Skip to main content
SpringerLink
Log in

Morphostructural and histochemical dynamics of Euterpe precatoria (Arecaceae) germination

  • Regular Paper – Morphology/Anatomy/Structural Biology
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

The fruits of Euterpe precatoria, popularly known as açaí palm, have been commercially exploited for use in food and beverages because of their medicinal and energetic properties. However, despite the growing demand, little is known about the seeds germination, until now, its main form of propagation. In this context, we have characterized the structure of the zygotic embryo and described temporally the germination process of E. precatoria with emphasis on the morpho-anatomical and histochemical aspects. For this end, we have collected and analyzed zygotic embryo and seedlings samples before sowing and at different periods after sowing—2, 4, 6, 8, 10, 15, 20, 30, 40, 50, and 60 days. The embryo has an oblique embryonic axis and mainly protein reserves. Seed germination is classified as cryptocotyledonar, hypogeal, and adjacent ligular and we observed seedlings at 20 days after sowing (33.3%), although anatomical evidence of the beginning of the germination process have been observed at 15 days. The day-20 was histologically marked by the expansion of the ligule, beginning of second eophyll differentiation, and complete root protrusion. This stage was characterized by the total consumption of protein reserves and increased starch grains. The occurrence of 100% of root and ligula emission was verified at day-60, which characterizes a slow and heterogeneous process. The morphological marker of the E. precatoria germination is the exit of the proximal region (cotyledonary petiole) of the embryo from within the seed by the lifting of the operculum and the species has some peculiarities, such as the presence of high concentrations of phenolic compounds and idioblasts before and throughout the germination process, and starch grains located on the embryonic axis. We can verify that the consumption of protein reserves of the embryo is related to the energy supply necessary for root protrusion.

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
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

AR:

Adventitious root

BOD:

Biochemical oxygen demand

CC:

Cotyledonary cavity

CN:

Cotyledonary node

CP:

Cotyledonary petiole

CS:

Cotyledonary slit

CT:

Cataphyll

DR:

Distal region

E:

Eophyll

EA:

Embryonic axis

EC:

Endocarp

END:

Endosperm

EP:

Epidermis

EST:

Stomata

EX:

Exocarp

FI:

Fiber

GB:

Germ bud

GM:

Ground meristem

HA:

Haustorium

HR:

Hypocotyl-radicle axis

IBGE:

Brazilian Institute of Geography and Statistics

ID:

Idioblast

INV:

Invagination

IS:

Intercellular space

L:

Leaflet

LEA:

Late embryogenesis abundant

LI:

Ligule

LP:

Leaf primordium

MF:

Mesocarp fiber

MS:

Mesocarp

NaOCl:

Sodium hypochlorite

OP:

Operculum

P:

Protein

PA:

Parenchyma

PAS:

Periodic Acid-Schiff

PC:

Procambium

pH:

Hydrogen potential

PHC:

Phenolic compounds

PL:

Plumule

PMR:

Primary root

PR:

Proximal region

PT:

Protoderm

RAM:

Root apical meristem

RC:

Root cap

SAM:

Shoot apical meristem

SR:

Secondary root

VB:

Vascular bundle

VE:

Vessel element

XP:

Xylidine Ponceau

ZE:

Zygotic embryo

References

  • Aguiar MO, Mendonça MS (2002) Aspectos morfo-anatômicos do embrião de Euterpe precatoria Mart. durante o processo germinativo. Act Bot Bras 16:241–249

    Google Scholar 

  • Aguiar MO, Mendonça MS (2003) Morfo-anatomia da semente de Euterpe precatoria Mart. (Palmae). Rev Bras Sem 25:37–42

    Google Scholar 

  • Alang ZC, Moir GFJ, Jones LH (1988) Composition, degradation and utilization of endosperm during germination in the oil palm (Elaeis guineensis). Ann Bot 61:261–268

    CAS  Google Scholar 

  • Araújo MGP, Leitão AM, Mendonça MS (2000) Morfologia do fruto e da semente de inajá (Attalea maripa (Aubl.) Mart.) – Palmae. Rev Bras Sem 22:31–38

    Google Scholar 

  • Baker WJ, Dransfield J (2016) Beyond Genera Palmarum: progress and prospects in palm systematics. Bot J Linn Soc 182:207–233

    Google Scholar 

  • Baskin MB, Baskin CC (2014) What kind of seed dormancy might palms have? Seed Sci Res 24:17–22

    Google Scholar 

  • Bernardes RSA (2010) Aspectos fisiológicos e bioquímicos da germinação de sementes de açaí (Euterpe oleracea Mart. e Euterpe precatoria Mart.) submetidas ao aumento da temperatura. Dissertation, Instituto Nacional de Pesquisas da Amazônia

