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Protoplasma

pp 1–16 | Cite as

Formation pattern in five types of pollen tetrad in Pseuduvaria trimera (Annonaceae)

  • Bingxin Li
  • Fengxia Xu
Original Article

Abstract

In basal angiosperms, there are several types of permanent tetrad but their formation pattern remains elusive. Pseuduvaria trimera has five types of tetrads and is the species with the most abundant tetrad types in Annonaceae. In order to interpret the formation pattern of different tetrad types, pollen development was investigated from the microspore mother cell stage to the bicellular pollen stage and the ultrastructure of pollen wall in the five tetrad types using light microscopy, transmission electron microscopy, and confocal laser scanning microscopy. Both successive and intermediate cytokinesis were observed within the same anther. The nucleus location of the microspores together with cytokinesis determine the number and the spatial arrangement of callose plates, and further have an effect on the tetrad types. The anthers with or without septation and the arrangement of microsporocytes might be also related to the tetrad type. The individual pollen grains within the tetrads are connected with each other by crosswall cohesion and cytoplasmic channels at localized points in the proximal walls. The various types of tetrads, cytokinesis, and cohesion in P. trimera reflect the high diversity in pollen development, which enhances the dramatic variety in pollen morphology in this family. Our observations of the development of tetrads provided some new insights for interpreting the factors influencing the types of tetrads, and reported the existence of a cytoplasmic channel in Annonaceae for the first time.

Keywords

Cytokinesis Pollen development Microsporogenesis Tetrad·cohesion Pollen tetrad Pseuduvaria trimera 

