted by Alexander Sennikov: 18 Jun. 2016; published: 15 Jul. 2016
1
the sections A. sect. Atraphaxis and A. sect. Tragopyrum (M. Bieb.) Meisn., Lovelius described a monotypic section,
A. sect. Physopyrum (Popov) Lovelius for A. teretifolia (Popov) Kom. with a spheroidal perianth and terete linear leaf
blades. Aside from these macro-morphological characters, she used the pollen shape and fine LM-characteristics of the
exine structure (Aleshina et al. 1978, Lovelius & Sjabrjaj 1981) as essential diagnostic traits.
The genus Atraphaxis is one of the most problematic taxa in the family Polygonaceae. The delimitation of
Atraphaxis species can be difficult owing partly to phenotypic plasticity, partly to hybridization and polyploidy, and
partly to the low number of morphological characters separating taxa.
A number of varieties described by Ledebour (1830, 1847–49) seemingly correspond to some species by Jaubert
& Spach (1844–46), which leads to confusion and chaos in the nomenclature and identification of the taxa. A number
of species were described from SW and Central Asia since the most comprehensive taxonomic treatments by Pavlov
(1936) and Lovelius (1979), therefore calling for a new revision of the genus. As early as in the 19th century, Krasnov
(1888) stressed the morphological uniformity of the genus and demonstrated that each of species or variety described
in Atraphaxis has a unique combination of a few character states remaining stable in cultivation, such as the length of
internodes and axes of generative shoots, the lignification level of generative shoots becoming spiny or not, the width
and length of the leaf blade; the merosity of the flower and the number of stamens.
Possible hybridization events make the classification of the genus even more complicated. Based solely on
morphology, Kovalevskaja (1971) suggested putative hybridization between A. pyrifolia Bunge and A. seravshanica
Pavlov, A. pungens (M.Bieb.) Jaub. & Spach and A. frutescens (L.) K. Koch, A. virgata (Regel) Krasn. and A. frutescens,
A. virgata and A. pungens, and described intermediate forms between A. spinosa L. and A. replicata Lam.
Large proportions (48–83%) of distorted pollen grains in some species of Atraphaxis (reviewed in Aleshina et al.
1978) may argue for the irregularities in meiosis and therefore for the processes of hybridization.
Both diploids and polyploids were detected in Atraphaxis, and diverse chromosome numbers were discovered
in A. frutescens (Table 1). The variability of the pollen size was also observed in many species (Table 1). This may
indicate the existence of cryptic polyploid complexes within traditionally recognized taxa (i.g. A. billardierei Jaub. &
Spach, A. bracteata Losinsk., A. laetevirens Jaub. et Spach, A. pungens, A. replicata, A. spinosa).
TABLE 1. Summary of pollen size (Ryabkova 1987, Bao & Li 1993, Ge & Liu 1994, Yurtseva et al. 2014) and chromosome
numbers for Bactria and Atraphaxis.
Species
Small pollen
Polar axis, μm
Mean (min-max)
Bactria ovczinnikovii
A. angustifolia
A. ariana
A. atraphaxiformis
A. aucherii
A. avenia
A. badghysii
A. billardierei
A. bracteata
A. caucasica
A. canescens
A. compacta
Chromosome
number
35.6 (31.8–38.7)
26.1 (23.7–27.6)
33.5 (31.8–34.4)
31.3 (25.8–33.1)
22.2
27.5 (24.3–30.7)
30
30.4 (27.0–34.4)
31.8 (25.8–35.7)
24.0 (22.5–25.0)
23.3 (22.1–24.3)
A. fischeri
22.5 (19.8–24.2)
24.3 (22.1–25.5)
25.9 (20.8–31.9)
27.1 (22.5–30.0)
A. irtyshensis
A. karataviensis
Large pollen
polar axis, μm
mean (min-max)
30.7 (28.5–32.1)
30.2 (29.5–31.1)
A. daghestanica
A. decipiens
A. frutescens
Medium pollen
polar axis, μm
mean (min-max)
27.8 (25.5–30.0)
29.5 (28.0–30.7)
41.0 (36.1–44.3)
2n ≈ 45 (Edman 1931)
2n = 22 (Tian et al. 2009)
35.5 (29.0–45.6)
36.3 (35.0–37.5)
29.7 (29.0–30.1)
27.6 (25.0–31.3)
30.2 (28.0–32.6)
20.2 (17.5–22.5)
40.0 (35.0–42.5)
38.1 (35.0–41.3)
2n = 16 (Ekimova et al. 2009,
2012)
2n ≈ 45 (Edman 1931)
37
36.3 (31.8–40.4)
...continued on the next page
2 • Phytotaxa 268 (1) © 2016 Magnolia Press
YURTSEVA ET AL.
TABLE 1. (Continued)
Species
A. kopetdagensis
A. laetevirens
A. lanceolata
A. manshurica
A. muschketowi
A. pungens
A. pyrifolia
Small pollen
Polar axis, μm
Mean (min-max)
24.1 (20.0–27.5)
23.6 (22.5–27.5)
22.4 (13.8–25.0)
20
A. replicata
A. rodinii
A. seravshanica
21.05 (17.5–32.5)
A. spinosa
19.2 (17.5–20.0)
A. teretifolia
A. toktogulica
A. tortuosa
A. virgata
20.2 (17.5–22.5)
Medium pollen
polar axis, μm
mean (min-max)
28.9 (25.3–35.3)
32
32.5 (27.6–35.7)
27.7 (25.8–31.8)
32.8 (30–37.5)
26.8 (24.0–29.2)
31.5 (30.0–33.0)
27.1 (21.5–30.9)
Large pollen
polar axis, μm
mean (min-max)
36.6 (31.6–47.3)
33.1 (30.9–37.5)
40.0 (37.5–41.3)
Chromosome
number
2n ≈ 45 (Edman 1931)
2n = 22 (Tian et al. 2009)
2n = 48 (Ekimova et al. 2009,
2012)
39.0 (37.5–42.5)
38.5 (35.0–43.0)
40.8 (39.0–42.6)
44.9 (40.0–49.0)
35.6 (31.0–39.7) 33.0
(30.1–34.6)
33.3 (30.0–37.5)
2n ≈ 45, 48 (Edman 1931)
26.8 (25.1–28.2)
28.2 (26.4–31.0)
29.7 (27.5–34.0)
26.3 (23.2–28.8)
26.6 (25.2–28.0)
Irregularities in the number and location of the pollen ectoapertures are found in plant polyploids (Hong & Lee
1983; Van Leewen et al. 1988, Mignot et al. 1994, Nadot et al. 2000; Hong et al. 2005), and particularly observed in
Polygonum (Borzova & Sladkov 1968, 1969), as well as in Atraphaxis. While putative diploids have small tricolporate
pollen grains, a great portion of large 4-loxocolporate, 6-pantocolporate, syncolporate pollen, or pollen with ring-like
shape of ectoapertures was detected in A. laetevirens Jaub. & Spach, A. pyrifolia Bunge, A. seravschanica Pavlov
(Ryabkova 1987), A. aucherii Jaub. & Spach, A. billardierei, A. canescens Bunge, A. compacta Ledeb., A. decipiens
Jaub. & Spach, A. frutescens, A. karataviensis Pavlov & Lipsh., A. muschketowi Krasn., A. replicata, A. rodinii Botsch.,
A. spinosa, A. teretifolia, A. virgata (see more in Yurtseva et al. 2014).
Agamospermy (diplospory) is often accompanied by hybridization and allopolyploidy in plants (Carmak 1997,
Whitton et al. 2008, Lo et al. 2010) and also seems to be the way of “stabilizing” hybrids (e.g., Campbell et al. 1997,
Fehrer et al. 2007, Krak et al. 2013). In Atraphaxis, this phenomenon was undoubtfully documented for A. frutescens
(Edman 1931; Sitnikov 1986, 1991).
In the light of the nomenclatural confusion and paucity of diagnostic characters in Atraphaxis, a molecular
phylogenetic approach in combination with morphological analysis may be useful for the delimitation of the taxa.
Putative hybridization, allopolyploidy and agamospermy create certain difficulties for ITS-based phylogenetic
reconstructions (Baldwin et al. 1993, Wendel et al. 1995a, b, Wendel 2000, Buckler & Holtsford 1996, Buckler et
al. 1997, Barkman & Simpson 2002, Álvarez & Wendel 2003, Bailey et al. 2003, Volkov 2007; Poczai & Hyvönen
2010). Therefore, in this study, we focused mostly on plastid sequence data as well as on the analysis of morphological
traits.
