Skip to main content
SpringerLink
Log in

Androecium anatomy of Isertia laevis, a polysporangiate species of Rubiaceae

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

In this study, we performed an anatomical analysis of the polysporangiate anthers and the development of pollen in Isertia laevis (Rubiaceae) with the aim to elucidate the internal structure of these atypical anthers. For this purpose, flowers in successive stages of development were dissected and the anthers were processed for conventional anatomical analysis. The material was examined using light microscopy and scanning electron microscopy. The present study shows that the anthers of Isertia laevis have two thecae divided into multiple microsporangia. This division is due to the presence of transverse and longitudinal septa formed of parenchyma and idioblasts with crystals. The septa appear together with the microsporangia and remain in the mature anther, even developing fibrous thickening. As the anther matures, the idioblasts in the septa accumulate crystals until they break, facilitating the separation of the septa from the outer wall of the theca, and thus apparently assisting the process of dehiscence. The mature anther opens through the longitudinal dehiscence of each theca. In addition to the anatomy of the anther, the development and morphology of the pollen, and the presence of orbicules are described. The structure of the anthers of I. laevis is discussed with other polysporangiate species in the Rubiaceae and angiosperms.

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

Similar content being viewed by others

References

  • Amaral MCE, Bittrich V, Endress PK, Stevens PF (2017) The unique morphology of resin-producing multilocellate anthers and their evolution in Clusia (Clusiaceae). Bot J Linn Soc 184:79–93

    Google Scholar 

  • Andersson L, Antonelli A (2005) Phylogeny of the tribe Cinchoneae (Rubiaceae), its position in Cinchonoideae, and description of a new genus, Ciliosemina. Taxon 54:17–28

    Google Scholar 

  • Baumgratz JFA, Souza MLDR, Woodgyer EM, Nic Lughadha EM (1996) Polysporangiate anthers: described for the first time in Melastomataceae. Kew Bull 51(1):133–144

    Google Scholar 

  • Bonner LJ, Dickinson HG (1989) Anther dehiscence in Lycopersicon esculentum Mill. I. Structural aspects. Wezc- Phvtol 113:97–115

    Google Scholar 

  • Boom BM (1984) A revision of Isertia (Isertieae: Rubiaceae). Brittonia 36(4):425–454

    Google Scholar 

  • Bremer B, Thulin M (1998) Collapse of Isertieae, re-establishment of Mussaendeae, and a new genus of Sabiceeae (Rubiaceae); phylogenetic relationships based on rbcL data. Plant Syst Evol 211:71–92

    Google Scholar 

  • Chatin M (1866) The placentoid, a new organ of anthers. Ann Mag Nat Hist 17:395–397

    Google Scholar 

  • D’Arcy G, Keating RC (1996) The anther: form, function, and phylogeny. Cambridge University Press, New York, 351 p

    Google Scholar 

  • Dávila N, Vicentini A (2016) Isertia psammophila (Isertieae, Rubiaceae), a new species from white-sand areas of the Brazilian Amazon. Phytotaxa 257(2):174–180

    Google Scholar 

  • Delprete P (1996) Notes on the taxonomic position of the monotypic Brazilian genus Kerianthera (Rubiaceae). Opera Bot Belg 7:271–275

    Google Scholar 

  • Endress PK, Stumpf S (1990) Non-tetrasporangiate stamens in the angiosperms: structure, systematic distribution and evolutionary aspects. Bot Jahrb Syst 112:193–240

    Google Scholar 

  • Erdtman C (1966) Pollen morphology and plant taxonomy-Angiosperms (An introduction to palynology). Revised Edition. Haner Pub. Co., New York

    Google Scholar 

  • Gonzalez AM, Cristóbal CL (1997) Anatomía y ontogenia de semillas de Helicteres lhotzkyana (Sterculiaceae). Bonplandia 9:287–294

    Google Scholar 

  • Govaerts R, Ruhsam M, Andersson L, Robbrecht E, Bridson DM, Davis AP, Schanzer I, Sonké B (2011) World checklist of Rubiaceae. Royal Botanic Gardens, Kew. Available at: http://www.kew.org/wcsp/rubiaceae

    Google Scholar 

  • Grandtner MM, Chevrette J (2013) Dictionary of trees, Volume 2: South America: nomenclature, taxonomy and ecology. Academic, Amsterdam, 1172 pp

    Google Scholar 

  • Horner HT, Wagner BL (1980) The association of druse crystals with the developing stomium of Capsicum annuum (Solanaceae) anthers. Am J Bot 67(9):1347–1360