Notes

Acknowledgements

We are grateful to Dr. Louis Ronse De Craene for helping with the manuscript revision and two anonymous reviewers for their helpful suggestions. We also thank Senior Engineer Xinlan Xu and Junior Rufang Deng (South China Botanical Garden, Chinese Academy of Science) for their technical assistance with the TEM and Dr. Guifamg Yang for providing Fig. 2g–j. This work was financially supported by the National Natural Science Foundation of China (grant number 31270227), the Science and Technology Project of Guangdong Province (grant number 2017A030303062), and the Science and Technology Project of Guangzhou City (grant number 201804010100).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Albert B, Gouyon PH, Ressayre A (2009) Microsporogenesis variation in Codiaeum producing inaperturate pollen grain. CR Biol 332:507–516.  https://doi.org/10.1016/j.crvi.2009.02.001 CrossRefGoogle Scholar
  2. Albert B, Nadot S, Dreyer L, Ressayre A (2010) The influence of tetrad shape and intersporal callose wall formation on pollen aperture pattern ontogeny in two eudicot species. Ann Bot 106:557–564.  https://doi.org/10.3732/ajb.0900264 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Albert B, Ressayre A, Nadot S (2011) Correlation between pollen aperture pattern and callose deposition in late tetrad stage in three species producing atypical pollen grains. Am J Bot 98:189–196.  https://doi.org/10.3732/ajb.1000195 CrossRefPubMedGoogle Scholar
  4. 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.  https://doi.org/10.1111/boj.12385 CrossRefGoogle Scholar
  5. Bhandari NN (1971) Embryology of the Magnoliales and comments on their relationships. J Arnold Arbor Harv Univ 52:1–39Google Scholar
  6. Blackmore S, Crane PR (1988) Systematic implications of pollen and spore ontogeny. In: Humphries CJ (ed) Ontogeny and systematics. Columbia University Press, New York, pp 83–115Google Scholar
  7. Brown RC, Lemmon BE (1988) Microtubules associated with simultaneous cytokinesis of coenocytic microsporocytes. Am J Bot 75:1848–1856.  https://doi.org/10.2307/2444739 CrossRefGoogle Scholar
  8. Brown RC, Lemmon BE (1992) Control of division plane in normal and griseofulvin-treated microsporocytes of Magnolia. J Cell Sci 103:1031–1038Google Scholar
  9. Brown RC, Lemmon BE (1998) Division polarity and plasticity of the meiosis I spindle in Cypripedium californicum (Orchidaceae). Protoplasma 203:168–174.  https://doi.org/10.1007/bf01279473 CrossRefGoogle Scholar
  10. Brown RC, Lemmon BE (2005) γ-Tubulin and microtubule organization during microsporogenesis in Ginkgo biloba. J Plant Res 118:121–128.  https://doi.org/10.1007/s10265-005-0199-1 CrossRefPubMedGoogle Scholar
  11. Brown RC, Lemmon BE, Brown R, Lemmon B (1996) Nuclear cytoplasmic domains, microtubules and organelles in microsporocytes of the slipper orchid Cypripedium californicum a. Gray dividing by simultaneous cytokinesis. Sex Plant Reprod 9:145–152CrossRefGoogle Scholar
  12. Brownfield L, Yi J, Jiang H, Minina EA, Twell D, Köhler C (2015) Organelles maintain spindle position in plant meiosis. Nat Commun 6:6492.  https://doi.org/10.1038/ncomms7492 CrossRefPubMedGoogle Scholar
  13. Chatrou LW, Pirie MD, Erkens RHJ, Couvreur TLP, Neubig KM, Abbott JR, Mols JB, Mass JW, Saunders RMK, Chase MW (2012) A new subfamilial and tribal classification of the pantropical flowering plant family Annonaceae informed by molecular phylogenetics. Bot J Linn Soc 169:5–40CrossRefGoogle Scholar
  14. Couvreur TLP, Botermans M, van Heuven BJ, van der Ham R (2008) Pollen morphology within the Monodoraclade, a diverse group of five African Annonaceae genera. Grana 47:185–210.  https://doi.org/10.1080/00173130802256913 CrossRefGoogle Scholar
