Skip to main content
SpringerLink
Log in

Review on tapetal ultrastructure in angiosperms

Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The appearance of new cellular structures and characteristics in the tapetum suggests that there is still much to discover that would help to better understand the tapetum functions.

Abstract

The ultrastructure of the tapetum provides important information for the understanding of the functions performed by this tissue. Since there are no reviews on the subject, we aim to collect all the detailed information about the tapetum ultrastructure present until this moment in order to lay the foundations for future research. Detailed information on the tapetal ultrastructure of 80 species from 45 different families: 2 species with invasive non-syncytial tapetum, 11 with plasmodial and 67 with a secretory tapetum was collected. These studies allowed to establish (a) the most usual cytological characteristics of this tissue, (b) unique characteristics and/or cellular structures in tapetum cells, (c) the ultrastructural changes that occur in different types of tapetum, during the progress of microsporogenesis and microgametogenesis, and (d) the most recognized ultrastructural traits of the tapetum that cause androsterility. The structure of these cells is related to their function in each developmental stage. Since most species present their particular ultrastructure and may sometimes, share some traits within families, there is not a model plant on tapetum ultrastructure. However, knowing the general cytological aspect of the tapetum may help distinguish between patterns of cytoplasmic disorganization due to tapetum degeneration from technical failures of the preparation. Moreover, as the amount of species analyzed increases, unknown tapetal organelles or traits may be identified that might be associated to particular functions of this tissue. On the other hand, different ultrastructural changes may be related to the metabolisms and the regulation of normal/abnormal tapetum development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (Canada)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Data availability

The data sets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

ER:

Endoplasmic reticulum

mMC:

Microspore mother cell

RER:

Rough endoplasmic reticulum

SER:

Smooth endoplasmic reticulum

SLB:

Sporopollenin-like bodies

PCD:

Programmed cell death

PAS:

Periodic acid–Schiff

RNAs:

Ribonucleic acids

TEM:

Transmission electron microscope

References

  • Albertsen MC, Palmer RG (1979) A comparative light and electron microscopic study of microsporogenesis in male sterile (MS) and male fertile soybeans (Glycine max (L.) Merr.). Am J Bot 66(3):253–265

  • Amela García M, Galati BG, Anton AM (2002) Microsporogenesis, microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae). Bot J Linn Soc 139(4):383–394

  • Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460

    Article  CAS  PubMed  Google Scholar 

  • Balk J, Leaver CJ (2001) The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell 13(8):1803–1818

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baluska F (2006) Communication in plants. Springer, Berlin

  • Banerjee U (1967) Ultrastructure of the tapetal membranes in grasses. Grana 7(2–3):1967

    Google Scholar 

  • Bhandari NN (1984) The microsporangium. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 53–121

  • Bino RJ (1985) Ultrastructural aspects of cytoplasmic male sterility in Petunia hybrida. Protoplasma 127(3):230–240

    Article  Google Scholar 

  • Brighigna L, Papini A (1993) The ultrastructure of the tapetum of Tillandsia albina Mez Et Purpus. Phytomorphology 43:264–274

    Google Scholar 

  • Budar F, Pelletier G (2001) Male sterility in plants: occurrence, determinism, significance and use. C R Séances Acad Sci Sér 3, Sci Vie 324(6):543–550

  • Chen L, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65(1):579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen HN, Zhao CH, Liu XR, Liu JX (2012) Pollen development of Cardiocrinum giganteum (Wall.) Makina in China. Plant Syst Evol 298(8):1557–1565

  • Ciampolini F, Nepi M, Pacini E (1993) Tapetum development in Cucurbita pepo (Cucurbitaceae). Plant Syst Evol 7(Suppl.):13–22

  • Clausen P (1927) Ueber das verhalten des antheren-tapeturns bel einigen monokotylen und ranales. Bot Arch 18:1–27

    Google Scholar 

  • Clément C, Audran JC (1993) Orbicule wall surface characteristics in Lilium (Liliaceae) An ultrastructural and cytochemical approach. Grana 32(6):348–353

