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Pollen morphology and of (Polygoneae, )

O. V. Yurtseva, E. E. Severova & I. Yu. Bovina

Plant Systematics and Evolution

ISSN 0378-2697 Volume 300 Number 4

Plant Syst Evol (2014) 300:749-766 DOI 10.1007/s00606-013-0917-4

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Plant Syst Evol (2014) 300:749–766 DOI 10.1007/s00606-013-0917-4

ORIGINAL ARTICLE

Pollen morphology and taxonomy of Atraphaxis (Polygoneae, Polygonaceae)

O. V. Yurtseva • E. E. Severova • I. Yu. Bovina

Received: 21 June 2013 / Accepted: 7 September 2013 / Published online: 15 October 2013 Ó Springer-Verlag Wien 2013

Abstract Pollen grains of 32 of Atraphaxis L. characters and probable interspecific hybridization. The including six species previously attributed to L. Atraphaxis L. comprises about 30 species distributed s.str. were investigated with LM (acetolysed pollen) and throughout Southeastern , Southwestern and Central SEM (dry pollen). Pollen grains of all studied species are Asia, South Siberia, Mongolia, and China (Pavlov 1936; spheroidal to oblong-spheroidal, mostly tricolporate, rarely Borodina 1989; Lovelius 1979). 4-6-loxocolporate, ellipsoidal in equatorial view, rounded- Based on the presence of shrubby life form and woody trilobed or trilobed in polar view, with striate or striato- pith parenchyma, Dammer (1893) attributed Atraphaxis, perforate, reticulato-foveolate, or reticulato-perforate Pteropyrum Jaub. et Spach and Calligonum L. to the tribe sporoderm ornamentation. Exine sculpture is the most Atraphaxideae, while Perdrigeat (1900) moved them to the variable feature, differing in width, distinctness, and tribe Calligoneae, and Gross (1913)—to subtribe Atraph- spacing of the striae, which are divided by grooves with axinae of the tribe Polygoneae. Haraldson (1978) specu- small pits or perforations in rows. The most distinct vari- lated that Atraphaxis was an ancestor of Polygonum L. ants of sporoderm ornamentation are connected by a full s.str., on the basis of both sharing lignificated collenchyma, range of transitions. Striato-perforate ornamentation is assimilation tissue and absciss layer in the , assim- common in species with the perianth typical for ilation tissue in the stem and both lacking trichomes on the Atraphaxis, whereas reticulato-foveolate or reticulato-per- filaments. Atraphaxis and Polygonum L. s.str. possess forate sporoderm ornamentation was found in species with thyrses with axillary cymes of flowers (Gross 1913). the perianth of Polygonum-type. Similarity of Atraphaxis, Polygonum L. s.str. and Polygo- nella Michx. was demonstrated in petiole and stem anat- Keywords Atraphaxis Á Polygonum Á Polygonaceae Á omy, and in the structure of perianth and fruit (Haraldson Pollen Á Sporoderm Á Taxonomy 1978; Ronse Decraene and Akeroyd 1988; Ronse Decraene et al. 2000). The genus Polygonum L. s.str. has the cam- panulate perianth with a short and wide tube and oblong Introduction of equal size, the genus Atraphaxis differing by the perianth with a long filiform tube and 4–5 tepals, the inner The taxonomy of the genus Atraphaxis L. is complex ones becoming significantly enlarged in fruiting (Linnaeus and uncertain due to high variability of morphological 1753; Boissier 1879; Brandbyge 1993). Recent molecular-phylogenetic reconstructions based on chloroplast genes (rbcL, matK, trnL, trnF), nuclear gene O. V. Yurtseva (&) Á E. E. Severova Á I. Yu. Bovina LEAFY and ITS 1–2 sequences confirmed that Atraphaxis Department of Higher , Faculty of Biology, is closely related to Polygonum L. s.str. and Polygonella Lomonosov Moscow State University, Leninskie Gory, 1-12, 119 991 Moscow, Russia Michx., all three attributed to the tribe Polygoneae along e-mail: [email protected] with Knorringia (Chukav.) Tzvelev, Adans., E. E. Severova Meisner, Houtt., and e-mail: [email protected] T.M.Schust., whereas Calligonum and Pteropyrum belong 123 Author's personal copy

