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Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis

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Abstract

Variations in pollen characters and tapetum behavior were recently acknowledged in the early-divergent family Nymphaeaceae and even within the genus Nymphaea, which probably is not monophyletic; some traits such as infratectum and tapetum type are also a matter of different interpretations. In this study, developmental characters of the pollen grains and tapetum in Nymphaea subgenus Hydrocallis are provided for the first time. Observations were made in N. amazonum, N. gardneriana, and N. prolifera using light, scanning, and transmission electron microscopy. Tapetum is of the secretory type and produces orbicules. At microspore and pollen grain stages, the distal and proximal walls differ considerably. This result supports the operculate condition of the aperture in Hydrocallis, and such aperture might be plesiomorphic for Nymphaeoideae. The infratectum is intermediate, composed of inter-columellae granular elements, robust columellae consisting of agglomerated granules, complete columellae, and fused columellae. Narrow microchannels are present and persist until the mature pollen grain stage. The membranous granular layer is often present in the pollen grains of Nymphaeaceae. In N. gardneriana, this layer is most probably a component of the intine because it is lost after acetolysis. Orbicules in the Nymphaeaceae are characterized as spherical or subspherical, with a smooth sporopolleninic wall that surrounds an electron-lucent core and with individual orbicules that usually merge to give irregular aggregations. The aperture, pollen wall ultrastructure, and the tapetum of the studied species are discussed in an evolutionary and systematic context, and these characters are also compared with those of other angiosperm lineages.

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References

  • Ansari R, Jeeja G, Jayalakshmi SK (2005) Pollen morphology of Nymphaea Linn. J Palynol 41:139–152

    Google Scholar 

  • APG IV (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 181:1–20

  • Bhowmik S, Datta BK (2012) Pollen dimorphism of several members of Nymphaeaceae and Nelumbonaceae: an index of geographical and ecological variation. Not Sci Biol4:38–44

  • Borsch T, Hilu KW, Wiersema JH, Löhne C, Barthlott W, Wilde V (2007) Phylogeny of Nymphaea (Nymphaeaceae): evidence from substitutions and microstructural changes of the chloroplast trnT-F region. Int J Plant Sci 168:639–671

    Article  CAS  Google Scholar 

  • Borsch T, Löhne C, Wiersema JW (2008) Phylogeny and evolutionary patterns in Nymphaeales: integrating genes, genomes and morphology. Taxon 57:1052–1081

    Google Scholar 

  • Borsch T, Löhne C, Mbaye MS, Wiersema J (2011) Towards a complete species tree of Nymphaea: shedding further light on subgen. Brachyceras and its relation-ships to the Australian water-lilies. Telopea 13:193–217

    Article  Google Scholar 

  • Chapman GP (1987) The tapetum. Int Rev Cytol 107:111–125

    Article  Google Scholar 

  • Coiro M, Barone Lumaga MR (2013) Aperture evolution in Nymphaeaceae: insights from a micromorphological and ultrastructural investigation. Grana 52:192–201

    Article  Google Scholar 

  • Dai H, Zhou Q (2010) Embryological studies in Nymphaea lotus (Nymphaeaceae). Acta Bot Boreali-Occidentalia Sinica 30:78–84 (in Chinese)

    Google Scholar 

  • Debasis B, Mondal AK (2012) Studies on production, morphology and free amino acids of pollen of four members in the genus Nymphaea L. (Nymphaeaceae). Int J Sci Nat 3:705–718

    Google Scholar 

  • Doyle JA (2005) Early evolution of angiosperm pollen as inferred from molecular and morphological phylogenetic analyses. Grana 44:227–251

    Article  Google Scholar 

  • Doyle JA (2009) Evolutionary significance of granular exine structure in the light of phylogenetic analyses. Rev Palaeobot Palynol 156:198–210

