Skip to main content
SpringerLink
Log in

Structural aspects of cypsela and seed development of Trichocline catharinensis (Cabrera): a Brazilian endemic species

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

Abstract

This is the first study to describe in a timescale morphohistological and ultrastructural characteristics of fruit (cypsela) and seed development in Trichocline catharinensis, which was completed 21 days after anthesis (DAA). At anthesis, we identified an ovary with three differentiated regions, including the inner epidermis, inner part, and outer epidermis. The mature ovule showed an integument with the outer epidermis, integumentary parenchyma, and endothelium. Cells around the endothelium form the periendothelial zone with thick cell walls that showed Periodic acid-Schiff (PAS)–positive reaction. The periendothelial zone and endothelium showed degradation of the cells during embryogenesis. The main stages of embryo development from fecundation through mature seed were identified. The ripe cypsela showed the pericarp (exocarp), seed coat (exotesta), and remaining endosperm surrounding the embryo. Mature embryos were straight with shoot apical meristem (SAM), and root apical meristem (RAM) was separated by the hypocotyl. Light microscopy (LM) and transmission electron microscopy (TEM) analyses indicate cells with characteristics of meristem cells, as well as proteins and lipid bodies and mitochondria with few cristae in cotyledon cells. Our findings provide insight into taxonomic and physiological studies by detailing cypsela and seed ontogenesis from an endemic and vulnerable Asteraceae from southern Brazil. This study is also a starting point for establishing the biological criteria for seed harvesting and future studies of seed physiology and conservation of plant genetic resource.

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

Similar content being viewed by others

Abbreviations

CBB:

Coomassie brilliant blue (stain)

DAA:

Day(s) after anthesis

ER:

Endoplasmic reticulum

LM:

Light microscopy

lbs:

Lipid bodies

PAS:

Periodic acid-Schiff (stain)

pbs:

Protein bodies

PCD:

Programmed cell death

RAM:

Root apical meristem

SAM:

Shoot apical meristem

TB-O:

Toluidine blue (stain)

TEM:

Transmission electron microscopy

TUNEL:

Terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling

References

  • Aguado M, Martínez-Sánchez JJ, Reig-Arminana J, García-Breijo FJ, Franco JA, Vicente MJ (2011) Morphology, anatomy and germination response of heteromorphic achenes of Anthemis chrysantha J. Gay (Asteraceae), a critically endangered species. Seed Sci Res 21:283–294. https://doi.org/10.1017/S0960258511000183

    Article  Google Scholar 

  • Batista MF, da Silva Santos L, Muller RH, de Souza LA (2015) Seed characters and their usefulness in the separation of Asteraceae species. Acta Sci Biol Sci 37:505. https://doi.org/10.4025/actascibiolsci.v37i4.27964

    Article  CAS  Google Scholar 

  • Bouman F (1974) Developmental studies of the ovule, integuments and seed in some angiosperms. Dissertation, University of Amsterdam

  • Bradford KJ (2018) Interpreting biological variation: seeds, populations and sensitivity thresholds. Seed Sci Res 28(3):158–167

  • Cabrera AL, Klein RM (1973) Compostas tribo Mutisieae. In: Cabrera AL, Klein RM (eds) Flora ilustrada catarinense. Herbário Barbosa Rodrigues, Itajaí, p 94

    Google Scholar 

  • Caccere R, Teixeira SP, Centeno DC, Rita de Cássia L, Braga MR (2013) Metabolic and structural changes during early maturation of Inga vera seeds are consistent with the lack of a desiccation phase. J Plant Physiol 170:791–800. https://doi.org/10.1016/j.jplph.2013.01.002

    Article  CAS  PubMed  Google Scholar 

  • Chen B-X, Shi C-Y, Huang J-M, Wang M, Liu J-X (2014) Megasporogenesis, female gametophyte development and embryonic development of Ambrosia L. in China. Plant Syst Evol 300:197–208. https://doi.org/10.1007/s00606-013-0872-0