    Article  Google Scholar 

  • Costa ML, Sobral R, Ribeiro Costa MM, Amorim MI, Coimbra S (2015) Evaluation of the presence of arabinogalactan proteins and pectins during Quercus suber male gametogenensis. Ann Bot 115(1):81–92

    Article  CAS  PubMed  Google Scholar 

  • D’Arcy WG (1996) Anthers and stamens and what they do. In: D’Arcy WG, Keating RC (eds) The anther: form, function and phylogeny. Cambridge University Press, Cambridge, pp 1–24

    Google Scholar 

  • Davis GL (1966) Systematic embryology of the angiosperms. Wiley, New York

    Google Scholar 

  • Dickinson HG, Bell PR (1972) The role of the tapetum in the formation of sporopollenin-containing structures during microsporogenesis in Pinus banksiana. Planta 107(3):205–215

    Article  CAS  PubMed  Google Scholar 

  • Dickinson HG, Lewis D (1973) The formation of the tryphine coating the pollen grains of Raphanus, and its properties relating to the self-incompatibility system. Proc R Soc B Biol Sci 184(1075):149–165

    CAS  Google Scholar 

  • Du K, Xiao Y, Liu Q, Wu X, Jiang J, Wu J, Fang Y, Xiang Y, Wang Y (2019) Abnormal tapetum development and energy metabolism associated with sterility in SaNa-1A CMS of Brassica napus L. Plant Cell Rep 38(5):545–558

    Article  CAS  PubMed  Google Scholar 

  • Ekici N, Dane F (2012) Ultrastructural studies on the sporogenous tissue and anther wall of Leucojum aestivum (Amaryllidaceae) in different developmental stages. Anais Acad Brasil Ci 84:951–960

    Article  Google Scholar 

  • Fernando DD, Cass DD (1994) Plasmodial tapetum and pollen wall development in Butomus umbellatus (Butomaceae). Am J Bot 81:1592–1600

    Article  Google Scholar 

  • Fitzgerald MA, Calder DM, Knox RB (1993) Secretory events in the freeze-substituted tapetum of the orchid Pterostylis concinna. In: Hesse M, Pacini E, Willemse M (eds) The tapetum. Plant Syst Evol (Suppl.), vol 7. Springer, Vienna, pp 53–62

  • Furness CA (2013) Evolution of pollen and tapetal characters in Ochnaceae (Malpighiales). Int J Plant Sci 174(8):1134–1152

    Article  Google Scholar 

  • Furness CA, Rudall PJ (1998) The tapetum and systematics in monocotyledons. Bot Rev 64(3):201–239

    Article  Google Scholar 

  • Furness CA, Rudall PJ (2001) The tapetum in basal angiosperms: early diversity. Int J Plant Sci 162(2):375–392

    Article  Google Scholar 

  • Gabara B (1975) Characterization of fibrous compound of Golgi vesicles in tapetai cells of Delphinium. Protoplasma 86:159–168

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2014) Sporoderm and tapetum development in Eupomatia laurina (Eupomatiaceae). An interpretation. Protoplasma 251(6):1321–1345

    Article  PubMed  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2016) Simulation of exine patterns by sellf-assembly. Plant Syst Evol 302:1135–1156

    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(3–4):147–173

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Rowley JR (2010) A new look at sporoderm ontogeny in Persea americana and the hidden side of development. Ann Bot 105(6):939–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Polelova S (2011) Exine and tapetum development in Symphytum officinale (Boraginaceae). Exine substructure and its interpretation. Plant Syst Evol 296:101–120

    Article  Google Scholar 

  • Gabarayeva N, Polevova S, Grigorjeva V, Severova E, Volkova O, Blackmore S (2019) Suggested mechanisms underlying pollen wall development in Ambrosia trifida (Asteraceae: Heliantheae). Protoplasma 256(2):555–574