    Article  Google Scholar 

  • Doyle JA, Endress PK (2000) Morphological phylogenetic analysis of basal angiosperms: comparison and combination with molecular data. Int J Plant Sci 161(S6):S121–S153

    Article  CAS  Google Scholar 

  • Echlin P, Godwin H (1969) The ultrastructure and ontogeny of pollen in Helleborus foetidus L. III. The formation of the pollen grain wall. J Cell Sci 5:459–477

    CAS  PubMed  Google Scholar 

  • El-Ghazaly G, Huysmans S (2001) Re-evaluation of a neglected layer in pollen wall development with comments on its evolution. Grana 40:3–16

    Article  Google Scholar 

  • El-Ghazaly G, Huysmans S, Smets EF (2001) Pollen development of Rondeletia odorata (Rubiaceae). Am J Bot 88:14–30

    Article  CAS  PubMed  Google Scholar 

  • Endress PK, Doyle JA (2009) Reconstructing the ancestral angiosperm flower and its initial specializations. Am J Bot 96:22–66

    Article  PubMed  Google Scholar 

  • Erdtman GB (1960) The acetolysis method: a revised description. Svensk Bot Tidskr 54:561–564

    Google Scholar 

  • Erdtman GB, Berglund B, Praglowski J (1961) An introdution to a Scandinavian pollen flora. Alnqvist & Wiksell, Uppsala

    Google Scholar 

  • Furness CA (2008) A review of the distribution of plasmodial and invasive tapeta in Eudicots. Int J Plant Sci169:207–223

  • Furness CA, Rudall PJ (2001) The tapetum in basal angiosperms: early diversity. Int J Plant Sci 162:375–392

    Article  Google Scholar 

  • Furness CA, Rudall PJ (2003) Apertures with lids: distribution and significance of operculate pollen in monocotyledons. Int J Plant Sci164:835–854

  • Gabarayeva NI (1991) Patterns of development in primitive angiosperm pollen. In: Blackmore S, Barnes SH (eds) Pollen and spores: patterns of diversification. Calderon Press, Oxford, pp 257–268

    Google Scholar 

  • Gabarayeva NI (1996) Sporoderm development in Liriodendron chinense (Magnoliaceae): a probable role of the endoplasmic reticulum. Nord J Bot 16:307–323

    Article  Google Scholar 

  • Gabarayeva NI, El-Ghazaly G (1997) Sporoderm development in Nymphaea mexicana (Nymphaeaceae). Plant Syst Evol 204:1–19

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2010) Sporoderm ontogeny in Chamaedorea microspadix (Arecaceae): self-assembly as the underlying cause of development. Grana 49:91–114

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2012) Sporoderm development and substructure in Magnolia sieboldii and other Magnoliaceae: an interpretation. Grana 51:119–147

    Article  Google Scholar 

  • Gabarayeva NI, Hemsley AR (2006) Merging concepts: the role of self-assembly in the development of pollen wall structure. Rev Palaeobot Palynol 138:121–139

    Article  Google Scholar 

  • Gabarayeva NI, Rowley JR (1994) Exine development in Nymphaea colorata (Nymphaeaceae). Nord J Bot 14:671–691

    Article  Google Scholar 

  • Gabarayeva NI, Walles B, El-Ghazaly G, Rowley JR (2001) Exine and tapetum development in Nymphaea capensis (Nymphaeaceae): a comparative study. Nord J Bot 21:529–548

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Rowley JR (2003) Sporoderm ontogeny in Cabomba aquatica (Cabombaceae). Rev Palaeobot Palynol 127:147–173

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Polevova S, Hemsley AR (2016) Pollen wall and tapetum development in Plantago major L. (Plantaginaceae): assisting self-assembly. Grana. doi:10.1080/00173134.2016.1159729

    Google Scholar 

  • Galati BG (1985) Estudios embriológicos en Cabomba australis (Nymphaeaceae) I. La esporogénesis y las generaciones sexuadas. Bol Soc Argent Bot 24:9–47

