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Pollen vacuoles and their significance

Abstract

Vacuoles of several types can be observed in pollen throughout its development. Their physiological significance reflects the complexity of the biological process leading to functional pollen grains. Vacuolisation always occurs during pollen development but when ripe pollen is shed the extensive translucent vacuoles present in the vegetative parts in previous stages are absent. Vacuole functions vary according to developmental stage but in ripe pollen they are mainly storage sites for reserves. Vacuoles cause pollen to increase in size by water accumulation and therefore confer some degree of resistance to water stress. Modalities of vacuolisation occur in pollen in the same manner as in other tissues. In most cases, autophagic vacuoles degrade organelles, as in the microspore after meiosis, and can be regarded as cytoplasm clean-up following the transition from the diploid sporophytic to the haploid gametophytic state. This also occurs in the generative cell but not in sperm cells. Finally, vacuoles have a function when microspores are used for pollen embryogenesis in biotechnology being targets for stress induction and afterwards contributing to cytoplasmic rearrangement in competent microspores.

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References

  1. Alexandersson E, Fraysse L, Sjovall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484

    PubMed  Article  CAS  Google Scholar 

  2. Aouali N, Laporte P, Clément C (2001) Pectin secretion and distribution in the anther during pollen development in Lilium. Planta 213:71–79

    PubMed  Article  CAS  Google Scholar 

  3. Baldi BG, Franceschi VR, Loewus FA (1987) Localization of phosphorus and cation reserves in Lilium longiflorum pollen. Plant Physiol 83:1018–1021

    PubMed  Article  CAS  Google Scholar 

  4. Baskin CC, Baskin JM (1998) Seeds: ecology biogeography and evolution of dormancy and germination. Academic Press, San Diego

    Google Scholar 

  5. Benito-Moreno RM, Macke F, Hause MT, Alwen A, Heberle-Bors E (1988) Sporophytes and male gametophytes from in vitro cultured, immature tobacco pollen. In: Cresti M, Gori P, Pacini E (eds) Sexual reproduction in higher plants. Springer, Berlin, pp 137–142

    Google Scholar 

  6. Blackmore S, Barnes S (1990) Pollen wall development in angiosperms. In: Blackmore S, Knox RB (eds) Microspore: evolution and ontogeny. Academic Press, London, pp 173–192

    Google Scholar 

  7. Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168

    PubMed  Article  CAS  Google Scholar 

  8. Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478

    PubMed  Article  CAS  Google Scholar 

  9. Bots M, Feron R, Uehlein N, Weterings K, Kaldenhoff R, Mariani T (2005) PIP1 and PIP2 aquaporins are differentially expressed during tobacco anther and stigma development. J Exp Bot 56:113–121

    PubMed  CAS  Google Scholar 

  10. Brown RC, Lemmon BE (1981) Aperture development in spore of the moss, Trematodon longicollis Mx. Protoplasma 106:273–287

    Article  Google Scholar 

  11. Butow R, Rodriguez-Garcia MI, Alché JD, Gorska-Brylass A (1997) Calcium in electron-dense globoids during pollen grain maturation in Chlorophytum elatum R.Br. Planta 203:413–421

    Article  Google Scholar 

  12. Cass DD, Karas I (1975) Development of sperm cells in barley. Can J Bot 53:1051–1062

    Article  Google Scholar 

  13. Chang T, Neuffer MG (1989) Maize microsporogenesis. Genome 32:232–244

    Article  Google Scholar 

  14. Christensen JE, Horner HT (1974) Pollen pore development and its spatial orientation during microsporogenesis in the grass Sorghum bicolor. Am J Bot 61:604–623

    Article  Google Scholar 

  15. Clément C, Audran JC (1996) In vivo and in vitro pollen maturation of Lilium. Influence of carbohydrates. Acta Soc Bot Pol 65:73–82

    Google Scholar 

  16. Clément C, Pacini E (2001) Anther plastids in angiosperms. Bot Rev 67:54–73

    Article  Google Scholar 

  17. Clément C, Chavant L, Burrus M, Audran JC (1994) Anther starch variations in Lilium during pollen development. Sex Plant Reprod 7:347–356

    Article  Google Scholar 

  18. Clément C, Laporte P, Audran JC (1998) The loculus content and tapetum during pollen development in Lilium. Sex Plant Reprod 11:94–106

    Article  Google Scholar 

  19. Clément C, Sangwan RS, Sangwan BS (2005) Microspore embryo induction and development in higher plants: cytological and ultrastructural aspects. In: Palmer CE, Keller WA, Kasha KJ (eds) Haploids in crop improvement II. Springer, Berlin, pp 53–72