    Article  Google Scholar 

  • Colette A, Lu K-J, Weijers D (2015) Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142:420–430. https://doi.org/10.1242/dev.111500

    Article  CAS  Google Scholar 

  • de Oliveira Franca R, De-Paula OC, Carmo-Oliveira R, Marzinek J (2015) Embryology of Ageratum conyzoides L. and A. fastigiatum RM King & H. Rob.(Asteraceae). Acta Bot Bras 29:08–15. https://doi.org/10.1590/0102-33062014abb3609

    Article  Google Scholar 

  • Dinneny JR, Yanofsky MF (2005) Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned. Bioessays 27:42–49. https://doi.org/10.1002/bies.20165

    Article  CAS  PubMed  Google Scholar 

  • Dodeman VL, Ducreux G, Kreis M (1997) Zygotic embryogenesis versus somatic embryogenesis. J Exp Bot 48:1493–1509

    CAS  Google Scholar 

  • dos Santos Julio PG, Oliveira DMT (2009) Morfoanatomia comparada e ontogênese do pericarpo de Bidens gardneri Baker e B. pilosa L.(Asteraceae). Braz J Bot 32:109–116. https://doi.org/10.1590/S0100-84042009000100011

    Article  Google Scholar 

  • Farrant JM, Pammenter N, Berjak P, Walters C (1997) Subcellular organization and metabolic activity during the development of seeds that attain different levels of desiccation tolerance. Seed Sci Res 7:135–144. https://doi.org/10.1017/S0960258500003470

    Article  CAS  Google Scholar 

  • Figueiredo R, Duarte P, Pereira S, Pissarra J (2006) The embryo sac of Cynara cardunculus: ultrastructure of the development and localisation of the aspartic proteinase cardosin B. Sex Plant Reprod 19:93–101. https://doi.org/10.1007/s00497-006-0026-4

    Article  CAS  Google Scholar 

  • Frangiote-Pallone S, de Souza LA (2014) Pappus and cypsela ontogeny in Asteraceae: structural considerations of the tribal category. Revista Mexicana de Biodiversidad 85:62–77. https://doi.org/10.7550/rmb.32809

    Article  Google Scholar 

  • Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 426:147–153. https://doi.org/10.1038/nature02085

    Article  CAS  PubMed  Google Scholar 

  • Funk VA, Susanna A, Stuessy TF, Robinson H (2009) Classification of Compositae. In: Funk VA, Susanna A, Stuessy T, Bayer R (eds) Systematics, evolution and biogeography of the Compositae, pp 171–189

    Google Scholar 

  • Gahan PB (1984) Plant histochemistry and cytochemistry. Academic Press

  • Galastri NA, Oliveira DMTD (2010) Morfoanatomia e ontogênese do fruto e semente de Vernonia platensis (Spreng.) Less.(Asteraceae). Acta Bot Bras 24:73–83. https://doi.org/10.1590/S0102-33062010000100008

    Article  Google Scholar 

  • Goldberg RB, De Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266:605–614. https://doi.org/10.1126/science.266.5185.605

    Article  CAS  PubMed  Google Scholar 

  • Gordon E, McCandless E (1973) Ultrastructute and histochemistry of Chondrus crispus Stackhouse. Nova Scotian Inst Sci Proc

  • Gotelli MM, Galati BG, Medan D (2008) Embryology of Helianthus annuus (Asteraceae). In: Ann Bot Fenn, vol 2. BioOne, pp 81–96

  • Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Proc Natl Acad Sci 102:2238–2243

    Article  CAS  Google Scholar 

  • Haywood V, Kragler F, Lucas WJ (2002) Plasmodesmata: pathways for protein and ribonucleoprotein signaling. Plant Cell 14:S303–S325

    Article  CAS  Google Scholar 

  • Jana BK, Mukherjee SK (2014) Diversity of cypselar features and their taxonomic significance in three species of the genus Centaurea, tribe Cardueae of Asteraceae. Diversity and conservation of plants and traditional knowledge, pp 233–240