    Google Scholar 

  • Huysmans S, El-Ghazaly G, Nilsson S, Smets E (1997) Systematic value of tapetal orbicules: a preliminary survey of the Cinchonoideae (Rubiaceae). Can J Bot 75:815–826

    Google Scholar 

  • Huysmans S, El-Ghazaly G, Smets E (1998a) Orbicules in Angiosperms: morphology, function, distribution, and relation with tapetum types. Bot Rev 64(3):240–272

    Google Scholar 

  • Huysmans S, Robbrecht E, Smets E (1998b) A collapsed tribe revisited: pollen morphology of the Isertieae (Cinchonoideae–Rubiaceae). Rev Palaeobot Palynol 104:85–113

    Google Scholar 

  • Hyde HA (1955) Oncus, a new term in pollen morphology. New Phytol 54:255–256

    Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Judkevich MD, Gonzalez AM, Salas RM (2020a) A new species of Randia (Rubiaceae) and the taxonomic significance of foliar anatomy in the species of Randia of the Southern Cone of America. Syst Bot 45(3):607–619

    Google Scholar 

  • Judkevich MD, Salas RM, Gonzalez AM (2020b) Anther structure and pollen development in species of Rubiaceae and anatomical evidence of pathway to morphological dioecy. An Acad Bras Ciênc (in press)

  • Kirkbride JH (1985) Manipulus rubiacearum IV. Kerianthera (Rubiaceae), a new genus from Amazonian Brazil. Brittonia 37(1):109–116

    Google Scholar 

  • Lersten NR (1971) A review of septate microsporangia in vascular plants. Iowa State Coll J Sci 45:487–497

    Google Scholar 

  • Lima JF, Romero R, Simão DG (2019) Polysporangiate anthers in Microlicia D.Don (Melastomataceae Juss.). Feddes Repert 130:9–18

  • Luque R, Sousa HC, Kraus JE (1996) Métodos de coloração de Roeser (1972) - modificado - de Kropp (1972) visando a substituição do azul de astra por azul de alcião 8 GS ou 8 GX. Acta Bot Bras 10:199–212

    Google Scholar 

  • Oliveira CT, Giacomin LL, Zappi DC (2011) Kerianthera longiflora (Rubiaceae), a remarkable new species from eastern Brazil, with some observations on K. preclara. Kew Bull 66:1–6

    Google Scholar 

  • Pacini E, Franchi GG, Hesse M (1985) The tapetum: its form, function, and possible phylogeny in Embryophyta. Plant Syst Evol 149:155–185

    Google Scholar 

  • Pandey R, Pandey CN (2013) Microsporogenesis and microgemetogenesis in a cryptoviviparous mangrove species- Aegiceras corniculatum (L.) Blanco. JPS 2(2):53–60

    Google Scholar 

  • Patel VC, Skvarla JJ, Raven PM (1984) Pollen characters in relation to the delimitation of Mirtales. Ann Missouri Bot Gar 71:858–969

    Google Scholar 

  • Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143:1–81

  • Robayo C, Marquínez X, Raz L, Nickrent DL (2020) Floral anatomy of the plant Psittacanthus schiedeanus (Loranthaceae). Rev Biol Trop 68(1):1–11

    Google Scholar 

  • Robbrecht E (1981) Studies in tropical African Rubiaceae (II). Bull Jard Bot Nat Belg 51:359–378

    Google Scholar 

  • Robbrecht E (1984) The delimitation and taxonomic position of the tropical African genera Leptactiua and Dictyandra (Rubiaeeae). Plant Syst Evol 145:105–118

    Google Scholar 

  • Robbrecht E, Manen JF (2006) The major lineages of the coffee family (Rubiaceae, Angiosperms). Syst Geogr Plants 76:85–145

    Google Scholar 

  • Romero MF, Salas RM, Gonzalez AM (2017) Pollen development and orbicule and pollen grain morphology in species of Cephalanthus (Rubiaceae-Naucleeae) from the Americas. Aust J Bot 65:233–247

    Google Scholar 

  • Ruggiero F, Bedini G (2020) Phylogenetic and morphologic survey of orbicules in angiosperms. Taxon 69:543–566

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16:46–60

    Google Scholar 

  • Sonké B, Djuikouo MK, Robbrecht E (2007) Calycosiphonia pentamera sp. nov. (afrotropical Rubiaceae) from the ‘Lower Guinea’ area. Nord J Bot 25:275–280

    Google Scholar 

  • Suaza-Gaviria V, Pabón-Mora N, González F (2016) Development and morphology of flowers in Loranthaceae. Int J Plant Sci 177(7):559–578