    Chapter  Google Scholar 

  20. Cran DR (1979) The ultrastructure of fern gametophyte cells. In: Dyer AF (ed) The experimental biology of ferns. Academic Press, London, pp 171–213

    Google Scholar 

  21. Dai S, Li L, Chen T, Chong K, Xue Y, Wang T (2006) Proteomic analyses of Oryza sativa mature pollen reveal novel proteins associated with pollen germination and tube growth. Proteomics 6:2504–2529

    PubMed  Article  CAS  Google Scholar 

  22. Dettmer J, Schubert D, Calvo-Weimar O, Stierhof Y-D, Schmidt R, Schumacher K (2005) Essential role of V-ATPase in male gametophyte development. Plant J 41:117–124

    PubMed  Article  CAS  Google Scholar 

  23. Dottge JD (1973) The fine structure of algal cells. Academic Press, London

    Google Scholar 

  24. Evans DE, Taylor PE, Singh MB, Knox RB (1991) Quantitative analysis of lipids and protein from the pollen of Brassica napus L. Plant Sci 73:117–126

    Article  CAS  Google Scholar 

  25. Evans DE, Taylor PE, Singh MB, Knox RB (1992) The interrelationship between the accumulation of lipids, protein and level of acyl carrier protein during development of Brassica napus L. pollen. Planta 186:343–354

    Article  CAS  Google Scholar 

  26. Footitt S, Cohn MA (2001) Developmental arrest: from sea urchin to seeds. Seed Sci Res 11:2–16

    Article  Google Scholar 

  27. Franchi GG, Bellani LM, Nepi M, Pacini E (1996) Types of carbohydrate reserves in pollen: localization, systematic distribution and ecophysiological significance. Flora 191:143–159

    Google Scholar 

  28. Franchi GG, Nepi M, Pacini E (2002) Partially hydrated pollen: taxonomic distribution, ecological and evolutionary significance. Plant Syst Evol 234:211–227

    Article  CAS  Google Scholar 

  29. Garrido D, Vicente O, Heberle-Bors E, Rodriguez-Garcia I (1995) Cellular changes during the acquisition of embryogenic potential in isolated pollen grains of Nicotiana tabacum. Protoplasma 186:220–230

    Article  Google Scholar 

  30. Helsper JPFG, Linskens HF, Jackson JF (1984) Phytate metabolism in Petunia pollen. Phytochemistry 23:1841–1845

    Article  CAS  Google Scholar 

  31. Heslop-Harrison J (1979) An interpretation of the hydrodynamics of pollen. Am J Bot 66:737–743

    Article  Google Scholar 

  32. Heslop-Harrison J (1987) Pollen germination and pollen-tube growth. Int Rev Cytol 107:1–78

    Article  Google Scholar 

  33. Heslop-Harrison J, Heslop-Harrison Y, Heslop-Harrison JS (1997) Motility in ungerminated grass pollen: association of myosin with polysaccharide-containing wall-precursors bodies (P bodies). Sex Plant Reprod 10:65–66

    Article  Google Scholar 

  34. Hicks GR, Rojo E, Hong S, Carter DG, Raikhel N (2004) Germinating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol 134:1227–1239

    PubMed  Article  CAS  Google Scholar 

  35. Hoekstra FA, van Zijderweld MH, Heidekamp F, van der Mark F (1993) Microspore culture of Hordeum vulgare L.: the influence of density and osmolality. Plant Cell Rep 12:661–665

    Article  Google Scholar 

  36. Holmes-Davis R, Tanaka CK, Vensel WH, Hurkman WJ, McCormick S (2005) Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5:4864–4884

    PubMed  Article  CAS  Google Scholar 

  37. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652

    PubMed  Article  CAS  Google Scholar 

  38. Howden R, Park SK, Moore JM, Orme J, Grossniklaus U, Twell D (1998) Selection of T-DNA tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149:621–631

    PubMed  CAS  Google Scholar 

  39. Ikeda S, Nasrallah JB, Dixit R, Preiss S, Nasrallah ME (1997) An aquaporin-like gene required for the Brassica self-incompatibility response. Science 276:1564–1566

    PubMed  Article  CAS  Google Scholar 

  40. Indrianto A, Barinova I, Touraev A, Heberle-Bors E (2001) Tracking individual wheat microspores in vitro: identification of embryogenic microspores and body axis formation in the embryo. Planta 212:163–174

