Abstract
Direct growth of a pollen tube is an effective mechanism of sperm delivery characteristic for the majority of seed plants. In most cases, only one tube grows from one grain to perform the delivery function; meanwhile in Picea the appearance of two tubes from a single pollen grain is quite common during in vitro germination. Here, we describe the phenomenon of bipolar germination and test two hypotheses on its nature and possible role in gametophyte functioning. The hypothesis on “trophic” function of multiple tubes provoked by poor nutrition discussed in literature was not confirmed by in vitro growth tests; bipolar germination strongly decreased with lowering sucrose availability. The highest proportion of bipolar germination occurred in optimal conditions. We then assumed that bipolar germination occurs because turgor pressure is a non-directional force and effective systems of cell wall mechanical regulation are lacking. In hypertonic medium, bipolar germination was sufficiently lower than in isotonic medium, which was consistent with prediction of the «mechanical» hypothesis. Scanning electron microscopy and fluorescence microscopy analysis of pollen morphology and cell wall dynamics during both types of germination showed that the appearance of a single tube or bipolar germination depends on the extension of exine rupture. Cell wall softening by short-term ·OH treatment sufficiently decreased the percent of bipolar germination without affecting total germination efficiency. We concluded that mechanical properties of the cell wall and turgor pressure could shift the balance towards one of the germination patterns.
Similar content being viewed by others
References
Blackmore S, Cannon M (1983) Palynology and systematics of morinaceae. Rev Palaeobot Palynol 40:207–226
Chebli Y, Kroeger J, Geitmann A (2013) Transport logistics in pollen tubes. Mol Plant 6:1037–1052. https://doi.org/10.1093/mp/sst073
Chen T, Wu X, Chen Y, Li X, Huang M, Zheng M, Baluska F, Samaj J, Lin J (2009) Combined proteomic and cytological analysis of Ca2+-calmodulin regulation in Picea meyeri pollen tube growth. Plant Physiol 149:1111–1126. https://doi.org/10.1104/pp.108.127514
Cui Y, Ling Y, Zhou J, Li X (2015) Interference of the histone deacetylase inhibits pollen germination and pollen tube growth in Picea wilsonii Mast. PLoS One 10:1–15. https://doi.org/10.1371/journal.pone.0145661
Dawkins MD, Owens JN (2012) In vitro and in vivo pollen hydration, germination, and pollen-tube growth in white spruce, Picea glauca (Moench) Voss. Int J Plant Sci 154:506–521. https://doi.org/10.1086/297134
Derksen J, Rutten T, Van Amstel T et al (1995) Regulation of pollen tube growth. Acta Bot Neerl 44:93–119
De Win AHN, Knuiman B, Pierson ES, et al (1996) Development and cellular organization of Pinus sylvestris pollen tubes. Sex Plant Reprod 9:93–101. https://doi.org/10.1007/BF02153056
Fernando D, Quinn C, Brenner E, Owens J (2010) Male gametophyte development and evolution in extant gymnosperms. Int J Plant Dev Biol 4:47–63
Friedman WE (1987a) Growth and development of the male gametophyte of Ginkgo biloba within the ovule (in vivo). Am J Bot 74:1797–1815
Friedman WE (1987b) Morphogenesis and experimental aspects of growth and development of the male gametophyte of Ginkgo biloba in vitro. Am J Bot 74:1816–1830
Friedman WE (1993) The evolutionary history of the seed plant male gametophyte. Tree 8(1):15–21
Hesse M, Zetter R, Halbritter H et al (2009) Pollen terminology. In: An illustrated handbook, 1st edn. Springer, Wien and New York
Hill JP, Lord EM (1987) Dynamics of pollen tube growth in the wild radish Raphanus raphanistrum (Brassicaceae). II morphology, cytochemistry and ultrastructure of transmitting tissues, and path of pollen tube growth. Am J Bot 74:988–997
Johri BM (1992) Haustorial role of pollen tubes. Ann Bot 70:471–475
Kim G, Lee S, Shin S, Park Y (2018) Three-dimensional label-free imaging and analysis of Pinus pollen grains using optical diffraction tomography. Sci Rep 8:1782. https://doi.org/10.1038/s41598-018-20113-w
