Establishment of apex-polarity.
Elongation of the pollen tube is a highly coordinated process involving polarized secretion of cell wall and membrane materials to the apical region. We investigated changes in the localization of soluble NSF attachment proteins (SNAREs) in developing pollen grains and the pollen tube for transgenic Arabidopsis expressing pollen-specific plasma-membrane Qa-SNAREs (SYP124, 125 and 131) fused with the green fluorescent protein (GFP). The expression of SYP124 and SYP125 was firstly detected in the microspore nuclear membrane during pollen mitosis II. Although SYP124, 125 and 131 accumulated throughout the cytosol in the mature pollen grain, GFP-SYP124 and GFP-SYP125 were highly concentrated in the apical or subapical regions of the elongating pollen tube with slightly different localization patterns, whereas GFP-SYP131 was uniformly localized to the plasma membrane of the pollen tube. The apex-focused polarity of GFP-SYP125 was established coincident with formation of a Ca2+ gradient before pollen germination. These results suggest that SNAREs function differentially in the same cells and that at least two distinct membrane transport pathways are involved in the pollen development and the pollen tube germination and elongation.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Angold RE (1968) The formation of the generative cell in the pollen grain of Endymion non-scriptus (L). J Cell Sci 578:573–578
Assaad FF, Qiu J, Youngs H, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129
Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52:570–582
Boutté Y, Frescatada-Rosa M, Men S, Chow C, Ebine K, Gustavsson A, Johansson L, Ueda T, Moore I, Jürgens G, Grebe M (2010) Endocytosis restricts Arabidopsis KNOLLE syntaxin to the cell division plane during late cytokinesis. EMBO 29:546–558
Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865
Catalano CM, Czymmek KJ, Gann JG, Sherrier DJ (2007) Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 225:541–550
Chen T, Teng N, Wu X, Wang Y, Tang W, Šamaj J, Baluška F, Lin J (2007) Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiol 48:19–30
Cheung AY, Wu H (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
Eisenach C, Chen Z, Grefen C, Blatt MR (2012) The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K+ channel activity with vegetative growth. Plant J 69:241–251
Enami K, Ichikawa M, Uemura T, Kutsuna N, Hasezawa S, Nakagawa T, Nakano A, Sato MH (2009) Differential expression control and polarized distribution of plasma membrane-resident SYP1 SNAREs in Arabidopsis thaliana. Plant Cell Physiol 50:280–289
Fasshauer D, Sutton RB, Brunger AT, Jahn R (1998) Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc Natl Acad Sci USA 95:15781–15786
Fujiwara M, Uemura T, Ebine K, Nishimori Y, Ueda T, Nakano A, Sato MH, Fukao Y (2014) Interactomics of Qa-SNARE in Arabidopsis thaliana. Plant Cell Physiol 55:781–789
Geitmann A, Emons AMC (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245
Hicks GR, Rojo E, Hong S, Carter DG, Raikhel NV (2004) Geminating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol 134:1227–1239
Higashiyama T, Inatsugi R, Sakamoto S, Sasaki N, Mori T, Kuroiwa H, Nakada T, Nozaki H, Kuroiwa T, Nakano A (2006) Species preferentiality of the pollen tube attractant derived from the synergid cell of Torenia fournieri. Plant Physiol 142:481–491
Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85
Ichikawa M, Hirano T, Enami K, Fuselier T, Kato N, Kwon C, Voigt B, Schulze-Lefert P, Baluška F, Sato MH (2014) Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana. Plant Cell Physiol 55:790–800
Iwano M, Shiba H, Miwa T, Che F, Takayama S, Nagai T, Miyawaki A, Isogai A (2004) Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136:3562–3571
Iwano M, Entani T, Shiba H, Kakita M, Nagai T, Mizuno H, Miyawaki A, Shoji T, Kubo K, Isogai A, Takayama S (2009) Fine-tuning of the cytoplasmic Ca2+ concentration is essential for pollen tube growth. Plant Physiol 150:1322–1334