    PubMed  Article  CAS  Google Scholar 

  41. Jacquard C, Mazeyrat-Gourbeyre F, Devaux P, Boutilier K, Baillieul F, Clément C (2009) Microspore embryogenesis in barley: anther pre-treatment stimulates plant defence gene expression. Planta 229:393–402

    PubMed  Article  CAS  Google Scholar 

  42. Jakobsen MK, Poulsen LR, Schulz A, Fleurat-Lessard P, Moller A, Husted S, Schiott M, Amtmann A, Palmgren MG (2005) Pollen development and fertilization in Arabidopsis is dependent on the male gametogenesis impaired anthers gene encoding a type V P-type ATPase. Genes Dev 19:2757–2769

    PubMed  Article  CAS  Google Scholar 

  43. John P (1991) Fructan quality and fructan synthesis. Biochem Soc T 19:569–572

    CAS  Google Scholar 

  44. Kjellbom P, Larsson C, Johansson I, Karlsson M, Johanson U (1999) Aquaporins and water homeostasis in plants. Trends Plant Sci 4:308–314

    PubMed  Article  Google Scholar 

  45. Knox RB, Ducker SC (1991) The evolution of gametes—from motility to double fertilization. In: Blackmore S, Barnes SH (eds) Pollen and spores-pattern of diversification. Systematic Association Special Volume n°44. Clarendon Press, Oxford, pp 345–361

    Google Scholar 

  46. Kuang A, Musgrave ME (1996) Dynamics of vegetative cytoplasm during generative cell formation and pollen maturation in Arabidopsis thaliana. Protoplasma 194:81–90

    PubMed  Article  CAS  Google Scholar 

  47. Kumlehn J, Lörz H (1999) Monitoing sporophytic development of individual microspores of barley (Hordeum vulgare L.). In: Clément C, Pacini E, Audran JC (eds) Anther and pollen: from biology to biotechnology. Springer, Berlin, pp 183–190

    Google Scholar 

  48. Luu D-T, Maurel C (2005) Acquaporins in a challenging environment: molecular gears for adjusting plant water status. Plant Cell Environ 28:85–96

    Article  CAS  Google Scholar 

  49. Maeshima M, Ishikawa F (2008) ER membrane aquaporins in plants. Eur J Physiol 456:709–716

    Article  CAS  Google Scholar 

  50. Maraschin SF, Vennik M, Lamers GEM, Spaink HP, Wang M (2005) Time-lapse tracking of barley androgenesis reveals position-determined cell death within pro-embryos. Planta 220:531–540

    Article  CAS  Google Scholar 

  51. Margulis L, Schwartz KV (1982) Five Kingdoms: an illustrated guide to the phyla of life on earth. Freeman and Co, San Francisco

    Google Scholar 

  52. Marty F (1999) Plant vacuoles. Plant Cell 11:587–599

    PubMed  Article  CAS  Google Scholar 

  53. Maurel C (1997) Aquaporins and water permeability of plant membranes. Annu Rev Plant Physiol Plant Mol Biol 48:399–429

    PubMed  Article  CAS  Google Scholar 

  54. McConchie CA, Knox RB (1989) Pollination and reproductive biology of seagrasses. In: Larkum AWD, McComb AJ, Sheperd SA (eds) Biology of seagrasses. Elsevier, Amsterdam, pp 74–111

    Google Scholar 

  55. McConchie CA, Hough T, Knox RB (1987) Ultrastructural analysis of the sperm cells of mature pollen of maize, Zea mays. Protoplasma 139:9–19

    Article  Google Scholar 

  56. McCormick S (2004) Control of male gametophyte development. Plant Cell 16:142–153

    Article  Google Scholar 

  57. McCormick S, Curie C, Eyal Y, Muschietti J, Dirks L, Kulikauskas R (1994) Molecular biology of male gametogenesis. Euphytica 79:245–250

    Article  CAS  Google Scholar 

  58. Mckenzie A, Heslop-Harrison J, Dickinson HG (1967) Elimination of ribosomes during meiotic prophase. Nature 215:997–999

    Article  Google Scholar 

  59. Mimura T, Kura-Hotta M, Tsujimura T, Ohnishi M, Miura M, Okazaki Y, Miura M, Maeshima M, Washitani-Nemoto S (2003) Rapid increase of vacuolar volume in response to salt stress. Planta 216:397–402