    Article  CAS  PubMed  Google Scholar 

  • Galati BG (1996) Tapetum development in Sagittaria montevidensis Cham.et Schlecht (Alismataceae). Phytomorphology 46(1):7–17

  • Galati BG, Rosenfeldt S (1998) The pollen development in Ceiba insignis (Kunth) Gibbs and Semir ex Chorisia speciosa St Hil. (Bombacaceae). Phytomorphology 48:121–129

    Google Scholar 

  • Galati BG, Strittmatter LI (1999) Microsporogenesis and microgametogenesis in Jacaranda mimosifolia (Bignoniaceae). Phytomorphol Int J Plant Morphol 49:147–155

  • Galati BG, Monacci F, Gotelli MM, Rosenfeldt S (2007) Pollen, tapetum and orbicule development in Modiolastrum malvifolium (Malvaceae). Ann Bot 99(4):755–763

    Article  PubMed  PubMed Central  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 

  • Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5(10):1217–1229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gotelli MM, Galati BG, Medan D (2008) Embryology of Helianthus annuus (Asteraceae). Ann Bot Fenn 45(2):81–96

    Article  Google Scholar 

  • Gotelli M, Galati B, Medan D (2012) Pollen, tapetum, and orbicule development in Colletia paradoxa and Discaria americana (Rhamnaceae). Sci World J 2012:1–8

  • Gotelli MM, Galati BG, Zarlavsky G, Medan D (2016) Pollen and microsporangium development in Hovenia dulcis (Rhamnaceae): a different type of tapetal cell ultrastructure. Protoplasma 253(4):1125–1133

    Article  PubMed  Google Scholar 

  • Gotelli MM, Lattar EC, Zarvlasky G, Galati BG (2020) Pollen and microsporangium development in Ziziphus jujuba, Z. mucronata, Paliurus spina-christi and Gouania ulmifolia (Rhamnaceae). Anais Acad Brasil CI 92(2):1–13

  • Graça Sajo M, Furness CA, Prychid CJ, Rudall PJ (2005) Microsporogenesis and anther development in Bromeliaceae. Grana 44(2):65–74

    Article  Google Scholar 

  • Grant I, Beversdorf WD, Peterson RL (1986) A comparative light and electron microscopic study of microspore and tapetal development in male fertile and cytoplasmic male sterile oilseed rape (Brassica napus). Can J Bot 64(5):1055–1068

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Haddad IVN, de Sá-Haiad B, de Santiago-Fernandes LDR, Machado SR (2019) Pollen grain development and male sterility in the perfect flowers of Maytenus obtusifolia Mart. (Celastraceae). Protoplasma 256(3):745–761

  • Hernould M, Suharsono S, Zabaleta E, Carde JP, Litvak S, Araya A, Mouras A (1998) Impairment of tapetum and mitochondria in engineered male-sterile tobacco plants. Plant Mol Biol 36(4):499–508

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison J (1969) An acetolysis-resistant membrane investing tapetum and sporogenous tissue in the anthers of certain Compositae. Canad J Bot 47(4):541–542

    Article  Google Scholar 

  • Hesse M (1993) Pollenkitt development and composition in Tilia platyphyllos (Tiliaceae) analyzed by conventional and energy filtering TEM. In: Plant Syst Evol, vol 7(Suppl.). Springer, Vienna, pp 39–52

  • Hesse M, Hess MW (1993) Recent trends in tapetum research. A cytological and methodological review. In: Hesse M, Pacini E, Willemse M (eds) The tapetum. Plant Syst Evol (Suppl.), vol 7. Springer, Vienna, pp 127–145

  • Hoefert LL (1971) Ultrastructure of tapetal cell ontogeny in Beta. Protoplasma 73(3):397–406

    Article  Google Scholar 

  • Holford P, Croft J, Newbury HJ (1991) Structural studies of microsporogenesis in fertile and male-sterile onions (Allium cepa L.) containing the cms-S cytoplasm. Theor Appl Genet 82(6):745–755