Recent molecular phylogenetic reconstructions based on plastid regions (rbcL, matK, trnL–trnF) as well as on the
nuclear loci LEAFY and ITS1–2 (Lamb Frye & Kron 2003, Galasso et al. 2009, Sanchez et al. 2009, 2011, Yurtseva et
al. 2010, Schuster et al. 2011a, b, 2015) showed that Atraphaxis is a sister of Polygonum s. lat. (incl. Polygonella) (tribe
Polygoneae). These phylogenetic reconstructions led to re-evaluations of the generic circumscription of Atraphaxis.
For example, based on the results of phylogenetic analyses, several species of Polygonum, with equal-sized perianth
segments but the stem lignification and habit typical of Atraphaxis, have been transferred to Atraphaxis (Yurtseva
et al. 2010, Schuster at al. 2011b, Yurtseva et al. 2012), and these results were confirmed by observations of pollen
morphology (Yurtseva et al. 2014), life history, and other morphological chracteristics (Yurtseva et al. 2016). The latest
yet preliminary circumscription of Atraphaxis (Schuster et al. 2011a, b; Tavakkoli et al. 2015; Yurtseva et al. 2016)
therefore includes the following new members: A. ariana (Grigorj.) T.M. Schust. & Reveal (= Polygonum arianum
Grigorj.), A. atraphaxiformis (Botsch.) T.M. Schust. & Reveal (= P. atraphaxiforme Botsch.), A. toktogulica (Lazkov)
T.M. Schust. & Reveal (= P. toktogulicum Lazkov), and A. tortuosa Losinsk.
ATRAPHAXIS (POLYGONEAE)
Phytotaxa 268 (1) © 2016 Magnolia Press • 3
The phylogenetic analyses of Atraphaxis (21 species) (Zhang et al. 2014) argue for the division of the genus
into two major clades, with A. teretifolia (monotypic A. section Physopyrum) nested in one subclade, and A. section
Atraphaxis, which includes the generic type A. spinosa, as part of the second subclade. Dual or ambiguous positions of
some accessions in the plastid phylogeny of Zhang et al. (2014) were possibly caused by erroneous determination of
the voucher specimens or reciprocal hybridization of parental species both served as maternal plants for the hybrids.
The most recent phylogenetic approach of Tavakkoli et al. (2015), based on 11 species of Atraphaxis (nrDNA
ITS1–2 plus combined cpDNA matK and rpl32–trnL(UAG) data sets), do not support the traditional sectional division
of Atraphaxis s. str. (Jaubert & Spach 1844–46, Meisner 1857, Boissier 1879, Pavlov 1936, Lovelius 1979). Tavakkoli
et al. (2015) also recovered Polygonum sect. Spinescentia Boiss. as a sister to Atraphaxis and transferred this clade
to Atraphaxis under the name A. sect. Polygonoides Tavakkoli & Osaloo Kasempoor. According to Tavakkoli et al.
(2015), A. sect. Polygonoides includes former Polygonum aridum Boiss. & Hausskn., P. botuliforme Mozaffarian, P.
dumosum Boiss., P. khajeh-jamali Khosravi & Poormahdi, P. salicornioides Jaub. & Spach, and P. spinosum H.Gross.
However, all of these species are quite different from Atraphaxis, as this genus is treated traditionally (Yurtseva et al.
2016), in habit, perianth morphology, and the ornamentation of the sporoderm. Therefore, the attribution of this group
to Atraphaxis by Tavakkoli et al. (2015) is questionable from a morphological standpoint (Yurtseva et al. 2016).
Our phylogenetic and palynological studies placed a morphologically distinctive endemic from Pamir, Polygonum
ovczinnikovii Czukav. (Czukavina 1962), into Atraphaxis (Yurtseva et al. 2012, 2014), which was subsequently
recognized as A. ovczinnikovii (Czukav.) O.V.Yurtseva. This species turned out to be represented by two species,
which were transferred to a new genus, Bactria O.V.Yurtseva & E.V.Mavrodiev (Yurtseva et al. 2016), due to the
differences in the morphology of perianth, ochreas and sporoderm ornamentation. The last example shows that a
thorough investigation of morphology combined with molecular study helps to resolve taxonomical problems.
The Herbaria of V.L. Komarov Botanical Institute, Russian Academy of Sciences (RAS), Saint Petersburg, Russia
(LE) and Lomonosov Moscow State University, Faculty of Biology, Moscow, Russia (MW) keep a large number
of specimens of Atraphaxis from Mongolia collected in 1970–1980 by V.I.Grubov, I.A.Gubanov, R.V.Kamelin and
others. We found that some of those collections have been misidentified as A. bracteata (Losina-Losinskaya 1927)
or A. virgata (Krasnov 1888). Grubov (1982), Borodina (1989), and Gubanov (1996) listed A. bracteata as present in
Dzungarian Gobi, Mongolia, but their characters only weakly correspond to the morphology of the type specimen of A.
bracteata (LE!). We therefore suggest that the presence of A. bracteata was erroneously indicated for the Dzungarian
Gobi and some other regions of Mongolia.
Cleary, the genus Atraphaxis requires a taxonomic revision, and our recent work is the first step towards
synthesizing the recent findings and adding new data to resolve the phylogeny of this group. Due to the number
of plastid loci, our phylogeny still remains preliminary, but in combination with the morphological data it appears
sufficient for recognition of challenging taxonomic entities.
In this study we aimed, 1) to obtain the best sampled phylogeny of Atraphaxis using three regions of the plastid
genome (trnL(UAA) intron, trnL–trnF IGS, and rpl32–trnL(UAG) IGS); 2) to specify the phylogenetic placement of one
of the specimens from the Dzungarian Gobi previously identified as A. bracteata; 3) to investigate whether there are
morphological apomorphies that distinguish the latter from other species of Atraphaxis growing in Mongolia.
Materials & Methods
Plant Material
The morphological study involved ca. 1000 specimens of Atraphaxis and Polygonum stored in the herbaria of
V.L.Komarov Botanical Institute (LE); Lomonosov Moscow State University, Moscow, Russia (MW); Tsitsin Main
Botanical Garden, RAS, Moscow, Russia (MHA); and Main Botanical Garden, National Academy of Science, Bishkek,
Kyrgyzstan (FRU).
The identification of the samples used in the study was conducted after examination of the type specimens of
species of Atraphaxis and Polygonum (LE, MW), or their high-resolution images (P—https://science.mnhn.fr/taxon/
genus/atraphaxis, LINN—http://linnean-online.org/linnaean_herbarium.html, B—http://ww2.bgbm.org/herbarium/).
Taxonomic treatments of Atraphaxis from Turkey (Cullen 1967), Pakistan (Qaiser 2001), Iran (Rechinger & SchimanCzeika 1968, Tavakkoli et al. 2015), the former USSR (Pavlov 1936, Grossheim 1930, Grossheim 1945, Krechetovitch
1937, Rzazade 1952, Drobow 1953, Kastschenko 1953, Avetisjan 1956, Bajtenov & Pavlov 1960, Kovalevskaja 1971,
Kutateladze 1975, Kashina 1992, Nikiforova 2005, Grabovskaya-Borodina 2012), Central Asia (Borodina 1989),
4 • Phytotaxa 268 (1) © 2016 Magnolia Press
YURTSEVA ET AL.
Mongolia (Gubanov 1996), and China (Bao & Grabovskaya-Borodina 2003) were consulted for identification of our
specimens.
The morphological characteristics of the specimens from the Dzungarian Gobi (Table 2) were compared to some
species listed in the flora of Mongolia (Grubov 1982, Borodina 1989, Gubanov 1996, Bao & Grabovskaya-Borodina
2003): A. bracteata, A. compacta Ledeb., A. pungens, and A. virgata.
The molecular study involved 33 species (65 accessions) of Atraphaxis, 6 species of Polygonum sect. Spinescentia,
and Bactria ovczinnikovii. Appendix 1 contains voucher information and GenBank accession numbers for the samples
used in the study.
TABLE 2. Characteristics of Atraphaxis pungens, the Dzungarian Gobi collection (= A. kamelinii), A. compacta, A. bracteata,
and A. virgata growing in Mongolia (own observations).