  15. Dahl O, Rowley JR (1991) Microspore development in Calluna (Ericaceae). Exine formation. Ann Sci Nat Bot Paris 13 Ser 11:155–176Google Scholar
  16. Doyle JA, Le Thomas A (1994) Cladistic analysis and pollen evolution in Annonaceae. Acta Bot Gallica 141:149–170.  https://doi.org/10.1080/12538078.1994.10515148 CrossRefGoogle Scholar
  17. Doyle JA, Le Thomas A (2012) Evolution and phylogenetic significance of pollen in Annonaceae. Bot J Linn Soc 169:190–221CrossRefGoogle Scholar
  18. Fitzgerald MA, Calder DM, Knox RB (1993) Character states of development and initiation of cohesion between compound pollen grains of Acacia paradoxa. Ann Bot 71:51–59CrossRefGoogle Scholar
  19. Furness CA (2007) Why does some pollen lack apertures? A review of inaperturate pollen in eudicots. Bot J Linn Soc 155:29–48CrossRefGoogle Scholar
  20. Furness CA, Rudall PJ (1999) Microsporogenesis in monocotyledons. Ann Bot 84:475–499.  https://doi.org/10.1006/anbo.1999.0942 CrossRefGoogle Scholar
  21. Furness CA, Rudall PJ, Sampson FB (2002) Evolution of microsporogenesis in angiosperms. Int J Plant Sci 163:235–260CrossRefGoogle Scholar
  22. Gabarayeva NI (1992) Sporoderm development in Asimina triloba (Annonaceae) I. The developmental events before callose dissolution. Grana 31:213–222.  https://doi.org/10.1080/00173139209432033 CrossRefGoogle Scholar
  23. Gabarayeva NI (1993) Sporoderm development in Asimina triloba (Annonaceae). II. The developmental events after callose dissolution. Grana 32:210–220.  https://doi.org/10.1080/00173139309429984 CrossRefGoogle Scholar
  24. Gan YY, Liu Y, Xu FX (2015) Pollen morphology of selected species from Annonaceae. Grana 54:271–281.  https://doi.org/10.1080/00173134.2015.1096302 CrossRefGoogle Scholar
  25. Gottsberger G, Meinke S, Porembski S (2011) First records of flower biology and pollination in African Annonaceae: Isolona, Piptostigma, Uvariodendron, Monodora and Uvariopsis. Flora 206:498–510.  https://doi.org/10.1016/j.flora.2010.08.00 CrossRefGoogle Scholar
  26. Guo X, Tang CC, Thomas DC, Couvreur TLP, Saunders RMK (2017) A mega-phylogeny of the Annonaceae: taxonomic placement of five enigmatic genera and support for a new tribe, Phoenicantheae. Sci Rep 7:7323CrossRefPubMedPubMedCentralGoogle Scholar
  27. Heslop-Harrison J (1968) Pollen wall development. Science 161:220–237CrossRefGoogle Scholar
  28. Hesse M, Halbritter H, Weber M (2009) Beschorneria yuccoides and Asimina triloba (L.) dun:examples for proximal polar germinating pollen in angiosperms. Grana 48:151–159.  https://doi.org/10.1080/00173130903024343 CrossRefGoogle Scholar
  29. Knox RB, McConchie CA (1986) Structure and function of compound pollen. Pollen and spores: form and function. Academic Press, London, pp 265–282Google Scholar
  30. Li CJ, Fan BQ (1997) Changes in the 3-dimensional distribution of mitochondria during meiotic divisions of mouse oocytes. Theriogenology 48:33–41CrossRefPubMedGoogle Scholar
  31. Li PS, Thomas DC, Saunders RMK (2015) Phylogenetic reconstruction, morphological diversification and generic delimitation of Disepalum (Annonaceae). PLoS One 10:1–24.  https://doi.org/10.1371/journal.pone.0143481 CrossRefGoogle Scholar
  32. Liu Y, Xu FX (2012) Pollen morphology of four selected species in the Annonaceae. Plant Diversity 34:443–452.  https://doi.org/10.3724/SP.J.1143.2012.12044 CrossRefGoogle Scholar
  33. Locke JF (1936) Microsporogenesis and cytokinesis in Asimina triloba. Bot Gaz 98:159–168.  https://doi.org/10.1086/334624 CrossRefGoogle Scholar
  34. Lora J, Herrero M, Hormaza JI (2014) Microspore development in Annona (Annonaceae): differences between monad and tetrad pollen. Am J Bot 101:1508–1518.  https://doi.org/10.3732/ajb.1400312 CrossRefPubMedGoogle Scholar
