Skip to main content
SpringerLink
Log in

Exocarp structure in the genus Atraphaxis (Polygonaceae, Polygoneae)

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Exocarp anatomy of 30 species of Atraphaxis has been studied to shed light on possible diagnostic and phylogenetic significance of carpological characters. The diversity of the exocarp structure observed in Atraphaxis was comparable to that in the entire tribe Polygoneae. The size of the exocarp cells, the size and shape of the lumen and its branching were the most variable. The radial size of the exocarp cells and the thickening of the walls determined the size and shape of the lumen in the exocarp cells of ripe fruits. The occurrence of the types of the exocarp cells among species of Atraphaxis only partly confirmed an earlier morphology-based division of the genus into three sections. Optimizations of the evolution of exocarp characters using parsimony on plastid phylogeny of Atraphaxis showed homoplastic changes in many characters and the absence of subclades with unique synapomorphies. Some new species identified using plastid data were confirmed by exocarp characters. Species with thick exocarp are distributed mainly in mountain regions of Central Asia, whereas species with thin exocarp are widespread in steppes and semi-deserts of Eurasia. Fruit coloration associated with the amount of phenolic compounds in the exocarp cells might be related to differences in the timing of seed germination. Species with light-brown fruits are widespread, while those with dark or black fruits are mostly local endemics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aleshina LA, Lovelius OL, Sjabrjaj SV (1978) Explorationes morphologiae pollinis specierum generis Atraphaxis L. florae URSS. In: Klokov M (ed) Novosti sistematiki vysshikh i nizshikh rasteniy (Novitates systematicae plantarum vascularium et non vascularium 1977). Naukova dumka, Kiev, pp 108–122

    Google Scholar 

  • Baasanmunkh S, Urgamal M, Oyuntsetseg B, Sukhorukov AP, Tsegmed Z, Son DC, Erst A, Oyundelger K, Kechaykin AA, Norris J, Kosachev P, Ma J-S, Chang KS, Choi HJ (2022) Flora of Mongolia: annotated checklist of native vascular plants. PhytoKeys 192:63–169. https://doi.org/10.3897/phytokeys.192.79702

    Article  PubMed  PubMed Central  Google Scholar 

  • Bao B, Grabovskaya-Borodina AE (2003) Atraphaxis L. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China 5. Science Press, Beijing, pp 328–332

    Google Scholar 

  • Bentham G, Hooker JD (1880) Polygonaceae. In: Bentham G, Hooker JD (eds) Genera plantarum ad exemplaria imprimis in herbariis Kewensibus servata definita 3(1). Reeve & Co, London, pp 88–105

    Google Scholar 

  • Boissier E (1879) Flora Orientalis sive enumeratio plantarum in Oriente a Graecia et Aegypto ad Indiae fines hucusque observatorum 4. Apud. H. Georg Bibliopolam, Lugduni, Genevae et Basel.

  • Borodina AE (1989) Polygonaceae. In: Borodina AE, Grubov VI, Grudzinskaja IA, Menitsky JL (eds) Plantae Asiae Centralis 9. Nauka, Leningrad, pp 77–129

    Google Scholar 

  • Brandbyge J (1993) Polygonaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants 2. Springer, Berlin, pp 531–544. https://doi.org/10.1007/978-3-662-02899-5_63

    Chapter  Google Scholar 

  • Cullen J (1967) Atraphaxis L. In: Davis PH (ed) Flora of Turkey and the East Aegean islands 2. Edinburgh University Press, Edinburgh, pp 266–267

    Google Scholar 

  • Dammer U (1893) Polygonaceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, T. 3, Abt. 1a. Engelmann, Leipzig, pp 1–36

    Google Scholar 

  • Fedotova TA (1991) Polygonaceae. In: Takhtajan A (ed) Anatomia seminum comparativa. T. 3. Nauka, Leningrad, pp 83–94

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678

    Article  PubMed  Google Scholar 

  • Geiger H, Fuggerera H (1979) Über den Chemismus der Wiesner-Reaktion auf Lignin. Z Naturf b 34:1471–1472. https://doi.org/10.1515/znb-1979-1028