Characters
Life history
Size, cm
Shoots
A. pungens
Shrub
50–150
Straight, stout, spiny
Bark color of second
year shoot
Color of annual shoot
Creamy, exfoliating
A. kamelinii
Shrub
100–150
Straight, stout,
unarmed
Creamy, exfoliating
Creamy, glabrous
Creamy, glabrous
Leaf blade shape
Broadly-elliptical,
oval, oblong,
lanceolate
10–20 × 5–10
Elliptical, rhomboidelliptical
A. virgata
Shrub
150–200
Straight, slender,
unarmed
Gray, fibrously
disintegrating
Creamy, finely
ribbed
Oblong-elliptical,
oblanceolate
10–20 × 5–10
Circular, broadlyovate or rhomboidelliptical
4–7 × 4–5
A. bracteata
Shrub
100–300
Straight, slender,
unarmed
Gray-brown,
exfoliating
Light-brown, terete,
glabrous
Obovate, oval to linear
15–60 × 10–25
20–25 × 7–9
Entire, flat, finely
crenulate
Obtuse or shortpointed, acuminate
Broadly cuneate
Thick
Bluish-green
Reticulate adaxially
and abaxially
Entire, flat or slightly
revolute
Obtuse or shortpointed
Broadly cuneate
Thick
Bluish-green
Pinnate abaxially and
adaxially
Entire, flat, or slightly
revolute
Obtuse, or shortpointed
Broadly cuneate
Thick
Bluish-green
Pinnate abaxially and
adaxially
Strongly undulatecrenulate
Sharply pointed, almost
subulate
Rounded
Leathery
Green
Reticulate abaxially and
adaxially
Thyrses, (length, cm)
Lateral
(1.5–3.0)
Terminal racemes of
thyrses (10.0–15.0)
Mainly lateral (1.5)
Terminal racemes of
thyrses (10.0–15.0)
Inflorescence structure
(Number of cymes in
thyrse)
Petiole length, mm
Perianth tube length,
mm
Perianth color
Segments number
Outer segments size,
(length × width) mm
Inner segments size, mm
Inner segments shape
Achene merosity
Achene color
Achene size, (length ×
width) mm
Achene surface
Styles
Congested
(5–6)
Spaced
(5–10)
Congested
(5–6)
Spaced
(10)
Slightly revolute,
finely crenulate
Obtuse, or shortpointed
Cuneate
Thick
Bluish-green
Smooth adaxially,
with midvein
abaxially
Terminal racemes
of thyrses (10.0–
15.0)
Congested
(20–23)
3.0
2.7–6.8
1.5–3.0
2.0–2.5
1.5–3.0
1.5–2.6
3.0–6.0
1.5–2.1
0.5–1.0
2.5–3.0
White & pinkish
2+3
3.2–5.6 × 2.5–4.1
Deeply pink
2 + 2(3)
2.0–2.8 × 3.0
White & pink
2+2
2.2–4.5 × 2.2–4.0
White & pink
2+3
2.0–3.0 × 2.0–3.0
White & pink
2+3
2.0–2.5 × 1.2–1
4.5–7.0 × 4.5–8.2
Circular
3
Dark-brown to black
2.6–3.3 × 1.3–2.0
4.5–5.9 × 6.0–7.5
Circular to reniform
2–3
Dark-brown to black
4.2–4.5 × 2.5
6.0–8.0 × 7.4–10.0
Circular to reniform
2–3
Light-brown
3.0–4.8 × 2.0–4.1
5.5–6.5 × 7.0–8.0
Circular-rhomboid
3
Dark-brown to black
4.0–5.0 × 1.5–2.5
4.5–5.0 × 3.5–4.0
Oblong-elliptical
3
Light-brown
3.0–3.7 × 1.5–1.7
Smooth, glossy
Connate at the very
base
Capitate
Smooth, glossy
Connate at the very
base
Capitate
Smooth, dull
Free
Smooth, glossy
Free
Smooth, dull
Free
Flattened-capitate
Capitate
Capitate
Leaf blade size (length
×width), mm
Leaf blade margin
Leaf blade apex
Leaf blade base
Leaf blade consistency
Leaf blade color
Venation
Stigmas
ATRAPHAXIS (POLYGONEAE)
A. compacta
Shrub
50
Stout, short, spiny
Gray, fibrously
disintegrating
Creamy, glabrous
Phytotaxa 268 (1) © 2016 Magnolia Press • 5
DNA isolation and amplification
DNA was extracted from herbarium specimens using a NucleoSpin Plant Extraction Kit (Macherey-Nagel, Germany)
with a yield of DNA ranging from 0.005 to 0.1 mg per 0.1 g of plant material.
The cpDNA trnL(UAA) intron, trnL–trnF IGS, and rpl32–trnL(UAG) IGS regions were used because of their utility
in Polygonaceae and high variability (Tavakkoli et al. 2010, 2015, Schuster et al. 2011a, b). The primers of Taberlet at
al. (1991) and Shaw et al. (2007) were used for amplification of these regions.
PCR was performed in a 0.02 ml mixture containing 10–20 ng DNA, 5 pmol of each primer and MaGMix (Dialat
LTD, Russia), containing 0.2 mM of each dNTP, 2.0 mM MgCl2, and 2.5 units of Smart Taq polymerase. 1.0 mM of
DMSO was included for amplification of nrDNA regions with high GC content.
Amplification of nrDNA ITS and cpDNA trnL(UAA) intron and trnL–trnF IGS regions was performed under the
following cycling conditions: hold 95°C, 3 min; 94°C, 30 s; 58°C, 30 s; 72°C, 30 s; repeat 30–33 cycles; extend 72°C,
3 min. Amplification of the rpl32–trnL(UAG) IGS region was performed using the following program: hold 95°C, 3 min;
94°C, 30 s; 52°C, 30 s; 72°C, 60 s; repeat 35 cycles; extend 72°C, 5 min.
Purification of PCR products and DNA sequencing
Amplification products were purified by electrophoresis (Sambrook et al. 1989) and one-band DNA fragments were
extracted from the gel and purified using the GFXTM PCR DNA, Gel Band Purification Kit (GE HealthCare, USA) or
Evrogene Cleanup Mini kit (Russia). The purified PCR products were then used as a template in sequencing reactions
with the ABI Prism BigDye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems, USA) following
the standard protocol provided for a 3100 Avant Genetic Analyzer (Applied Biosystems, USA). Sanger sequences
were produced at the Genome Center (Engelhardt Institute of Molecular Biology RAS, Moscow). Forward and reverse
sequences were assembled and edited with BioEdit v.7.2.0. (Hall 1999).
Sequences used in phylogenetic analyses and the alignment strategy
Our present study of Atraphaxis incorporates the members of the genus Atraphaxis as circumscribed by Yurtseva et
al. (2016), the members of Polygonum sect. Spinescentia, which rank clearly requires future clarification, and Bactria
ovczinnikovii, which was selected as an outgroup based on the previous results (Yurtseva et al. 2016).
Voucher information and GenBank numbers are presented in Appendix 1.
All sequences were aligned using MAFFT (Katoh et al. 2002; Katoh & Standley 2013) following MAFFT’s LINS-i alignment strategy (Katoh et al. 2002; Katoh & Standley 2013), with the default settings set for the gap opening
penalty and the offset value.
Aligned plastid matrices were manually concatenated and analyzed as a single contiguous dataset. The combined
aligned chloroplast matrix for cpDNA trnL(UAA) intron, trnL–trnF IGS, and rpl32–trnL (UAG) IGS regions includes
2199 characters for a total of 72 accessions. For the cpDNA rpl32–trnL region 33 accessions were produced for this
study, 27 were generated previously, and 11 were downloaded from GenBank (2015) http://www.ncbi.nlm.nih.gov).
For the trnL(UAA) intron, trnL–trnF IGS regions, 25 accessions were obtained for this study, and 27 were sequenced
previously.
Phylogenetic analyses
The Maximum Likelihood (ML) analysis was performed with PhyML v. 3.0 (Guindon & Gascuel 2003, Guindon et
al. 2010), with an estimated proportion of invariable sites and empirical nucleotide equilibrium frequencies. We took
a BioNJ tree as the starting tree, and defined the strategy of the tree topology search as ‘‘best of NNIs and SPRs’’
following with ten random starts. The GTR + G + I model was determined as the best choice for both Bayesian and
ML analyses following the automatic PhyML Smart Model Selection option (Guindon et al. 2010) based on Akaike
information criteria. Branch supports were calculated with the approximate likelihood-ratio test (aLRT) (Guindon et
al. 2010).
A Bayesian analysis (BI) was conducted with MrBayes v. 3.1.2 (Ronquist & Huelsenbeck 2003) as implemented
in CIPRES (Miller et al. 2010). Two runs with four chains each were run for 10 million generations with a burning of
2.5 million generations; the chains were sampled every 1000 generations with default parameters. At the end of the
runs, the standard deviation of split frequencies between the two runs had fallen to 0.0060. Tracer ver. 1.6 (Rambaut et
al. 2014) was used to confirm that chains had converged and a plateau in likelihoods was obtained.
We use following terminology to describe levels of statistical support—“moderate”: 0.80–0.90 aLRT/0.90–0.95
Bayesian posterior probabilities (pp) and “strong” (or well): 0.91–1.00 aLRT/0.96–1.00 pp.