  • Horner HT Jr (1977) A comparative light-and electron-microscopic study of microsporogenesis in male-fertile and cytoplasmic male-sterile sunflower (Helianthus annuus). Am J Bot 64(6):74–759

    Article  Google Scholar 

  • Hsieh K, Huang AH (2005) Lipid-rich tapetosomes in Brassica tapetum are composed of oleosin-coated oil droplets and vesicles, both assembled in and then detached from the endoplasmic reticulum. Plant J 43(6):889–899

    Article  CAS  PubMed  Google Scholar 

  • Hsieh K, Huang AH (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum–derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19(2):582–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang MD, Chen TLL, Huang AH (2013) Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol 163(3):1218–1229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiménez JLU, Fernández PH, Schlag MG, Hesse M (1995) Pollen and tapetum development in male fertile Rosmarinus officinalis L.(Lamiaceae). Grana 34(5):305–316

  • Kaul MLH (1988) Male sterility in higher plants. Springer, New York, p 1005

  • Kaul MLH (2012) Male sterility in higher plants. Springer, New York

  • Keijzer CJ (1987) The processes of anther dehiscence and pollen dispersal: ii. the formation and the transfer mechanism of pollenkitt, cell‐wall development of the loculus tissues and a function of orbicules in pollen dispersal. New Phytol 105(3):499–507

  • Koch I, Alves DM, Souto LS (2018) Anther wall and pollen development in two species of Rauvolfia L. (Apocynaceae). Braz J Bot 41(1):175–184

  • Konyar ST (2014) Ultrastructure of microsporogenesis and microgametogenesis in Campsis radicans (L.) Seem.(Bignoniaceae). Plant Syst Evol 300(2):303–320

  • Ku S, Yoon H, Suh HS, Chung YY (2003) Male-sterility of thermosensitive genic male-sterile rice is associated with premature programmed cell death of the tapetum. Planta 217(4):559–565

    Article  CAS  PubMed  Google Scholar 

  • Lallemand B, Erhardt M, Heitz T, Legrand M (2013) Sporopollenin biosynthetic enzymes interact and constitute a metabolon localized to the endoplasmic reticulum of tapetum cells. Plant Physiol 162(2):616–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile angiosperms. Bot Rev 38(3):425–454

    Article  Google Scholar 

  • Lattar EC, Galati BG, Ferrucci MS (2012) Ultrastructural study of pollen and anther development in Luehea divaricata (Malvaceae, Grewioideae) and its systematic implications: Role of tapetal transfer cells, orbicules and male germ unit. Flora 207(12):888–894

    Article  Google Scholar 

  • Lattar EC, Galati BG, Ferrucci MS (2014) Comparative study of anther development, microsporogenesis microgametogenesis in species of Corchorus, Heliocarpus, Luehea and Triumfetta (Malvaceae: Grewioideae) from South America. N Z J Bot 52(4):429–445

  • Lee SLJ, Gracen VE, Earle ED (1979) The cytology of pollen abortion in c-cytoplasmic male-sterile corn anthers. Am J Bot 66(6):656–667

    Article  Google Scholar 

  • Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18(11):2999–3014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Suen DF, Huang CY, Kung SY, Huang AH (2012) The maize tapetum employs diverse mechanisms to synthesize and store proteins and flavonoids and transfer them to the pollen surface. Plant Physiol 158(4):1548–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li N, Xu C, Li-Beisson Y, Philippar K (2016) Fatty acid and lipid transport in plant cells. Trends Plant Sci 21(2):145–158

    Article  CAS  PubMed  Google Scholar 

  • Liu HF, Kirchoff BK, Wu GJ, Liao JP (2007) Microsporogenesis and male gametogenesis in Jatropha curcas L. (Euphorbiaceae) 1. J Torrey Bot Soc 134(3):335–343