750 O. V. Yurtseva et al. to the tribe Calligoneae (Lamb Frye and Kron 2003; San- blades served as a basis for recognition of three sections chez et al. 2009, 2011; Schuster et al. 2011a, b). The (Aleshina et al. 1978; Lovelius and Sjabrjaj 1981). Section affinity of Atraphaxis and Polygonum was confirmed by the Atraphaxis L. (A. spinosa, A. replicata, A. karataviensis, analysis of chloroplast regions (Tavakkoli et al. 2010; Sun A.compacta) with dimeric flowers and short lateral thyrses and Zhang 2012). is characterized by spheroidal slightly trilobed pollen with Our phylogenetic investigations of the tribe Polygoneae small endoapertures and distinct columellae with closed based on nuclear ITS 1–2 sequences showed the affinity capita. Section Tragopyrum (Bieb.) Meissn. (A. musch- of Atraphaxis to Fallopia, Polygonella, and Polygonum ketowi, A. caucasica, A. pyrifolia, A. laetevirens, A. bil- (Yurtseva et al. 2010, 2012a, b, c). In ML-tree three species lardierei, A. avenia, A. frutescens, and A. badhysi) with of Polygonum (Polygonum arianum Grigorj., P. atraphax- pentamerous perianth, trimeric , and long lateral iforme Botsch., and P. toktogulicum Lazkov) entered the and terminal thyrses differs by distinctly trilobed pollen clade of Atraphaxis. Schuster et al. (2011b) transferred grains with elliptic endoapertures and thin columellae with them to the genus Atraphaxis with new nomenclature slightly closed capita. Atraphaxis teretifolia (Popov) combinations. Our recent analysis based on the extended Komarov ex Pavlov (=Atraphaxis jrtyschensis Chang data on ITS 1–2 fragments (Yurtseva et al. in preparation) Y.Yang & Y.L.Han) from monotypic section Physopyrum showed that in ML-tree Atraphaxis atraphaxiformis (Popov) Lovelius differs by lineate leaves and has small (Botsch.) T.M.Schust. & Reveal (=Polygonum atraphaxi- oblong slightly trilobed pollen grains with distinct endo- forme Botsch.), Atraphaxis toktogulica (Lazkov) apertures and thin columellae with non closed capita. Bo- T.M.Schust. & Reveal (=Polygonum toktogulicum Lazkov), vina (1996) studied sporoderm sculpture (SEM) of 21 Atraphaxis tortuosa Losinsk. (=Polygonum tortuosum species of Atraphaxis from the territory of the former (Losinsk.) Lovelius), and Atraphaxis ariana (Grigorj.) USSR and described four types of sporoderm ornamenta- T.M.Schust. & Reveal (=Polygonum arianum Grigorj.) are tion, which do not consistent with sections or subgenera nested among typical members of Atraphaxis, while within the genus. P. ovczinnikovii Chukav. occupies basal position in the Bao and Li (1993) studied sporoderm of pollen grains clade of Atraphaxis. Hereafter these species will be treated (SEM) in ten species of Atraphaxis from China and dis- as the members of the genus Atraphaxis. These taxa as well tinguished two types of the sporoderm ornamentation: as P. popovii Borodina are characterized by campanulate striate (A. pungens, A. jrtyschensis, A. laetevirens, A. deci- perianth typical for the genus Polygonum; therefore, they piens, A. pyrifolia) and striato-reticulate (A. frutescens, were initially or later classified as the members of the genus A. spinosa, A. compacta, A. bracteata, A. manshurica), Polygonum (Grigorjev 1933; Komarov 1936; Chukavina which do not correspond to the taxonomic division of the 1962, 1968, 1971; Botschantzev 1965; Lovelius 1975; genus Atraphaxis. Ge and Liu (1994) studied pollen grains Borodina 1989; Lazkov and Sultanova 2002). in 12 species of Atraphaxis from China. In most of The genus Atraphaxis L. was formed by combining the the studied species the pollen grains were prolate or sub- genera Tragopyron Bieb. and Atraphaxis L. by Jaubert and prolate with striate sporoderm ornamentation (A. replicata, Spach (1844–1846) who subdivided Atraphaxis into sub- A. spinosa, A. compacta, A. laetevirens, A. virgata, genera Euatraphaxis, Tragatraphaxis, and Tragopyrum. A. frutescens, A. decipiens, A. jrtyschensis, A. pungens, Later, taxonomists recognized two to five sections or sub- A. muschketowi, A. pyrifolia), with an exception of genera in the genus Atraphaxis based on flower merosity and A. bracteata that differs from other species by more inflorescence structure (Meisner 1857; Boissier 1879;Kras- elongated pollen (P:E = 1.88) with striato-reticulate nov 1888; Pavlov 1936; Aleshina et al. 1978; Lovelius 1979). ornamentation. Zhou et al. (1999) characterized pollen The data on pollen grains of Atraphaxis are incomplete surface of A. manshurica and A. laetevirens as striato- and often controversial. Pollen grains were described for perforate. some species as 3-(4)-colporate, spheroidal-prolate or Borzova and Sladkov (1969) showed that pollen of prolate, rounded or elliptical in equatorial view, round- Polygonum ovczinnikovii (=Atraphaxis ovczinnikovii) and trilobed in polar view, with striate, reticulato-striate, stri- P. atraphaxiforme (=A. atraphaxiformis) differ from pol- ato-perforate or striato-foveolate ornamentation (Nowicke len of other members of the genus Polygonum by and Skvarla 1977; 1979; Kupriyanova and Aleshina 1978; fine characteristics of exine structure. According to Bao Ryabkova 1987; Bao and Li 1993; Filina et al. 1994; Hong (1993), sporoderm ornamentation of A. tortuosa Losinsk. 1995; Bovina 1996). (=P. intramongolicum Fu & Zhao) and Polygonum gla- Aleshina et al. (1978) described the pollen (LM) of 18 reosum Schischk. differs from striate surface of the most species of the genus Atraphaxis from the territory of the species of Atraphaxis. Our own preliminary study of pollen former USSR. Fine characteristics of exine structure along morphology of A. atraphaxiformis, A. toktogulica, A. tor- with the morphology of flowers, inflorescences, and leaf tuosa, and A. ariana previously placed into the genus 123 Author's personal copy

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Table 1 Summary of pollen morphological data for Atraphaxis Species Polar axis (P, Equatorial P/E No. of Abnormal Exine lm) mean diameter (E, mean ectoapertures morphology thickness min–max lm) mean (lm) min–max