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Light microscopy (LM)
LM-images were made with the stereoscopic microscope Stemi 2000-C Carl Zeiss (Zeiss, Germany) using the camera
Axiocam-MR and program AxioVision V. 4.8 free edition. The samples used for photographing and measurements are
listed in Appendix 2.
Results
Plastid phylogeny of Atraphaxis
The results of ML and BI of the combined chloroplast data matrix with Bactria ovczinnikovii , taken as an outgroup,
showed (Fig. 1) that a strongly supported clade (0.93/1.00) Polygonum sect. Spinescentia (P. aridum, P. dumosum, P.
khajeh-jamali, P. salicornioides, and P. spinosum) is a sister to Atraphaxis s. str., but P. botuliforme is nested in the
Atraphaxis s. str. clade and is associated with one accession (132) of A. frutescens.
The topology of the combined plastid phylogeny of Atraphaxis s. str. is as follows: Atraphaxis s. str. clade is strongly
supported (0.90/0.99), with A. ariana recovered as a moderately supported sister to the rest of the genus (0.92/0.90);
A. sect. Tragopyrum in its traditional understanding appeared as non-monophyletic, whereas the members of the
type section (A. compacta, A. fischeri Jaub. & Spach, A. karataviensis, A. replicata, A. spinosa) plus A. binaludensis
formed the most derived moderately supported clade (0.81/0.92). Two accessions of A. teretifolia (monotypic A. sect.
Physopyrum) formed a strongly supported clade (0.95/0.99), which is recognized as a putative sister of A. caucasica
plus well-supported (A. rodinii plus A. badghysi) (0.99/0.99) (Fig. 1).
Position of the collection from the Dzungarian Gobi in plastid topology
The collection from the Dzungarian Gobi, Mongolia (LE) was identified as most similar to A. bracteata by R. Kamelin,
but in our plastid topology it is well-supported (0.94/0.99) as a sister to a moderately supported subclade of three
accessions of A. pungens (0.87/0.93)(Fig. 1). Atraphaxis bracteata (157) from China is not closely related to the
collection from the Dzungarian Gobi, nor does it belong to the Mongolian A. virgata, which is in a different subclade
with A. frutescens. This result clearly demonstrates that the collection from the Dzungarian Gobi is not related to A.
bracteata or A. virgata by maternal lineage. The collection from the Dzungarian Gobi is also distant from A. spinosa
and A. compacta, which are likely part of the most derived subclade in Atraphaxis (Fig. 1).
Morphological distinctions of the collection from the Dzungarian Gobi from the other species from Mongolia
The collection from the Dzungarian Gobi is a shrub with racemes of bracteose thyrses 10–12 cm long composed of 5–
10 well spaced out cymes of 1–2 flowers (Figs. 2–3), leaf blades elliptical to rhomboid-elliptical, with pinnate venation
visible adaxially and abaxially (Fig. 3C–D), perianth tetramerous or pentamerous (Fig. 4A–D), achenes lenticular or
triquetrous with three style branches fused at the base, and capitate stigmas (Fig. 4D–G).
The comparison of our specimen with other species growing in Mongolia (Table 2) shows that the collection from
the Dzungarian Gobi has a combination of characteristics of A. pungens, A. compacta, and possibly A. virgata.
It resembles A. pungens in the creamy color of its annual shoots and the elliptical to rhomboid-elliptical leaf blades,
which in A. pungens vary in shape from elliptical to oblanceolate, and are obtuse, shortly acuminate, or shortly pointed.
In contrast to the second-year shoots of A. pungens, which have the gray bark, the second-year shoots in the specimens
from the Dzungarian Gobi have the creamy-pinkish bark. Atraphaxis pungens has compact thyrses which are 1.5–3 cm
long, composed of 5–6 congested cymes of 2–6 flowers; the thyrses occupy lateral positions at annual or second-year
shoots, the latter later becoming spiny. The collection from the Dzungarian Gobi has unarmed shoots with elongated
thyrses which are 10–15 cm long, composed of 5–10 well-spaced cymes of 2 flowers; the thyrses terminate annual
shoots and axillary branchlets, which appear simultaneously with the terminal thyrse, e.g. sylleptically (Weberling
1989), so the annual shoots are terminated by the racemes of thyrses.
The collection from the Dzungarian Gobi often has a tetramerous perianth and lenticular achenes, which are
characteristics of A. sect. Atraphaxis. Of 34 flowers examined, 62% had a tetramerous perianth and lenticular achenes,
6% had a tetramerous perianth and trigonous achenes, 6% had a pentamerous perianth and lenticular achenes, and 26%
had a pentamerous perianth and trigonous achenes.
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FIGURE 1. Plastid phylogeny of Atraphaxis, Polygonum sect. Spinescentia and outgroup (Bactria ovczinnikovii). The best tree from
ML analysis of the combined plastid dataset: trnL intron, trnL-trnF IGS, and rpl32–trnL(UAG) IGS regions of cpDNA (– log likelihood:
5639.238874). Numbers above the branches indicate the aLRT support values (equal or more than 0.8 shown) from ML analysis/posterior
probabilities equal or more than 0.9 from the BI of the same matrix. The members of A. sect. Atraphaxis, A. sect. Physopyrum, and A. sect.
Tragopyrum are indicated. Atraphaxis kamelinii and A. bracteata are shown in bold. Image: E. Mavrodiev.
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The collection from the Dzungarian Gobi has circular-reniform inner segments which are 4.5–5.0 × 6.0–6.5 mm in
size, outer segments of 2.0–2.5 × 3.0 mm, and a short filiform part of the perianth tube 2.0–2.5 mm long, which is equal
in length to the outer segments and is joined to a pedicel with articulation (Fig. 4A–D, 5A–B). Judging by the perianth
size (Table 3), this collection is close to A. compacta from Kazakhstan (Fig. 5C), or A. replicata from Kyrgyzstan (Fig.
5D).
Atraphaxis pungens has a pentamerous perianth and trimerous achenes (Fig. 5F–I). Three inner segments are
rotundate-reniform, 5.0–7.0 × 4.5–8.2 mm in the fruiting stage. Two outer segments are oblong-ovate, 3.3–5.6 × 2.7–
4.1 mm long. The filiform part of the perianth tube (3.0–7.0 mm long) is usually twice as long as the outer segments,
and longer than in the collection from the Dzungarian Gobi. The achenes of A. pungens are trigonous, rhomboidelliptical or pyriform, black and glossy, with three style branches fused at the base, and small stigmas (Fig. 5J–L).
The ratio of inner to outer segment length varies in range 1.3–1.7 in A. pungens, and is equal to 2.1 in the
collection from the Dzhungarian Gobi, varying in range 2.0–2.5 in A. compacta and A. replicata (Table 3, Fig. 5C–D).
The filiform part of the perianth tube joined to a pedicel has similar length in the collection from the Dzungarian Gobi,
A. compacta, and A. replicata (Table 3).
Despite the mainly tetramerous perianth with circular-reniform inner segments, the short filiform part of the
perianth tube, and lenticular achenes, the collection from the Dzungarian Gobi is habitually different from A. compacta
and A. spinosa from the type section of Atraphaxis, which occur in Mongolia. These species are small shrubs with short
spiny shoots and lateral compact thyrses 1.0–1.5 cm long composed of 5–6 congested cymes of 1(2) flowers.
The specimen from the Dzungarian Gobi in the overall appearance resembles A. bracteata and A. virgata, which
are shrubs with straight elongated shoots terminated by the racemes of thyrses. However, A. virgata differs by its
oblanceolate leaf blades with a finely crenulate-papillate, slightly revolute margin, smooth or longitudinally wrinkled
(when dried) at the upper surface, with a single main vein beneath. It has terminal recemes of thyrses composed of 20–
23 congested cymes of 1–2 flowers; the perianth with cordiate or oblong-elliptical inner segments (Fig. 5E), and lightbrown trigonous achenes. Atraphaxis bracteata differs by its obovoid or broadly oval leaf blades which are sharply
pointed and strongly undulate at margin, and its perianth with sub-equal segments, the outer ones spread horizontally
in fruiting. Hence, our specimen from the Dzungarian Gobi is fairly different from both taxa.
