Anatomy of vegetative organs in Allionia (Nyctaginaceae), with emphasis on the vascular system

  • Israel L. Cunha Neto Department of Botany, Institute of Bioscience, University of São Paulo
  • Juliana P. Silva Department of Botany, Institute of Bioscience, University of São Paulo
  • Veronica Angyalossy Department of Botany, Institute of Bioscience, University of São Paulo
Keywords: Allionia choisyi, Allionia incarnata, Caryophyllales, Nyctagineae, ontogeny, cambial variants


Allionia is a small genus within the tribe Nyctagineae (Nyctaginaceae) which has a controversial, infrageneric delimitation. Here, we investigated the two known species of Allionia in order to characterize the anatomy of leaves, stems and roots, with further notes on vascular system development. Additionally, the present study aimed to broaden our knowledge of stem vascular diversity and to survey for anatomical features with diagnostic value in distinguishing A. choisyi from A. incarnata. Leaf anatomy of other Nyctagineae taxa was also analysed. Anatomical and ontogenetic observations from the vegetative organs in Allionia revealed no diagnostic features to distinguish the two species. We illustrated the occurrence of Kranz anatomy, which in Nyctaginaceae is only known in Allionia, Boerhavia, and Okenia. The stem primary vascular system was unusual in showing a polycyclic eustele (medullary bundles + continuous concentric procambium). Likewise, mature stems and roots show vascular cambial variants (successive cambia) that arise from the pericycle. The anatomy and histochemistry of multicellular glan-dular trichomes observed in aerial organs were presented. Raphids were seen in all organs. Although no strong xerophytic features were observed in Allionia, several characteristics can be associated with their arid habitats. Our findings on the vascular system of Allionia showed the two species to be much the same and reinforced earlier findings that the stem anatomy of Nyctaginaceae is complex and intriguing.


Alexander, P.J., N.A. Douglas, H. Ochoterena, H. Flores-Olvera, & M.J. Moore. 2014. Recent finding on the gypsum flora of the rim of the Guadalupe Mountains, New Mexico, U.S.A.: A new Species of Nerisyrenia (Brassicaceae), a new state record, and an update checklist. J. Bot. Res. Inst. Texas 8:383–393.

Angyalossy, V., M.R. Pace, R.F. Evert, C.R. Marcati, A.A. Oskolski, T. Terrazas, E. Kotina, F. Lens, S.C. Mazzoni-viveiros, & G. Angeles. 2016. IAWA list of microscopic bark features. IAWA J. 37:517–615.

Antonucci, N.P. 2010. Estudos anatômicos, ultra-estruturais e bioquímicos da síndrome Kranz em folhas de duas espécies de Gomphrena L. (Amaranthaceae). (Doctoral dissertation). Universidade de São Paulo, São Paulo, Brazil.

Balfour, E. 1965. Anomalous secondary thickening in Chenopodiaceae, Nyctaginaceae and Amaranthaceae. Phytomorphology 15:111–122.

Barbosa, A.C.F., M.R. Pace, L. Witovisk, & V. Angyalossy. 2010. A new method to obtain good anatomical slides of heterogeneous plant parts. IAWA J. 31:373–383.

Bittrich, V. & U. Kuhn. 1993. Nyctaginaceae. In: Kubitzki, K., J.G. Rohwer, V. Bittrich, eds. The families and genera of flowering plants, vol. 2. Springer, Berlin, Germany.

Borer C.H., M.N. Hamby, & L.H. Hutchinson. 2012. Plant tolerance of a high calcium environment via foliar partitioning and sequestration. J. Arid Environ. 85:128–131.

Cain, A. J. 1947. The use of Nile blue in the examination of lipids. J. Cell Sci. 3:383–392.

Carlquist, S. 2001. Comparative wood anatomy. Systematic, ecological and evolutionary aspects of dicotyledon wood. Springer, Berlin, Germany.

Carlquist, S. 2004. Lateral meristems, successive cambia and their products: A reinterpretation based on roots and stems of Nyctaginaceae. Bot. J. Linn. Soc. 146:129–143.

Carlquist, S. 2007. Successive cambia revisited: Ontogeny, histology, diversity, and functional significance. J. Torrey Bot. Soc. 134:301–332.