    Google Scholar 

  • Jenik PD, Gillmor CS, Lukowitz W (2007) Embryonic patterning in Arabidopsis thaliana. Annu Rev Cell Dev Biol 23:207–236. https://doi.org/10.1146/annurev.cellbio.22.011105.102609

    Article  CAS  PubMed  Google Scholar 

  • Jensen WA (1962) Botanical Histochemistry. Principles and practices. Freeman, San Francisco

    Google Scholar 

  • Jimenez-Lopez JC, Zienkiewicz A, Zienkiewicz K, Alché JD, Rodríguez-García MI (2016) Biogenesis of protein bodies during legumin accumulation in developing olive (Olea europaea L.) seed. Protoplasma 253:517–530. https://doi.org/10.1007/s00709-015-0830-5

    Article  CAS  PubMed  Google Scholar 

  • Johansen DA (1940) Plant microtechnic. Mc Grow Hill Book Company, Inc, New York

    Google Scholar 

  • Jones L, Milne JL, Ashford D, McQueen-Mason SJ (2003) Cell wall arabinan is essential for guard cell function. Proc Natl Acad Sci 100:11783–11788. https://doi.org/10.1073/pnas.1832434100

    Article  CAS  PubMed  Google Scholar 

  • Jouannic S, Lartaud M, Hervé J, Collin M, Orieux Y, Verdeil JL, Tregear JW (2011) The shoot apical meristem of oil palm (Elaeis guineensis ; Arecaceae): developmental progression and dynamics. Ann Bot 108:1477–1487. https://doi.org/10.1093/aob/mcr019

    Article  PubMed  PubMed Central  Google Scholar 

  • Jürgens G (2001) Apical–basal pattern formation in Arabidopsis embryogenesis. EMBO J 20:3609–3616. https://doi.org/10.1093/emboj/20.14.3609

    Article  PubMed  PubMed Central  Google Scholar 

  • Kapil RN, Tiwari SC (1978) The integumentary tapetum. Bot Rev 44:457-490. https://doi.org/10.1007/bf02860847

  • Katinas L, Pasini E (2016) Typifications in the genus Trichocline (Asteraceae: Mutisieae). Willdenowia 46:27–35

    Article  Google Scholar 

  • Katinas L, Pruski J, Sancho G, Tellería MC (2008) The subfamily Mutisioideae (Asteraceae). Bot Rev 74:469–716

    Article  Google Scholar 

  • Kermode AR (2011) Plant storage products (carbohydrates, oils and proteins). eLS

  • Kolczyk J, Stolarczyk P, Płachno BJ (2014) Comparative anatomy of ovules in Galinsoga, Solidago and Ratibida (Asteraceae). Acta Biol Cracov Ser Bot 56:115–125. https://doi.org/10.2478/abcsb-2014-0024

    Article  Google Scholar 

  • Koltunow A, Johnson SD, Bicknell RA (1998) Sexual and apomictic development in Hieracium. Sex Plant Reprod 11:213–230

    Article  Google Scholar 

  • Leprince O, Hendry G, McKersie B (1993) The mechanisms of desiccation tolerance in developing seeds. Seed Sci Res 3:231–246

    Article  Google Scholar 

  • Leprince O, Pellizzaro A, Berriri S, Buitink J (2017) Late seed maturation: drying without dying. J Exp Bot 68:827–841

    CAS  PubMed  Google Scholar 

  • Long RL, Gorecki MJ, Renton M, Scott JK, Colville L, Goggin DE, Commander LE, Westcott DA, Cherry H, Finch-Savage WE (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biol Rev 90:31–59

    Article  Google Scholar 

  • Maheswari Devi H (1957) Embryological studies in Compositae. Proc Plant Sci 46:68–74. https://doi.org/10.1007/BF03052108

    Article  Google Scholar 

  • Manning J, Simka B, Boatwright J, Magee A (2016) A revised taxonomy of Gerbera sect. Gerbera (Asteraceae: Mutisieae). S Afr J Bot 104:142–157