TABLE 3. Perianth sizes in Atraphaxis pungens, the collection from the Dzungarian Gobi (= A. kamelinii), A. compacta, and
A. replicata. The origin of the samples see in Appendix 2.
Species, sample
Inner segments, mm
Outer segments, mm
Ratio: IS/OS length/ Filiform part of
Achene size, mm
IS/OS width
perianth tube, mm
1.7/2.5
5.3
3.5 × 2.0
3.5 × 3.0
A. pungens, Lomonosova 6.0 × 7.5
& Ivanova 2408
7.0 × 8.2
5.6 × 4.1
1.25/2.0
6.8
2.8 × 1.5
A. pungens, Volkova &
Rachkovskaya 7373
4.6–5.0 × 5.7–6.4
3.3 × 2.7
1.5/2.3
2.3–2.5
2.1–2.5 × 1.1
A. pungens, Gubanov
3563
3.8 × 3.4
1.4/1.6
3.2
A. pungens, Maltseva & 5.5 × 5.5
Selisheva
4.4–5.0 × 4.5–5.5
3.2–3.8 × 3.0
1.3/1.8
3.6–4.5
4.8 × 2.4
A. pungens, Neifeld &
Margasova
2.0–2.8 × 3.0
2.1/2.5
2.0–2.5
4.2–4.5 × 2.5
A. kamelinii, Daryima & 4.5–5.9 × 6.0–7.5
Kamelin 765 (50)
2.2–2.5 × 2.2–2.5
2.5/3.0
1.5–1.7
4.8 × 4.1
A. compacta, Pavlov 160 6.0–6.3 × 7.4–7.5
(45)
2.8 × 2.4
2.0/3.8
2.3–2.5
4.5–5.0 × 3.5–4.0
A. replicata, Kuvaev 518- 5.1–6.5 × 6.8–9.0
3 (31)
IS—inner segment of perianth, OS—outer segments of perianth. Numbers in brackets are sample numbers in Appendix 1.
Discussion
Plastid phylogeny of Atraphaxis
The results of the Maximum Likelihood and Bayesian analyses of the combined plastid data matrix confirmed
Polygonum sect. Spinescentia (Atraphaxis sect. Polygonoides) as a sister of the narrowly defined Atraphaxis with 33
species (Tavakkoli et al. 2015; Yurtseva et al. 2016) (Fig. 1).
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We also confirmed that Atraphaxis botuliformis (Polygonum botuliforme) is deeply nested in Atraphaxis in plastid
phylogeny. This caespitose perennial herb, with sausage-shaped succulent leaves and axillary cymes of flowers at
annual shoots, is a local endemic of Central Iran (Tehran region) (Mozaffarian 1988, 2012). It is morphologically quite
different from other species of Atraphaxis but has the striate-perforate ornamentation of sporoderm (Tavakkoli et al.
2015), peculiar to Atraphaxis (Yurtseva et al. 2014). In ITS-based phylogeny it is however nested in Polygonum sect.
Spinescentia (A. sect. Polygonoides) (Tavakkoli et al. 2015, Yurtseva et al. 2016). This conflict likely indicates the
ancient hybrid origin of A. botuliformis and needs special study.
Atraphaxis sect. Atraphaxis is characterized by having a tetramerous perianth and a dimerous gynoecium, and it
is likely the most derived clade of Atraphaxis, which, if A. binaludensis is included, has moderate support (0.81/0.92).
Similarly to many members of A. sect. Atraphaxis, A. binaludensis has spinescent shoots, broadly obovate-rhomboid
small (5–6 × 4–5 mm) leaf blades with abaxially prominent reticulate nervation and a slightly revolute margin, but
differs by a pentamerous perianth (Tavakkoli et al. 2014), common in A. sect. Tragopyrum. A presumable hybrid origin
of this taxon needs additional study. A pentamerous perianth is also usual in a presumable hybrid of A. fischeri and A.
frutescens, in which a pentamerous perianth and trigonous achenes, and a tetramerous perianth and lenticular achenes
can be found with the same frequency.
We confirmed the monophyly of A. teretifolia (monotypic A. sect. Physopyrum) (Zhang et al. 2014), which is a
sister to the clade of morphologically distinct A. caucasica, A. badghysi, and A. rodinii, though there is no support for
this relationship. As shown by Zhang et al. (2014), we confirm that A. sect. Tragopyrum is polyphyletic and requires
further revisions (Fig. 1).
Placement and morphological distinctions of the collection from the Dzungarian Gobi
The collection from the Dzungarian Gobi appeared as a strongly supported sister to the A. pungens clade. However,
the morphological characteristics of this collection only partly correspond to the morphology of A. pungens (Table 1,
Figs. 4–5). The collection from the Dzungarian Gobi region has creamy second-year shoots, terminated by racemes
of elongated thyrses with well-spaced cymes of 2 flowers, a mainly dimerous perianth with circular-reniform inner
segments which are 2.0–2.5 times longer than its outer segments, the latter being equal to the filiform perianth tube,
and mainly lenticular achenes (Figs. 2–4). Atraphaxis pungens has stout, spiny second-year shoots covered with gray
bark, compact lateral thyrses with congested cymes of 2–6 flowers, a pentamerous perianth with inner segments, which
are 1.3–1.7 times longer than outer segments, the latter being equal to or shorter than the filiform perianth tube, and
trimerous achenes (Fig. 5F–L). Both taxa share glaucous rhomboid-elliptical or elliptical leaf blades and black shiny
achenes with short styles fused at the base.
Due to the mostly maternal inheritance of plastids in Angiosperms (Hagemann & Schröder 1989), the highly
supported grouping of the collection from the Dzungarian Gobi with A. pungens in the plastid topology of Atraphaxis
(Fig. 1) might indicate that A. pungens (or any closely related taxon) served as a putative maternal plant for this
collection.
The collection from the Dzungarian Gobi is also clearly distinct from all other taxa growing in Mongolia and
China (Grubov 1982, Borodina 1989, Gubanov 1996). In particular, it strongly differs from A. bracteata (LosinaLosinskaya 1927) in various aspects (Table 2).
Atraphaxis bracteata is characterized as a 1–3 m tall shrub with racemes of thyrses, green, leathery, broadly
obovate or oval leaves, sharply pointed at the tip and strongly undulate at margins. The perianth has subequal segments,
three reniform-orbicular inner ones surrounding the achene, and two spreading outer segments when in fruit (Bao &
Grabovskaya-Borodina 2003).
Among all of the species reported from Mongolia, the accession from the Dzungarian Gobi most corresponds to
the description of A. virgata as “a shrub 1.5–2 m tall with gray-green oblanceolate or oblong-elliptical leave blades
with veins that are conspicuous only abaxially, margin flat or slightly downward revolute” (Krasnov 1888, Gubanov
1996, Borodina 1989, Bao & Grabovskaya-Borodina 2003). But in contrast to A. virgata, which is characterized
by racemes of thyrses with 20–23 congested cymes of flowers, oblong-elliptical inner segments, and light-brown
trigonous achenes, our plant has well-spaced 5–10 cymes, leaf blades with veins visible adaxially and abaxially,
circular-reniform inner segments, often dimerous flowers, and black achenes.
In short, the collection from the Dzungarian Gobi combines the shrubby habit and the racemes of thyrses present
in A. virgata and A. bracteata, the elongated thyrses with far-spaced cymes of flowers peculiar of A. bracteata and A.
frutescens, the elliptical or rhomboid-elliptical leaf blades of A. pungens and A. compacta, the circular-reniform inner
perianth segments and lenticular achenes of A. sect. Atraphaxis, and black color of achenes peculiar of A. pungens.
Combined with the results of the phylogenetic analysis (Fig. 1), and due to the morphological distinctiveness of
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the collection from the Dzungarian Gobi, we describe it as the new species Atraphaxis kamelinii O.V.Yurtseva, spec.
nov. The possibility of a hybrid origin of this species and its relationship with A. pungens (or a closely related taxon),
a putative maternal parent, needs to be examined with nuclear data and cytological studies.
Conclusions
1. The preliminary 3-loci/65 tips plastid phylogeny of Atraphaxis showed that the morphologically distinct collection
of Atraphaxis from the Dzungarian Gobi, which had previously been assigned by R. Kamelin (LE) to Atraphaxis
bracteata, is actually closely related to A. pungens.
2. This collection is morphologically quite different from all species of Atraphaxis growing in Mongolia and
neighbouring countries (Table 2). It combines the morphological characteristics of A. pungens, A. virgata, as well as
of the species of A. sect. Atraphaxis, and is recognizable due to its own remarkable morphology.
3. Morphological differences of the collection from the Dzungarian Gobi from A. pungens and other taxa are so
noticeable that it deserves to be described as a distinct species, Atraphaxis kamelinii O.V.Yurtseva, spec. nov.
4. The results of the phylogenetic analyses, as well as the unusual morphology of the proposed new species
combining characters of several taxa, suggest a possible hybrid origin of the newly described species, but more
investigations are necessary to fully understand the origin of A. kamelinii.
