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Sucrose concentration in the growth medium affects the cell wall composition of tobacco pollen tubes

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Abstract

The cell wall of pollen tubes is organized in both spatial and temporal order to allow the pollen tube to grow according to external conditions. The deposition of methyl-esterified and acid pectins in addition to callose/cellulose occurs according to a series of temporally succeeding events. In this work, we attempted to determine how the composition of the external growth medium (in terms of osmolarity) could affect the deposition of cell wall components. Pollen tubes of tobacco were grown in a hypotonic medium and then analyzed for the distribution of pectins and callose/cellulose [as well as for the distribution of the enzyme callose synthase (CALS)]. The data indicate that pollen tubes grown in a hypotonic medium show changes of the initial growth rate followed by modification of the deposition of acid pectins and, to a lesser extent, of CALS. These observations indicate that, under the osmolarity determined by the growth medium, pollen tubes adapt their cell wall to the changing conditions of growth.

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References

  • Anderson JR, Barnes WS, Bedinger P (2002) 2,6-Dichlorobenzonitrile, a cellulose biosynthesis inhibitor, affects morphology and structural integrity of petunia and lily pollen tubes. J Plant Physiol 159:61–67

    Article  CAS  Google Scholar 

  • Aouar L, Chebli Y, Geitmann A (2010) Morphogenesis of complex plant cell shapes: the mechanical role of crystalline cellulose in growing pollen tubes. Sex Plant Reprod 23:15–27

    Article  PubMed  Google Scholar 

  • Benkert R, Obermeyer G, Bentrup F-W (1997) The turgor pressure of growing lily pollen tubes. Protoplasma 198:1–8

    Article  Google Scholar 

  • Bosch M, Hepler PK (2005) Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell 17:3219–3226

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bosch M, Hepler PK (2006) Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth. Planta 223:736–745

    Article  CAS  PubMed  Google Scholar 

  • Bosch M, Cheung AY, Hepler PK (2005) Pectin methylesterase, a regulator of pollen tube growth. Plant Physiol 138:1334–1346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bougourd S, Marrison J, Haseloff J (2000) An aniline blue staining procedure for confocal microscopy and 3D imaging of normal and perturbed cellular phenotypes in mature Arabidopsis embryos. Plant J 24:543–550

    Article  CAS  PubMed  Google Scholar 

  • Boyer JS (2009) Evans Review: cell wall biosynthesis and the molecular mechanism of plant enlargement. Funct Plant Biol 36:383–394

    Article  CAS  Google Scholar 

  • Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Amer J Bot 50:859–865

    Article  CAS  Google Scholar 

  • Brownfield L, Ford K, Doblin MS, Newbigin E, Read S, Bacic A (2007) Proteomic and biochemical evidence links the callose synthase in Nicotiana alata pollen tubes to the product of the NaGSL1 gene. Plant J 52:147–156

    Article  CAS  PubMed  Google Scholar 

  • Brownfield L, Wilson S, Newbigin E, Bacic A, Read S (2008) Molecular control of the glucan synthase-like protein NaGSL1 and callose synthesis during growth of Nicotiana alata pollen tubes. Biochem J 414:43–52

    Article  CAS  PubMed  Google Scholar 

  • Cai G, Romagnoli S, Moscatelli A, Ovidi E, Gambellini G, Tiezzi A, Cresti M (2000) Identification and characterization of a novel microtubule-based motor associated with membranous organelles in tobacco pollen tubes. Plant Cell 12:1719–1736

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cai G, Faleri C, Del Casino C, Emons AMC, Cresti M (2011) Distribution of callose synthase, cellulose synthase and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol 155:1169–1190

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cardenas 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  CAS  PubMed Central  PubMed  Google Scholar 

  • Chebli Y, Kaneda M, Zerzour R, Geitmann A (2012) The cell wall of the Arabidopsis pollen tube—spatial distribution, recycling, and network formation of polysaccharides. Plant Physiol 160:1940–1955

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen LQ, Ye D (2007) Roles of pectin methylesterases in pollen-tube growth. J Int Plant Biol 49:94–98

    CAS  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  PubMed  Google Scholar 

  • Cresti M, van Went JL (1976) Callose deposition and plug formation in Petunia pollen tubes in situ. Planta 133:35–40