A. angustifolia Jaub. et Spach. 35.6 30.4 1.17 3 2.4 31.8–38.7 27.5–34.4 A. ariana (Grigorj.) T.M.Schust. & Reveal 30.7 25.8 1.19 3 1.60 (= Polygonum arianum Grigorj.) 28.5–32.1 24.1–29.2 A. atraphaxiformis (Botsch.) T.M.Schust. & Reveal 30.2 26.6 1.13 3 1.80 (= Polygonum atraphaxiforme Botsch.) 29.5–31.1 25.4–27.4 A. aucherii Jaub. et Spach 26.1 21.0 1.20 3 Loxocolporate 1.93 23.7–27.6 19.2–22.6 (70 %), syncolporate A. avenia Botsch. 33.5 26.2 1.28 3 2.90 31.8–34.4 23.2–28.3 A. badghysi Kult. (Botschantzev 281 LE) 31.3 27.0 1.15 3 Partly rugulate 2.25 25.8–33.1 20.6–30.1 A. billardierei Jaub. et Spach 22.2 22.07 1.06 [3 Loxocolporate 1.88 20.9–23.7 (80–90 %), some syncolporate A. bracteata Losinsk. 27.5 23.3 1.18 3 1.79 24.3–30.7 20.3–28.7 A. caucasica (Hoffm.) Pavlov 30.4 25.2 1.20 3 2.20 27.0–34.4 18.6–30.9 A. canescens Bunge 31.8 23.8 1.34 [3 Loxocolporate 2.04 25.8–35.7 17.2–27.5 (100 %), syncolporate A. compacta Ledeb. 35.5 29.0 1.22 >3 Loxocolporate 2.35 (50 %) 29.0–45.6 20.6–38.1 A. daghestanica (Lovelius) Lovelius (Mailov MHA) 23.3 20.3 1.15 3 1.30 22.1–24.3 19.2–21.2 A. daghestanica (Lovelius) Lovelius (Guseinov and 29.7 25.5 1.16 3 2.13 Tzvelev 723 LE) 29.0–30.1 24.9–25.7 A. decipiens Jaub. et Spach 30.2 28.6 1.05 3 Loxocolporate, 2.25 28.0–32.6 25.8–31.8 syncolporate A. frutescens (L.) K.Koch 25.9 26.4 1.02 [3 Loxocolporate, 1.75 syncolporate 20.8–31.9 19.6–30.0 A. karataviensis Pavlov & Lipsch. 36.3 31.2 1.16 [3 Loxocolporate 2.2 31.8–40.4 29.7–34.4 (25 %), partly syncolporate A. kopetdagensis Kovalevsk. 28.9 26.6 1.09 3 2.13 25.3–35.3 24.9–31.8 Atraphaxis laetevirens (Ledeb.) Jaub. et Spach 36.6 26.5 1.38 3 2.15 31.6–47.3 23.2–33.5 A. lanceolata (Bieb.) Meisn. 33.1 28.9 1.14 3 2.44 30.9–37.5 26.7–32.7 A. muschketowi Krasn. 32.5 27.9 1.12 [3 Syncolporate 2.43 27.6–35.7 25.8–30.7 (10–15 %) A. ovczinnikovii (Czukav.) O.V.Yurtseva 29.5 24.9 1.18 3 1.70 (= Polygonum ovczinnikovii Czukav.) 28.0–30.7 23.4–26.3

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Table 1 continued Species Polar axis (P, Equatorial P/E No. of Abnormal Exine lm) mean diameter (E, mean ectoapertures morphology thickness min–max lm) mean (lm) min–max

A. pungens (Bieb.) Jaub. et Spach 27.7 26.3 1.06 3 2.01 25.8–31.8 24.5–27.9 A. pyrifolia Bunge 26.8 22.6 1.18 3 1.66 24.0–29.2 18.9–29.2 A. replicata Lam. 27.1 23.3 1.16 3 1.90 21.5–30.9 18.9–27.5 A. rodinii Botsch. 38.5 31.6 1.21 [3 Loxocolporate, 2.25 35.0–43.0 28.0–36.6 syncolporate, ring-like form of ectoapertures (100 %) A. seravschanica Pavlov 44.9 36.5 1.23 3 3.01 40.0–49.0 30.5–40.0 A. spinosa L. (Klinkova and Suprun MW) 22.5 20.3 1.10 3 1.30 19.8–24.2 17.5–23 A. spinosa L. (Onipchenko MW) 24.3 21.9 1.10 3 1.61 22.1–25.5 20.4–23.1 A. spinosa L. (Shvedchikova MW) 33.0 26.8 1.10 [3 Loxocolporate 2.20 30.1–34.6 24.9–31.6 (100 %), syncolporate A. spinosa L. (Artemenko MW) 35.6 28.6 1.25 [3 Loxocolporate 1.96 31.0–39.7 23.6–31.9 (50 %) A. teretifolia (Popov) Komarov ex Pavlov 26.8 23.6 1.14 [3 Loxocolporate 1.45 (= A. jrtyschensis Chang Y.Yang & Y.L.Han) 25.1–28.2 22.1–25.3 (100 %), syncolporate, ring-like form of ectoapertures A. toktogulica (Lazkov) T.M.Schust. & Reveal 28.2 24.5 1.15 3 2.02 (= Polygonum toktogulicum Lazkov) 26.4–31.0 24.1–29.5 A. tortuosa Losinsk. (= Polygonum intramongolicum 29.7 24.1 1.23 3 Some regulate, 2.04 Fu & Zhao; = P. tortuosum (Losinsk.) Lovelius) 27.5–34 21.9–25.1 warped A. virgata (Regel.) Krasn. 26.3 22.6 1.16 3 Loxocolporate, 2.21 23.2–28.8 20.6–24.0 syncolporate, ring-like-form of ectoapertures

Polygonum showed that their pollen grains are similar to data and with the results of own molecular-phylogenetic the pollen of Atraphaxis (Yurtseva et al. 2012b). analysis. Given that the palynological characteristics of the genus Atraphaxis proved to be important for its intrageneric taxonomy, the objectives of this study were, first, to Materials and methods examine pollen morphology of as many as possible mem- bers of the genus Atraphaxis, including the species for- We examined the specimens of 32 species of Atraphaxis, merly placed into the genus Polygonum, using light and including 6 species of Polygonum: 35 specimens with scanning electron microscopy; second, to compare pollen light microscopy (LM), and 38 specimens with scanning characteristics of the species with the taxonomical structure electron microscopy (SEM). Pollen samples were of the genus Atraphaxis that is based on morphological obtained from the palynological collection of the

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Fig. 1 LM micrographs of pollen grains of Atraphaxis L. a–c A. (Botschantzev 281 LE). k A. ariana (=P. arianum) (Chukavina 800 ovczinnikovii (=P. ovczinnikovii) (Nepli LE). d A. atraphaxiformis LE). l A. teretifolia (Pavlov 333 MW). m A. karataviensis (Bots- (=P. atraphaxiforme) (Abdusaljamova 65 LE). e–g A. toktogulica chantzev and Kamelin 392 LE). n A. spinosa (Artemenko MW). o A. (=P. toktogulicum) (Aidarova et al. LE). h A. angustifolia (Ter- spinosa (Klinkova and Suprun MW). p A. spinosa (Onipchenko MW). Minosyan LE). i A. aucherii (Aucher-Eloy 3271 LE). j A. badghysi To the same scale; scale bar is 10 lm

Department of Higher Plants, Biological Faculty, Lo- Light microscopy (LM) monosov Moscow State University, or received from a number of herbaria, i.e., Komarov Botanical Institute, St. Pollen samples were acetolyzed according to standard Petersburg, Russia (LE), Lomonosov Moscow State Uni- method (Erdtman 1971): dry anthers were placed in the versity, Moscow, Russia (MW), Tsitsyn Botanical Gar- glacial acetic acid for 12 h, incubated in the mixture of den, Moscow, Russia (MHA), and Botanical Institute of concentrated sulphuric acid and acetic anhydride (1:9) at the Tajikistan Academy of Sciences, Dushanbe, Tajikistan 95 °C for 5 min in a water bath, and then centrifugated. (TAD). The specimens used in the study are listed in The supernatant was discharged, and the sediment washed ‘‘Voucher information’’. three times by distilled water, and placed in glycerine.