Taxonomy
Atraphaxis kamelinii O.V.Yurtseva, spec. nov. (Figs. 2–5)
Type:—MONGOLIA. [Khovd aimag]: the Dzungarian Gobi, S slope of Saertaengijin-Khuvch Uul [Mt.] near junction to Khaldzan-Ula
[Mts.], 27 July 1984, Daryima & Kamelin 765 (LE! holotype).
Shrubs ca 1 m tall. Stem erect, stout, glabrous; woody shoots inclined-spreading, brown, much branched, not spiny,
slightly ribbed, creamy, epidermis exfoliating and fibrously disintegrating, making light-brown or creamy wood.
Current-year shoots are branched forming racemes of thyrses with branchlets departing at a nearly right angle. Annual
shoots and branchlets 10–15 cm long are straight, soon lignified, slightly ribbed, glabrous, leafy with internodes 5–10
mm, or terminated by thyrses 5–10 cm long with 5–10 spaced cymes of 1–3 flowers in axils of developed or reduced
leaf blades. Ocreas at vegetative shoots are tubulate, 5–6 mm, membranous, brownish at base, transparent above and
cleft into two linear-lanceolate lacinulas with two faintly visible veins at both sides of leaf blade, and finely incisoserrated short middle lacinula. Ocreolas in thyrses are oblique funnel-form, 2–5 mm, membranous, brownish at base,
transparent above and cleft into 2 sharp teeth. Leaf blades bluish-green or glaucous, thick, oblong-elliptic, 10–20 ×
5–10 mm, gradually narrowed to a petiole 1.5–3 mm, glabrous, with prominent midvein and faint lateral veins. Margin
entire, flat, or slightly revolute, glabrous, apex obtuse or short-pointed. Segments 4 or rarely 5, bright-pink; outer
segments two, reflexed towards pedicel in fruit, reniform-orbicular, ca. 2.0–2.8 × 3.0 mm, prominently reticulateveined; inner segments two or three, circular-reniform in fruit, 4.5–5.9 × 6.0–7.5 mm in diam., base nearly cordate,
venation prominently reticulate, margin slightly undulate. Perianth tube 2.0–2.5 mm, filiform, joined to a pedicel (ca.
4.5 mm long) with articulation. Stamens 8, filaments subulate-lanceolate, gradually dilatated towards base. Achenes
4.2–4.5 × 2.5 mm, ovoid, gradually acuminate, lenticular or unequally-trigonous, with strongly concave faces, ribs
sharp, almost winged, surface smooth, glossy, dark-brown to black.
Styles 2(3), 0.3 mm long, fused at the base, with stigmas capitate, papillate.
Fl.—May–June. Fr.—June–Aug.
Distribution:—Endemic of the Dzungarian Gobi in SW Mongolia, Khovd aimag (Fig. 6).
Ecology:—Mountain slopes, granites, sandy sairs.
Etymology:—The species is named after Rudolf V. Kamelin (1938–2016), famous for his studies on the flora and
florogenesis of Central Asia.
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FIGURE 2. Holotype of Atraphaxis kamelinii O.V.Yurtseva, sp. nov. Image: O. Yurtseva.
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FIGURE 3. Shoots and thyrses of Atraphaxis kamelinii (LE! holotype, see also Fig. 2). A. Bracteose thyrses with spaced cymes of 1–2
dimerous flowers; B. Top of annual shoot with branchlets terminated by thyrses; C, D. Abaxial and adaxial view of leaf blades; E. The
bases of annual shoots with axillary vegetative and generative branchlets. Scale bar = 1 mm (C–D). Images: O. Yurtseva.
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FIGURE 4. Perianths and achenes of Atraphaxis kamelinii (LE! holotype). A. Cyme of two flowers with tetramerous (on the left) and
pentamerous (on the right) perianths; B, C. Flower with pentamerous perianth and trimerous gynoecium; D. Flower with tetramerous
perianth (inner segment is removed) hiding lenticular achene; E. The top of triquetrous achene with three styles and capitate stigmas; F.
Triquetrous achenes; G. Three style branches fused at the base and terminated by capitate stigmas. Scale bar = 1 mm (A–F); = 0.5 mm
(G). Images: O. Yurtseva.
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FIGURE 5. Perianths (A–I) and achenes (J–L) of Atraphaxis kamelinii, A. compacta, A. replicata, A. virgata, and A. pungens. A–B. A.
kamelinii from the Dzungarian Gobi, Daryima & Kamelin 765 (LE); C. A. compacta, Kazakhstan, Pavlov 160 (MW); D. A. replicata,
Kuvaev 518-3 (MW); E. A. virgata, Mongolia, Gubanov 2634 (MW); F, J–K. A. pungens, Russia, Tuva, Neifeld & Margasova (MHA); G.
A. pungens, Mongolia, Gubanov 3563 (MW); H, L. A. pungens, Mongolia, Volkova & Rachkovskaya 7373 (LE); I. A. pungens, Russia,
Tuva, Maltseva & Selisheva (MW). Scale bar = 1 mm (A–I); = 0.2 mm (K); = 0.5mm (J, L). Images: O. Yurtseva.
Taxonomic relationships:—The new species might be closely related to A. pungens as a putative maternal taxon,
with which it shares the shrubby habit, branchlets of the annual shoots departing at almost right angle, elliptical or
rhomboid-elliptical leaf blades, black glossy achenes, perianth size, but differs by creamy-pinkish, not spiny secondyear shoots, and mainly dimerous flowers.
Atraphaxis kamelinii also resembles A. virgata because of the shrubby habit and racemes of thyrses, but differs
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in the shape and venation of leaf blades, far-spaced cymes of flowers, circular-reniform inner segments, and black,
glossy, and mainly lenticular achenes.
The new species is similar to A. bracteata due to the shrubby habit and racemes of thyrses, but differs by creamy
annual shoots, elliptical bluish-green leaf blades entire at the margin, outer perianth segments reflected to a pedicel and
mainly lenticular achenes.
It is morphologically similar to A. spinosa and A. compacta with mainly tetramerous flowers, almost reniform
inner segments and lenticular achenes, but differs by lacking spiny shoots, elongated thyrses with 5–10 spaced cymes
of flowers, and achenes that are almost black and glossy.
Other specimen seen (paratype):—MONGOLIA. Khovd (=Khobdo) aimag: the Dzungarian Gobi, [somon
Bulgan], 15 km S of the settlement Bulgan, granites, sandy sairs, N 45°57’, E 91°31’, 17 June 2004, Dyachenko &
Kosachev (ALTB!).
FIGURE 6. Distribution map of Atraphaxis kamelinii. Distribution area is indicated by black circle. Map: M. Olonova.
Acknowledgements
We are grateful to Dr. G.A.Lazkov (Institute for Biology & Pedology, National Academy of Sciences of Kyrgyzstan),
Prof. M.G.Pimenov, Prof. V.G.Onipchenko, Prof. A.P.Sukhorukov, Dr. D.F.Lyskov (Lomonosov Moscow State
University, Russia), Prof. M.V.Olonova (Tomsk State University, Russia), Drs. E.A.Arhipova, Yu.I.Bulany (Saratow
State University, Russia), Dr. G.Yu.Klinkova (Volgograd State University, Russia), who collected the specimens
used in this study. We wish to thank the curators of the Herbarium of V.L.Komarov Botanical Institute (LE) Dr.
O.V.Cherneva, Dr. A.E.Borodina, Prof. V.I.Dorofeev, Dr. G.L.Kudryashova, the staff of the Herbaria of Lomonosov
Moscow State University (MW) and Tsitsin Main Botanical Garden RAS (MHA), Russia for their kind permission to
take samples for molecular investigations. We would like to thank Prof. M.V.Olonova for preparing the distribution
map. We thank Dr. M.A.Gitzendanner (University of Florida, USA) and Dr. Charlotte Germain-Aubrey (University
of Florida, USA) for helpful discussion. This work was supported in part by the Soltis Laboratory of Molecular
Systematics and Evolutionary Genetics (UF, FLMNH). We thank an anonymous reviewer and Dr. Alexander Sennikov
for useful suggestions and constructive criticism which helped to improve the text of the manuscript.
The molecular study was supported by the Russian Science Foundation (project № 14–50–00029) and the
morphological study was carried out in accordance to Government order for the Lomonosov Moscow State University
(project No. AAAA-A16-116021660045-2).
16 • Phytotaxa 268 (1) © 2016 Magnolia Press
YURTSEVA ET AL.
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20 • Phytotaxa 268 (1) © 2016 Magnolia Press
YURTSEVA ET AL.
APPENDIX 1. Taxa, voucher information, current sample and GenBank accession numbers used in the study. Herbarium
acronyms according to Index Herbariorum. Asterisked are sequences obtained from Genbank.