    Article  Google Scholar 

  • GenBank (2022) GenBank®. National Library of Medicine, Bethesda. Available at: https://www.ncbi.nlm.nih.gov/genbank/

  • Ghimire B, Choi GE, Jeong MJ, Lee H, Lee KM, Son SW, Lee CH, Suh GU (2016) Fruit morphology and anatomy of Persicaria chinensis (Polygonaceae). J Jap Bot 91:218–225

    Google Scholar 

  • Graham SA, Wood CE (1965) The genera of Polygonaceae in the South Eastern United States. J Arnold Arbor 46:91–121

    Article  Google Scholar 

  • Gubanov IA (1996) Conspectus of flora of Outer Mongolia: vascular plants. Valang, Moscow

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence editor alignment and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hatfield R, Vermerris W (2001) Lignin formation in plants. The dilemma of linkage specificity. Pl Physiol 126:1351–1357. https://doi.org/10.1104/pp.126.4.1351

    Article  CAS  Google Scholar 

  • Hendry GAF, Thompson K, Moss CJ, Edwards E, Thorpe PC (1994) Seed persistence: a correlation between seed longevity in the soil and ortho–dihydroxyphenol concentration. Funct Ecol 8:658–664. https://doi.org/10.2307/2389929

    Article  Google Scholar 

  • Huang G, McCrate AJ, Varriano-Marston E, Paulsen GM (1983) Caryopsis structural and imbibitional characteristics of some hard red and white wheats. Cereal Chem 60:161–165

    Google Scholar 

  • Ivlev VI (2008) Introduction of rare and disappearing plants in Central Kazakhstan. Bot Res Sib Kaz (Bot Issl Sibiri Kazakhstana) 14:79–89

    Google Scholar 

  • Jaubert H–FC, Spach E (1844–1846) Illustrationes Plantarum Orientalium 2. Roret, Paris. Tabs. 101–200

  • Katoh K, Misawa K, Kuma K, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molec Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan M, Cavers PB, Kane M, Thompson K (1997) Role of the pigmented seed coat of proso millet (Panicum miliaceum L.) in imbibition, germination and seed persistence. Seed Sci Res 7:21–26. https://doi.org/10.1017/S0960258500003329

    Article  Google Scholar 

  • Kong MJ, Hong SP (2018) Comparative achene morphology of Persicaria sect. Cephalophilon and related taxa (Polygonaceae). Korean J Pl Taxon 48:134–142. https://doi.org/10.11110/kjpt.2018.48.2.134

    Article  Google Scholar 

  • Kostina MV, Yurtseva OV (2021) Structure and developmental rhythm of shoot systems of A. frutescens (L.) K. Koch., A. replicata Lam., and A. pyrifolia Bunge (Atraphaxis L., Polygonaceae). Contemp Probl Ecol 14:241–254. https://doi.org/10.1134/S1995425521030070

    Article  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molec Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lattanzio V, Lattanzio VM, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem Adv Res 661:23–67

    Google Scholar 

  • Lattanzio V, Kroon PA, Quideau S, Treutter D (2008) Plant phenolics—secondary metabolites with diverse functions. In: Daayf F, Lattanzio V (eds) Recent advances in polyphenol research. Blackwell, Chichester, pp 1–35. https://doi.org/10.1002/9781444302400.ch1

    Chapter  Google Scholar 

  • Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annual Rev Pl Biol 41:455–496. https://doi.org/10.1146/annurev.pp.41.060190.002323

    Article  CAS  Google Scholar 

  • Li X, Zhao X, Wang Z, Dong Z (2010) Seed dormancy-breaking and germination requirements of two Atraphaxis species. Bull Bot Res 30:600–603. https://doi.org/10.7525/j.issn.1673-5102.2010.05.014

    Article  CAS  Google Scholar 

  • Li X, Zhao X, Yu R (2011) Effects of seed maturation time and dry storage on germination of two Atraphaxis species. Acta Ecol Sin 30:3727–3732

    Google Scholar 

  • Lonay H. 1922. Génèse et anatomie des péricarpes et des spermodermes chez les Polygonaceés. Mém Soc Roy Sci Liége, Sér. 3, Tome 2, Part 2, 6: 1–109

