What are the "sticky rings" on stems of Anulocaulis and related taxa (Nyctaginaceae) from arid regions?

  • Israel Lopes da Cunha Neto Department of Botany, Institute of Bioscience, University of Sao Paulo
  • Veronica Angyalossy Department of Botany, Institute of Bioscience, University of Sao Paulo
  • Norman A. Douglas Department of Biology, University of Florida
Keywords: anatomy, Caryophyllales, Nyctagineae, secretory structures, Chihuahuan Desert, glandular trichomes

Abstract

Anulocaulis, commonly known as “ringstem,” is a small, unusual genus restricted to the Chihuahuan, Sonoran, and Mojave deserts of North America. Here we combined light microscopy and histochemical tests to characterize for the first time the “sticky structures” (here called secretory rings) found on the stem internodes of Anulocaulis. The secretory rings were shown to be groups of epidermal cells, or unicellular glandular trichomes, which largely differ from their neighboring cells both in structure and histochemistry. The cells start to differentiate in early stages of stem development. They begin as regular epidermal cells, but later their anticlinal and external tangential walls start to enlarge. At maturity the cells become remarkably elongated, even balloon-like, with dense cytoplasmic content. Although the secretory rings have been reported as “mucilaginous structures” based on morphological observations, preliminary histochemical analyses showed that its exudate is complex, including a mixture of mucilage, proteins, and phenolic compounds. Future investigations are needed to compare the anatomy of the secretory rings within related genera of Nyctaginaceae and characterize the chemical components of their exudate more specifically to search for potential homologies and adaptive functions of these structures.

References

Anandan, S., A. Rudolph, T. Speck, & O. Speck. 2018. Comparative morphological and anatomical study of self-repair in succulent cylindrical plant organs. Flora 241:1–7.

Ballego-Campos, I. & E.A.S. Paiva. 2018. Colleters in the vegetative axis of Aechmea blanchetiana (Bromeliaceae): Anatomical, ultrastructural and functional aspects. Austral. J. Bot. 66:379–387.

Bittrich, V. & U. Kühn. 1993. Nyctaginaceae. In: K. Kubitzki, J.G. Rohwer & V. Bittrich, eds. The families and genera of flowering plants, Vol. 2. Springer, Berlin, Germany. Pp. 473–486.

Bukatch, F. 1972. Bemerkungen zur Doppelfärbung Astrablau-Safranin. Mikrokosmos 61:255.

Christodoulakis, N.S., H. Tsimbani & C. Fasseas. 1990. Leaf structural peculiarities in Sarcopoterium spinosum, a seasonally dimorphic subshrub. Ann. Bot. 65:291–296.

Demarco, D. 2017. Histochemical analysis of plant secretory structures. In: C. Pellicciari & M. Biggiogera, eds. Histochemistry of single molecules. Methods in molecular biology. Vol. 1560. Springer, New York, U.S.A. Pp. 313–330.

Douglas, N.A. & P.S. Manos. 2007. Molecular phylogeny of Nyctaginaceae: Taxonomy, biogeography, and characters associated with a radiation of xerophytic genera in North America. Amer. J. Bot. 94:856–872.

Douglas, N.A. & R. Spellenberg. 2010. A new tribal classification of Nyctaginaceae. Taxon 59:905–910.

Evert, R.F. 2006. Esau’s plant anatomy: Meristems, cells, and tissues of the plant body – their structure, function, and development. 3rd edn. JohnWiley and Sons, Hoboken.

Fahn, A. 1979. Secretory tissues in plants. Academic Press, London, U.K., New York, San Francisco, U.S.A.

Fernandes, V.F., M. Thadeo, V.C. Dalvi, & R.M.S.A. Meira. 2017. Secretory structures in Casearia sylvestris Sw. (Salicaceae): Diversity, mechanisms of secretion, and exudate complexity. Int. J. Pl. Sci. 178:288–301.

Gregory, M. & P. Baas. 1989. A survey of mucilage cells in vegetative organs of the dictotyledons. Israel J. Bot. 38:125–174.

Hernández-Ledesma, P., H. Flores-Olvera, & H. Ochoterena. 2010. Cladistic analysis and taxonomic synopsis of Anulocaulis Standl. (Nyctaginaceae) based on morphological data. Syst. Bot. 35:858–876.

Johansen, D.A. 1940. Plant microtechnique. McGraw-Hill, New York, U.S.A.