  • Liu RS, Qiu YL, Wei DM, Liu HH, Zhu XY, Tian HQ, Teixeira da Silva JA (2011) Distribution of starch and neutral lipids in the developing Anthers of Ipomoea cairica. Annal Bot Fenn 48(3):256–262

    Article  Google Scholar 

  • Lombardo G, Carraro L (1976) Tapetal ultrastructural changes during pollen development. I. Studies on Antirrhinum maius. Caryologia 29(1):113–125

    Article  Google Scholar 

  • Loukides CA, Broadwater AH, Bedinger PA (1995) Two new male-sterile mutants of Zea mays (Poaceae) with abnormal tapetal cell morphology. Am J Bot 82(8):1017–1023

    Article  Google Scholar 

  • Luo XD, Dai LF, Wang SB, Wolukau JN, Jahn M, Chen JF (2006) Male gamete development and early tapetal degeneration in cytoplasmic male-sterile pepper investigated by meiotic, anatomical and ultrastructural analyses. Plant Breed 125(4):395–399

    Article  Google Scholar 

  • Mamun EA, Cantrill LC, Overall RL, Sutton BG (2005) Cellular organization and differentiation of organelles in pre-meiotic rice anthers. Cell Biol Int 29(9):792–802

    Article  PubMed  Google Scholar 

  • Misset MT, Gourret JP (1984) Accumulation of smooth cisternae in the tapetal cells of Ulex europaeus L. (Papilionoideae). J Cell Sci 72(1):65–74

  • Muniraja M, Vijayalakshmi G, Naik ML, Bhaskar VV, Khan PSSV (2018) A developmental study on anther wall and pollen in Mangifera indica L. var. Beneshan (Anacardiaceae). S Afr J Bot 119:142–153

    Article  Google Scholar 

  • Murgia M, Charzynska M, Rougier M., Cresti M (1991) Secretory tapetum of Brassica oleracea L.: polarity and ultrastructural features. Sex Plant Reprod 4(1):28–35

  • Murphy DJ, Ross JH (1998) Biosynthesis, targeting and processing of oleosin-like proteins, which are major pollen coat components in Brassica napus. Plant J 13(1):1–16

    CAS  PubMed  Google Scholar 

  • Owen HA, Makaroff CA (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185(1):7–21

  • Pacini E (1990) Tapetum and microspore function. In: Blackmore S, Franchi R (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, Cresti M (1978) Ultrastructural characteristics of the tapetum and microspore mother cells in Lycopersicon peruvianum during meiotic prophase. Bull Soc Bot Fr Act Bot 1–2:121–128

    Google Scholar 

  • Pacini E, Hesse M (2005) Pollenkitt—its composition, forms and functions. Flora 200(5):399–415

    Article  Google Scholar 

  • Pacini E, Juniper BE (1983) The ultrastructure of the formation and development of the amoeboid tapetum in Arum italicum miller. Protoplasma 117:116–129

    Article  Google Scholar 

  • Pacini E, Keijzer CJ (1989) Ontogeny of intruding non-periplasmodial tapetum in the wild chicory, Cichorium intybus (compositae). Plant Syst Evol 167:149–164

    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, Brighigna L (1999) Programmed-cell-death events during tapetum development of angiosperms. Protoplasma 207(3):213–221

    Article  Google Scholar 

  • Papini A, Mosti S, van Doorn WG (2014) Classical macroautophagy in Lobivia rauschii (Cactaceae) and possible plastidial autophagy in Tillandsia albida (Bromeliaceae) tapetum cells. Protoplasma 251(3):719–725

  • Parish RW, Li SF (2010) Death of a tapetum: a programme of developmental altruism. Plant Sci 178(2):73–89

    Article  CAS  Google Scholar 

  • Parkinson BM (1995) The tapetum in Schizaea pectinata (Schizaeaceae) and a comparison with the tapetum in Psilotum nudum (Psilotaceae). Plant Syst Evol 196(3):161–172

    Article  Google Scholar 

  • Parteka LM, Mariath JEA, Vanzela ALL, Silvério A (2021) Nuclear variations and tapetum polyploidy related to pollen grain development in Passiflora L. (Passifloraceae). Cell Biol Int 45:462–474