  • Lovelius OL (1978) Compositio specierum, Distributio geographica et cohaerentia oecologica generis Atraphaxis L. (Polygonaceae). In: Klokov MV (ed) Novosti sistematiki vysshikh i nizshikh rasteniy (Novitates systematicae plantarum vascularium et non vascularium 1977). Naukova dumka, Kiev, pp 85–108

    Google Scholar 

  • Lovelius OL (1979) Synopsis generis Atraphaxis L. (Polygonaceae). Novosti Sist Vyssh Rast 15:114–128

    Google Scholar 

  • Marek S (1954) Cechy morfologiczne i anatomiczne owoców rodzajów Polygonum L. i Rumex L. oraz klucze do ich oznaczania (Morphological and anatomical features of the fruits of genera Polygonum L., Rumex L. and keys for their determination). Monogr Bot 2:77–161. https://doi.org/10.5586/mb.1954.002

    Article  Google Scholar 

  • Matilla A, Gallardo M, Puga-Hermida MI (2005) Structural, physiological and molecular aspects of heterogeneity in seeds: a review. Seed Sci Res 15:63–76. https://doi.org/10.1079/SSR2005203

    Article  CAS  Google Scholar 

  • Meisner CF (1857) Polygonaceae. In: de Candolle AP (ed) Prodromus systematis naturalis regni vegetabilis 14. Masson, Paris, pp 1–186

    Google Scholar 

  • Miroslavov EA (1974) Struktura i funktsiya epidermy lista pokrytosemennykh (The structure and function of the epidermis of the angiosperm leaf). Nauka, Leningrad

    Google Scholar 

  • Mohamed-Yasseen Y, Barringer SA, Splittstoesser WE, Costanza S (1994) The role of seed coats in seed viability. Bot Rev 60:426–439. https://doi.org/10.1007/BF02857926

    Article  Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Nixon KC (2002) WinClada, version 1.00.08. Computer program published and distributed by the author, Ithaca. Available at: http://www.cladistics.com

  • Pavlov VN (1970) Atraphaxis L. In: Komarov VL (ed) Flora of the USSR (Flora SSSR) 5. Izdatel'stvo Akademii Nauk SSSR, Moskva & Leningrad, 1936, pp 392–411. [Translated from Russian by Dr Landau N, Israel Program for Scientific Translations, Jerusalem 1970]

  • Patzlaff A, McInnis S, Courtenay A, Surman C, Newman LJ, Smith C, Bevan MW, Mansfield Sh, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Pl J 36:743–754. https://doi.org/10.1046/j.1365-313X.2003.01916.x

    Article  CAS  PubMed  Google Scholar 

  • Powell AA (1989) The importance of genetically determined seed coat characteristics to seed quality in grain legumes. Ann Bot (Oxford) 63:169–175. https://doi.org/10.1093/oxfordjournals.aob.a087720

    Article  Google Scholar 

  • Puga-Hermida MI, Gallardo M, del Carmen R-G, Matilla AJ (2003) The heterogeneity of turnip–tops (Brassica rapa) seeds inside the silique affects germination, the activity of the final step of the ethylene pathway, and abscisic acid and polyamine content. Funct Pl Biol 30:767–775. https://doi.org/10.1071/FP03053

    Article  CAS  Google Scholar 

  • Rechinger KH, Schiman-Czeika M (1968) Polygonaceae. In: Rechinger KH (ed) Flora Iranica 56/28. Academishe Druck-u.Verlagsanstalt, Graz, pp 1–88

    Google Scholar 

  • Ronse De Craene LP, Hong SP, Smets E (2000) Systematic significance of fruit morphology and anatomy in tribes Persicarieae and Polygoneae (Polygonaceae). Bot J Linn Soc 134:301–337. https://doi.org/10.1111/j.1095-8339.2000.tb02356.x

    Article  Google Scholar 

  • Roth I (1977) Fruits of angiosperms. Handbuch der Pflanzenanatomie 10(1), 2nd edn. Borntraeger, Berlin

    Google Scholar 

  • Royal Botanic Gardens Kew (2021) Seed Information Database (SID). Version 7.1. Available at: http://data.kew.org/sid/