    Article  Google Scholar 

  • Martins MAG, Oliveira DMT (2007) Morfoanatomia comparada dos frutos em desenvolvimento de Vernonia brevifolia Less. e V. herbacea (Vell.) Rusby (Asteraceae). Braz J Bot:101–112

  • Marzinek J, Oliveira DM (2010) Structure and ontogeny of the pericarp of six Eupatorieae (Asteraceae) with ecological and taxonomic considerations. An Acad Bras Cienc 82:279–291

    Article  Google Scholar 

  • Marzinek J, De-Paula OC, Oliveira DMT (2008) Cypsela or achene? Refining terminology by considering anatomical and historical factors. Braz J Bot 31:549–553

    Article  Google Scholar 

  • McCartney L, Ormerod AP, Gidley MJ, Knox JP (2000) Temporal and spatial regulation of pectic (1→ 4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. Plant J 22:105–113

    Article  CAS  Google Scholar 

  • Moore JP, Vicré-Gibouin M, Farrant JM, Driouich A (2008) Adaptations of higher plant cell walls to water loss: drought vs desiccation. Physiol Plant 134:237–245

    Article  CAS  Google Scholar 

  • Moura EF, Ventrella MC, Motoike SY (2010) Anatomy, histochemistry and ultrastructure of seed and somatic embryo of Acrocomia aculeata (Arecaceae). Sci Agric 67:399–407

    Article  Google Scholar 

  • Müntz K (1998) Deposition of storage proteins. In: Protein trafficking in plant cells, Springer, pp 77–99

  • Musiał K, Kościńska-Pająk M (2013) Ovules anatomy of selected apomictic taxa from Asteraceae family. Mod Phytomorphol 3:35–38

    Google Scholar 

  • Musiał K, Kościńska-Pająk M, Sliwinska E, Joachimiak AJ (2012) Developmental events in ovules of the ornamental plant Rudbeckia bicolor Nutt. Flora-Morphol Distrib Funct Ecol Plants 207:3–9. https://doi.org/10.1016/j.flora.2011.07.015

    Article  Google Scholar 

  • Musiał K, Płachno B, Świątek P, Marciniuk J (2013) Anatomy of ovary and ovule in dandelions (Taraxacum, Asteraceae). Protoplasma 250:715–722

    Article  Google Scholar 

  • Nakajima K, Benfey PN (2002) Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14:S265–S276

    Article  CAS  Google Scholar 

  • Nakajima JN, Loeuille B, Heiden G, Dematteis, M, Hattori EKO, Magenta MAG, Ritter MR, Mondin CA, Roque N, Ferreira SC, Borges RA, Soares PN, Almeida G, Schneider A, Sancho G, Saavedra MM, Liro, RM, Pereira ACM, Moraes MD, Silva GAR, Medeiros JD, Lorencini TS, Teles AM, Monge M, Siniscalchi CM, Souza-Buturi FO, Bringel JR JBA, Carneiro CR, Pasini E, Oliveira CT (2016) Asteraceae in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro. Available in: . Accessed 20 Jan 2016

  • Nieuwland J, Scofield S, Murray JAH (2009) Control of division and differentiation of plant stem cells and their derivatives. Semin Cell Dev Biol 20:1134–1142

  • Pasini E, Ritter MR (2012) O gênero Trichocline Cass.(Asteraceae, Mutisieae) no Rio Grande do Sul, Brasil. Revista Brasileira de Biociências 10

  • Płachno BJ, Świątek P, Kozieradzka-Kiszkurno M, Majeský Ľ, Marciniuk J, Stolarczyk P (2015) Are obligatory apomicts invested in the pollen tube transmitting tissue? Comparison of the micropyle ultrastructure between sexual and apomictic dandelions (Asteraceae, Lactuceae). Protoplasma 252:1325–1333. https://doi.org/10.1007/s00709-015-0765-x