Carlquist, S. 2010. Caryophyllales: A key group for understanding wood anatomy character states and their evolution. Bot. J. Linn. Soc. 164:342–393.

Carlquist, S. 2012. How wood evolves: A new synthesis. Botany 90:901–940.

Carolin, R.C., S.W.L. Jacobs, & M. Vesk. 1978. Kranz cells and mesophyll in the Chenopodiales. Austral. J. Bot. 5:683–698.

Chen, F.S., D.H. Zeng, T.J. Fahey, C.Y. Yao, & Z.Y. Yu. 2010. Response of leaf anatomy of Chenopodium acuminatum to soil resource availability in a semiarid grassland. Pl. Ecol. 209:375–382.

Cunha Neto, i.l., f.m. Martins, g.v. Somner, & n. Tamaio. 2018. Successive cambia in liana stems of Paullinieae and their evolutionary significance in Sapindaceae. Bot. J. Linn. Soc. 186: 66–88.

Cunha Neto, I.L., V. Angyalossy, & N.A. Douglas. 2019. What are the “sticky rings” on stems of Anulocaulis and related taxa (Nyctaginaceae) from arid regions? J. Bot. Res. Inst. Texas 2:477–485.

Cunha Neto, I.L., M.R. Pace, N.A. Douglas, M.H. Nee, C.F.C. Sa, M.J. Moore, & V. Angyalossy. 2020. Diversity, distribution, development and evolution of medullary bundles in Nyctaginaceae. Amer. J. Bot. 107: 1–19.

David R, & JP. Carde. 1964. Coloration différentielle des inclusions lipidiques et terpéniques des pseudophylles du Pin maritime au moyen du réactif Nadi. C. R. Acad. Sci. Paris 258: 1338–1340.

Debary, A. 1884. Comparative anatomy of the vegetative organs of the phanerogams and ferns. Clarendon Press, Oxford, UK.

Dickinson W.C. Integrative plant anatomy. 2000. Harcourt Academic Press, New York, U.S.A.

Doria L.C., D.S. Podadera, M. del Arco, T. Chauvin, E. Smets, S. Delzon, & F. Lens. 2018. Insular woody daisies (Argyranthemum, Asteraceae) are more resistant to drought-induced hydraulic failure than their herbaceous relatives. Funct. Ecol. 32:1467–1478.

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.

Esau, K. & V.I. Cheadle. 1969. Secondary growth in Bougainvillea. Ann. Bot. 33:807–819.

Fisher, D.B. 1968. Protein staining of ribboned epon sections for light microscopy. Histochemie 1:92–96.

Fay J.J. 1980. Nyctaginaceae. In: Gómez-Pompa A. ed. Flora de Veracruz 13. Instituto Nacional de Investigaciones sobre Recursos Bióticos, Xalapa, Mexico. Pp. 1–54.

Franceschi, V.R. & P.A Nakata. 2005. Calcium oxalate in plants: Formation and function. Ann. Rev. Pl. Biol. 56:41–71.

Gerlach, G. 1969. Botanische Mikrotechnik, eine Einführung. Thieme, Stuttgart, Germany.

Gibson, A.C. 1994. Vascular tissues. In: H.D. Behnke & T.J. Mabry, eds. Caryophyllales: Evolution and systematics. Springer, Berlin, Germany. Pp. 45–74.

Gregory, M. & Baas, P. 1989. A survey of mucilage cells in vegetative organs of the dicotyledons. Israel J. Bot. 2–3:125–174.

Haberlandt, G. 1882. Die physiologischen Leistungen der Pflanzengewebe. Trewendt.

Heimerl, A. 1932. Nyctaginaceen-Studien. Notizblatt des Botanischen Gartens und Museums zu Berlin-Dahlem, Germany. Pp. 450–470.

Hernandez-Ledesma, P. & H. Flores-Olvera. 2003. Nyctaginaceae de Hidalgo, México. Anales Inst. Biol. Univ. Nac. Auton. México, Bot. 74:231–287.

Hernandez-Ledesma, P., T. Terrazas, & H. Flores-Olvera. 2011. Comparative stem anatomy of Mirabilis (Nyctaginaceae). Pl. Syst. Evol. 292:117–132.

Hernandez-Ledesma, P. et al. 2015. A taxonomic backbone for the global synthesis of species diversity in the angiosperm order Caryophyllales. Willdenowia 45:281–383.