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Fig. 2 LM micrographs of pollen grains of Atraphaxis L. a A. frutes- (Mailov MHA). i A. kopetdagensis (Germ. 527 LE). j A. pyrifolia cens (Kuminova and Kuprianov MW). b A. virgata (Soskov TAD). (Alferova and Udintseva MHA). k A. bracteata Gubanov and Grubov c A. decipiens (Nikiforov MHA). d A. muschketowi (Trubacheva I89 MW). l A. rodinii (Gorelova 2198 LE). To the same scale; scale MW). e–g A. pungens (Khanminchun 4821 MW). h A. daghestanica bar is 10 lm

Then the pollen was mounted in glycerol jelly on glass 15–20 kV. The terminology follows that of Hesse et al. slides (Wodehouse 1959). Observations and measurements (2009), and Kupriyanova and Aleshina (1972) were made with stereoscopic light microscope Leica DME. Ten regularly shaped and fully expanded pollen grains were measured in each sample. All the measurements were Results and discussion made at the magnification of 4009, and the averages of ten values are presented in Table 1. LM-images were made Pollen characteristics of Atraphaxis and related species with stereoscopic light microscope Carl Zeiss AXIO- of Polygonum PLAN-2 at the magnification of 1,0009. Pollen grains of all investigated species of Atraphaxis and Scanning electron microscopy (SEM) Polygonum have similar morphology. They are tricolpo- rate, spheroidal or oblong-spheroidal (P/E = 1.2–1.4), Pollen was extracted from dry anthers, transferred onto elliptical or almost circular in equatorial view, rounded- aluminium stages, and glued to a drop of varnish nail, then trilobed or trilobed in polar view. The colpi (ectoapertures) coated with gold or alloy of platinum and palladium using are distinct, deep, and long. The ora are distinct, lalongate JFC-1100E sputter and studied under the scanning elec- or circular. The exine is tectate, two-layered, columellate, tronic microscopes Camscan-S2 and JEOL JSM-6380LA at and the sexine is slightly thicker than the nexine (Figs. 1, 2).

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Fig. 3 SEM micrographs of pollen grains of Atraphaxis L. a normal with ring-like form of ectoapertures of A. muschketowi. d loxocolpo- tricolporate pollen grains of A. spinosa. b–f irregularities in the rate, syncolporate pollen grains of A. frutescens. e syncolporate and number and position of apertures. b loxocolporate, syncolporate hexacolporate pollen grains of A. rodinii. f pollen grain with ring-like pollen grains and pollen with ring-like form of ectoapertures of form of ectoapertures of A. teretifolia A. spinosa. c loxocolporate, syncolporate pollen grains and pollen

The surface of sporoderm is striate, striato-perforate, re- syncolporate, or with ring-like form of ectoapertures. ticulato-foveolate, or reticulato-perforate, with distinct or Aberrant pollen grains were detected in half of the species smoothened striae and small pits or perforations between listed in Table 1. the striae (Figs. 3–9). Samples of A. aucherii, A. billardierei, A. canescens, A. rodinii, A. spinosa (Shvedchikova MW), and A. teretifolia Pollen size contain more than 50 % of aberrant pollen grains. In the samples of A. compacta, A. decipiens, A. frutescens, A. The species of Atraphaxis vary in pollen size (Table 1). karataviensis, A. muschketowi, A. spinosa (Artemenko The majority of them have pollen with P = 25–34 lm. MW), and A. virgata the portion of loxocolporate pollen Small pollen grains (P = 22–24 lm) were found in A. bil- grains does not exceed 50 %. Aberrant pollen grains were lardierei, one of two samples of A. daghestanica, and in detected among the species with both large and small two of four samples of A. spinosa, which are presumably pollen grains (Table 1; Fig. 3a–f; Fig. 6g, h, l, n; Fig. 9f, i). diploids. Putative polyploid samples of A. daghestanica (Guseinov and Tzvelev 723 LE) and A. spinosa (Shvedc- The ornamentation of sporoderm hikova MW; Artemenko MW) have larger pollen grains. Atraphaxis angustigolia, A. replicata, A. compacta, The majority of the species of Atraphaxis and some species A. karataviensis, A. laetevirens, and A. rodinii have pollen previously attributed to Polygonum have striate or striato- grains with P = 35–39 lm. Atraphaxis seravschanica has perforate ornamentation, with rows of pits or perforations the largest pollen grains (P = 44–45 lm). Together with between the striae. The length and width of the striae, their A. avenia it has maximal thickness of exine (Table 1). density and orientation, the size and number of pits and A. ovczinnikovii, A. toktogulica, A. atraphaxiformis, perforations are highly variable. The pits are circular and A. tortuosa, and A. ariana, previously attributed to some are perforated. The size and shape of perforations and Polygonum, have medium size pollen (P = 29–31 lm). the proportion of perforated pits vary even within a single sample of one species. The striae can be straight or Irregularities in the number and position of apertures branching, protruded or smooth and plane. They are ori- ented mainly meridionally at mesocolpium and chaotically Many species have deviations from the normal pollen at apocolpium, but sometimes the orientation of the striae morphology in the number and position of ectoapertures. varies within one pollen grain. Some species previously Along with tricolporate pollen predominating in the most attributed to Polygonum on the basis of perianth mor- of the species, some samples include pollen grains phology possess reticulato-foveolate or reticulato-perforate with more than three ectoapertures: 4-6-loxocolporate, pollen surface. 123 Author's personal copy

