Skip to main content

Acropetally developing vascular bundles coexisting with basipetally developing and basally blindly ended vascular bundles in scapes of Eriocaulon taquetii (Eriocaulaceae, monocotyledons)

Journal of Plant Research volume 134, pages 765–778 (2021)Cite this article

Abstract

In various monocotyledons, there are basally blindly ended stem vascular bundles, which never connect to the vascular bundles of roots. These blindly ended vascular bundles seem to be unsuitable for transferring water in terrestrial plants. In the present study, we aim to clarify the trace of the blindly ended stem vascular bundles in whole plants, and consider the evolutional process for holding such vascular bundles in the stem. We examined a whole stem vasculature of Eriocaulon taquetii (Eriocaulaceae, monocotyledons) by observation of serial transverse sections, cut by a manual rotary microtome, and viewed under an epifluorescence microscope. Our investigation revealed a threedimensional reconfiguration of the scape vasculature and detected basipetally developing and basally blindly ended vascular bundles, originated from involucral bracts and arranged with acropetally developing vascular bundles alternately in the scape internode. The basipetally developing and basally blindly ended vascular bundles, which originate from the primodia of foliar organs, have been reported in various commelinids. The characteristic vascular bundles would be homologous and presumed to be a synapomorphy of commelinids. These vascular bundles are considered to be a relic characteristic from ancestral semiaquatic plants of monocotyledons.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

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

References

  • Aloni R (2010) The induction of vascular tissues by auxin. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action! Kluwer Academic Publishers, Dordrech, pp 471–492

    Google Scholar 

  • APG IV (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

    Google Scholar 

  • Ayensu ES (1972) Dioscoreales. In: Metcalfe CR (ed) Anatomy of the monocotyledons IV, 182 pp with16 plates, Clarendon Press, Oxford

  • Bayer EM, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C (2009) Integration of transport-based models for phyllotaxis and midvein formation. Genes Dev 23:373–384

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bell A (1980) The vascular pattern of a rhizomatous ginger (Alpinia speciosa L. Zingiberaceae). 1. The aerial axis and its development. Ann Bot 46:203–212

    Google Scholar 

  • Bercu R (2005) Contribution to the anatomy of Sagittaria sagittifolia L. (Alismataceae). J Biol Res 4:213–215

    Google Scholar 

  • Blunden G, Binns WW (1970) The leaf anatomy of Yucca glauca Nutt. Bot J Linn Soc 63:133–141

    Google Scholar 

  • Blunden G, Jewers K (1973) The comparative leaf anatomy of Agave, Beschorneria, Doryanthes and Furcraea species (Agavaceae: Agaveae). Bot J Linn Soc 66:157–179

    Google Scholar 

  • Bond J, Donaldson L, Hill S, Hitchcock K (2008) Safranin fluorescent staining of wood cell walls. Biotech Histochem 83:161–171

    CAS  PubMed  Google Scholar 

  • Bosabalidis AM, Evert RF, Russin WA (1994) Ontogeny of the vascular bundles and contiguous tissues in the maize leaf blade. Am J Bot 81:745–752

    Google Scholar 

  • Chonan N, Kawahara H, Matsuda T (1974) Morphology on vascular bundles of leaves in gramineous crops I. Observation on vascular bundles of leaf blades, sheaths and internodes in rice plants. Proc Crop Sci Soc Jpn 43:425–432 (in Japanese with English abstract)

    Google Scholar 

  • Claßen-Bockhoff R, Franke D, Krämer H (2020) Early ontogeny defines the diversification of primary vascular bundle systems in angiosperms. Bot J Linn Soc XX 1–27 with 13 figures

  • Esau K (1953) Plant anatomy. Wiley, New York

    Google Scholar 

  • Evans PS (1965) Intercalary growth in the aerial shoot of Eleocharis acuta R. Br. Prodr Ann Bot 29:205–217

    Google Scholar 

  • Fischer JB (1970) Xylem derived from the intercalary meristem of Cyperus alternifolius. Bull Torrey Bot Club 97:58–66

    Google Scholar 

  • Fischer JB, French JC (1976) The occurrence of intercalary and uninterrupted meristems in the internodes of tropical monocotyledons. Am J Bot 63:510–525

    Google Scholar 

  • Gifford EM, Foster AS (1989) Morphology and evolution of vascular plants, 3rd edn. Freeman WH and company, New York

    Google Scholar 

  • Givnish TJ, Zuluaga A, Spalink D, Gomez MS, Lam VKY, Saarela JM, Sass C et al (2018) Monocot plastid phylogenomics, timeline, net rates of species diversification, the power of multi-gene analyses, and a functional model for the origin of monocots. Am J Bot 105:1888–1910