    Article  PubMed  PubMed Central  Google Scholar 

  • Płachno BJ, Kurczyńska E, Świątek P (2016) Integument cell differentiation in dandelions (Taraxacum, Asteraceae, Lactuceae) with special attention paid to plasmodesmata. Protoplasma 253:1365–1372. https://doi.org/10.1007/s00709-015-0894-2

    Article  CAS  PubMed  Google Scholar 

  • Probert RJ, Daws MI, Hay FR (2009) Ecological correlates of ex situ seed longevity: a comparative study on 195 species. Ann Bot 104:57–69

    Article  Google Scholar 

  • Pullaiah T (1981) Studies in the embryology ofHeliantheae (Compositae). Plant Syst Evol 137:203–214

    Article  Google Scholar 

  • Rogge-Renner GD, Steiner N, Schmidt ÉC, Bouzon ZL, Farias FL, Guerra MP (2013) Structural and component characterization of meristem cells in Araucaria angustifolia (Bert.) O. Kuntze zygotic embryo. Protoplasma 250:731–739. https://doi.org/10.1007/s00709-012-0457-8

    Article  PubMed  Google Scholar 

  • Rudall PJ (1997) The nucellus and chalaza in monocotyledons: structure and systematics. Bot Rev 63:140–181. https://doi.org/10.1007/BF02935930

    Article  Google Scholar 

  • Schmidt EC, Scariot LA, Rover T, Bouzon ZL (2009) Changes in ultrastructure and histochemistry of two red macroalgae strains of Kappaphycus alvarezii (Rhodophyta, Gigartinales), as a consequence of ultraviolet B radiation exposure. Micron 40:860–869

    Article  CAS  Google Scholar 

  • Schmidt ÉC, Dos Santos R, Horta PA, Maraschin M, Bouzon ZL (2010) Effects of UVB radiation on the agarophyte Gracilaria domingensis (Rhodophyta, Gracilariales): changes in cell organization, growth and photosynthetic performance. Micron 41:919–930. https://doi.org/10.1016/j.micron.2010.07.010

    Article  CAS  PubMed  Google Scholar 

  • Schmidt ÉC, Pereira B, dos Santos RW, Gouveia C, Costa GB, Faria GSM, Scherner F, Horta PA, Martins RP, Latini A, Ramlov F, Maraschin M, Bouzon ZL (2012) Responses of the macroalgae Hypnea musciformis after in vitro exposure to UV-B. Aquat Bot 100:8–17. https://doi.org/10.1016/j.aquabot.2012.03.004

    Article  CAS  Google Scholar 

  • Singh MB, Bhalla PL (2006) Plant stem cells carve their own niche. Trends Plant Sci 11:241–246. https://doi.org/10.1016/j.tplants.2006.03.004

    Article  CAS  PubMed  Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  CAS  Google Scholar 

  • Steiner N et al (2015) Toward establishing a morphological and ultrastructural characterization of proembryogenic masses and early somatic embryos of Araucaria angustifolia (Bert.) O. Kuntze. Protoplasma 253:487-501. https://doi.org/10.1007/s00709-015-0827-0

  • Sul RGD (2014) Decreto n. ° 52.109, de 02 de dezembro de 2014 vol 233

  • Tan-Wilson AL, Wilson KA (2012) Mobilization of seed protein reserves. Physiol Plant 145:140–153. https://doi.org/10.1111/j.1399-3054.2011.01535.x

    Article  CAS  PubMed  Google Scholar 

  • van Baarlen P, Verduijn M, van Dijk PJ (1999) What can we learn from natural apomicts? Trends Plant Sci 4:43–44

    Article  Google Scholar 

  • Veloso VHS, Ribeiro LM, Mercadante-Simões MO, Nunes YRF (2016) Cytological aspects of recalcitrance in dormant seeds of Mauritia flexuosa (Arecaceae). Acta Physiol Plant 38:171. https://doi.org/10.1007/s11738-016-2194-7