  35. Lora J, Testillano PS, Risueno MC, Hormaza JI, Herrero M (2009) Pollen development in Annona cherimola mill. (Annonaceae). Implications for the evolution of aggregated pollen. BMC Plant Biol 9:129.  https://doi.org/10.1186/1471-2229-9-129 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Nadot S, Forchioni A, Penet L, Sannier J, Ressayre A (2006) Links between early pollen development and aperture pattern in monocots. Protoplasma 228:55–64.  https://doi.org/10.1007/s00709-006-0164-4 CrossRefPubMedGoogle Scholar
  37. Nadot S, Furness CA, Sannier J, Penet L, Triki-Teurtroy S, Albert B, Ressayre A (2008) Phylogenetic comparative analysis of microsporogenesis in angiosperms with a focus on monocots. Am J Bot 95:1426–1436.  https://doi.org/10.3732/ajb.0800110 CrossRefPubMedGoogle Scholar
  38. Pacini E, Hesse M (2002) Types of pollen dispersal units in orchids, and their consequences for germination and fertilization. Ann Bot 89:653–664.  https://doi.org/10.1093/aob/mcf138 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Parulekar NK (1970) Annonaceae. Proceedings of the symposium on comparative embryology of Angiosperms. Bulletin of the Indian National Science Academy, New Delhi, pp 38–41Google Scholar
  40. Penet L (2012) Premeiotic microsporocyte cell shape influences shape of tetrads during microsporogenesis. Int J Plant Sci 173:375–381.  https://doi.org/10.1086/664716 CrossRefGoogle Scholar
  41. Penet L, Nadot S, Ressayre A, Forchioni A, Dreyer L, Gouyon P (2005) Multiple developmental pathways leading to a single morphology: monosulcate pollen (examples from the Asparagales). Ann Bot 95:331–343.  https://doi.org/10.1093/aob/mci030 CrossRefPubMedGoogle Scholar
  42. Periasamy K, Thangavel S (1988) Anther development in Xylopia nigricans. Plant Sci 98:251–255Google Scholar
  43. Periasamy K, Kandasamy MK (1981) Development of the anther of Annona squamosa L. Ann Bot 48:885–893CrossRefGoogle Scholar
  44. Periasamy K, Swamy BGL (1959) Studies in the Anonnaceae. I. Microsporogenesis in Cananga odorata and Miliusa wrightiana. Phytomorphology 9:251–263Google Scholar
  45. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143:1–81CrossRefGoogle Scholar
  46. Rangaswamy NS, Subramanyan J, Tandon R, Bhuskute SR (2001) Microspore tetrad analysis: can either type of microsporogenesis engender tetrads of all configurations? Phytomorphology 51:573–586Google Scholar
  47. Ressayre A (2001) Equatorial aperture pattern in monocots: same definition rules as in eudicots? The example of two species of Pontederiaceae. Int J Plant Sci 162:1219–1224CrossRefGoogle Scholar
  48. Ressayre A, Dreyer L, Triki-Teurtroy S, Forchioni A, Nadot S (2005) Post-meiotic cytokinesis and pollen aperture pattern ontogeny: comparison of development in four species differing in aperture pattern. Am J Bot 92:576–583.  https://doi.org/10.3732/ajb.92.4.576 CrossRefPubMedGoogle Scholar
  49. Ressayre A, Godelle B, Raquin C, Gouyon PH (2002) Aperture pattern ontogeny in angiosperms. J Exp Zool 294:122–135.  https://doi.org/10.1002/jez.10150 CrossRefPubMedGoogle Scholar
  50. Ressayre A, Mignot A, Siljak-Yakovlev S, Raquin C (2003) Postmeiotic cytokinesis and pollen aperture number determination in eudicots: effect of the cleavage wall number. Protoplasma 221:257–268.  https://doi.org/10.1007/s00709-002-0075-y PubMedCrossRefGoogle Scholar
  51. Rodkiewicz B, Duda E (1988) Aggregations of organelles in meiotic cells of higher-plants. Acta Soc Bot Pol 57:637–654.  https://doi.org/10.5586/asbp.1988.058 CrossRefGoogle Scholar
  52. Sampson FB (2000) Pollen diversity in some modern Magnoliids. Int J Plant Sci 161:193–210.  https://doi.org/10.1086/317573 CrossRefGoogle Scholar
  53. Sastri RLN (1957) On the division of pollen mother cells in some Annonaceae. Sci Cult 22:633–634Google Scholar