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Fig. 4 SEM micrographs of tricolporate pollen grains of Atraphaxis L. striato-perforate ornamentation with smoothened widely spaced striae. a, d, g, j, l, n equatorial view; b, e, h polar view; c, f, i, k, m, o sporoderm j, k A. tortuosa, striato-perforate ornamentation with smoothened ornamentation. a–c A. ovczinnikovii, reticulato-foveolate ornamenta- widely spaced striae. l, m A. popovii, reticulato-foveolate ornamenta- tion with 4-6-angular pits. d–f A. toktogulica, reticulato-foveo- tion with 4-5-angular pits. n, o A. angustifolia, striato-perforate late ornamentation with polygonal lumina. g–i A. atraphaxiformis, ornamentation with smoothened widely spaced striae

Depending on the distinctness of the striae, size, and the (=P. ovczinnikovii), A. popovii (=P. popovii) number of perforations and pits in rows, several variants of (Fig. 4a–c, l, m). Both species have Polygonum-type sporoderm ornamentation are recognized. campanulate perianth. 2. Reticulato-perforate ornamentation with polygonal 1. Reticulato-foveolate ornamentation with 4-5-6-angular shallow lumina with a single (rarely two) perforation pits. The lumina are sharply defined or smoothened at in the center. Adjacent lumina are arranged in rows of edges, rarely perforated at the bottom, and perforations 2–3 (4) oriented meridionally and divided laterally are few and small, mainly single at the lumina. This by hardly visible smoothened striae 0.05 lm thick. type of ornamentation was detected in A. ovczinnikovii

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Fig. 5 SEM micrographs of tricolporate pollen grains of Atraphaxis striae and slit-like grooves. g, h A. ariana, striato-perforate L. a, c, e, g, i, k equatorial view; b, d, f, h, j, l sporoderm ornamentation with distinct intensively branching striae. i, j A. ornamentation. a, b A. aucherii, striato-perforate ornamentation with teretifolia, striato-perforate ornamentation with distinct intensively smoothened widely spaced striae. c, d A. badghysi, striato-perforate branching striae. k, l A. karataviensis, striato-perforate ornamentation ornamentation with smoothened widely spaced striae. e, f A. with distinct intensively branching striae badghysi, striato-foveolate ornamentation with smoothened merging

The perforations are numerous and large. This type of A. badghysi besides the normal pollen contains pollen pollen surface was found in A. toktogulica (=P. grains with striato-foveolate (see 7 below) or rugulate toktogulicum) (Fig. 4d–f). pollen surface (Fig. 5e, f). 3. Striato-perforate ornamentation with widely spaced 4. Striato-perforate ornamentation with distant, distinct, smoothened striae divided by shallow grooves wider protruding, 0.25–0.4 lm thick, intensively branching than striae. The striae are narrow (0.10–0.25 lm), and merging striae. The grooves between the striae are as meridionally oriented at the mesocolpium. The wide as the striae and contain 2–7 (10) pits or small grooves formed by 2–6 adjacent lumina contain 2–6 perforations in a row (rarely in two rows) at the bottom. pits or perforations located in a row. The perforations This type of surface was found in A. ariana (=P. are small, rounded, varying in number. This type was arianum) with the perianth of Polygonum-type and found in A. atraphaxiformis, A. tortuosa with the linear leaves (Fig. 5g, h), and in many species of Polygonum-type perianth (Fig. 4g–i, j, k), and in Atraphaxis. Among them there is A. teretifolia, a single A. angustifolia, A. aucherii, and A. badghysi charac- representative of the section Physopyrum (Fig. 5i, j). terized by the Atraphaxis-type perianth and linear This type of pollen surface is typical for all members of leaves (Fig. 4n, o; Fig.5a–d). One of the samples of the section Atraphaxis with dimeric gynoecium and

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Fig. 6 SEM micrographs of pollen grains of Atraphaxis L. a, d, e, g, (Onipchenko MW). g–i syncolporate pollen grain of A. spinosa h, j, l, n equatorial view; b polar view; c, f, i, k, m, o striato-perforate (Nenevsky MW). j, k tricolporate pollen grain of A. compacta sporoderm ornamentation with distinct thin striae. a–c tricolporate (Chilikina 46 MW). l, m loxocolporate pollen grain of A. canescens pollen grain of A. spinosa (Klinkova and Suprun MW). d tricolporate (Pavlov 167 MW). n, o loxocolporate pollen grain of A. frutescens pollen grain of A. replicata. e, f tricolporate pollen grain of A. spinosa (Ogureeva 7772 MW)

shorter lateral thyrses: A. karataviensis (Fig. 5k, l), A. decipiens (Fig. 7e, f), and the species with lateral A. spinosa (Fig. 6a–c, e, f, g–i), A. replicata (Fig. 6d), thyrses, such as A. pungens (Fig. 7g, h), A. muschketowi A. compacta (Fig. 6j, k), and A. canescens (Fig. 6l, m), (Fig. 7i, j), A. caucasica (Fig. 8a, b), A. laetevirens and for many members of the section Tragopyrum with (Fig. 8c, d), A. daghestanica (Fig. 8e, f). A half of pollen trimeric gynoecium. Among them there are species with grains of A. muschketowi possess aberrations in the terminal thyrses, such as A. frutescens (Fig. 6n, o), ectoaperture form (Fig. 3c) and abnormal surface with A. lanceolata (Fig. 7a, b), A. virgata (Fig. 7c, d), and locally dilatated striae 0.4–1 lm thick (Fig. 7k, l).