  • Bornman CH, Dickens OSP, Van Der Merwe CF, Coetzee J, Botha AM (2003) Somatic embryos of Picea abies behave like isolated zygotic embryos in vitro but with greatly reduced physiological vigour. S Afr J Bot 69:176–185

    CAS  Google Scholar 

  • Carey AN, Miller MG, Fisher DR, Bielinski DF, Gilman CK, Poulose SM, Shukitt-Hale B (2017) Dietary supplementation with the polyphenol-rich açaí pulps (Euterpe oleracea Mart. and Euterpe precatoria Mart.) improves cognition in aged rats and attenuates inflammatory signaling in BV-2 microglial cells. Nutr Neurosci 20:238–245

    CAS  PubMed  Google Scholar 

  • Carvalho JEU, Nascimento WMO (2018) Technological innovations in the propagation of Açaí palm and Bacuri. Rev Bras Fruticultura 40:664–679

    Google Scholar 

  • Copeland LO, Mcdonald MB (1999) The Chemistry of seeds. In: Copeland LO, Mcdonald MB (eds) Principles of seed science and technology. Springer, Boston, pp 40–58

    Google Scholar 

  • Demason DA (1984) Growth parameters in the cotyledon of date seedlings. Bot Gaz 145:176–183

    Google Scholar 

  • Demason DA (1985) Histochemieal and ultrastructural changes in the haustorium of date (Phoenix dactylifera L.). Protoplasma 126:168–177

    Google Scholar 

  • Demason DA (1988a) Embryo structure and storage reserve histochemistry in the palm Washingtonia filifera. Am J Bot 75:330–337

    Google Scholar 

  • Demason DA (1988b) Seedling development in Washingtonia filifera (Arecaceae). Bot Gaz 149:45–56

    Google Scholar 

  • Dias DS, Ribeiro LM, Lopes PSN, Melo GA, Müller M, Munné-Bosch S (2018) Haustorium–endosperm relationships and the integration between developmental pathways during reserve mobilization in Butia capitata (Arecaceae) seeds. Ann Bot 122:267–277

    Google Scholar 

  • Gentil DFO, Ferreira SAN (2005) Morfologia da plântula em desenvolvimento de Astrocaryum aculeatum Meyer (Arecaceae). Acta Amaz 35:337–342

    Google Scholar 

  • Graham IA (2008) Seed storage oil mobilization. Annu Rev Plant Biol 59:115–142

    CAS  PubMed  Google Scholar 

  • Henderson F (2006) Morphology and anatomy of palm seedlings. Bot Rev 72:273–329

    Google Scholar 

  • Instituto Brasileiro de Geografia e Estatística—IBGE (2017) Brazilian Institute of Geography and Statistics Produção da Extração Vegetal e da Silvicultura, 32: 1–8. https://biblioteca.ibge.gov.br/visualizacao/periodicos/74/pevs_2017_v32_informativo.pdf. Accessed 13 Jun 2019

  • Johansen D (1940) Plant microtechnique. Mc Graw Hill, New York, p 523

    Google Scholar 

  • Kang J, Thakali KM, Xie C, Kondo M, Tong Y, Ou B, Jensen G, Medina MB, Schauss AG, Wu X (2012) Bioactivities of açaí (Euterpe precatoria Mart.) fruit pulp, superior antioxidant and anti-inflammatory properties to Euterpe oleracea Mart. Food Chem 133:671–677

    CAS  Google Scholar 

  • Karnovsky MJA (1965) Formaldehyde-glutaraldeyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Lima MJR, Hong TD, Arruda YMBC, Mendes AMS, Ellis RH (2014) Classification of seed storage behaviour of 67 Amazonian tree species. Seed Sci Technol 42:363–392

    Google Scholar 

  • Lorenzi H, Souza HM, Cerqueira LSC, Costa JTM, Ferreira E (2004) Palmeiras brasileiras e exóticas cultivadas. Instituto Plantarum, Nova Odessa (in Portuguese)

    Google Scholar 

  • Magalhães HM, Lopes PSN, Ribeiro LM, Sant’anna-Santos BF, Oliveira DMT (2013) Structure of the zygotic embryos and seedlings of Butia capitata (Arecaceae). Trees 27:273–283

    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

    Google Scholar 

  • Moura ACF, Ribeiro LM, Mazzottini-dos-Santos HC, Mercadante-Simões MO, Nunes YRF (2019) Cytological and histochemical evaluations reveal roles of the cotyledonary petiole in the germination and seedling development of Mauritia flexuosa (Arecaceae). Protoplasma 256:1299–1316

    Google Scholar 

  • Mazzottini-dos-Santos HC, Ribeiro LM, Oliveira DMT (2017) Roles of the haustorium and endosperm during the development of seedlings of Acrocomia aculeata (Arecaceae): dynamics of reserve mobilization and accumulation. Protoplasma 254:1563–1578