    Google Scholar 

  • Galati BG (2003) Ubisch bodies in Angiosperms. In: Pandey AK, Dhakal MR (eds) Advances in plant reproductive biology, vol II. Narendra, Delhi, pp 1–21

    Google Scholar 

  • Galati BG, Zarlavsky G, Rosenfeldt S, Gotelli MM (2012) Pollen ontogeny in Magnolia liliflora Desr. Plant Syst Evol 298:527–534

    Article  Google Scholar 

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

    Google Scholar 

  • Grigorjeva V, Gabarayeva N (2015) The development of sporoderm, tapetum and Ubisch bodies in Dianthus deltoides (Caryophyllaceae): self-assembly in action. Rev Palaeobot Palynol 219:1–27

    Article  Google Scholar 

  • Hesse M, Zetter R (2005) Ultrastructure and diversity of recent and fossil zona-aperturate pollen grains. Plant Syst Evol 255:145–176

    Article  Google Scholar 

  • Ito M (1984) Studies in the floral morphology and anatomy of Nymphaeales. II. Floral anatomy of Nymphaea tetragona George. Acta Phytotax Geobot 35:94–102

    Google Scholar 

  • Ito M (1987) Phylogenetic systematics of the Nymphaeales. Bot Mag (Tokyo) 100:17–35

    Article  Google Scholar 

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

    Google Scholar 

  • Jones MR, Clarke GCS (1981) Nymphaeaceae. Rev Palaeobot Palynol 33:57–67

    Article  Google Scholar 

  • Khanna P (1964) Morphological and embryological studies in Nymphaeaceae I: Euryale ferox Salisb. Proc Indian Acad Sci 59:237–243

    Google Scholar 

  • Khanna P (1965) Morphological and embryological studies in Nymphaeaceae. II: Brasenia schreberi Gmel. and Nelumbo nucifera Garten. Aust J Bot 13:379–387

    Article  Google Scholar 

  • Khanna P (1967) Morphological and embryological studies in Nymphaeaceae III. Victoria cruziana D'Orb. and Nymphaea stellata Willd. Bot Mag (Tokyo) 80:305–312

    Article  Google Scholar 

  • Kreunen SS, Osborn JM (1999) Pollen and anther development in Nelumbo (Nelumbonaceae). Am J Bot 86:1662–1676

    Article  CAS  PubMed  Google Scholar 

  • Les DH, Schneider EL, Padgett DJ, Soltis PS, Soltis DE, Zanis M (1999) Phylogeny, classification and floral evolution of water lilies (Nymphaeaceae; Nymphaeales): a synthesis of non-molecular, rbcL, matK, and 18S rDNA data. Syst Bot 24:28–46

    Article  Google Scholar 

  • Löhne C, Borsch T, Wiersema JH (2007) Phylogenetic analysis of Nymphaealesusing fast-envolving and noncoding chloroplast markers. Bot J Linn Soc 154:141–163

    Article  Google Scholar 

  • Lu L, Wortley AH, Li D, Wang H, Blackmore S (2015) Evolution of angiosperm pollen. 2. The basal angiosperms. Ann Mo Bot Gard 100:227–269

    Article  Google Scholar 

  • Luque R, Sousa HC, Graus JE (1996) Métodos de coloracão de Roeser (1972) modificado Kropp, E., 1972. Visando a substituicão do azul de astra por azul de alcião8GS ou 8GX. Acta Bot Brasil 10:199–212

    Article  Google Scholar 

  • Meyer NR (1964) Palynological studies in Nymphaeaceae. Bot Zhurn 49:1421–1429

    Google Scholar 

  • Meyer-Melikian NR, Diamondopulu N (1996) Ultrastructure of pollen grains of the order Nymphaeales. Bot Zhurn 81:1–9 (in Russian)