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Fig. 7 SEM micrographs of pollen grains of Atraphaxis L. a, c, e, g, tricolporate pollen grain of A. pungens. i–l syncolporate (i) and i, k equatorial view; b, d, f, h, j, l sporoderm ornamentation. a, b tricolporate (k) pollen grain of A. muschketowi with thin striae (j) and tricolporate pollen grain of A. lanceolata, c, d syncolporate pollen locally dilatated (l) striae grain of A. virgata. e, f tricolporate pollen grain of A. decipiens. g, h

5. Striato-perforate ornamentation with the striae (Fig. 9a–c), A. pyrifolia (Fig. 9d, e), A. tournefortii 0.10–0.20 lm thick, distinct and protruding, mainly (Fig. 9h, k), chaotic orientation—in A. billardierei short and straight, divided by deep short grooves with (Fig. 9f, g). 2–4 (rarely more) large perforations in a row. This type 7. Striato-foveolate ornamentation with the striae was found in presumably closely related species A. 0.25–0.6 lm thick, smoothened, merging or contact- kopetdagensis (Fig. 8g, h), A. avenia (Fig. 8i, j), and ing laterally, divided by narrow grooves. The grooves A. seravschanica (Fig. 8k, l). Sporoderm ornamenta- are small, slit-like, meridionally or equatorially tion of A. kopetdagensis is distinct due to especially oriented, the pits or perforations are hardly visible. large perforations, divided by thin bridges in a groove, This type of ornamentation was found in the pollen of so that the surface is similar to the dual reticulum. A. rodinii (Fig. 9i, l), in one sample of A. badghysi 6. Striato-perforate ornamentation with wide plane striae (Fig. 5e, f) together with the pollen with striato- 0.4–0.7 lm thick, divided by deep narrow grooves. perforate surface (variant 3, Fig. 5c, d), and in The striae are distinct, protruding, oriented chaotically A. tournefortii (Fig. 9j) along with the pollen with or meridionally, the perforations in the bottom of the striato-perforate surface (Fig. 9h, k). This ornamenta- grooves sometimes are hardly visible. Meridional tion may be the result of irregularities in the course of orientation of the striae was found in A. bracteata sporoderm development.

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Fig. 8 SEM micrographs of the pollen of Atraphaxis L. a, c, e, g, i, grooves with 2–4 perforations. a, b A. caucasica. b, c A. laetevirens. k tricolporate pollen in equatorial view; b, d, f striato-perforate e, f A. daghestanica (Bekova MHA). g, h A. kopetdagensis. sporoderm ornamentation with long chaotically oriented striae; h, j, i, j A. avenia. k, l A. seravschanica l striato-perforate ornamentation with short striae divided by short

Relationships of Atraphaxis and Polygonum based in the study have the pollen grains similar to Atraphaxis, on pollen morphology differing from the pollen of closely related genera Polygonum L. s. str. and Polygonella. The striate or striato-reticulate pollen surface of the genus The genus Polygonum L. s. str. has prolate to spheroidal Atraphaxis was considered a unique character in the family tricolporate pollen (rarely panto-hexacolporate) with sev- Polygonaceae (Aleshina et al. 1978; Nowicke and Skvarla eral types of exine ornamentation (Hong et al. 2005). 1977, 1979; Hong 1995). According to Bao and Li (1993) Palynotype Avicularia sensu Hedberg (1946) possesses and Hong (1995), striate ornamentation of pollen in psilate or microspinulate exine surface, palynotype Atraphaxis is different from reticulato-foveolate ornamen- Pseudomollia sensu Hong (Hong et al. 2005) is charac- tation in Pteropyrum, Parapteropyrum A.J.Li, and Cal- terised by verrucate ornamentation at poles and meso- ligonum attributed to the tribe Atraphaxideae. colpia, and mostly psilate one around the ectoapertures. Our results showed that sporoderm ornamentation in the Palynotype Duravia sensu Hedberg (1946) also present in genus Atraphaxis is more variable and can be described as Polygonella is characterized by semi-tectate exine at the striate or striato-perforate, reticulato-foveolate, and retic- poles and mesocolpia, and reticulate or foveolate ulato-perforate. Several variants of the sporoderm orna- exine around the ectoapertures. Thus, sporoderm surface mentation represent the extreme types connected by clearly differentiates Atraphaxis from Polygonum and transitional forms. All the species of Polygonum involved Polygonella. 123 Author's personal copy

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Fig. 9 SEM micrographs of pollen grains of Atraphaxis L. a, d, f, h, of A. billardirei with thick striae oriented chaotically. h, k tricolporate i, j equatorial view; c polar view; b, e, g, k, l sporoderm pollen grain of A. tournefortii with thick striae oriented meridionally. ornamentation. a–c tricolporate pollen of A. bracteata with thick j aberrant pollen grain of A. tournefortii with slit-like grooves and striae oriented meridionally. d, e tricolporate pollen of A. pyrifolia striae oriented equatorially. i, l aberrant pollen of A. rodinii with with thick striae oriented meridionally. f, g syncolporate pollen grain merging striae and slit-like grooves

All the species previously attributed to the genus tortuosum) have striato-perforate sporoderm ornamentation Polygonum on the basis of perianth morphology have the with distant and smoothened striae, divided by wide and same size and shape of pollen grains as the members of the shallow grooves, with rows of perforations or foveolae at genus Atraphaxis. Atraphaxis ovczinnikovii (=P. ovczin- the bottom, the same as in the pollen of A. angustifolia, A. nikovii), A. popovii (=Polygonum popovii), and A. tok- aucherii, and A. badghysi. Atraphaxis ariana (=P. aria- togulica (=P. toktogulicum) differ by reticulato-foveolate num) has striato-perforate sporoderm ornamentation with or reticulato-perforate sporoderm ornamentation with distinct protruding striae and deep and narrow grooves, polygonal lumina with a single (rarely two) pit or perfo- typical for the majority of species of Atraphaxis. Thus, ration. The pollen of these species are more similar to the there is no hiathus in the pollen characteristics between pollen of some species of Calligonum (Ge 1993; Hong these species and typical members of Atraphaxis. 1995; Zhang and Xi 1997) and Pteropyrum from the tribe The results of our SEM investigation of sporoderm Calligoneae, and Parapteropyrum tibeticum (Hong 1995) ornamentation did not support the results of LM palyno- related to Fagopyrum Mill. with reticulate pollen surface logical study of Atraphaxis (Aleshina et al. 1978; Lovelius (Van Leeuwen et al. 1988). The pollen grains of A. atra- and Sjabrjaj 1981), which confirmed the division of the phaxiformis (=P. atraphaxiforme) and A. tortuosa (=P. genus Atraphaxis into three sections. The majority of the

