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Actin filament organization and polarity in pollen tubes revealed by myosin II subfragment 1 decoration

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Abstract

The actin cytoskeleton plays a crucial role in pollen tube growth. In elongating pollen tubes the organization and arrangement of actin filaments (AFs) differs between the shank and apical region. However, the orientation of AFs in pollen tubes has not yet been successfully demonstrated. In the present work we have used myosin II subfragment 1 (S1) decoration to determine the polarity of AFs in pollen tubes. Electron microscopy studies revealed that in the shank of the tube bundles of AFs exhibit uniform polarity with those close to the cell cortex having their barbed ends oriented towards the tip of the pollen tube while those in the cell center have their barbed ends oriented toward the base of the tube. At the subapex, some AFs are organized in closely packed and longitudinally oriented bundles and some form curved bundles adjacent to the cell membrane. In contrast, few AFs are dispersed with random orientation in the extreme apex of the pollen tube. Our results confirm that the direction of cytoplasmic streaming within pollen tubes is determined by the polarity of AFs in the bundles.

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Abbreviations

GFP:

Green fluorescent protein

EGTA:

Ethylene glycol tetraacetic acid

Mes:

Sigma BioUltra buffer

References

  • Cai G, Moscatelli A, Cresti M (1997) Cytoskeletal organization and pollen tube growth. Trends Plant Sci 2:86–91

    Article  Google Scholar 

  • Cárdenas L, Lovy-Wheeler A, Wilsen KL, Hepler PK (2005) Actin polymerization promotes the reversal of streaming in the apex of pollen tubes. Cell Motil Cytoskeleton 61:112–127

    Article  PubMed  Google Scholar 

  • Cárdenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol 146:1611–1621

    Article  PubMed  Google Scholar 

  • Chen CY, Wong EI, Vidali L, Estavillo A, Hepler PK, Wu H, Cheung AY (2002) The regulation of actin organization by actin-depolymerizing factor in elongating pollen tubes. Plant Cell 14:2175–2190

    Article  PubMed  CAS  Google Scholar 

  • Chen T, Teng N, Wu X, Wang Y, Tang W, Amaj J, Baluka 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

    Article  PubMed  CAS  Google Scholar 

  • Cheung AY, Wu HM (2004) Overexpression of an Arabidopsis formin stimulates supernumerary actin cable formation from pollen tube cell membrane. Plant Cell 16:257–269

    Article  PubMed  CAS  Google Scholar 

  • Derksen J, Ruttens T, van Amstel T, de Win A, Doris F, Steer M (1995) Regulation of pollen tube growth. Acta Bot Neerl 44:93–119

    Google Scholar 

  • Feijó JA, Costa SS, Prado AM, Becker JD, Certal AC (2004) Signalling by tips. Curr Opin Plant Biol 7:589–598

    Article  PubMed  Google Scholar 

  • Fu Y, Wu G, Yang Z (2001) GTPase dependent dynamics of tip localized F-actin controls tip growth in pollen tubes. J Cell Biol 152:1019–1032

    Article  PubMed  CAS  Google Scholar 

  • Geitmann A, Snowman BN, Emons AMC, Franklin-Tong VE (2000) Alternations in the actin cytoskeleton of pollen tubes are induced by the self-incompatibility reaction in Papaver rhoeas. Plant Cell 12:1239–1252

    Article  PubMed  CAS  Google Scholar 

  • Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11:2349–2363

    Article  PubMed  CAS  Google Scholar 

  • Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Bio 117:159–187

    Article  Google Scholar 

  • Hwang JU, Gu Y, Lee YJ, Yang Z (2005) Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 16:5385–5399

    Article  PubMed  CAS  Google Scholar 

  • Justus CD, Anderhag P, Goins JL, Lazzaro MD (2004) Microtubules and microfilaments coordinate to direct a fountain streaming pattern in elongating conifer pollen tube tips. Planta 219:103–109

    Article  PubMed  CAS  Google Scholar 

  • Kohno T, Shimmen T (1988) Accelerated sliding of pollen tube organelles along Characeae actin bundles regulated by Ca2+. J Cell Biol 106:1539–1543

    Article  PubMed  CAS  Google Scholar 

  • Kohno T, Chaen S, Shimmen T (1990) Characterization of the translocator associated with pollen tube organelles. Protoplasma 154:179–183

    Article  Google Scholar 

  • Lancelle SA, Hepler PK (1992) Ultrasructure of freeze-substituted pollen tubes of Lilium longiflorum. Protoplasma 167:215–230