    CAS  PubMed  Google Scholar 

  • Govindarajalu E (1967) Further contribution to the anatomy of the Alismataceae: Sagittaria guayanensis H.B.K. ssp. lappula (D. Don) Bogin. Proc India Acad Sci – Sect B 65: 142–152

  • Harb RK, El-Kobisy OS, Desoukey SF (2016) Anatomical and chemical investigations on Asparagus officinalis L. (Asparagaceae). Arab Univ J Agric Sci 24:655–664

    Google Scholar 

  • Hare CL (1945) The structure and development of Eriocaulon septangulare With. J Linn Soc Bot 53:422–448

    Google Scholar 

  • Heywood VH (1978) Flowering plants of the world. Oxford Univ Press, London

    Google Scholar 

  • Holm T (1901) Eriocaulon decangulare L.: An anatomical study. Bot Gaz 31:17–37

    Google Scholar 

  • Maze J (1977) The vascular system of the inflorescence axis of Andropogon gerardii (Gramineae) and its bearing on concepts of monocotyledon vascular tissue. Am J Bot 64:504–515

    Google Scholar 

  • Nikon Instruments Inc (2020) Fern sorus thin section, G-2A Longpass Emission (Wide Bandwidth Excitation) Green Set. (https://www.microscopyu.com/techniques/fluorescence/nikon-fluorescence-filter-sets/green-excitation-filter-sets/green-excitation-g-2a-longpass-emission), 2020. 5. 30

  • Oliveira FMG, Scatena VL, Oriani A (2015) Anatomy of vegetative organs and inflorescence axis of Orectanthe sceptrum (Xyridaceae–Poales). J Torrey Bot Soc 142:258–268

    Google Scholar 

  • Pereira RA, Rodrigues AC (2012) Morphoanatomy of the underground stem of Androtrichum trigynum (Cyperaceae). Rodriguésia 63:305–319

    Google Scholar 

  • Povilus RA, DaCosta JM, Grassa C, Satyaki PRV, Moeglein M, Jaenisch J, Xi Z, Mathews S, Gehring M, Davis CC, Friedman WE (2020) Water lily (Nymphaea thermarum) genome reveals variable genomic signatures of ancient vascular cambium loses. Proc Nat Acad Sci USA 117:8649–8656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodrigues AC, Estelita MEM (2009) Morphoanatomy of the stem in Cyperaceae. Acta Bot Bras 23:889–901

    Google Scholar 

  • Rudall P (1991) Lateral meristems and stem thickening growth in monocotyledons. Bot Rev 57:150–163

    Google Scholar 

  • Saikawa M (2016) Not all of the vascular bundles are distributed widely and scattered irregularly throughout the transverse-sectional area of monocotyledonous stem. Bull Tokyo Gakugei Univ Div Nat Sci 68:229–243 (in Japanese with English abstract)

    Google Scholar 

  • Sajo MG (1999) Systematic vegetative anatomy and ensiform leaf development in Xyris (Xyridaceae). Bot J Linn Soc 130:171–182

    Google Scholar 

  • Scarpella E, Meijer H (2004) Pattern formation in the vascular system of monocot and dicot plant species. New Phytol 164:209–242

    CAS  PubMed  Google Scholar 

  • Scatena VL, Giulietti AM (1996) The taxonomy and morphological and anatomical differentiation of populations of Leiothrix crassifolia (Eriocaulaceae). Plant Syst Evol 199:243–258

    Google Scholar 

  • Scatena VL, Rosa MM (2001) Morphology and anatomy of the vegetative organs and scapes from Aphorocaulon (Paepalanthus, Eriocaulaceae). Br Arch Biol Technol 44:49–58

    Google Scholar 

  • Scatena VL, Giulietti AM, Cardoso VA (1999) Anatomia de raízes, escapos e folhas de espécies de Eriocaulon L. (Eriocaulaceae). Bol Bot Univ São Paulo 18:11–20

    Google Scholar 

  • Scatena VL, Vich DV, Parra LR (2004) Anatomia de escapos, folhas e brácteas de Syngonanthus sect. Eulepis (Bong. ex Koern.) Ruhland (Eriocaulaceae). Acta Bot Bras 18:825–837

    Google Scholar 

  • Scatena VL, Giulietti AM, Bolba EL, van den Berg C (2005) Anatomy of Brazilian Eriocaulaceae: correlation with taxonomy and habitat using multivariate analyses. Plant Syst Evol 253:1–22