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762 O. V. Yurtseva et al. species in all three sections of Atraphaxis possess striato- species into the genus Atraphaxis. Proximal position of A. perforate sporoderm ornamentation with the distinct striae ovczinnikovii and A. toktogulica in the clade of Atraphaxis of 0.25–0.4 lm thickness (variant 4). Some members of the leads us to conclude that the perianth of Polygonum-type section Tragopyrum have slightly different types of striato- and reticulate-foveolate sporoderm ornamentation repre- perforate ornamentation, varying in the thickness and dis- sent the ancestral state for the genus Atraphaxis. tinctness of the striae and the size of perforations or pits between them. Evolutionary trends of the pollen types of Atraphaxis Similarly, our palynological results do not support the results of molecular-phylogenetic research of Atraphaxis According to Walker (1974), the reduction of exine from based on five chloroplast regions that confirmed the divi- tectate-imperforate to tectate-perforate and to semitectate sion of the genus to three groups (Sun and Zhang 2012), or intectate one could be regarded as the main trend in the but agree with the results of our own moleculer-phyloge- pollen evolution of the angiosperms. This evolutionary netic reconstruction based on of ITS 1–2 structure trend of pollen morphology is confirmed in Polygonaceae (Yurtseva et al. 2012b; Yurtseva et al. in preparation). In (Van Leeuwen et al. 1988) and is likely present in the our ML-tree all the members of the genus Atraphaxis enter genus Atraphaxis as well. The basal position of A. ovc- a common highly supported clade with subclades not zinnikovii and A. toktogulica in the ML tree based on ITS associated with three sections of the genus Atraphaxis 1–2 sequences (Yurtseva et al. in preparation) lets us to (Pavlov 1936; Lovelius 1979; Lovelius and Sjabrjaj 1981). suppose that typical for them reticulato-foveolate or retic- Atraphaxis ovczinnikovii (=P. ovczinnikovii) occupies basal ulato-perforate exine pattern with polygonal lumina is the position in the clade of Atraphaxis. Atraphaxis toktogulica most primitive state in the genus Atraphaxis. The trans- (=P. toktogulicum) and A. ariana (=P. arianum) form a formation to striato-perforate ornamentation characteristic subclade with A. badghysi. Atraphaxis tortuosa (=P. tor- of most of the species of the genus possibly occurred by the tuosum) and A. atraphaxiformis (=P. atraphaxiforme) are way of the arranging of polygonal lumina in rows, the nested in the clade among the typical members of lowering of the rows of pits or perforations, and the rising Atraphaxis. of lateral edges of adjacent lumina, which processes have The members of the genus Atraphaxis and the species led to the formation of the striae. Widely spaced smooth- previously classified as the members of the genus Poly- ened striae with small pits between them were found in gonum have a number of common traits. They are or A. atraphaxiformis, A. tortuosa with the perianth of undershrubs with the pseudoterminal thyrses, the flowers in Polygonum-type and in A. badghysi with the tepals of equal axillary cymes, alternate leaves, nodes with ochrea, trigo- size. Our results indicate that these species occupy basal nous achenes, 6–8 with a dilatate base, and with positions in the ML tree. The majority of the species of the absence of clear nectaries (Haraldson 1978; Ronse Atraphaxis with the perianth with long filiform tube and Decraene and Akeroyd 1988; Brandbyge 1993). In com- enlarged inner tepals are characterized by striato-perforate paring with Polygonum, the majority of the species of At- ornamentation with distinct protruding striae divided by raphaxis are characterized by spheroidal flower buds with a deep grooves with pits or perforations at the bottom. These long filiform perianth tube and inner tepals significantly types of sporoderm ornamentation seem to represent the enlarged in fruiting. According to our observations, most advanced state. Atraphaxis ovczinnikovii (P. ovczinnikovii), A. toktogulica (=P. toktogulicum), A. atraphaxiformis (=P. atraphaxi- Hybridization events and pollen morphology forme), and A. tortuosa (=P. tortuosum) have campanulate perianth typical for Polygonum, divided into ’–5/6 in 5 The uncovered irregularities in pollen morphology and the ovate, elliptical or oblong keeled tepals. Atraphaxis ariana large proportion of abnormal pollen grains likely point at (=P. arianum) has campanulate perianth divided into 3/4 in the hybrid origin of some species. Four-six-loxocolporate 5 ovate greatly expanded tepals. Atraphaxis popovii pollen grains were found in Polygonum aviculare L. s.str., (=P. popovii) has spheroidal flower bud with five equal P. arenastrum Boreau, P. patulum M. Bieb., P. rurivagum rounded-oblong tepals and extremely short filiform tube. Jord. ex Boreau, P. turkestanicum Sumnev., P. raii Bab., The variability of the perianth structure observed among P. boreale (Lange) Small, and P. oxyspermum C.A. Mey. the members of Atraphaxis and shrubby species of & Bunge which are known as polyploids with chromosome Polygonum is likely to be a manifestation of intrageneric numbers 2n = 40, 60, 80, whereas diploid species with polymorphism. Profound similarity in the life form, inflo- 2n = 20 have tricolporate pollen grains (Hedberg 1946; rescence structure, perianth structure, pollen shape, and Borzova and Sladkov 1968; Chromosome numbers of sporoderm ornamentation, along with the similarity of ITS flowering plants 1969; Van Leeuwen et al. 1988; Yurtseva 1–2 region of nrDNA give good reasons to include these 2002; Hong et al. 2005). 123 Author's personal copy