    Article  Google Scholar 

  • Lancelle SA, Cresti M, Hepler PK (1987) Ultrasructure of the cytoskeleton in freeze-substituted pollen tubes of Nicotiana alata. Protoplasma 140:141–150

    Article  Google Scholar 

  • Li Y, Zee SY, Liu YM, Huang BQ, Yen LF (2001) Circular F-actin bundles and a G-actin gradient in pollen and pollen tubes of Lilium davidii. Planta 213:722–730

    Article  PubMed  CAS  Google Scholar 

  • Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK (2005) Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221:95–104

    Article  PubMed  CAS  Google Scholar 

  • Margossian SS, Lowely S (1982) Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol 85:55–71

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T, Lenartowska M, Miller KG (2006) Myosin VI stabilizes an actin network during Drosophila spermatid individualization. Mol Biol Cell 17:2559–2571

    Article  PubMed  CAS  Google Scholar 

  • Noguchi T, Lenartowska M, Rogat AD, Frank DJ, Miller KG (2008) Proper cellular reorganization during Drosophila spermatid individualization depends on actin structures composed of two domains, bundles and meshwork, that are differentially regulated and have different functions. Mol Biol Cell 19:2363–2372

    Article  PubMed  CAS  Google Scholar 

  • Ren H, Xiang Y (2007) The function of actin-binding proteins in pollen tube growth. Protoplasma 230:171–182

    Article  PubMed  CAS  Google Scholar 

  • Tang X, Lancelle SA, Hepler PK (1989) Fluorescence microscopic localization of actin in pollen tubes: comparsion of actin antibody and phalloidin staining. Cell Motil Cytoskeleton 12:216–224

    Article  PubMed  CAS  Google Scholar 

  • Tominaga M, Yokota E, Vidali L, Sonobe S, Hepler PK, Shimmen T (2000) The role of plant villin in the organization of the actin cytoskeleton, cytoplasmic streaming and the architecture of the transvacuolar strand in root hair cells of Hydrocharis. Planta 210:836–843

    Article  PubMed  CAS  Google Scholar 

  • Tylor LP, Hepler PK (1997) Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 48:461–491

    Article  Google Scholar 

  • Vidali L, Hepler PK (2001) Actin and pollen tube growth. Protoplasma 215:64–76

    Article  PubMed  CAS  Google Scholar 

  • Vidali L, Yokota E, Cheung AY, Shimmen T, Hepler PK (1999) The 135 kDa actin-bundling protein from Lilium longiforum pollen is the plant homologue of villin. Protoplasma 209:283–291

    Article  CAS  Google Scholar 

  • Vidali L, McKenna ST, Hepler PK (2001) Actin polymerization is essential for pollen tube growth. Mol Biol Cell 12:2534–2545

    PubMed  CAS  Google Scholar 

  • Yokota E, Shimmen T (1999) The 135-kDa actin-bundling protein from lily pollen tubes arranges F-actin into bundles with uniform polarity. Planta 209:264–266

    Article  PubMed  CAS  Google Scholar 

  • Yokota E, Takahara K, Shimmen T (1998) Actin-bundling protein isolated from pollen tubes of lily. Biochemical and immunocytochemical characterization. Plant Physiol 116:1421–1429

    Article  PubMed  CAS  Google Scholar 

  • Yokota E, Vidali L, Tominaga M, Tahara H, Orii H, Morizane Y, Hepler PK, Shimmen T (2003) Plant 115-kDa actin-filament bundling protein, P-115-ABP, is a homologue of plant villin and is widely distributed in cells. Plant Cell Physiol 44:1088–1099

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Tatsuhiko Noguchi (Laboratory of Morphogenetic Signaling, Center for Developmental Biology, RIKEN Kobe, Japan) for inspiration to modify the actin S1 decoration technique in plant cells, and Deborah J. Frank (Biology Department, Washington University in St. Louis, US) for critical reading of the manuscript. We also thank Olga Narbutt and Michal Swidzinski for their excellent technical assistance. This project was supported by the Ministry of Science and Higher Education in Poland, grant No. N303 023 32/1034.

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  1. Laboratory of Developmental Biology, Faculty of Biology and Earth Sciences, Nicolaus Copernicus University, Gagarina 9, 87-100, Torun, Poland

    Marta Lenartowska & Anna Michalska

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  1. Marta Lenartowska
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  2. Anna Michalska
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Correspondence to Marta Lenartowska.

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Lenartowska, M., Michalska, A. Actin filament organization and polarity in pollen tubes revealed by myosin II subfragment 1 decoration. Planta 228, 891–896 (2008). https://doi.org/10.1007/s00425-008-0802-5

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