    Google Scholar 

  • Sharmann BC (1942) Developmental anatomy of the shoot of Zea mays L. Ann Bot 6: 245–282, Plate VII

  • Sheikh N, Kumar Y (2017) Foliar epidermal, stem and petiole anatomy of Meghalayan Dioscorea L. (Dioscoreaceae) and its systematic implication. Bangladesh J Plant Taxon 24:53–63

    Google Scholar 

  • Stant MY (1964) Anatomy of the Alismataceae. J Linn Soc (Bot) 59:1–42

    Google Scholar 

  • Stevens PF (2001 onwards) Angiosperm Phylogeny Website. Version 14, July 2017 [and more or less continuously updated since]." will do. http://www.mobot.org/MOBOT/research/APweb/.

  • Stützel T (1998) Eriocaulaceae. In: The families and genera of vascular plants IV-flowering plants: Monocotyledons-Alismataceae and Commelinaceae (except Gramineae), (ed) Kubitzki K. Springer-Verlag, Berlin, pp 197–207

    Google Scholar 

  • Takada J (2017) A guide of Eriocaulon plants of Japan, 125 pp (in Japanese). Akita Kyodo Printing Co Ltd, Akita

    Google Scholar 

  • Tan AS, Rao AN (1974) Studies on the developmental anatomy of Dioscorea sansibarensis Pax (Dioscoreaceae). Bot J Linn Soc 69:211–227

    Google Scholar 

  • Tomlinson PB (1969) Commelinales–Zingiberales. In: Metcalfe CR (ed) Anatomy of the Monocotyledons, vol. III, 446 pp. Clarendon Press, Oxford

  • Tomlinson PB (1995) Non-homology of vascular organisation in monocotyledons and dicotyledons. In: Rudall PJ, Cribb PJ, Cutler DF, Humphries CJ (eds) Monocotyledons: systematic and evolution. Royal Botanic Gardens, Kew, Kew, pp 589–622

    Google Scholar 

  • Tomlinson PB, Spangler R (2002) Developmental features of the discontinuous stem vascular system in the rattan palm Calamus (Arecaceae-Calamoideae-Calamineae). Am J Bot 89:1128–1141

    PubMed  Google Scholar 

  • Tomlinson PB, Fisher JB, Spangler RE, Richer RA (2001) Stem vascular architecture in the rattan palm Calamus (Arecaceae-Calamoideae-Calaminae). Am J Bot 88:797–809

    CAS  PubMed  Google Scholar 

  • Vita RSB, Menzes NL, Pellegrini MOO, Melo-de-Pinna GFA (2019) A new interpretation on vascular architecture of the cauline system in Commelinaceae (Commelinales). PLoS ONE 14:e0218383

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann WH, Tomlinson PB (1965) Anatomy of the palm Rhapis excelsa I Mature vegetative axis. J Arnold Arbor 46:160–177

    Google Scholar 

  • Zimmermann WH, Tomlinson PB (1968) Vascular construction and development in the aerial stem of Prionium (Juncaceae). Am J Bot 55:1100–1109

    Google Scholar 

  • Zimmermann WH, Tomlinson PB (1972) The vascular system of monocotyledonous stems. Bot Gaz 133:141–155

    Google Scholar 

Download references

Acknowledgments

We thank Jun Takada (Akita Natural History Society, Japan) for helping us to collect materials. We thank three anonymous reviewers for their helpful comments. This work was partially supported by JSPS KAKENHI Grant number JP26440205 (to Y.E.).

Author information

Authors and Affiliations

  1. Graduate School of Science and Engineering, Ibaraki University, Bunkyo 2-1-1, Mito, 310-8512, Japan

    Yasuhiko Endo & Fumiya Sugawara

  2. Karabe 4-26-38, Narita, 286-0036, Japan

    Katsuhiro Yashiro

Authors
  1. Yasuhiko Endo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fumiya Sugawara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katsuhiro Yashiro
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yasuhiko Endo.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Endo, Y., Sugawara, F. & Yashiro, K. Acropetally developing vascular bundles coexisting with basipetally developing and basally blindly ended vascular bundles in scapes of Eriocaulon taquetii (Eriocaulaceae, monocotyledons). J Plant Res 134, 765–778 (2021). https://doi.org/10.1007/s10265-021-01292-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-021-01292-6

Keywords

  • Acropetally developing
  • Basipetally developing
  • Blindly ended vascular bundle
  • Eriocaulon taquetii
  • Monocotyledon
  • Synapomorphy