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The genus Atraphaxis is poorly studied in terms of manuscript and helpful suggestions. The study was supported by the chromosome numbers. Atraphaxis frutescens is a diploid Russian Foundation for Basic Research (project No. 11-04-01300-a). with 2n = 16 (Ekimova et al. 2012), and a hexaploid with 2n & 45 (Edman 1931). Polyploidy was found in A. spinosa with 2n & 45 and 2n = 48 (Edman 1931; Chro- Voucher information mosome numbers of flowering plants 1969), in A. lanceo- lata and A. billardierei with 2n & 45 (Edman 1931), and Atraphaxis angustigolia Jaub. et Spach.—Armenia, inter in A. pungens with 2n = 48 (Ekimova et al. 2012). Ordubad et Akilis. 3.06.1914. Woronov (MW); Armenia., Atraphaxis bracteata and A. manshurica are diploids with Megri d., Agarak, slope of Zangezur Ridge. 1.06.1973. 2n = 22 (Tian et al. 2009). Allopolyploidy via hybridiza- Shvedchikova (MW) [SEM]; Caucasus, Ordubad. tion of diploid species seems to be the most probable way 13.05.1934. Ter-Minosyan (LE) [LM]. of speciation followed by apomixis reported for A. frutes- Atraphaxis ariana (Grigorj.) T.M.Schust. & Reveal cens (Edman 1931; Sitnikov 1991). (= Polygonum arianum Grigorj.)—Turkmenskaya SSR, Among the species with known chromosome numbers vill. Morgunovsky, 25.04.1988. Gorelova (LE) [SEM]; the specimens of A. billardierei, A. bracteata, and A. Turkmenistan, [Badghyz, Kushka d.,] Morgunovsky, pungens with small pollen grains are apparently diploids 730 m a.s.l., 05.1964. n 800. Chukavina (LE) [LM]. (Table 1). The specimens of A. spinosa, A. daghestanica, Atraphaxis atraphaxiformis (Bots- and A. frutescens (=A. lanceolata) with small (22–24 lm) ch.) T.M.Schust. & Reveal (= Polygonum atraphaxi- and large (30–36 lm) pollen grains are apparently diploids forme Botsch.)—Tajikistan, Turkestan ridge, confl. of the and polyploids, correspondingly (Table 1; Figs. 1 and 2). Kshemysh and the Bel-Su. 03.07.1963. n 65. Abdusal- Four-, six-loxocolporate pollen grains were detected jamova (LE) [SEM, LM]. mainly in the specimens of Atraphaxis species with pollen Atraphaxis avenia Botsch.—South Tajikistan, Bag on of large or medium size, although they predominate in the the river Pjandzh, right bank of the river Shpilyau. specimens with small pollen in A. billardierei. The large 1.06.1960. n 779. Botschantzev and Egorova (LE) [SEM, proportion of 4-6-loxocolporate or syncolporate pollen LM]. grains, or the pollen with ring-like form of ectoapertures Atraphaxis aucherii Jaub. et Spach—West Persia, was detected as well in the samples of A. aucherii, A. Iran, Mazanderan, Bakhtiar Mts, Arabistan, Mulla-Ili, Gi- canescens, A. compacta, A. decipiens, A. frutescens, A. lang. 15.05.1904. n 341. Gadd (LE) [SEM]; Persia, n 3271. karataviensis, A. muschketowi, A. rodinii, A. spinosa Aucher-Eloy (LE) [LM]. (Shvedchikova MW; Artemenko MW; Nenevsky MW), A. Atraphaxis badghysi Kult.—Turkmenistan, Maryiskaya teretifolia, and A. virgata (Table 1). These species are reg. 35 km S of Shor-Tepe. 4.04.1952. Zhudova and Gru- likely to be of hybrid origin. zdeva (MW); Turkmenistan, Badghys, S of saline Nam- aksaar. 25.04.1976. n 259. Botschantzev (LE) [SEM]; New names and combinations Turkmenia, in cliff Kzyl-Dzhar, NE of lake Er-Oylan-duz. 16.04.1964. n 281. Botschntsev (LE) [LM]. Atraphaxis ovczinnikovii (Czukav.) O.V.Yurtseva, comb. Atraphaxis billardierei Jaub. et Spach—Turkey, Prov. ¨ nov. : Polygonum ovczinnikovii Czukav. in Izv. Akad. Nevsehir, Urgu¨p. 1300 m. 24.05.1960. n 8469. Stainton Nauk Tadzhiksk. SSR, Otd. Biol. Nauk 2(9): 62. 1962; and Henderson (LE) [SEM, LM]. Chukav. in Fl. Tadzhiksk. SSR, 3: 250. 1968. Atraphaxis bracteata Losinsk.—Mongolia, E of Altay Atraphaxis popovii (Borodina) O.V.Yurtseva, comb. Goby, ridge Hurh-Ula, South Goby aimag. 20-30 km S of nov. : Polygonum popovii Borodina in Rast. Tsentr. Nomgon. 30.07.1989. n 89. Gubanov and Grubov (MW) Azii 9: 104. 1989. [SEM, LM]. Atraphaxis caucasica (Hoffm.) Pavlov—Georgia, Ak- Acknowledgments The work was performed at the User Facilities haltsikhe d., cl. Akhaltsikhe, 1080 m. a.s.l. 26.05.1973. Center of M.V.Lomonosov Moscow State University with the finan- Schvedchikova (MW) [SEM]; Georgia, Gory distr., Gori- cial support from the Ministry of Education and Science of the sdzhvary. 19.05.1949. Lorkipanidze (LE) [LM]. Russian Federation. We thank the staff of the User Facilities Center Atraphaxis canescens for support and assistance. We are grateful to the curators of the Bunge—Kazakhstan, Dzhambul Herbaria LE, MW, MHA, and TAD for allowing us to examine the reg., Mts Chu-Ili, top of Sunhar-Tyube (Han-Tau). specimens and take pollen samples. We are grateful to O. A. Volkova, 14.05.1951. n 167. Pavlov (MW) [SEM]; East Kazakhstan, N. I. Filina, A. G. Bogdanov, and S. V. Polevova for technical N of Izbaksan, outflow of Cherny Irtysh, foothills of Mt. assistance; to G. Yu. Klinkova, N. A. Suprun, and V. G. Onipchenko who collected some specimens for this study. We should like to thank Chakylmaak. 10.05.1863. n 370. Potanin (LE) [LM]. Dr. S. B. Yazvenko (LGL Limited, Canada) for reviewing the Eng- Atraphaxis compacta Ledeb.—Kazakhstan, Syr-Darya lish, and two anonymous reviewers for their critical reading of the reg. Mts Kara-Tau, Kos-Degeres. 11.05.1936. n 46.

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