Kalde M, Nühse TS, Findlay K, Peck SC (2007) The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc Natl Acad Sci USA 104:11850–11855
Kania U, Fendrych M, Friml J (2014) Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol 4:140017
Lipka V, Kwon C, Panstruga R (2007) SNARE-Ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174
Lukowitz W, Mayer U, Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84:61–71
Müller I, Wagner W, Völker A, Schellmann S, Nacry P, Küttner F, Schwarz-Sommer Z, Mayer U, Jürgens G (2003) Syntaxin specificity of cytokinesis in Arabidopsis. Nat cell Biol 5:531–535
Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T (2007) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104:34–41
Okuda S, Higashiyama T (2010) Pollen tube guidance by attractant molecules: LUREs. Cell Struct Funct 35:45–52
Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799
Peer WA (2011) Plasma membrane protein trafficking. In: Murphy AS, Peer WA, Schulz B (eds) The Plant Plasma Membrane. Plant cell monographs, vol 19. Springer, Berlin, pp 31–56
Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144:6–17
Silva PA, Ul-Rehman R, Rato C, Di Sansebastiano GP, Malhó R (2010) Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. BMC Plant Biol 10:179
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767
Sutter J, Campanoni P, Tyrrell M, Blatt MR (2006) Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1K+ Channel at the Plasma Membrane. Plant Cell 18:935–954
Tian G, Mohanty A, Chary SN, Li S, Paap B, Drakakaki G, Kopec CD, Li J, Ehrhardt D, Jackson D, Rhee SY, Raikhel NV, Citovsky V (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol 135:25–38
Uemura T, Ueda T, Ohniwa RL, Nakano A, Takeyasu K, Sato MH (2004) Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-golgi network in plant cells. Cell Struct Funct 29:49–65
Ul-Rehman R, Silva PÂ, Malhó R (2011) Localization of Arabidopsis SYP125 syntaxin in the plasma membrane sub-apical and distal zones of growing pollen tubes. Plant Signal Behav 6:665–670
Wang T, Xiang Y, Hou J, Ren H (2008) ABP41 is involved in the pollen tube development via fragmenting actin filaments. Mol Plant 1:1048–1055
Zhang Z, Feechan A, Pedersen C, Newman M, Qiu J, Olesen KL, Thordal-Christensen H (2007) A SNARE-protein has opposing functions in penetration resistance and defence signalling pathways. Plant J 49:302–312
Zhang H, Qu X, Bao C, Khurana P, Wang Q, Xie Y, Zheng Y, Chen N, Blanchoin L, Staiger CJ, Huang S (2010) Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell 22:2749–2767
Zhu J, Wu X, Yuan S, Qian D, Nan Q, An L, Xiang Y (2014) Annexin5 plays a vital role in Arabidopsis pollen development via Ca2+-dependent membrane trafficking. PLoS One 9:e102407
Zonia L, Munnik T (2008) Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J Exp Bot 59:861–873
We thank G Jürgens (Universität Tübingen) for valuable discussions on this research project. This work was supported by the Ministry of Education, Culture, Sports, Science and Technology, Japan; a-grant-in-aid for Scientific Research on Innovative Areas (No. 25119720), and the Strategic Research Funds of Kyoto Prefectural University to M.H.S. The Ministry of Education, Culture, Sports, Science and Technology, Japan [Grants-in-Aid to M.Ichikawa for Scientific Research for Plant Graduate Students from Nara Institute of Science and Technology].
Conflict of interest
The authors declare no conflict of interests.
Communicated by Zhenbiao Yang.
About this article
Cite this article
Ichikawa, M., Iwano, M. & Sato, M.H. Nuclear membrane localization during pollen development and apex-focused polarity establishment of SYP124/125 during pollen germination in Arabidopsis thaliana . Plant Reprod 28, 143–151 (2015) doi:10.1007/s00497-015-0265-3
- Ca2+ gradient
- Membrane trafficking
- Pollen germination