IAWA Committee. 1989. IAWA list of microscopic features for hardwood identification. IAWA Bull. n.s. 10:219–332.

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

Kraus, J.E. & M. Arduin. 1997. Manual básico de métodos em morfologia vegetal. EDUR, Rio de Janeiro, Brazil.

Leme, c.l.d., i.l. Cunha neto, & v. Angyalossy. 2020. How the neotropical liana Machaerium multifoliolatum (Fabaceae) develop their distinctive flattened stems? Flora 269: 151629.

Lopez, H.A. & A.M. Anton. 2006. Nyctaginaceae. In: A.T. Hunziker ed., Flora fanerogámica Argentina, Programa Proflora, Córdoba, Argentina. Pp. 1–22.

Lugo, M.A., K.O. Reinhart, E. Menoyo, E.M. Crespo, & C. Urcelay. 2015. Plant functional traits and phylogenetic relatedness explain variation in associations with root fungal endophytes in an extreme arid environment. Mycorrhiza 2:85–95.

Mauseth, J.D. 1988. Plant anatomy. The Benjamin/Cummings Publishing Company, Menlo Park, California, U.S.A.

Mikesell, J.E. & R.A Popham. 1976. Ontogeny and correlative relationships of the primary thickening meristem in Four-O’clock plants (Nyctaginaceae) maintained under long and short photoperiods. Amer. J. Bot. 63:427–437.

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.

Merlo, M.E., J.F. Mota, & P. Sanchez Gomez. 2011. Ecofisiología y adaptaciones de las plantas vasculares a las características físicas y químicas de sustratos especiales. In: Mota, J.F., Sánchez- P. Gómez & J.S. Guirado Romero, eds. Diversidad vegetal de las yeseras ibéricas. ADIF-Mediterráneo Asesores Consultores. Almería, Spain. Pp. 51–74.

Molano-Flores, B. 2001. Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann. Bot. 3:387–391.

Mota, J.F., J.A. Garrido-Becerra, M.E. Merlo, J.M. Medina-Cazorla, & P. Sanchez-Gomez. 2017. The edaphism: Gypsum, dolomite and serpentine flora and vegetation. In: Loidi, J. ed. The vegetation of the Iberian Peninsula. Springer, Cham., New York, U.S.A. Pp. 277–354.

Mulroy, T.W. & P.W. Rundel. 1977. Annual plants: Adaptations to desert environments. Bioscience 2:109–114.

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. Mac Cully. 1964. Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373.

Ocampo, G., N.K. Koteyeva, E.V. Voznesenskaya, E.E. Edwards, T.L. Sale, R.F. Sage, & J.T. Columbus. 2013. Evolution of leaf anatomy and photosynthetic path-ways in Portulacaceae. Amer. J. Bot. 100:2388–2402.

Pace, M.R., V. Angyalossy, P. Acevedo-rodriguez, & J. Wen. 2018. Structure and ontogeny of successive cambia in Tetrastigma (Vitaceae), the host plants of Rafflesiaceae. J. Syst. Evol. 56:394–400.

Palacio S., M. Aitkenhead, A. Escudero, G. Montserrat-Marti, M. Maestro, & J. Robertson. 2014a. Gypsophile chemistry unveiled: Fourier Transform Infrared (FTIR) spectroscopy provides new insight into plant adaptations to gypsum soils. PLoS One 9:107–285.

Palacio S., J. Azorin, G. Montserrat-Marti, J.P. Ferrio. 2014b. The crystallization water of gypsum rocks is a relevant water source for plants. Nat. Commun. 5:46–60.

Pearse, A. 1985. Carbohydrates and mucosubstances. In: Histochemistry theoretical and applied Analytical technology. Churchill Livingstone, Edinburgh London Melbourne New York. 2:675–753.

Phillips, B. 1976. Anatomy and developmental morphology of Allionia L. (Nyctaginaceae). Ph.D. dissertation. The University of Arizona, Tucson, U.S.A.

Rajput, K.S. & K.S. Rao. 1998. Cambial anatomy and absence of rays in the stem of Boerhaavia species (Nyctaginaceae). Ann. Bot. Fennici 35:131–135.