    Article  CAS  Google Scholar 

  • Verdeil J-L, Alemanno L, Niemenak N, Tranbarger TJ (2007) Pluripotent versus totipotent plant stem cells: dependence versus autonomy? Trends Plant Sci 12:245–252

    Article  CAS  Google Scholar 

  • von Arnold S, Sabala I, Bozhkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tissue Organ Cult 69:233–249

    Article  Google Scholar 

  • Weigel D, Jürgens G (2002) Stem cells that make stems. Nature 415:751–754

    Article  CAS  Google Scholar 

  • Werker E (1997) Seed anatomy. Gebruder Borntraeger Verlagsbuchhandlung

  • Wesley-Smith J, Walters C, Pammenter N, Berjak P (2015) Why is intracellular ice lethal? A microscopical study showing evidence of programmed cell death in cryo-exposed embryonic axes of recalcitrant seeds of Acer saccharinum. Ann Bot 115:991–1000. https://doi.org/10.1093/aob/mcv009

    Article  PubMed  PubMed Central  Google Scholar 

  • West M, Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell 5:1361–1369

    Article  Google Scholar 

  • Western TL (2012) The sticky tale of seed coat mucilages: production, genetics, and role in seed germination and dispersal. Seed Sci Res 22:1–25

    Article  CAS  Google Scholar 

  • Yurukova-Grancharova P, Robeva-Davidova P, Vladimirov V (2006) On the embryology and mode of reproduction of selected diploid species of Hieracium sl (Asteraceae) from Bulgaria. Flora-Morphol Distrib Funct Ecol Plants 201:668–675. https://doi.org/10.1016/j.flora.2006.01.003

    Article  Google Scholar 

  • Zanin A, Longhi-Wagner HM, Rieper M (2010) Fitofisionomia das formações campestres do Campo dos Padres, Santa Catarina, Brasil. INSULA Revista de Botânica 38:42

    Article  Google Scholar 

  • Zhang Z, Laux T (2011) The asymmetric division of the Arabidopsis zygote: from cell polarity to an embryo axis. Sex Plant Reprod 24:161–169. https://doi.org/10.1007/s00497-010-0160-x

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the staff of the Central Laboratory of Electron Microscopy (LCME) and Plant Cell Biology Laboratory of the Federal University of Santa Catarina, Florianópolis, Santa Catarina, Brazil.

Funding

This work was supported by the National Council for Scientific and Technological Development (CNPq, Brazil), Proc. No. (311156/2017-7 457940/2014-0). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) -Finance Code 001.

Author information

Authors and Affiliations

  1. Plant Physiology Laboratory, Department of Botany, Federal University of Santa Catarina, Florianópolis, SC, 88040-900, Brazil

    Rosa Angelica Elias, Ana Paula Lando, Willian G. Viana, Jacqueline Ortiz, Cláudia Dias da Costa & Neusa Steiner

  2. Plant Cell Biology Laboratory, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, C.P. 476, Florianópolis, SC, 88049-900, Brazil

    Éder Carlos Schmidt

  3. Department of Biology, State University of Maringá, Av. Colombo 5790, Zona 7, Maringá, Paraná, 87020-900, Brazil

    Luiz Antônio Souza

  4. Plant Developmental Physiology and Genetics Laboratory, Department of Plant Science, Federal University of Santa Catarina, Florianópolis, SC, 88034-001, Brazil

    Miguel Pedro Guerra

Authors
  1. Rosa Angelica Elias
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Paula Lando
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Willian G. Viana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jacqueline Ortiz
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cláudia Dias da Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Éder Carlos Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luiz Antônio Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Miguel Pedro Guerra
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Neusa Steiner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Neusa Steiner.

Additional information

Handling Editor: Peter Nick

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

Elias, R.A., Lando, A.P., Viana, W.G. et al. Structural aspects of cypsela and seed development of Trichocline catharinensis (Cabrera): a Brazilian endemic species. Protoplasma 256, 1495–1506 (2019). https://doi.org/10.1007/s00709-019-01361-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01361-7

Keywords

Search

Navigation