    Article  CAS  PubMed  Google Scholar 

  • Cresti M, Pacini E, Ciampolini F, Sarfatti G (1977) Germination and early tube development in vitro of Lycopersicum peruvianum pollen: ultrastructural features. Planta 136:239–247

    Article  CAS  PubMed  Google Scholar 

  • Derksen J, Janssen GJ, Wolters-Arts M, Lichtscheidl I, Adlassnig W, Ovecka M, Doris F, Steer M (2011) Wall architecture with high porosity is established at the tip and maintained in growing pollen tubes of Nicotiana tabacum. Plant J 68:495–506

    Article  CAS  PubMed  Google Scholar 

  • Ferguson C, Teeri TT, Siika-aho M, Read SM, Bacic A (1998) Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206:452–460

    Article  CAS  Google Scholar 

  • Geitmann A, Ortega JKE (2009) Mechanics and modeling of plant cell growth. Trends Plant Sci 14:467–478

    Article  CAS  PubMed  Google Scholar 

  • Geitmann A, Li Y-Q, Cresti M (1996) The role of cytoskeleton and dictyosome activity in the pulsatory growth of Nicotiana tabacum and Petunia hybrida pollen tubes. Bot Acta 109:102–109

    Article  CAS  Google Scholar 

  • Hepler PK, Rounds CM, Winship LJ (2013) Control of cell wall extensibility during pollen tube growth. Mol Plant 6:998–1017

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hill AE, Shachar-Hill B, Skepper JN, Powell J, Shachar-Hill Y (2012) An osmotic model of the growing pollen tube. PLoS One 7:e36585

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Idilli AI, Morandini P, Onelli E, Rodighiero S, Caccianiga M, Moscatelli A (2013) Microtubule depolymerization affects endocytosis and exocytosis in the tip and influences endosome movement in tobacco pollen tubes. Mol Plant 6:1109–1130

    Article  CAS  PubMed  Google Scholar 

  • Kroeger J, Geitmann A (2012a) The pollen tube paradigm revisited. Curr Opin Plant Biol 15:618–624

    Article  PubMed  Google Scholar 

  • Kroeger JH, Geitmann A (2012b) Pollen tube growth: getting a grip on cell biology through modeling. Mech Res Comm 42:32–39

    Article  Google Scholar 

  • Kroeger JH, Zerzour R, Geitmann A (2011) Regulator or driving force? The role of turgor pressure in oscillatory plant cell growth. PLoS One 6:e18549. doi:10.1371/journal.pone.0018549

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kroh M, Knuiman B (1982) Ultrastructure of cell wall and plugs of tobacco pollen tubes after chemical extraction of polysaccharides. Planta 154:241–250

    Article  CAS  PubMed  Google Scholar 

  • Laitiainen E, Nieminen KM, Vihinen H, Raudaskoski M (2002) Movement of generative cell and vegetative nucleus in tobacco pollen tubes is dependent on microtubule cytoskeleton but independent of the synthesis of callose plugs. Sex Plant Reprod 15:195–204

    Article  CAS  Google Scholar 

  • Li Y-Q, Chen F, Linskens HF, Cresti M (1994) Distribution of unesterified and esterified pectins in cell walls of pollen tubes of flowering plants. Sex Plant Reprod 7(145–152):145–152

    Google Scholar 

  • Li Y-Q, Faleri C, Geitmann A, Zhang HQ, Cresti M (1995) Immunogold localization of arabinogalactan proteins, unesterified and esterified pectins in pollen grains and pollen tubes of Nicotiana tabacum L. Protoplasma 189:26–36

    Article  CAS  Google Scholar 

  • Li Y-Q, Zhang H-Q, Pierson ES, Huang F-Y, Linskens HF, Hepler PK, Cresti M (1996) Enforced growth-rate fluctuation causes pectin ring formation in the cell wall of Lilium longiflorum pollen tubes. Planta 200:41–49

    Article  CAS  Google Scholar 

  • Loguercio LL (2002) Pollen treatment in high osmotic potential: a simple tool for in vitro preservation and manipulation of viability in gametophytic populations. Braz J Plant Physiol 14:65–70

    Google Scholar 

  • Lopez-Casado G, Matas AJ, Dominguez E, Cuartero J, Heredia A (2007) Biomechanics of isolated tomato (Solanum lycopersicum L.) fruit cuticles: the role of the cutin matrix and polysaccharides. J Exp Bot 58:3875–3883