Rajput, S., V.S. Patil, & K.K. Kapadne. 2009. Structure and development of secondary thickening meristem in Mirabilis jalapa (Nyctaginaceae). Polish Bot. J. 54:113–121.

Rasband, W.S. 2012. ImageJ: Image processing and analysis in Java. Astrophysics Source Code Library.

Ruiz N., D. Ward, & S. Saltz. 2002. Calcium oxalate crystals in leaves of Pancratium sickenbergeri: Constitutive or induced defense? Funct. Ecol. 16:99–105

Rupp, P. 1964. Polyglykol als Einbettungsmedium zum Schneiden botanischer Präparate. Mikrokosmos 53:123–128.

Ruzin, S.E. 1999. Plant microtechnique and microscopy. Oxford University Press, New York, U.S.A.

Rzedowski J. & Calderon, de R.G. eds. 2001. Flora fanerogámica del valle de México. Instituto de Ecología, A. C., Centro Regional del Bajío and Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, México.

Sandoval-Ortega M.H., M.W. Siqueiros-Delgado, R. Cerros-Tlatilpa, & G. Ocampo. 2020. La familia Nyctaginaceae (Caryophyllales) em Aguascalientes, México. Act. Bot. Mex. 127:e1673.

Scheck, H. 1893. Beiträge zur Biologie und Anatomie der Lianen im Besonderen der in Brasilien einheimische. Belträge zur Anatomie der Lianen. In: Schimper, AFW; Fischer, G. Botanische Mittheilungen aus der Tropens. Gustav Fischer, Jena, Germany.

Schwallier, R., B. Gravendeel, H. De Boer, S. Nylinder, B.J. Van Heuven, A. Sieder, & F. Lens. 2017. Evolution of wood anatomical characters in Nepenthes and close relatives of Caryophyllales. Ann. Bot. 119:1179–1193.

Schweingruber, F.H. 2011. Atlas of stem anatomy in herbs, shrubs and trees. Springer-Verlag, Berlin, Germany.

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

Spellenberg, R. 2012. Nyctaginaceae. In: N. Holmgren, P.K. Holmgren, J.L. Reveal, et al., Intermountain Flora Vol. 2, pt. A, New York Botanical Garden, Bronx, New York, U.S.A. Pp. 574–604.

Standley, P.C. 1931. The Nyctaginaceae and Chenopodiaceae of northwestern South America. Field Mus. Nat. Hist., Bot. Ser. 11:171–254.

Stevenson, D.W. & R.A. Popham. 1973. Ontogeny of the primary thickening meristem in seedlings of Bougainvillea spectabilis. Amer. J. Bot. 60:1–9.

Struwig, M., S.J. Siebert, & E.S. Klaassen. 2011. Nyctaginaceae. Bothalia 2:289–292.

Sukhorukov, A.P., M.V. Nilova, M.J. Moore, E.F.S. Rossetto, & N.A. Douglas. (In Press). Anatomical Diversity and evolution of the anthocarp in Nyctaginaceae. Bot. J. Linn. Soc.

Syvertsen, J.P., G.L. Nickell, R.W. Spellenberg, & G.L. Cunningham. 1976. Carbon reduction pathways and standing crop in three Chihuahuan Desert plant communities. S. W. Naturalist 21:311–320.

Turner, B.L. 1994. Revisionary study of the genus Allionia (Nyctaginaceae). Phytologia 77:45–55.

Voznesenskaya, E.V., N.K. Koteyeva, G.E. Edwards, & G. Ocampo. 2010. Revealing diversity in structural and biochemical forms of C4 photosynthesis and a C3–C4 intermediate in genus Portulaca L. (Portulacaceae). J. Exp. Bot. 61:3647–3662.

Waterfall, U.T. 1946. Observations on the desert gypsum flora of southwestern Texas and adjacent New Mexico. Amer. Midl. Naturalist 36:456– 466.

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

Zieminska, K., M. Westoby, & I.J. Wright. 2015. Broad anatomical variation within a narrow wood density range—a study of twig wood across 69 Australian angiosperms. PLoS ONE 10:e012489.

How to Cite
Cunha Neto, I. L., Silva, J. P., & Angyalossy, V. (2020). Anatomy of vegetative organs in Allionia (Nyctaginaceae), with emphasis on the vascular system. Journal of the Botanical Research Institute of Texas, 14(2), 373-394.