    Google Scholar 

  • Perdue TD, Loukides CA, Bedinger P (1992) The formation of cytoplasmic channels between tapetal cells in Zea mays. Protoplasma 171(1):75–79

    Article  Google Scholar 

  • Piffanelli P, Murphy DJ (1998) Novel organelles and targeting mechanisms in the anther tapetum. Trends Plant Sci 3(7):250–252

    Article  Google Scholar 

  • Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306(5696):702–704

    Article  CAS  PubMed  Google Scholar 

  • Platt KA, Huang AHC, Thomson WW (1998) Ultrastructural study of lipid accumulation in tapetal cells of Brassica napus L. cv. Westar during microsporogenesis. Int J Plant Sci 159:724–737

    Article  CAS  Google Scholar 

  • Polowick PL, Sawhney VK (1993) Differentiation of the tapetum during microsporogenesis in tomato (Lycopersicon esculentum Mill.), with special reference to the tapetal cell wall. Ann Bot 72:595–605. http://www.jstor.org/stable/42758986

  • Qiu Y, Liao L, Liu S, Mao D, Liu R (2017) Differences on the microsporogenesis and tapetal development of male fertile and cytoplasmic male sterile pepper (Capsicum annuum L.). Grana 56(3):215–227

  • Quilichini TD, Douglas CJ, Samuels AL (2014) New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Ann Bot 114(6):1189–1201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavan V (1997) Molecular embryology of flowering plants. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Reznickova SA, Willemse MTM (1980) Formation of pollen in the anther of Lilium. II. The function of the surrounding tissues in the formation of pollen and pollen wall. Acta Bot Neerl 29:141–156

    Article  Google Scholar 

  • Rodríguez-Rajo FJ, Vega-Maray AM, Asturias JA, Jato V, Seoane-Camba JA, Suárez-Cervera M (2010) The relationship between tapetum cells and microspores based on protein localization in Fraxinus angustifolia (Oleaceae) pollen grains. Int J Plant Sci 171(1):34–52

    Article  Google Scholar 

  • Rosenfeldt S, Galati BG (2005) Ubisch bodies and pollen ontogeny in Oxalis articulata Savigny. Biocell 29(3):271–278

    Article  PubMed  Google Scholar 

  • Ross JH, Murphy DJ (1996) Characterization of anther-expressed genes encoding a major class of extracellular oleosin-like proteins in the pollen coat of Brassicaceae. Plant J 9(5):625–637

    Article  CAS  PubMed  Google Scholar 

  • Rowley JR (1993) Cycles of hyperactivity in tapetal cells. In: Hesse M, Pacini E, Willemse M (eds) The tapetum. Plant. Syst. Evol. (Suppl.), vol 7. Springer, Vienna, pp 23–37

  • Rowley JR, Skvarla JJ (1987) Ontogeny of pollen in Poinciana (Leguminoseae). II. Microspore and pollen grain periods. Rev Palaeobot Palynol 50(3):313–331

  • Ruiter RK, Van Eldik GJ, Van Herpen RM, Schrauwen JA, Wullems GJ (1997) Characterization of oleosins in the pollen coat of Brassica oleracea. Plant Cell 9(9):1621–1631

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sager R, Lee JY (2014) Plasmodesmata in integrated cell signaling: insights from development and environmental signals and stresses. J Exp Bot 65(22):6337–6358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schols P, Furness CA, Merckx V, Wilkin P, Smets E (2005) Comparative pollen development in Dioscoreales. Int J Plant Sci 166(6):909–924

    Article  Google Scholar 

  • Sharma A, Singh MB, Bhalla PL (2015) Ultrastructure of microsporogenesis and microgametogenesis in Brachypodium distachyon. Protoplasma 252(6):1575–1586