    Google Scholar 

  • Sudhakaran S, Vaidyanathan R, Ganapathi A (1995) Microsporogenesis in a mangrove Rhizophora mucronata Lam. Thaiszia J Bot 5:27–30

    Google Scholar 

  • Tilney PM, Van Wyk AE (1997) Pollen morphology of Canthium, Keetia and Psydrax (Rubiaceae: Vanguerieae) in southern Africa. Grana 36:249–260

    Google Scholar 

  • Tilney PM, Van Wyk AE, Van Der Merwe CF (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

    PubMed  PubMed Central  Google Scholar 

  • Tobe H, Raven PH (1986) Evolution of polysporangiate anthers in Onagraceae. Am J Bot 73(4):475–488

    Google Scholar 

  • Tsou C, Johnson DM (2003) Comparative development of aseptate and septate anthers of Annonaceae. Am J Bot 90(6):832–848

    PubMed  Google Scholar 

  • Verellen JEF, Dessein S, Razafimandimbison AG, Smets E, Huysmans S (2007) Pollen morphology of the tribes Naucleeae and Hymenodictyeae (Rubiaceae– Cinchonoideae) and its phylogenetic significance. J Linn Soc Bot 153:329–341

    Google Scholar 

  • Verstraete B, Groeninckx I, Smets E, Huysmans S (2011) Phylogenetic signal of orbicules at family level: Rubiaceae as case study. Taxon 60:742–757

    Google Scholar 

  • Vinckier S, Smets E (2002) Systematic importance of orbicule diversity in Gentianales. Grana 41:158–182

    Google Scholar 

  • Vinckier S, Smets E (2005) A histological study of microsporogenesis in Tarenna gracilipes (Rubiaceae). Grana 44:30–44

    Google Scholar 

  • Wilson ZA, Song J, Taylor B, Yang C (2011) The final split: the regulation of anther dehiscence. J Exp Bot 62:1633–1649

    CAS  PubMed  Google Scholar 

  • Wolff D, Braun M, Liede S (2003) Nocturnal versus diurnal pollination success in Isertia laevis (Rubiaceae): a sphingophilous plant visited by hummingbirds. Plant Biol 5:71–78

  • Yue L, Kuang Y, Liao J (2017) Ontogeny of permanent tetrads in Gardenia jasminoides (Rubiaceae) provides insight into pollen evolution. Rev Palaeobot Palynol 47:120–132

    Google Scholar 

Download references

Acknowledgments

We thank María Florencia Romero and Mariela Núñez Florentín for providing the SEM photo of the pollen grains and orbicules used in this work. Special thanks are given to Finn Borchsenius, Henrik Balslev, and Birgitte Bergmann from Aarhus herbarium, Denmark, who kindly provided us with both fixed and herbarium materials.

Author contribution statement

RMS provided the plant material and gave data on the environment of the species. MDJ processed the plant material to make the histological preparations, took the microscopy photos, and prepared the figures. MDJ and AMG performed the anatomical interpretations. MDJ and AMG contributed in the discussions and approved the final manuscript.

Funding

This work was funded by PICTO-UNNE 0199/2011, PICT 2016-3517, and CONICET PIP-112-2011-0100906 grants.

Author information

Authors and Affiliations

  1. Instituto de Botánica del Nordeste, Consejo Nacional de Investigaciones Científicas y Técnicas, Universidad Nacional del Nordeste, Sargento Cabral 2131, CC 209, 3400, Corrientes, Argentina

    Marina D. Judkevich, Roberto M. Salas & Ana M. Gonzalez

  2. Facultad de Ciencias Exactas y Naturales y Agrimensura, Universidad Nacional del Nordeste, Av. Libertad 5279, CC 209, 3400, Corrientes, Argentina

    Roberto M. Salas

  3. Facultad de Ciencias Agrarias, Universidad Nacional del Nordeste, Sargento Cabral 2131, CC 209, 3400, Corrientes, Argentina

    Ana M. Gonzalez

Authors
  1. Marina D. Judkevich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Roberto M. Salas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana M. Gonzalez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina D. Judkevich.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Handling Editor: Benedikt Kost

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Judkevich, M.D., Salas, R.M. & Gonzalez, A.M. Androecium anatomy of Isertia laevis, a polysporangiate species of Rubiaceae. Protoplasma 258, 547–557 (2021). https://doi.org/10.1007/s00709-020-01582-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-020-01582-1

Keywords

Search

Navigation