Karban, R., E. LoPresti, A. Pepi, & P. Grof-Tisza. 2019. Induction of the sticky plant defense syndrome in wild tobacco. Ecology 00(00): e02746. 10.1002/ecy.2746

Krimmel, B.A. & I.S. Pearse. 2013. Sticky plant traps insects to enhance indirect defence. Ecol. Lett. 16:219–224.

Kuster, V.C., L.C. Silva, R.M.S.A Meira, & A.A. Azevedo. 2018. Structural adaptation and anatomical convergence in stems and roots of five plant species from a “Restinga” sand coastal plain. Flora 243:77–87.

LoPresti, E.F. 2015. Chemicals on plant surfaces as a heretofore unrecognized, but ecologically informative, class for investigations into plant defence. Biol. Rev. 91:1102–1117.

LoPresti, E.F. & R. Karban. 2016. Chewing sandpaper: grit, plant apparency, and plant defense in sand-entrappping plants. Ecology 97:826–833.

LoPresti, E.F., P., Grof-Tisza, M. Robinson, J. Godfrey & R. Karban. 2018. Entrapped sand as a plant defence: effects on herbivore performance and preference: Entrapped sand and caterpillar performance. Ecol. Entomol. 43:154–161.

LoPresti, E., B. Krimmel, & I.S. Pearse. 2018. Entrapped carrion increases indirect plant resistance and intra-guild predation on a sticky tarweed. Oikos 127:1033–1044.

Matthews, M.L. & P.K. Endress. 2006. Floral structure and systematics in four orders of rosids, including a broad survey of floral mucilage cells. Pl. Syst. Evol. 260:199–222.

McClellan, Y. & W.J. Boecklen. 1993. Plant mediation of ant–herbivore associations: The role of sticky rings formed by Boerhavia spicata. Coenoses 8:15–20.

Metcalfe, C.R. & L. Chalk. 1950. Anatomy of the dicotyledons: leaves, stems, and wood in relation to taxonomy with notes on economic uses. Clarendon Press, Oxford, UK.

Monteiro, R.F. & M.V. Macedo. 2014. First report on the diversity of insects trapped by a sticky exudate of the inflorescences of Vriesea bituminosa Wawra (Bromeliaceae: Tillandsioideae). Arthropod Pl. Interact. 8:519–523.

Moore, M.J., J.F. Mota, N.A. Douglas, H. Flores-Olvera, & H. Ochoterena. 2014. The ecology, assembly, and evolution of gypsophile floras. In: N. Rajakaruna, R. Boyd & T. Harris, eds. Plant ecology and evolution in harsh environments. Nova Science Publishers, Hauppauge, New York, U.S.A. Pp. 97–128.

O’Brien, T.P., N. Feder, & M.W. MacCully. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373.

Rudall, P. 2007. Anatomy of flowering plants, 3rd edn. Cambridge University Press, Cambridge, U.K.

Spellenberg, R. 1993. Taxonomy of Anulocaulis (Nyctaginaceae). Sida 15:373–389.

Spellenberg, R. 2003. Nyctaginaceae. In: Flora of North America Editoral Committee, eds. Flora of North America north of Mexico. Oxford University Press, New York, New York, U.S.A. Pp. 14–74.

Standley, P.C.1909. The Allioniaceae of the United States with notes on Mexican species. Contr. U.S. Natl. Herb. 12:303–389.

Tilney, P.M., A.E. van Wykm, & C.F. van der Merwe. 2014. The epidermal cell structure of the secondary pollen presenter in Vangueria infausta (Rubiaceae: Vanguerieae) suggests a functional association with protruding onci in pollen grains. PLoS ONE 9:e96405. doi:10.1371/journal.pone.0096405.

Voragen, A.G.J., G.J. Coenen, R.P. Verhoef, & H.A. Schols. 2009. Pectin, a versatile polysaccharide present in plant cell walls. Struct. Chem. 20:263–275.

Willson, J. & R. Spellenberg. 1977. Observations on anthocarp anatomy in the subtribe Mirabilinae (Nyctaginaceae). Madroño 24:104–111.

Published
2019-10-31
How to Cite
Lopes da Cunha Neto, I., Angyalossy, V., & Douglas, N. A. (2019). What are the "sticky rings" on stems of Anulocaulis and related taxa (Nyctaginaceae) from arid regions?. Journal of the Botanical Research Institute of Texas, 13(2), 477-485. https://doi.org/10.17348/jbrit.v13.i2.803