    Article  CAS  PubMed  Google Scholar 

  • Shi S, Ding D, Mei S, Wang J (2010) A comparative light and electron microscopic analysis of microspore and tapetum development in fertile and cytoplasmic male sterile radish. Protoplasma 241(1):37–49

    Article  PubMed  Google Scholar 

  • Shi X, Sun X, Zhang Z, Feng D, Zhang Q, Han L, Lu T (2015) GLUCAN SYNTHASE-LIKE 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice. Plant and Cell Physiol 56(3):497–509

    Article  CAS  Google Scholar 

  • Solís SM, Galati B, Ferrucci MS (2010) Microsporogenesis and microgametogenesis of Cardiospermum grandiflorum and Urvillea chacoensis (Sapindaceae, Paullinieae). Aust J Bot 58(7):597–604

    Article  Google Scholar 

  • Strittmatter LI, Galati BG, Monacci F (2000) Ubisch bodies in peritapetal membrane of Abutilon pictum Gill. (Malvaceae). Beitr Biol Pflanzen 71:393–402

    Google Scholar 

  • Strittmatter LI, Negrón-Ortiz V, Hickey JR (2006) Comparative microsporangium development in male-fertile and male-sterile flowers of Consolea (Cactaceae): When and how does pollen abortion occur. Grana 45(2):81–100

    Article  Google Scholar 

  • Sutthinon P, Samuels L, Meesawat U (2019) Pollen development in male sterile mangosteen (Garcinia mangostana L.) and male fertile seashore mangosteen (Garcinia celebica L.). Protoplasma 256(6):1545–1556

  • Suzuki T, Tsunekawa S, Koizuka C, Yamamoto K, Imamura J, Nakamura K, Ishiguro S (2013) Development and disintegration of tapetum-specific lipid-accumulating organelles, elaioplasts and tapetosomes in Arabidopsis thaliana and Brassica napus. Plant Sci 207:25–36

    Article  CAS  PubMed  Google Scholar 

  • Taylor ML, Osborn JM (2006) Pollen ontogeny in Brasenia (Cabombaceae, Nymphaeales). Am J Bot 93(3):344–356

    Article  PubMed  Google Scholar 

  • 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 

  • Testillano PS, Gonzalez-Melendi P, Fadon B, Sanchez-Pina A., Olmedilla A, Risueño MDC (1993). Immunolocalization of nuclear antigens and ultrastructural cytochemistry on tapetal cells of Scilla peruviana and Capsicum annuum. In: Hesse M, Pacini E, Willemse M (eds) The tapetum. Plant Syst Evol (Suppl.), vol 7. Springer, Vienna, pp 75–90

  • Tiwari SC, Gunning B (1986a) Cytoskeleton, cell surface and the development of invasive plasmodial tapetum in Tradescantia virginiana L. Protoplasma 133:89–99

    Article  Google Scholar 

  • Tiwari SC, Gunning B (1986b) Colchicine inhibits plasmodium formation and disrupts pathways of sporopollenin secretion in the anther tapetum of Tradescantia virginiana L. Protoplasma 133:115–128

    Article  CAS  Google Scholar 

  • Tütüncü Konyar S (2017) Ultrastructural aspects of pollen ontogeny in an endangered plant species, Pancratium maritimum L.(Amaryllidaceae). Protoplasma 254(2):881–900

  • Tütüncü Konyar S, Dane F (2013) Anther ontogeny in Campsis radicans (L.) Seem.(Bignoniaceae). Plant Syst Evol 299(3):567–583

  • Vardar F, Ünal M (2012) Ultrastructural aspects and programmed cell death in the tapetal cells of Lathyrus undulatus Boiss. Acta Biol Hung 63(1):52–66

    Article  PubMed  Google Scholar 

  • Vinckier S, Smets E (2005) A histological study of microsporogenesis in Tarenna gracilipes (Rubiaceae). Grana 44(1):30–44