Taxon
Locality, voucher information (herbarium code)
Atraphaxis angustifolia Jaub. &
Spach
A. ariana (Grigorj.) T.M. Schust.
& Reveal
A. atraphaxiformis (Botsch.) T.M.
Schust. & Reveal
Armenia, Megri d. Zangezur Ridge. 1.06.1973.
Shvedchikova (MW)
Turkmenistan, [Badghys], v. Morgunovsky.
25.04.1988. Gorelova (LE)
Kyrgyzstan, Alay Ridge, Kadamzhay.
19.07.2005. Lazkov (FRU)
Yurtseva et al. 2010
Uzbekistan, Alay, Turkestan Ridge, the Isphara.
07.1970. Kamelin 532 (LE)
Kyrgyzstan, Alay Ridge, the Gulcha basin,
Irgailysu, Sufi-Kurgan. 16.07.1987. Pimenov &
Klujkov 407 (MW)
Kyrgyzstan, Osh reg., Kara-Kulzha d., Alay
Ridge, basin of the Gulcha river, 2 km N of v.
Gulcha.10.08.2011. Lazkov (MW)
Tavakkoli et al. 2015
Turkmenistan, Er Oylan-Duz. 21.04.1965.
Meschcheryakov (LE)
Turkmenistan, Badkhyz, fixed sands to S of
saline Namaksaar. 25.06.1976. Botschantsev
259 (LE)
Tavakkoli et al. 2015
A. atraphaxiformis (Botsch.) T.M.
Schust. & Reveal
A. avenia Botsch.
A. avenia Botsch.
A. aucherii Jaub. & Spach
A. badghysi Kult.
A. badghysi Kult.
A. binaludensis S.Tavakkoli,
Mozaff. & Kaz. Osaloo
A. bracteata Losinsk.
A. caucasica (Hoffm.) Pavlov
A. caucasica (Hoffm.) Pavlov
A. compacta (Hoffm.) Pavlov
A. decipiens Jaub. & Spach
A. fischeri Jaub. & Spach
A. fischeri Jaub. & Spach
A. fischeri Jaub. & Spach
A. frutescens (L.) K.Koch
A. frutescens (L.) K.Koch
A. frutescens (L.) K.Koch
A. frutescens (L.) K.Koch
A. frutescens (L.) K.Koch
A. intricata Mozaff.
A. kamelinii O.V.Yurtseva
China, Inner Mongolia, Ikodzhoumen.
10.08.1957. Petrow (MW)
Georgia, Akhaltsihe. 26.05.1973. Schvedchikova
(MW)
Russia, Daghestan, v. Untsukul, 7-8.07.1967.
Bekova (MHA)
Kazakhstan, Dzambul reg., Chu-Ili Mts.,
Sunkar-Tube (Khan-Tau). 14.05.1951. Pavlov
160 (MW)
Kazakhstan, Karaganda reg., Ulu-Tau Mts.
9.08.1957. Karamysheva 1979 (LE)
Russia, Volgograd reg., Kirov d., Bolshaya
Otrada. 7.05.09. Klinkova & Suprun 4 (MW)
Russia, Volgograd reg., Kirov d., Bolshaya
Otrada. 7.05.09. Klinkova & Suprun 2 (MW)
West Kazakhstan, Atyrau reg. Inder. 04.05.2011.
Onipchenko (MW)
West Mongolia, Mongol Altay, Bayan-Olygiy
aimag, the Bulgan river basin, Ikh-Dzhergalanta.
27.07.1988. Kamelin et al. 2298 (MW)
Russia, Saratov reg., Khvalynsky d., Elshanka.
04.07.2011. Bulany (MW)
China, Xinjiang. 2010. Olonova (MW)
Russia, Orenburg gub., Chkalovsk reg.,
Guberlinsky hills, 15 km W of Guberlinskaya.
23.06.1950. Kirikov (MW)
Russia, Orenburg reg., Saraktash d., 7 km SE
of v. Gavrilovka. S. part of Sambula hills.
31.05.2011. Abramova (MW)
Tavakkoli et al. 2015
Mongolia, [Hovd (=Kobdo) aimag], the
Dzungarian Gobi, S slope of Saertaengijin-Khuvch
Uul (Mts.) near junction to Khaldzan-Ula (Mts.),
27.07.1984. Daryima & Kamelin 765 (LE)
Sample
num-ber
4
rpl32-trnL(UAG)
trnL-trnF
KU724453
KU508756
122
KU724454
KU508757
41
KU724455
KU508758
43
KU724456
KU508759
58
KU724457
KJ690694
140
KX192201
KX192173
13
AB976694*
KU724458
—
KU508760
123
KX192202
KX192174
AB976695*
—
157
KU724459
KU508761
55
KX192203
KX192175
130
KX192204
KX192176
45
KX192205
KX192177
116
KX192206
KJ690701
19
KX192208
KX192179
20
KX192207
KX192180
33
KU724460
KJ690713
1
KX192209
KX192181
66
KX192210
KJ690700
67
97
KU724461
KX192211
KJ690702
KX192182
132
KX192212
KX192183
50
AB976698*
KX192213
—
KJ690709
...continued on the next page
ATRAPHAXIS (POLYGONEAE)
Phytotaxa 268 (1) © 2016 Magnolia Press • 21
APPENDIX 1. (Continued)
Taxon
Locality, voucher information (herbarium code)
A. karataviensis Pavlov & Lipsch.
Kazakhstan, Syr-Darya-Kara-Tau, Tersakkan,
rocks. 4.07.1974. Kamelin 1489 (LE)
Kyrgyzstan, Ichkem-Tau Mts., Orlovka.
07.1973. Kamelin (LE)
Kazakhstan, Syr-Darya, Kara-Tau, in cliff
Kantagy. 3.07.1974. Kamelin 1444 (LE)
Turkmenistan, the Central Kopet Dagh, GeokTepe d., Kara-Agach. 30.05.1972. Mesheryakov
(LE)
Turkmenistan, Kazandzhik d. Trgoy Mts. 11–
15.05.1981. Proskuryakova (MHA)
Kazakhstan, Dzhungar Alatau, Kaikan Mts,
Glinovka. 18.06.1959. Goloskokov (MW)
Kazakhstan, Talas Alatau, Aksu-Dzabagly,
pass Kshy-Kaindy, Akshy-Aksu. 11.08.1948.
Kultiasov (MW)
NE China, Manchzhuriya, E slope of Khingan,
Kogusten-Golt. 14.07.1899. Potanin & Soldatov
(LE)
Kazakhstan, Tian Shan, Zaily Alatau, Alma-Ata
d., Mt. Kok-Tebe. 24.05.1998. Majorov 98-24в
(MW)
Kazakhstan, Zaily Alatau, Bolshaya AlmaAtinka, 1.06.1967. Radugin (LE)
Mongolia, Uver-Khangay, S of Tugrek,
Bajangyin-Nuru (spurs of Dzegest-Ula).
27.07.1983. Gubanov 7471 (MW)
Russia, Khakassia, Shira d., Borets, right
board of the river Son. 15.08.1993. Pimenov
&Vasilieva (MW)
Mongolia, Central aimag, Telengyim-Baishin,
Mt. Dzamryn-Ula. 23.06.1988. Budantsev et al.
27 (MW)
Tadjikistan, Badakhshan, Schugnan d. the Gunt,
Vozh × Shtamm. 02.08.2011. Klujkov et al. 26
(MW)
Tadjikistan, Central Pamir, Bokhud-river, cliff
Bokhud. 16.07.1986. Fedorov (MW)
Kyrgyzstan, Chatkal Ridge, basin of Aflatun,
7.06.2011. Lazkov (MW)
Kyrgyzstan, Alay Ridge, Osh d., the Ak-Bura
river, influent Kyrk-Kege. 12.08.2011. Lazkov
(MW)
Tavakkoli et al. 2015
A. karataviensis Pavlov & Lipsch.
A. karataviensis Pavlov & Lipsch.
A. kopetdagensis Kovalevsk.
A. kopetdagensis Kovalevsk.
A. laetevirens Jaub. & Spach
A. laetevirens Jaub. & Spach
A. manshurica Kitag.
A. muschketowi Krasn.
A. muschketowi Krasn.
A. pungens (M.Bieb.) Jaub. &
Spach
A. pungens (M.Bieb.) Jaub. &
Spach
A. pungens (M.Bieb.) Jaub. &
Spach
A. pyrifolia Bunge
A. pyrifolia Bunge
A. pyrifolia Bunge
A. pyrifolia Bunge
A. radkanensis S. Tavakkoli, Kaz.
Osaloo & Mozaff.