    PubMed  Google Scholar 

  • Müntz K (1996) Proteases and proteolytic cleavage of storage proteins in developing and germinating dicotyledonous seeds. J Exp Bot 47:605–622

    Google Scholar 

  • Neto MAM, Lobato AKS, Alves JD, Fátima P, Goulart P, Laughinghouse HD IV (2010) Seed and seedling anatomy in Euterpe oleracea Mart. during the germination process. J Food Agric Environ 8:1147–1152

    Google Scholar 

  • Neves SC, Ribeiro LM, Cunha IRG, Pimenta MAS, Mercadante-Simões MO, Lopes PSN (2013) Diaspore structure and germination ecophysiology of the babassu palm (Attalea vitrivir). Flora 208:68–78

    Google Scholar 

  • O'Brien TP, Mccylly ME (1981) The study of plant structure: principles and selected methods. Termarcarphi PTY LTD, Melbourne

    Google Scholar 

  • O'Brien TP, Feder N, Mccylly ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373

    CAS  Google Scholar 

  • Oliveira AB, Mendonça MS, Pacheco MG (2010) Aspectos anatômicos do embrião e desenvolvimento inicial de Oenocarpus minor Mart.: uma palmeira da Amazônia. Acta Bot Bras 24:20–24

    Google Scholar 

  • Oliveira NCC, Lopes PSN, Ribeiro LM, Mercandante-Simões MO, Oliveira LAA, Silvério FO (2013) Seed structure, germination, and reserve mobilization in Butia capitata (Arecaceae). Trees 27:1633–1645

    Google Scholar 

  • Orozco-Segovia A, Batis AI, Rojas-Arechiga M, Mendoza A (2003) Seed biology of palms. Palms 47:79–94

    Google Scholar 

  • Pacheco-Palencia EA, Duncan CE, Talcott ST (2009) Phytochemical composition and thermal stability of two commercial açai species, Euterpe oleracea and Euterpe precatoria. Food Chem 115:1199–1205

    CAS  Google Scholar 

  • Panza V, Láinez V, Maldonado S (2004) Seed structure and histochemistry in the palm Euterpe edulis. Bot J Linn Soc 145:445–453

    Google Scholar 

  • Pernollet JC (1978) Protein bodies of seeds: ultrastructure, biochemistry, biosynthesis and degradation. Phytochemistry 17:1473–1480

    CAS  Google Scholar 

  • Peixoto H, Roxo M, Krstin S, Röhrig T, Richling E, Wink M (2016) An anthocyanin-rich extract of acai (Euterpe precatoria Mart.) increases stress resistance and retards aging-related markers in Caenorhabditis elegans. J Agric Food Chem 64:1283–1290

    CAS  PubMed  Google Scholar 

  • Pinheiro CUB (2001) Germination strategies of palms: the case of Schippia concolor Burret in Belize. Brittonia 53:519–527

    Google Scholar 

  • Quiroga YMC, Gómez MSH, Mary L (2017) Componentes Bioactivos del Asai (Euterpe oleracea Mart. y Euterpe precatoria Mart.) y su efecto sobre la salud. Arch Venez Farmacol Terap 36:58–66

    Google Scholar 

  • Ribeiro LM, Souza PP, Rodrigues AG Jr, Oliveira TGS, Garcia QS (2011) Overcoming dormancy in macaw palm diaspores, a tropical species with potential for use as biofuel. Seed Sci Technol 39:303–317

    Google Scholar 

  • Ribeiro LM, Oliveira DMT, Garcia QS (2012) Structural evaluations of zygotic embryos and seedlings of the macaw palm (Acrocomia aculeata, Arecaceae) during in vitro germination. Trees 26:851–863

    Google Scholar 

  • Robertson BL (1983) Developmental anatomy of the seedling of Jubaeopsis caffra. S Afr J Bot 2:152–161

    Google Scholar 

  • Rocha E (2004) Potencial ecológico para o manejo de frutos de açaizeiro (Euterpe precatoria Mart.) em áreas extrativistas no Acre, Brasil. Acta Amaz 34:237–250

    Google Scholar 

  • Rodrigues JK, Mendonça MS, Gentil DFO (2015) Aspectos biométricos, morfoanatômicos e histoquímicos do pirênio de Bactris maraja (Arecaceae). Rodriguésia 66:075–085

    Google Scholar 

  • Sharma A, Kumar D, Kumar S, Rampuria S, Reddy AR, Kirti PB (2016) Ectopic Expression of an atypical hydrophobic group 5 LEA protein from wild peanut, Arachis diogoi confers abiotic stress tolerance in tobacco. PLoS ONE 11:1–31

    Google Scholar 

  • Silva-Cardoso IMA, Meira FS, Gomes ACMM, Scherwinski-Pereira JE (2019) Histology, histochemistry and ultrastructure of pre-embryogenic cells determined for direct somaticembryogenesis in the palm tree Syagrus oleracea. Physiol Plant 168:845–875

    Google Scholar 

  • Silva RS, Ribeiro LM, Mercadante-Simões MO, Nunes YRF, Lopes PSN (2014) Seed structure and germination in buriti (Mauritia flexuosa)—the swamp palm. Flora 209:674–685

    Google Scholar 

  • Souza J, Ribeiro LM, Mercadante-Simões MO (2017) Ontogenesis and functions of saxophone stem in Acrocomia aculeata (Arecaceae). Ann Bot 119:353–365

    Google Scholar 

  • Stone SL, Gifford DJ (1997) Structural and biochemical changes in loblolly pine (Pinus taeda L.) seeds during germination and early-seedling growth. I Storage protein reserves. Int J Plant Sci 158:727–737

    CAS  Google Scholar 

  • Sugimura Y, Murakami T (1990) Structure and function of the haustorium in germinating coconut palm seed. JARQ 24:1–14

    Google Scholar 

  • Tan-Wilson AL, Wilson K (2011) Mobilization of seed protein reserves. Physiol Plant 145:140–153

    PubMed  Google Scholar 

  • Tillich H-J (2007) Seedling diversity and the homologies of seedling organs in the order Poales (Monocotyledons). Ann Bot 100:1413–1429

    PubMed  PubMed Central  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 38:1–12

    CAS  Google Scholar 

  • Verdeil JL, Hocher V (2002) Digestion and absorption of food in plants: a plant stomach. Trends Plant Sci 7:280–281

    CAS  PubMed  Google Scholar 

  • Viana FAP, Costa AP, Moro FV, Pivetta KFL (2016) Morpho-anatomical characterization of diaspores and seedlings of Livistona rotundifolia. Ornam Hortic 22:249–255

    Google Scholar 

  • Vidal BC (1970) Dichroism in collagen bundles stained with xylidine-Ponceau 2R. Ann Histochim 15:289–296

    Google Scholar 

  • Viji V, Chandra R, Salim PN, Puthur JT (2015) Germination-associated morphological and anatomical changes in Corypha umbraculifera L. seeds. Phytomorphology 65:11–17

    Google Scholar 

  • Zienkiewicz A, Jiménez-López JC, Zienkiewicz K, Alché JD, Rodríguez-García MI (2011) Development of the cotyledon cells during olive (Olea europaea L.) in vitro seed germination and seedling growth. Protoplasma 248:751–765

    CAS  PubMed  Google Scholar 

  • Zona S (2004) Raphides in palm embryos and their systematic distribution. Ann Bot 93:415–421

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the National Council for Scientific and Technological Development, Brazil (CNPq Grant 426637/2016-0) and Coordination of Improvement of Higher Education Personnel, Brazil (Capes/Embrapa 001-2011/Grant 39) for financial support and fellowships.

Author information

Authors and Affiliations

  1. Department of Forest Engineering, University of Brasília, Brasília, Brazil

    Cheila Deisy Ferreira & Jéssica Cristina Barbosa Ferreira

  2. CNPq/Embrapa Postoctoral Fellowship Program, Embrapa Genetic Resources and Biotechnology, Brasília, DF, Brazil

    Inaê Mariê de Araújo Silva-Cardoso

  3. Federal University of Acre, Rio Branco, AC, Brazil

    Frederico Henrique da Silva Costa

  4. Embrapa Genetic Resources and Biotechnology, Av. W5 Norte (final), Brasília, 70770-917, Brazil

    Jonny Everson Scherwinski-Pereira

Authors
  1. Cheila Deisy Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Inaê Mariê de Araújo Silva-Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jéssica Cristina Barbosa Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frederico Henrique da Silva Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jonny Everson Scherwinski-Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JES-P and IMAS-C conceived and designed the research. CDF, IMAS-C, JCBF and FHSC collected and prepared the plant material and performed the anatomic cuts. CDF, IMAS-C and JCBF assisted microscopic examination and acquired the photographs. CDF and IMAS-C wrote the initial text. JES-P and IMAS-C wrote the final text. All authors read and approved the manuscript.

Corresponding author

Correspondence to Jonny Everson Scherwinski-Pereira.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

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

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ferreira, C.D., Silva-Cardoso, I.M.d., Ferreira, J.C.B. et al. Morphostructural and histochemical dynamics of Euterpe precatoria (Arecaceae) germination. J Plant Res 133, 693–713 (2020). https://doi.org/10.1007/s10265-020-01219-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-020-01219-7

Keywords

Search

Navigation