    Google Scholar 

  • Murthy GVS (2000) Pollen morphology of Nymphaeaceae (s.L.). Bull Bot Surv India 42:73–80

    Google Scholar 

  • Osborn JM (2000) Pollen morphology and ultrastructure of gymnospermous anthophytes. In: Harley MM, Morton CM, Blackmore S (eds) Pollen and spores: morphology and biology pp 163–185

  • Osborn JM, Taylor TN, Schneider EL (1991) Pollen morphology and ultrastructure of the Cabombaceae: correlations with pollination biology. Am J Bot 78:1367–1378

    Article  Google Scholar 

  • Pacini E (1990) Tapetum and microspore function. In: Blackmore S, Knox RB (eds) Microspores, evolution and ontogeny. Academic Press, London, pp 213–237

    Chapter  Google Scholar 

  • Pacini E (1997) Tapetum character states: analytical keys for tapetum types and activities. Can J Bot 75:1448–1459

    Article  Google Scholar 

  • Pacini E, Franchi GG (1993) Role of the tapetum in pollen and spore dispersal. Plant Syst Evol 7:1–11

    Article  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

    Article  Google Scholar 

  • Papini A, Mosti S, van Doorn WG (2013) Classical macroautophagy in Lobivia rauschii (Cactaceae) and possible plastidial autophagy in Tillandsia albida (Bromeliaceae) tapetum cells. Protoplasma 251:719–725. doi:10.1007/s00709-013-0567-y

    PubMed  Google Scholar 

  • Podoplelova Y, Ryzhakov G (2005) Phylogenetic analysis of the order Nymphaeales based on the nucleotide sequences of the chloroplast ITS2–4 region. Plant Sci 169:606–611

    Article  CAS  Google Scholar 

  • Remizowa MV, Sokoloff DD, Macfarlane TD, Yadav SR, Prychid CJ, Rudall PJ (2008) Comparative pollen morphology in the early-divergent angiosperm family Hydatellaceae reveals variation at the infraspecific level. Grana 47:81–100

    Article  Google Scholar 

  • Roland F (1965) I'rkisions sur la structure el I'ultrastructure d'unc tktradc calymmee. Pollen Spores 7:5–8

    Google Scholar 

  • Rowley JR (1993) Cycles of hyperactivity in tapetal cells. In: Hesse M, Pacini E, Willemse M (eds) The tapetum, cytology, function, biochemistry, and evolution. Springer, Vienna, pp 23–37

    Google Scholar 

  • Rowley JR, El-Ghazaly G, Rowley JS (1987) Microchannels in the pollen grain exine. Palynology 11:1–21

    Article  Google Scholar 

  • Rowley JR, Gabarayeva NI, Walles B (1992) Cyclic invasion of tapetal cells into loculi during microspore development in Nymphaea colorata (Nymphaceae). Am J Bot 79:801–808

    Article  Google Scholar 

  • Rowley JR, Skvarla JJ, El-Ghazaly G (2003) Transfer of material through the microspore exine from the loculus into the cytoplasm. Can J Bot 81:1070–1082

    Article  Google Scholar 

  • Sampson FB (2007) Variation and similarities in pollen features in some basal angiosperms, with some taxonomic implications. Plant Syst Evol 263:59–75

    Article  Google Scholar 

  • Sharma A, Singh MB, Bhalla PL (2015) Anther ontogeny in Brachypodium distachyon. Protoplasma 252:439–450

    Article  PubMed  Google Scholar 

  • Singh CB, Motial VS, Nair PKK (1969) Pollen morphology of Nymphaea. Plant Sci 1:53–56

    Google Scholar 

  • Skvarla JJ, Larson DA (1966) Fine structural studies of Zea mays pollen I: cell membranes and exine ontogeny. Am J Bot 53:1112–1125

    Article  Google Scholar 

  • Taylor ML, Osborn JM (2006) Pollen ontogeny in Brasenia (Cabombaceae, Nymphaeales). Am J Bot 93:344–356