  • Schatral A, Osborne JM (2006) Germination and dormancy states of seeds in the environmental weed Rumex vesicarius (Polygonaceae). I. Seed polymorphism and germination of extracted seeds. Austral J Bot 54:773–782. https://doi.org/10.1071/BT04201

    Article  Google Scholar 

  • Schuster TM, Reveal JL, Kron KA (2011) Phylogeny of Polygoneae (Polygonaceae: Polygonoideae). Taxon 60:1653–1666. https://doi.org/10.1002/tax.606010

    Article  Google Scholar 

  • Sirrine EF (1894) Structure of seed coats of Polygonaceae. Proc Iowa Acad Sci 2:128–135

    Google Scholar 

  • Tavakkoli S, Kazempour Osaloo Sh, Mozaffarian V, Maassoumi A (2015) Molecular phylogeny of Atraphaxis and the woody Polygonum species (Polygonaceae): taxonomic implications based on molecular and morphological evidence. Pl Syst Evol 301:1157–1170. https://doi.org/10.1007/s00606-014-1140-7

    Article  Google Scholar 

  • Thiers B. (2021, continuously updated) Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s virtual herbarium, Bronx. Available at: http://sweetgum.nybg.org/science/ih/. Accessed 18 Oct 2021

  • Webb DA (1993) Atraphaxis L. In: Tutin TG, Burges NA, Chater AO, Edmonson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea 1, 2nd edn. Cambridge University Press, Cambridge, p 108

    Google Scholar 

  • Yurtseva OV (2001) Ultrasculpture of achene surface in Polygonum section Polygonum (Polygonaceae) in Russia. Nordic J Bot 21:513–528. https://doi.org/10.1111/j.1756-1051.2001.tb00805.x

    Article  Google Scholar 

  • Yurtseva OV, Severova EE, Bovina IYu (2014) Pollen morphology and taxonomy of Atraphaxis (Polygoneae, Polygonaceae). Pl Syst Evol 300:749–766. https://doi.org/10.1007/s00606-013-0917-4

    Article  Google Scholar 

  • Yurtseva OV, Kuznetsova OI, Mavrodieva ME, Mavrodiev EV (2016a) What is Atraphaxis L. (Polygonaceae, Polygoneae): cryptic taxa and resolved taxonomic complexity instead of the formal lumping and the lack of morphological synapomorhies. PeerJ 4:1–52. https://doi.org/10.7717/peerj.1977

    Article  Google Scholar 

  • Yurtseva OV, Kuznetsova OI, Mavrodiev EV (2016b) A broadly sampled 3–loci plastid phylogeny of Atraphaxis (Polygoneae, Polygonoideae, Polygonaceae) reveals new taxa: I. Atraphaxis kamelinii spec. nov. from Mongolia. Phytotaxa 268:1–24. https://doi.org/10.11646/phytotaxa.268.1.1

    Article  Google Scholar 

  • Yurtseva OV, Severova EE, Mavrodiev EV (2017) Persepolium (Polygoneae): a new genus in Polygonaceae based on conventional maximum parsimony and three-taxon statement analyses of a comprehensive morphological dataset. Phytotaxa 314:151–194. https://doi.org/10.11646/phytotaxa.314.2.1

    Article  Google Scholar 

  • Yurtseva OV, Mavrodiev EV (2019) Caelestium genus novum (Polygonaceae, Polygoneae): evidence based on the results of molecular phylogenetic analyses of tribe Polygoneae, established with consideration of the secondary structure of the ITS rDNA regions. Novosti Sist Vyssh Rast 50:47–79. https://doi.org/10.31111/novitates/2019.50.47

    Article  Google Scholar 

  • Yurtseva OV, Lazkov GA, Ukrainskaja UA, Deviatov AG (2019) Caelestium (Polygonaceae, Polygoneae), evidence based on morphology. Novosti Sist Vyssh Rast 50:80–100. https://doi.org/10.31111/novitates/2019.50.80

    Article  Google Scholar 

  • Yurtseva OV, Badmaeva NK, Mavrodiev EV (2021a) A broadly sampled 3-loci plastid phylogeny of Atraphaxis (Polygoneae, Polygonoideae, Polygonaceae) reveals new taxa: II. Atraphaxis selengensis spec. nov. and A. davurica Jaub. et Spach from Russian Transbaikalia. Phytotaxa 484:44–74. https://doi.org/10.11646/phytotaxa.484.1.2