    PubMed  CAS  Google Scholar 

  60. Nagata N, Saito C, Sakai A, Kuroiwa H, Kuroiwa T (2000) Unique positioning of mitochondria in developing microspores and pollen grains in Pharbitis nil: mitochondria cover the nuclear surface at specific developmental stages. Protoplasma 213:74–82

    Article  Google Scholar 

  61. Neidhart HV (1979) Comparative studies of sporogenesis in Bryophytes. In: Clarke CGS, Duckett JS (eds) Bryophyte systematics. Academic Press, London, pp 251–280

    Google Scholar 

  62. Nepi M, Franchi GG, Pacini E (2001) Pollen hydration status at dispersal: cytophysiological features and strategies. Protoplasma 216:171–180

    PubMed  Article  CAS  Google Scholar 

  63. Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flügge U-F, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17:746–759

    Article  Google Scholar 

  64. O’Brien M, Bertrand C, Matton DP (2002) Characterization of a fertilization-induced and developmentally regulated plasma-membrane aquaporin expressed in reproductive tissues, in the wild potato Solanum chacoense Bitt. Planta 215:485–493

    PubMed  Article  Google Scholar 

  65. Oldenhof MT, Groot PFM, Visser JH, Schrauven JAM, Wullems GJ (1996) Isolation and characterization of a microspore-specific gene from tobacco. Plant Mol Biol 31:213–225

    PubMed  Article  CAS  Google Scholar 

  66. Pacini E (1996) Types and meaning of pollen carbohydrates reserves. Sex Plant Reprod 9:362–366

    Google Scholar 

  67. Pacini E (2000) From anther and pollen ripening to pollen presentation. Plant Syst Evol 22:19–43

    Article  Google Scholar 

  68. Pacini E, Franchi GG (1983) Pollen grain development in Smilax aspera and possible function of the loculus. In: Mulcahy DL, Ottaviano E (eds) Pollen: biology and implications in plant breeding. Elsevier Biomedical, New York, pp 183–190

    Google Scholar 

  69. Pacini E, Hesse M (2002) Types of pollen dispersal units in orchids, and their consequences for germination and fertilisation. Ann Bot 89:653–664

    PubMed  Article  Google Scholar 

  70. Pacini E, Hesse M (2004) Cytophysiology of pollen presentation and dispersal. Flora 199:273–285

    Google Scholar 

  71. Pacini E, Juniper BJ (1984) The ultrastructure of pollen grain development in Lycopersicum peruvianum. Caryologia 37:21–50

    Google Scholar 

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

    Article  Google Scholar 

  73. Pacini E, Bellani LM, Lozzi R (1986) Pollen, tapetum and anther development in two cultivars of sweet cherry (Prunus avium). Pytomorphology 36:197–210

    Google Scholar 

  74. Pacini E, Taylor PE, Singh MB, Knox RB (1992) Development of plastids, including amyloplasts and starch grains, in pollen and tapetum of rye-grass, Lolium perenne. Ann Bot 70:179–188

    Google Scholar 

  75. Pandolfi T, Pacini E, Calder DM (1993) Ontogenesis of monad pollen in Pterostylis plumosa (Orchidaceae, Neottioideae). Plant Syst Evol 186:175–185

    Article  Google Scholar 

  76. Peiter E, Maathuis FJ, Mills LN, Knight H, Pelloux J, Hetherington AM, Sanders D (2005) The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434:404–408

    PubMed  Article  CAS  Google Scholar 

  77. Pertl H, Schulze WX, Obermeyer G (2009) The pollen organelle membrane proteome reveals highly spatial-temporal dynamics during germination and tube growth of lily pollen. J Proteome Res 8:5142–5152

    PubMed  Article  CAS  Google Scholar 

  78. Reisen D, Marty M, Leborgne-Castel N (2005) New insights into the tonoplast architecture of plant vacuoles and vacuolar dynamics during osmotic stress. BMC Plant Biol 5:1–13

    Article  Google Scholar 

  79. Rojo E, Zouhar J, Kovaleva V, Hong S, Raikhel NV (2003) The AtC-VPS protein complex is localized to the tonoplast and the prevacuolar compartment in Arabidopsis. Mol Biol Cell 14:361–369

    PubMed  Article  CAS  Google Scholar 

  80. Ruiter RK, van Eldik GJ, van Herpen MMA, Schrauwen JM, Wullems GJ (1997) Expression in anthers of two genes encoding Brassica oleracea transmembrane channel proteins. Plant Mol Biol 34:163–168