    Article  CAS  PubMed  Google Scholar 

  • McKenna ST, Kunkel JG, Bosch M, Rounds CM, Vidali L, Winship LJ, Hepler PK (2009) Exocytosis precedes and predicts the increase in growth in oscillating pollen tubes. Plant Cell 21:3026–3040

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meng D, Gu Z, Yuan H, Wang A, Li W, Yang Q, Zhu Y, Li T (2014) The microtubule cytoskeleton and pollen tube Golgi-vesicle system are required for in vitro S-RNase internalization and gametic self incompatibility in apple. Plant Cell Physiol. doi:10.1093/pcp/pcu031

    PubMed  Google Scholar 

  • Messerli MA, Robinson KR (2003) Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models. Planta 217:147–157

    CAS  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005a) More than a leak sealant. The mechanical properties of callose in pollen tubes. Plant Physiol 137:274–286

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005b) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592

    Article  CAS  PubMed  Google Scholar 

  • Peng L, Zhang L, Cheng X, Fan LS, Hao HQ (2013) Disruption of cellulose synthesis by 2,6-dichlorobenzonitrile affects the structure of the cytoskeleton and cell wall construction in Arabidopsis. Plant Biol 15:405–414

    Article  CAS  PubMed  Google Scholar 

  • Persia D, Cai G, Del Casino C, Faleri C, Willemse MTM, Cresti M (2008) Sucrose synthase is associated with the cell wall of tobacco pollen tubes. Plant Physiol 147:1603–1618

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Picton JM, Steer MW (1981) Determination of secretory vesicle production rates by dictyosomes in pollen tubes of Tradescantia using cytochalasin D. J Cell Sci 49:261–272

    CAS  PubMed  Google Scholar 

  • Qin Y, Chen D, Zhao J (2007) Localization of arabinogalactan proteins in anther, pollen, and pollen tube of Nicotiana tabacum L. Protoplasma 231:43–53

    Article  CAS  PubMed  Google Scholar 

  • Rockel N, Wolf S, Kost B, Rausch T, Greiner S (2008) Elaborate spatial patterning of cell-wall PME and PMEI at the pollen tube tip involves PMEI endocytosis, and reflects the distribution of esterified and de-esterified pectins. Plant J 53:133–143

    Article  PubMed  Google Scholar 

  • Schopfer P (2006) Biomechanics of plant growth. Am J Bot 93:1415–1425

    Article  PubMed  Google Scholar 

  • Stepka M, Ciampolini F, Charzynska M, Cresti M (2000) Localization of pectins in the pollen tube wall of Ornithogalum virens L. Does the pattern of pectin distribution depend on the growth rate of the pollen tube? Planta 210:630–635

    Article  CAS  PubMed  Google Scholar 

  • Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Ann Rev Plant Physiol 35:585–657

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Tian GW, Chen MH, Zaltsman A, Citovsky V (2006) Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol 294:83–91

    Article  CAS  PubMed  Google Scholar 

  • Turner A, Bacic A, Harris PJ, Read SM (1998) Membrane fractionation and enrichment of callose synthase from pollen tubes of Nicotiana alata Link et Otto. Planta 205:380–388

    Article  CAS  PubMed  Google Scholar 

  • Wang Q, Kong L, Hao H, Wang X, Lin J, Samaj J, Baluska F (2005) Effects of Brefeldin A on pollen germination and tube growth. Antagonistic effects on endocytosis and secretion. Plant Physiol 139:1692–1703

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang W, Wang L, Chen C, Xiong G, Tan XY, Yang KZ, Wang ZC, Zhou Y, Ye D, Chen LQ (2011) Arabidopsis CSLD1 and CSLD4 are required for cellulose deposition and normal growth of pollen tubes. J Exp Bot 62:5161–5177

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang H, Zhuang X, Cai Y, Cheung AY, Jiang L (2013) Apical F-actin regulated exocytic targeting of NtPPME1 is essential for pollen tube cell wall construction and rigidity. Plant J 76:367–379

    Article  CAS  PubMed  Google Scholar 

  • Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2010) Under pressure, cell walls set the pace. Trends Plant Sci 15:363–369

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wolf S, Greiner S (2012) Growth control by cell wall pectins. