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Roles of the haustorium and endosperm during the development of seedlings of Acrocomia aculeata (Arecaceae): dynamics of reserve mobilization and accumulation

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Abstract

The mobilization of palm seed reserves is a complex process because of the abundance and diversity of stored compounds and results from the development of a highly specialized haustorium. This work focused on the important Neotropical oleaginous palm Acrocomia aculeata, with the aim of defining phases of seedling development associated with mobilization of reserves and elucidating the role of haustorium and endosperm in this process. Standard methods were performed, including biometric, anatomical, and histochemical analyses, as well as the evaluation of the activities of the enzymes endo-β-mannanase and lipase, throughout the reserve mobilization in seeds during germination and in seedlings. Seeds of A. aculeata stored large quantities of proteins, lipids, and polysaccharides in the embryo and endosperm. The mobilization of reserves initiated in the haustorium during germination and subsequently occurred in the endosperm adjacent to the haustorium, forming a gradually increasing zone of digestion. Proteins and polysaccharides were the first to be mobilized, followed by lipids and cell wall constituents. The haustorium activates and controls the mobilization, forming transitory reserves and translocating them to the vegetative axis, while the endosperm, which also has an active role, serves as a site of intense enzymatic activity associated with protein bodies. Seedling development can be described as occurring in six phases over a long period (approximately 150 days) due to the large amount of seed reserves. This process exhibits an alternation between stages of accumulation and translocation of protein, lipid, and carbohydrate reserves in the haustorium, which favors the seedling establishment and the reproductive success of the species.

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References

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

    Article  CAS  Google Scholar 

  • Berton LHC, Azevedo Filho A, Siqueira WJ, Colombo CA (2013) Seed germination and estimates of genetic parameters of promising macaw palm (Acrocomia aculeata) progenies for biofuel production. Ind Crop Prod 51:258–266

    Article  CAS  Google Scholar 

  • Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy. Springer, New York, USA

  • Bicalho EM, Motoike SY, Borges EEL, Ataíde GM, Guimarães VM (2016) Enzyme activity and reserve mobilization during macaw palm (Acrocomia aculeata). Acta Bot Bras 30:437–444

  • Borek S, Ratajczak W, Ratajczak L (2006) Ultrastructural and enzymatic research on the role of sucrose in mobilization of storage lipids in germinating yellow lupine seeds. Plant Sci 170:441–452

    Article  CAS  Google Scholar 

  • Buckeridge MS (2010) Seed cell wall storage polysaccharides: models to understand cell wall biosynthesis and degradation. Plant Physiol 154:1017–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • DeMason DA (1986) Endosperm structure and storage reserve histochemistry in the palm, Washingtonia filifera. Am J Bot 73:1332–1340

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • DeMason DA, Sekhar KNC, Harris M (1989) Endosperm development in the date palm (Phoenix dactylifera) (Arecaceae). Am J Bot 76:1255–1265

    Article  Google Scholar 

  • DeMason DA, Sexton R, Gorman M, Reid JSG (1985) Structure and biochemistry of endosperm breakdown in date palm (Phoenix dactylifera L.) seeds. Protoplasma 126:159–167

    Article  CAS  Google Scholar 

  • DeMason DA, Thomson WW (1981) Structure and ultrastructure of the cotyledon of date palm (Phoenix dactylifera L.). Bot Gaz 142:320–328

    Article  Google Scholar 

  • Dransfield J, Uhl NW, Asmussen CBA, Baker WJ, Harley MM, Lewis CE (2008) Genera palmarum: the evolution and classification of palms. Kew Publishing, Kew, UK

  • Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142

    Article  Google Scholar 

  • Fuchs C (1963) Fuchsin staining with NaOH clearing for lignified elements of whole plants or plant organs. Stain Technol 38:141–144

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137A–138A

    Google Scholar 

  • Linkies A, Graeber K, Knight C, Leubner-Metzger G (2010) The evolution of seeds. New Phytol 186:817–831

    Article  CAS  PubMed  Google Scholar 

  • Lorenzi H, Noblick L, Kahn F, Ferreira E (2010). Flora Brasileira: Arecaceae (palmeiras). Instituto Plantarum, Nova Odessa

  • Moura EF, Ventrella MC, Motoike SY (2010) Anatomy, histochemistry and ultrastructure of seed and somatic embryo of Acrocomia aculeata (Arecaceae). Sci Agr 67:375–495

    Article  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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Oliveira TGS, Junior AGR, Souza PP, Ribeiro LM (2013b) Use of phytoregulators in overcoming macaw palm seed dormancy. Acta Sci 35:505–511