    PubMed  Article  CAS  Google Scholar 

  81. Russell SD (1984) Ultrastructure of the sperm of Plumbago zeylanica: II. Quantitative cytology and three-dimensional organization. Planta 162:385–391

    Article  Google Scholar 

  82. Saini HS (1997) Effects of water stress on male gametophyte development in plants. Sex Plant Reprod 10:67–73

    Article  Google Scholar 

  83. Sangwan RS (1986) Formation and cytochemistry of nuclear vacuoles during meiosis in Datura. Eur J Cell Biol 40:210–218

    Google Scholar 

  84. Sangwan RS, Camefort H (1983) The tonoplast, a specific marker of embryogenic microspores of Datura cultured in vitro. Histochemistry 78:473–480

    PubMed  Article  CAS  Google Scholar 

  85. Sangwan RS, Sangwan-Norreel BS (1987) Ultrastructural cytology of plastids in pollen grains of certain androgenic and nonandrogenic plants. Protoplasma 138:11–22

    Article  Google Scholar 

  86. Sangwan RS, Mathivet V, Vasseur G (1989) Ultrastructural localization of acid phosphatase during male meiosis and sporogenesis in Datura: evidence for digestion of cytoplasmic structures in the vacuoles. Protoplasma 149:38–46

    Article  Google Scholar 

  87. Schlag M, Hesse M (1992) The formation of the generative cell in Polystachya pubescens (Orchidaceae). Sex Plant Reprod 5:131–137

    Article  Google Scholar 

  88. Sheoran IS, Pedersen EJ, Ross ARS, Sawhney VK (2009) Dynamics of protein expression during pollen germination in canola (Brassica napus). Planta 230:779–793

    PubMed  Article  CAS  Google Scholar 

  89. Soto G, Alleva K, Mazzella MA, Amodeo G, Muschiett JP (2008) AtTIP1;3 and AtTIP5;1, the only highly expressed Arabidopsis pollen-specific aquaporins, transport water and urea. FEBS Lett 582:4077–4082

    PubMed  Article  CAS  Google Scholar 

  90. Southworth D, Dickinson DB (1981) Ultrastructural changes in germinating lily pollen. Grana 20:29–35

    Article  Google Scholar 

  91. Speranza A, Calzoni GL, Pacini E (1997) Occurrence of mono- or disaccharides and polysaccharide reserves in mature pollen grains. Sex Plant Reprod 10:110–115

    Article  CAS  Google Scholar 

  92. Strompen G, Dettmer J, Stierhof Y-D, Schumacher K, Jürgens G, Mayer U (2005) Arabidopsis H+-ATPase subunit E isoform 1 is required for Golgi organization and vacuole function in embryogenesis. Plant J 41:125–132

    PubMed  Article  CAS  Google Scholar 

  93. Theunis CH, Cresti M, Milanesi C (1991) Studies of the mature pollen of Spinacia oleracea after freeze substitution and observed with confocal laser scanning fluorescence microscopy. Bot Acta 104:324–329

    Google Scholar 

  94. Touraev A, Vicente O, Heberle-Bors E (1997) Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:297–302

    Article  Google Scholar 

  95. Twell D, Ki Park S, Lalanne E (1998) Asymmetric division and cell-fate determination in developing pollen. Trends Plant Sci 3:305–310

    Article  Google Scholar 

  96. Weber M (1988) Metabolism of P-particles (polysaccharide particles) in mature pollen grains of Eryngium campestre L. (Apiaceae). Protoplasma 146:65–71

    Article  Google Scholar 

  97. Wilson C, Voronin V, Touraev A, Vicente O, Heberle-Bors E (1997) A developmentally regulated MAP kinase activated by hydration in tobacco pollen. Plant Cell 9:2093–2100

    PubMed  Article  CAS  Google Scholar 

  98. Wojnarowiez G, Caredda S, Devaux P, Sangwan RS, Clément C (2004) Effects of different osmotica on androgenesis and albinism in barley (Hordeum vulgare L.). J Plant Physiol 161:747–755

    PubMed  Article  CAS  Google Scholar 

  99. Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44:1192–1201

    PubMed  Article  CAS  Google Scholar 

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Correspondence to Christophe Clément.

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Pacini, E., Jacquard, C. & Clément, C. Pollen vacuoles and their significance. Planta 234, 217–227 (2011). https://doi.org/10.1007/s00425-011-1462-4

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Keywords

  • ER
  • Lysosomes
  • Pollen
  • Reserves
  • Vacuoles
  • Volume increase