Lawson AA (1926) A contribution to the life-history of Bowenia. Earth Environ Sci Trans R Soc Edinb 54:357–394
Lazzaro MD (1999) Microtubule organization in germinated pollen of the conifer Picea abies (Norway spruce, Pinaceae). Am J Bot 86:759–766. https://doi.org/10.2307/2656696
Lora J, Hormaza JI, Herrero M (2016) The diversity of the pollen tube pathway in plants: toward an increasing control by the sporophyte. Front Plant Sci 7:107. https://doi.org/10.3389/fpls.2016.00107
Maksimov N, Evmenyeva A, Breygina M, Yermakov I (2018) The role of reactive oxygen species in pollen germination in Picea pungens (blue spruce). Plant Reprod 18:761–767. https://doi.org/10.1007/s00497-018-0335-4
Matamoro-Vidal A, Raquin C, Brisset F, Colas H, Izac B, Albert B, Gouyon PH (2016) Links between morphology and function of the pollen wall: an experimental approach. Bot J Linn Soc 180:478–490. https://doi.org/10.1111/boj.12378
Owens JN, Catalano GL, Morris SJ, Aitken-Christie J (1995) The reproductive biology of kauri (Agathis australis). II. Male gametes, fertilization, and cytoplasmic inheritance. Int J Plant Sci 156:404–416
Owens JN, Takaso T, John Runions C (1998) Pollination in conifers. Trends Plant Sci 3:479–485. https://doi.org/10.1016/S1360-1385(98)01337-5
Owens JN, Bennett J, Hirondelle SL (2005) Pollination and cone morphology affect cone and seed production in lodgepole pine seed orchards. Can J For Res 35:383–400. https://doi.org/10.1139/X04-176
Pettitt JM (1977) Detection in primitive gymnosperms of proteins and glycoproteins of possible significance in reproduction. Nature 266:530–532
Robert Bagnell C (1975) Species distinction among pollen grains of Abies, Picea, and Pinus in the rocky mountain area (a scanning electron microscope study). Rev Palaeobot Palynol 19:203–220. https://doi.org/10.1016/0034-6667(75)90041-X
Rudall PJ, Bateman RM (2007) Developmental bases for key innovations in the seed-plant microgametophyte. Trends Plant Sci 12:317–326. https://doi.org/10.1016/j.tplants.2007.06.004
Runions CJ, Owens JN (1999) Sexual reproduction of interior spruce (Pinaceae). I . Pollen germination to archegonial maturation. Int J Plant Sci 160:631–640
Smirnova AV, Matveyeva NP, Polesskaya OG, Yermakov IP (2009) Generation of reactive oxygen species during pollen grain germination. Russ J Dev Biol 40:345–353. https://doi.org/10.1134/S1062360409060034
Smirnova A, Matveyeva N, Yermakov I (2013) Reactive oxygen species are involved in regulation of pollen wall cytomechanics. Plant Biol 16:252–257. https://doi.org/10.1111/plb.12004
Stone LM, Seaton KA, Kuo J, McComb JA (2004) Fast pollen tube growth in Conospermum species. Ann Bot 93:369–378. https://doi.org/10.1093/aob/mch050
Venalainen MO, Aronen TS, Haggman HM, Nikkanen TO (1999) Differences in pollen tube growth and morphology among Scots pine plus trees. For Genet 6:139–147
Williams JH (2008) Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Pnas 105:11259–11263. https://doi.org/10.1073/pnas.0800036105
Williams JH (2012) Pollen tube growth rates and the diversification of flowering plant reproductive cycles. Int J Plant Sci 173:649–661. https://doi.org/10.1086/665822
Wilms HJ (1981) Pollen tube penetration and fertilization in spinach. Acta Bot Neerl 30:101–122
Acknowledgments
Authors are grateful to White Sea Biological Station and Laboratory of electron microscopy of Moscow State University for technical opportunities to conduct experiments. This study was supported by Russian Foundation for Basic Research (project 18-34-00979).
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Anne-Catherine Schmit
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Breygina, M., Maksimov, N., Polevova, S. et al. Bipolar pollen germination in blue spruce (Picea pungens). Protoplasma 256, 941–949 (2019). https://doi.org/10.1007/s00709-018-01333-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-018-01333-3