    CAS  Google Scholar 

  • Oo KC, Stumpf (1983) Some enzymic activities in the germinating oil palm (Elaeis guineensis) seedling. Plant Physiol 73:1028–1032

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

    Google Scholar 

  • Paiva EAS, Pinho SZ, Oliveira DMT (2011) Large plant samples: how to process for GMA embedding? In: Chiarini-Garcia H, Melo RCN (eds) Light microscopy: methods and protocols. Springer/Humana Press, New York, pp. 37–49

    Chapter  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

    Article  Google Scholar 

  • Pinho GP, Matoso JRM, Silvério FO, Mota WC, Lopes PSN, Ribeiro LM (2014) A new spectrophotometric method for determining the enzymatic activity of endo-β-mannanase in seeds. J Brazil Chem Soc 25:1246–1252

    CAS  Google Scholar 

  • Pires TP, Souza ES, Kuki KN, Motoike SY (2013) Ecophysiological traits of the macaw palm: a contribution towards the domestication of a novel oil crop. Ind Crop Prod 44:200–210

    Article  CAS  Google Scholar 

  • Ribeiro LM, Garcia QS, Müller M, Munné-Bosch S (2015) Tissue-specific hormonal profiling during dormancy release in macaw palm seeds. Physiol Plantarum 153:627–642

    Article  CAS  Google Scholar 

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

    Article  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

    Article  Google Scholar 

  • Sass JE (1951) Botanical microtechnique. Iowa State College Press, Ames

    Book  Google Scholar 

  • Sekhar KNC, DeMason DA (1988) Quantitative ultrastructure and protein composition of date palm (Phoenix dactylifera) seeds: a comparative study of endosperm vs. embryo. Am J Bot 75:323–329

    Article  CAS  Google Scholar 

  • Sekhar KNC, DeMason DA (1990) Identification and immunocytochemical localization de α-galactosidase in resting and germinated date palm (Phoenix dactylifera L.) seeds. Planta 181:53–61

    Article  CAS  PubMed  Google Scholar 

  • Sugimuma Y, Murakami T (1990) Structure and function of the haustorium in germinating coconut palm seed. Jpn Agr Res Q 24:1–14

    Google Scholar 

  • Tan-Wilson AL, Wilson K (2012) Mobilization of seed protein reserves. Physiol Plantarum 145:140–153

    Article  CAS  Google Scholar 

  • Tonini PP, Carrara TB, Buckeridge MS (2010) Storage proteins and cell wall mobilisation in seeds of Sesbania virgata (Cav.) Pers. (Leguminosae). Trees 24:675–684

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Williams HA, Bewley JD, Greenwood JS, Bourgault R, Mo B (2001) The storage cell walls in the endosperm of Asparagus officinalis L. seeds during development and following germination. Seed Sci Res 11:305–315

    CAS  Google Scholar 

  • Zienkiewicz A, Zienkiewicz K, Rejón JD, Alché JD, Castro AJ, Rodríguez-García MI (2014) Olive seed protein bodies store degrading enzymes involved in mobilization of oil bodies. J Exp Bot 65:103–115

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG; Brazil, processo CRA-APQ-01335-13) for the financial support and Dr. Paulo Sérgio Nascimento Lopes, Dra. Gevany Paulino de Pinho (Universidade Federal de Minas Gerais, Montes Claros, Brazil), Dra. Maria Olívia Mercadante Simões (Universidade Estadual de Montes Claros, Montes Claros, Brazil), and Dra. Luzia Valentina Modolo (Universidade Federal de Minas Gerais, Belo Horizonte, Brazil) for the use of facilities and equipment of their laboratories and for the theoretical support. H.C.M.S. thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES; Brazil) for the doctoral fellowship she received, and D.M.T.O. and L.M.R. thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brazil, processes 308117/2014-0 and 304627/2015-1, respectively) for the productivity in research grants.

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Authors and Affiliations

  1. Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, 31270-901, Brazil

    Hellen Cássia Mazzottini-dos-Santos & Denise Maria Trombert Oliveira

  2. Departamento de Biologia Geral, Universidade Estadual de Montes Claros, Montes Claros, Minas Gerais, 39401-089, Brazil

    Leonardo Monteiro Ribeiro

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  1. Hellen Cássia Mazzottini-dos-Santos
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  2. Leonardo Monteiro Ribeiro
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Correspondence to Leonardo Monteiro Ribeiro.

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Mazzottini-dos-Santos, H.C., Ribeiro, L.M. & Oliveira, D.M.T. 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 (2017). https://doi.org/10.1007/s00709-016-1048-x

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