Advertisement

Plant Reproduction

, Volume 28, Issue 3–4, pp 143–151 | Cite as

Nuclear membrane localization during pollen development and apex-focused polarity establishment of SYP124/125 during pollen germination in Arabidopsis thaliana

  • Mie Ichikawa
  • Megumi Iwano
  • Masa H. SatoEmail author
Original Article

Abstract

Key message

Establishment of apex-polarity.

Abstract

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.

Keywords

Ca2+ gradient Membrane trafficking Polarity Pollen germination SNARE 

Notes

Acknowledgments

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].

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interests.

Supplementary material

497_2015_265_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 29 kb)
497_2015_265_MOESM2_ESM.docx (38 kb)
Supplementary material 2 (DOCX 37 kb)
497_2015_265_MOESM3_ESM.pdf (2.3 mb)
Supplementary material 3 (PDF 2379 kb)

Supplementary material 4 (MOV 681 kb)

497_2015_265_MOESM5_ESM.mov (986 kb)
Supplementary material 5 (MOV 986 kb)

References

  1. Angold RE (1968) The formation of the generative cell in the pollen grain of Endymion non-scriptus (L). J Cell Sci 578:573–578Google Scholar
  2. 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 15:5118–5129PubMedCentralCrossRefPubMedGoogle Scholar
  3. Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52:570–582CrossRefPubMedGoogle Scholar
  4. 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 29:546–558CrossRefGoogle Scholar
  5. Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865CrossRefGoogle Scholar
  6. 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 225:541–550CrossRefPubMedGoogle Scholar
  7. 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 48:19–30CrossRefPubMedGoogle Scholar
  8. Cheung AY, Wu H (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572CrossRefPubMedGoogle Scholar
  9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  10. 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 69:241–251CrossRefPubMedGoogle Scholar
  11. 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 50:280–289CrossRefPubMedGoogle Scholar
  12. 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 95:15781–15786PubMedCentralCrossRefPubMedGoogle Scholar
  13. 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 55:781–789CrossRefPubMedGoogle Scholar
  14. Geitmann A, Emons AMC (2000) The cytoskeleton in plant and fungal cell tip growth. J Microsc 198:218–245CrossRefPubMedGoogle Scholar
  15. 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 134:1227–1239PubMedCentralCrossRefPubMedGoogle Scholar
  16. 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 142:481–491PubMedCentralCrossRefPubMedGoogle Scholar
  17. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85PubMedCentralCrossRefPubMedGoogle Scholar
  18. 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 55:790–800CrossRefPubMedGoogle Scholar
  19. 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 136:3562–3571PubMedCentralCrossRefPubMedGoogle Scholar
  20. 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 150:1322–1334PubMedCentralCrossRefPubMedGoogle Scholar
  21. 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 104:11850–11855PubMedCentralCrossRefPubMedGoogle Scholar
  22. Kania U, Fendrych M, Friml J (2014) Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biol 4:140017PubMedCentralCrossRefPubMedGoogle Scholar
  23. Lipka V, Kwon C, Panstruga R (2007) SNARE-Ware: the role of SNARE-domain proteins in plant biology. Annu Rev Cell Dev Biol 23:147–174CrossRefPubMedGoogle Scholar
  24. Lukowitz W, Mayer U, Jürgens G (1996) Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84:61–71CrossRefPubMedGoogle Scholar
  25. 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 5:531–535CrossRefPubMedGoogle Scholar
  26. 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 104:34–41CrossRefPubMedGoogle Scholar
  27. Okuda S, Higashiyama T (2010) Pollen tube guidance by attractant molecules: LUREs. Cell Struct Funct 35:45–52CrossRefPubMedGoogle Scholar
  28. Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799PubMedGoogle Scholar
  29. 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 31–56CrossRefGoogle Scholar
  30. Sanderfoot A (2007) Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. Plant Physiol 144:6–17PubMedCentralCrossRefPubMedGoogle Scholar
  31. 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 10:179PubMedCentralCrossRefPubMedGoogle Scholar
  32. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedCentralCrossRefPubMedGoogle Scholar
  33. 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 18:935–954PubMedCentralCrossRefPubMedGoogle Scholar
  34. 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 135:25–38PubMedCentralCrossRefPubMedGoogle Scholar
  35. 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 29:49–65CrossRefPubMedGoogle Scholar
  36. 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 6:665–670PubMedCentralCrossRefPubMedGoogle Scholar
  37. Wang T, Xiang Y, Hou J, Ren H (2008) ABP41 is involved in the pollen tube development via fragmenting actin filaments. Mol Plant 1:1048–1055CrossRefPubMedGoogle Scholar
  38. 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 49:302–312CrossRefPubMedGoogle Scholar
  39. 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 22:2749–2767PubMedCentralCrossRefPubMedGoogle Scholar
  40. 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:e102407PubMedCentralCrossRefPubMedGoogle Scholar
  41. Zonia L, Munnik T (2008) Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. J Exp Bot 59:861–873CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Graduate School of Life and Environmental SciencesKyoto Prefectural UniversityKyotoJapan
  2. 2.Graduate School of Biological SciencesNara Institute of Science and TechnologyIkomaJapan
  3. 3.The Institute of Scientific and Industrial ResearchOsaka UniversityIbarakiJapan

Personalised recommendations