    Article  PubMed  Google Scholar 

  • Taylor ML, Gutman BL, Melrose NA, Ingraham AM, Schwartz JA, Osborn JM (2008) Pollen and anther ontogeny in Cabomba caroliniana (Cabombaceae, Nymphaeales). Am J Bot 95:399–413

  • Taylor ML, Hudson PJ, Rigg JM, Strandquist JN, Schwartz GJ, Thiemann TC, Osborn JM (2012) Tapetum structure and ontogeny in Victoria (Nymphaeaceae). Grana 51:107–118

    Article  Google Scholar 

  • Taylor ML, Hudson PJ, Rigg JM, Strandquist JN, Schwartz GJ, Thiemann TC, Osborn JM (2013) Pollen ontogeny in Victoria (Nymphaeales). Int J Plant Sci 174:1259–1276

    Article  Google Scholar 

  • Taylor ML, Cooper RL, Schneider EL, Osborn JM (2015) Pollen structure and development in Nymphaeales: insights into character evolution in an ancient angiosperm lineage. Am J Bot 102:1685–1702

    Article  PubMed  Google Scholar 

  • Tsou CH, Cheng PC, Tseng CM, Yen HJ, Fu YL, You TR, Walden DB (2015) Anther development of maize (Zea mays) and longstamen rice (Oryza longistaminata) revealed by cryo-SEM, with foci on locular dehydration and pollen arrangement. Plant Reprod 28:47–60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Volkova PA, Shipunov AB (2008) Morphological variation of Nymphaea (Nymphaeaceae) in European Russia. Nord J Bot 25:329–338

    Article  Google Scholar 

  • Walker JW (1974a) Evolution of exine structure in the pollen of primitive angiosperms. Am J Bot 61:891–902

    Article  Google Scholar 

  • Walker JW (1974b) Aperture evolution in the pollen of primitive angiosperms. Am J Bot 61:1112–1137

    Article  Google Scholar 

  • Walker JW, Doyle JA (1975) The bases of angiosperm phylogeny: palynology. Ann Mo Bot Gard 62:664–723

    Article  Google Scholar 

  • Weber M, Ulrich S (2010) The endexine: a frequently overlooked pollen wall layer and a simple method for detection. Grana 49:83–90

    Article  Google Scholar 

  • Wiersema JH (1987) A monograph of Nymphaea subgenus Hydrocallis (Nymphaeaceae). Syst Bot Monogr 16:1–112

    Article  Google Scholar 

  • Wodehouse RP (1935) Pollen grains. Their structure, identification and significance in science and medicine. McGraw-Hill, New York

    Google Scholar 

  • Xu FU, Kirchoff BK (2008) Pollen morphology and ultrastructure of selected species of Magnoliaceae. Rev Palaeobot Palynol 150:140–153

    Article  Google Scholar 

  • Zarlavsky GE (2014) Histología Vegetal. Técnicas simples y complejas. Soc Arg Bot. Buenos Aires, Argentina

  • Zavada MS (1984) Pollen wall development of Austrobaileya maculata. Bot Gaz 145:11–21

    Article  Google Scholar 

  • Zhou Q, Fu D (2008) Reproductive morphology of Nuphar (Nymphaeaceae), a member of basal angiosperms. Plant Syst Evol 272:79–96

    Article  Google Scholar 

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Acknowledgements

Financial support for this research was provided by the Universidad de Buenos Aires (UBACyT 20020120100056BA), Agencia Nacional de Promoción Científica, Tecnológica y de Innovación, Argentina (ANPCyT-UNNE, PICTO 2012-0202), and the Universidad Nacional del Nordeste (PI A012-2013).

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Zini, L.M., Galati, B.G., Zarlavsky, G. et al. Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis . Protoplasma 254, 1777–1790 (2017). https://doi.org/10.1007/s00709-016-1074-8

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