A. replicata Lam.
A. replicata Lam.
A. replicata Lam.
A. rodinii Botsch.
A. rodinii Botsch.
A. seravschanica Pavlov
Kazakhstan, Usturt, Mangistau reg., Beyneu.
3.06.2003. Sukhorukov (MW)
Kyrgyzstan, Alay, the Gulcha, Kyzyl-Kurgan.
08.07.1986. Kuvaev 518-3 (MW)
Russia, Saratov reg., Krasnoarmeysk d.,
between Belogorskoye and Nizhnya Bannovka
21.07.2011. Arhipova (MW)
Turkmenistan, Badhyz, Pynhangeshme Ridge.
27.04.1978. Gorelova (LE)
Turkmenistan, Badhyz, Akar-Cheshme.
11.05.1976. Botchantsev 679 (LE) Isotypus
Kyrgyzstan, Susamyr Mts, Chichkan valley,
Toktogul. 7.06.1996. Pimenov & Klujkov K9659 (MW)
Sample
num-ber
47
rpl32-trnL(UAG)
trnL-trnF
KX192215
KX192184
100
KU724462
KU508762
101
KX192214
KX192185
19
KX192216
KX192186
133
KU724463
KU508763
109
KU724464
KU508764
111
KX192217
KX192187
15
KX192218
KX192188
41
KU724465
KJ690697
61
KX192219
KX192189
115
KX192220
KJ690710
135
KX192221
KX192191
136
KU724466
KU508765
36
KU724467
KJ690696
104
KX192222
KJ690695
137
KX192223
KX192192
138
KX192224
KX192193
AB976701*
—
24
KU724468
KJ690714
31
KU724469
KJ690716
65
KX192225
KJ690711
54
KX192226
KX192194
107
KX192227
KX192195
60
KX192228
KJ690692
...continued on the next page
22 • Phytotaxa 268 (1) © 2016 Magnolia Press
YURTSEVA ET AL.
APPENDIX 1. (Continued)
Sample
num-ber
98
rpl32-trnL(UAG)
trnL-trnF
KU724470
KJ690693
34
KU724471
KJ690715
53
KX192229
KX192196
110
KX192230
KX192197
141
KU724472
KU508766
AB976705*
—
114
KX192231
KX192198
142
KU724473
KU508767
35
KU724474
KU508768
12
KU724475
KU508769
52
KU724476
KU508770
99
KU724477
KU508771
126
KU724478
KU508772
143
AB976706*
KX192232
—
KX192199
144
KX192233
KX192200
AB976693*
—
Tavakkoli et al. 2015
Tavakkoli et al. 2015
Tavakkoli et al. 2015
AB976696*
AB976697*
AB976700*
—
—
—
Tavakkoli et al. 2015
Tavakkoli et al. 2015
Tajikistan, Khablon reg. Shuroabad d. the
Piandzh, Bakhorak × Bag. 25.07.2013.
Ukrainskaya et al. 12. (MW)
AB976702*
AB976699*
KU724452
—
—
KU508754
Taxon
Locality, voucher information (herbarium code)
A. seravschanica Pavlov
Kyrgyzstan, Chatkal Ridge, Alabuksay, Alabuk.
2.09.1982. Borodina, Philatova (LE)
West Kazakhstan, Mangystau reg. Beyneu.
07.05.2011. Onipchenko (MW)
Armenia, Azizbeck d., Gerger forest, East ArpaTchay. 4.09.1951. Surova (MW)
Daghestan, Usukh-Tchay, the Samur valley.
9.07.1940. Elenevsky (MW)
Armenia, Ararat reg. Gorevan. 13.08.2012.
Lyskov (MW)
Tavakkoli et al. 2015
A. spinosa L.
A. spinosa L.
A. spinosa L.
A. spinosa L.
Atraphaxis suaedifolia Jaub. &
Spach
A. teretifolia (Popov) Kom.
A. teretifolia (Popov) Kom.
A. toktogulica (Lazkov)
T.M.Schust. & Reveal
A. tortuosa Losinsk.
A. tortuosa Losinsk.
A. tortuosa Losinsk.
A. tournefortii Jaub. & Spach
A. tournefortii Jaub. & Spach
A. virgata (Regel) Krasn.
A. virgata (Regel) Krasn.
Polygonum aridum Boiss. &
Hausskn. ex Boiss.
P. botuliforme Mozaff.
P. dumosum Boiss.
P. khajeh-jamali Khosravi &
Poormahdi
P. salicornioides Jaub. & Spach
P. spinosum H.Gross
Bactria ovczinnikovii (Czhukav.)
O.V. Yurtseva & E.V. Mavrodiev
(= Polygonum ovczinnikovii
Czukav.)
Kazakhstan, Karaganda reg. Navaly-Sora,
Mointy. 29.05.1951. Pavlov 382 (MW)
Kazakhstan, Karaganda reg., Dzheskazgan ×
Ula-Tau. 23.06.1958. Rachkovskaya 6185 (LE)
Kyrgyzstan, Susamyr Ridge, Kara-Dzhigach.
7.07.2005. Lazkov (FRU)
Mongolia, South Gobi aimag, SE of Nomgon,
Shilt-Ula Mt. 19.07.1974. Rachkovskaya &
Volkova 6525 (LE)
Mongolia, East Gobi aimag, SW of Khuvsgul.
30.07.1971. Isachenko & Rachkovskaya 1891
(LE)
Mongolia, South Gobi aimag, SE of KhanBogd.. 1972. Rachkovskaya & Guricheva 21581
(LE)
Turkey, Yozgat. 13.06.1975. Browicz & Zielinski
582 (LE)
Tavakkoli et al. 2015
Kazakhstan, South-Kazakhstan reg., Tulkubass
d., the riverheads of Mashat, 29.09.2012.
Sagalaev (MHA)
Kyrgyzstan, Kyrgyz Ridge, environs of
Bishkek. 18.06.2011. Lazkov (MW)
Tavakkoli et al. 2015
ATRAPHAXIS (POLYGONEAE)
134
Phytotaxa 268 (1) © 2016 Magnolia Press • 23
APPENDIX 2. Origin of the material used for LM micrographs and measurements in Table 3.
Atraphaxis compacta (Hoffm.) Pavlov. Kazakhstan, Dzambul reg., Chu-Ili Mts., Sunkar-Tube (Khan-Tau). 14.05.1951.
Pavlov 160 (MW)
Atraphaxis kamelinii O.V.Yurtseva. Mongolia, [Khovd (=Kobdo) aimag], the Dzungarian Gobi, S slope of SaertaengijinKhuvch Uul (Mts.) near junction to Khaldzan-Ula (Mts.), 27.07.1984. Daryima & Kamelin 765 (LE)
Atraphaxis replicata Lam. Kyrgyzstan, Alay, the Gulcha, Kyzyl-Kurgan. 08.07.1986. Kuvaev 518-3 (MW)
Atraphaxis pungens (M.Bieb.) Jaub. & Spach. Russia, Tuva Republic, Ulug-Khem d., Eastern slope of Tuva Basin to
the river Senek. 25.06.1977. Neifeld & Margasova (MHA)
Atraphaxis pungens (M.Bieb.) Jaub. & Spach. Mongolia, The south of Bulgan aimag, Northern spurs of Khangay,
90 km to SEE of Kharkhorin, southern macroslope of Mt. Tsetserleg, near the former Buddhist monastery. 3.07.1980.
Gubanov 3563 (MW)
Atraphaxis pungens (M.Bieb.) Jaub. & Spach. Russia, Tuva Republic, Ulug-Khem d., Uyuk ridge, southern slope,
near Bayan-Kol ferry, stony steppe. 6.08.1976. Lomonosova & Ivanova 2408 (MHA)
Atraphaxis pungens (M.Bieb.) Jaub. & Spach. Mongolia, Khovd aimag, 90 km to S of somon Bulgan, foothill plain
of Baytag-Bogdo ridge. 9.08.1977. Volkova &.Rachkovskaya 7373 (LE).
Atraphaxis pungens (M.Bieb.) Jaub. & Spach. Russia, Tuva Republic, Ulug-Khem d., environs of Shagonar, stony
slope of hills. 15.06.1977. Maltseva & Selisheva (MW)
Atraphaxis virgata (Regel) Krassn. Mongolia, Transaltay Gobi, Gobi-Altay aimag, Atas-Bogdo-Ula Mts. In hollows
on the slopes at an altitude of 1300-1600 m. a.s.l. 1.08.1978. Gubanov 2634 (MW).
24 • Phytotaxa 268 (1) © 2016 Magnolia Press
YURTSEVA ET AL.
Olga V. Yurtseva