    Article  Google Scholar 

  • Yurtseva OV, Severova EE, Deviatov AG, Olonova MV, Samigullin TH (2021b) Polygonum schischkinii is a member of Atraphaxis (Polygonaceae, Polygoneae): evidences from morphological and molecular analyses. Phytotaxa 491:193–216. https://doi.org/10.11646/phytotaxa.491.3.1

    Article  Google Scholar 

  • Yurtseva OV, Vasilieva NV, Kostikova VA, Samigullin TH (2022) A broadly sampled 3-loci plastid phylogeny of Atraphaxis (Polygoneae, Polygonoideae, Polygonaceae) reveals new taxa: III. Atraphaxis kuvaevii and cryptic species in Atraphaxis pungens (M.Bieb.) & Spach from Southern Siberia and Northern Mongolia. Phytotaxa (in press)

  • Zhang XX, Xiong XH, Xu F, Deng LN, Wang KM, Hou YT (2011) Exocarp anatomy of Polygonum and related species from Shandong Province. Pl Sci J 529:554–551

    Google Scholar 

  • Zhang M-L, Sanderson SC, Sun Y-X, Byalt VV, Hao X-L (2014) Tertiary montane origin of the Central Asian flora: evidence inferred from cpDNA sequences of Atraphaxis (Polygonaceae). J Integr Pl Biol 56:1125–1135. https://doi.org/10.1111/jipb.12226

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank O.V. Cherneva, A.E. Borodina, V.I. Dorofeev, A.P. Seregin, N.M. Reshetnikova, G.A. Lazkov, A.I. Shmakov, A.N. Kupriyanov, E.V. Banaev, V.V. Chepinoga and O.A. Anenkhonov for their kind permission to take samples for morphological investigations from Herbaria LE, MW, MHA, FRU, ALTB, KUZ, NS, NSK, IRKU and UUH. We are grateful to M.G.Pimenov, N.S. Gamova, S. Svirin and N.K. Badmaeva who collected some specimens used in this study. We thank A.C. Timonin for valuable comments that helped to improve the text. We thank anonymous Reviewers for their attentive attitude, helpful comments and advice.

Funding

This work was supported by the Russian Foundation for Basic Research, project no. 20-04-00033.

Author information

Authors and Affiliations

  1. Department of Higher Plants, Faculty of Biology, M.V. Lomonosov Moscow State University, Leninskie Gory, 1-12, Moscow, Russia, 119234

    Olga V. Yurtseva, Andrey G. Deviatov & Dmitry D. Sokoloff

Authors
  1. Olga V. Yurtseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrey G. Deviatov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dmitry D. Sokoloff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olga V. Yurtseva.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Human and animal rights

This article does not contain any research involving humans or animals as research objects.

Additional information

Handling Editor: Ferhat Celep.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Information on Electronic Supplementary Material

Information on Electronic Supplementary Material

Online resource 1. The origin of the material used for anatomical and molecular study. Left: Species names, the numbers of fruit samples and the voucher information (herbarium acronyms according to Index Herbariorum) for samples used in anatomical study of fruits. Right: DNA sample numbers and the voucher information for samples used in molecular studies, and GenBank numbers of sequences. In some cases, the same samples were used in both analyses, but in other cases, different samples were studied. “—” no data.

Online resource 2. The combined aligned plastid matrix for cpDNA trnL intron + trnL-F IGS and rpl32-trnL (UAG) IGS regions including 54 nucleotide sequences for accessions of Atraphaxis (52), Persepolium (1), and Bactria (1).

Online resource 3. Morphological characters of fruit and exocarp and their states used in Maximum Parsimony analyses.

Online resource 4. Morphological data matrix used in Maximum Parsimony analyses. “0” and “1” are character states, “ ? ” denotes unknown or ambiguous character state.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yurtseva, O.V., Deviatov, A.G. & Sokoloff, D.D. Exocarp structure in the genus Atraphaxis (Polygonaceae, Polygoneae). Plant Syst Evol 308, 32 (2022). https://doi.org/10.1007/s00606-022-01824-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00606-022-01824-0

Keywords

Search

Navigation