  54. Sastri RLN (1969) Comparative morphology and phylogeny of the Ranales. Biol Rev 44:291–319CrossRefGoogle Scholar
  55. Schnarf K (1931) Vergleichende Embryologie der Angiospermen. Borntraeger, Berlin, p 354Google Scholar
  56. Shao YY, Xu FX (2017) Studies on pollen morphology of selected species of Annonaceae from Thailand. Grana 57:161–177.  https://doi.org/10.1080/00173134.2017.1350204 CrossRefGoogle Scholar
  57. Stanley RG, Linskens HF (1974) Wall Formation. In: Pollen: biology, biochemistry, management. Springer-Verlag, New York, pp 13–28CrossRefGoogle Scholar
  58. Su YCF, Saunders RMK (2003) Pollen structure, tetrad cohesion and pollen-connecting threads in Pseuduvaria (Annonaceae). Bot J Linn Soc 143:69–78.  https://doi.org/10.1046/j.1095-8339.2003.00204 CrossRefGoogle Scholar
  59. Takahashi H, Sohma K (1980) Pollen development in Pyrola japonica Klenze. Scientific reports of Tôhoku university, series 4. Biology 38:57–71Google Scholar
  60. Taylor ML, Hudson PJ, Rigg JM, Strandquist JN, Green JS, Thiemann TC, Osborn JM (2013) Pollen ontogeny in Victoria (Nymphaeales). Int J Plant Sci 174:1259–1276.  https://doi.org/10.1086/673246 CrossRefGoogle Scholar
  61. Tsou CH, Fu YL (2002) Tetrad pollen formation in Annona (Annonaceae): Proexine formation and binding mechanism. Am J Bot 89:734–747.  https://doi.org/10.3732/ajb.89.5.734 CrossRefPubMedGoogle Scholar
  62. Tsou CH, Fu YL (2006) Octad pollen formation in Cymbopetalum (Annonaceae): the binding mechanism. Plant Syst Evol 263:13–23.  https://doi.org/10.1007/s00606-006-0471-4 CrossRefGoogle Scholar
  63. Tsou CH, Johnson DM (2003) Comparative development of aseptate and septate anthers of Annonaceae. Am J Bot 90:832–848CrossRefPubMedGoogle Scholar
  64. Vanblerkom J, Runner MN (1984) Mitochondrial reorganization during resumption of arrested meiosis in the mouse oocyte. Am J Anat 171:335–355.  https://doi.org/10.1002/aja.1001710309 CrossRefGoogle Scholar
  65. Waha M (1987) Different origins of fragile exines within the Annonaceae. Plant Syst Evol 158:23–27CrossRefGoogle Scholar
  66. Walker JW (1971a) Contributions to the pollen morphology and phylogeny of the Annonaceae. I. Grana 11:45–54.  https://doi.org/10.1080/00173137109427411 CrossRefGoogle Scholar
  67. Walker JW (1971b) Pollen morphology, phytogeography, and phylogeny of the Annonaceae. Contributions Gray Herbarium Harvard University 202:1–131Google Scholar
  68. Waterkeyn L (1962) Les parois microsporocytaires de nature callosique chez Helleborus et Tradescantia. Cellule 62:225–255Google Scholar
  69. Waterkeyn L, Beinfait A (1970) On a possible function of the callosic special wall in Ipomoea purpurea (L) Roth. Grana 10:13–20.  https://doi.org/10.1080/00173137009429852 CrossRefGoogle Scholar
  70. Xu F, Ronse de Craene LP (2012) Pollen morphology and ultrastructure of selected species from Annonaceae. Plant Syst Evol 299:11–24.  https://doi.org/10.1007/s00606-012-0698 CrossRefGoogle Scholar
  71. Xu LY, Hu SY (1986) The stain of thick resin sections. Chin Bull Bot 4:108–110Google Scholar
  72. Xue B, Su YCF, Thomas DC, Saunders RMK (2012) Pruning the polyphyletic genus Polyalthia (Annonaceae) and resurrecting the genus Monoon. Taxon 61:1021–1039Google Scholar
  73. Zhang CH, Guinel FC, Moffatt BA (2002) A comparative ultrastructural study of pollen development in Arabidopsis thaliana ecotype Columbia and male-sterile mutant apt1-3. Protoplasma 219:59–71CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical GardenChinese Academy of SciencesGuangzhouChina
  2. 2.College of Life SciencesUniversity of Chinese Academy of SciencesBeijingChina
  3. 3.Guangdong Provincial Key Laboratory of Applied Botany, South China Botanical GardenChinese Academy of SciencesGuangzhouChina

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