    Article  Google Scholar 

  • Vinckier SA, Janssens SB, Huysmans S, Vandevenne A, Smets EF (2012) Pollen ontogeny linked to tapetal cell maturation in Impatiens parviflora (Balsaminaceae). Grana 51(1):10–24

    Article  Google Scholar 

  • Wan L, Xia X, Hong D, Li J, Yang G (2010) Abnormal vacuolization of the tapetum during the tetrad stage is associated with male sterility in the recessive genic male sterile Brassica napus L. Line 9012A. J Plant Biol 53(2):121–133

  • Weber M (1992) The formation of pollenkitt in Apium nodiflorum (Apiaceae). Ann Bot 70:573–577

    Article  Google Scholar 

  • Wolter M, Scuffert C, Schill R (1988) The ontogeny of pollinia and elastoviscin in the anther of Doritis pulcherrima (Orchidaceae). Nord J Bot 8:77–88

    Article  Google Scholar 

  • Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4(7):759–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu SSH, Platt KA, Ratnayake C, Wang TW, Ting JTL, Huang AHC (1997) Isolation and characterization of novel neutral-lipid-containing organelles and globuli-filled plastids from Brassica napus tapetum. Proc Natl Acad Sci USA 94:12711–12716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Y, Min L, Wu Z, Yang L, Zhu L, Yang X, Yuan D, Guo X, Zhang X (2015) Defective pollen wall contributes to male sterility in the male sterile line 1355A of cotton. Sci Rep 5(1):1–8

    Google Scholar 

  • Xue CY, Li DZ (2005) Embryology of Megacodon stylophorus and Veratrilla baillonii (Gentianaceae): descriptions and systematic implications. Bot J Linn Soc 147:317–331

    Article  Google Scholar 

  • Yue L, Kuang Y, Liao J (2017) Ontogeny of permanent tetrads in Gardenia jasminoides (Rubiaceae) provides insight into pollen evolution. Rev Palaeobot Palynol 247:120–132

    Article  Google Scholar 

  • Zini LM, Galati GB, Solís SM, Ferrucci MS (2012) Anther structure and pollen development in Melicoccus lepidopetalus (Sapindaceae): an evolutionary approach to dioecy in the family. Flora 207(10):712–720

    Article  Google Scholar 

  • Zini LM, Galati BG, Zarlavsky G, Ferrucci MS (2017) Developmental and ultrastructural characters of the pollen grains and tapetum in species of Nymphaea subgenus Hydrocallis. Protoplasma 254(4):1777–1790

    Article  PubMed  Google Scholar 

Download references

Funding

Financial support for our research were provided by Universidad de Buenos Aires (UBACyT Grant No. 20020160100012BA).

Author information

Authors and Affiliations

  1. Cátedra de Botánica General, Facultad de Agronomía, Universidad de Buenos Aires, Av. San Martín 4453, C1417DSE, Buenos Aires, Argentina

    Marina Gotelli & Beatriz Galati

  2. Cátedra de Morfología de Plantas Vasculares, Facultad de Ciencias Agrarias (FCA-UNNE), Sargento Cabral 2131, 3400, Corrientes, Argentina

    Elsa Lattar & Lucía Melisa Zini

  3. Instituto de Botánica del Nordeste (IBONE-UNNE-CONICET), Sargento Cabral 2131, 3400, Corrientes, Argentina

    Elsa Lattar & Lucía Melisa Zini

  4. Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2620, Ciudad Autónoma de Buenos Aires, 1428, Buenos Aires, Argentina

    Sonia Rosenfeldt

  5. Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina

    Marina Gotelli, Elsa Lattar & Lucía Melisa Zini

Authors
  1. Marina Gotelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elsa Lattar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lucía Melisa Zini
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sonia Rosenfeldt
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Beatriz Galati
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marina Gotelli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Gerhard Leubner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gotelli, M., Lattar, E., Zini, L.M. et al. Review on tapetal ultrastructure in angiosperms. Planta 257, 100 (2023). https://doi.org/10.1007/s00425-023-04138-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-023-04138-8

Keywords

search

Navigation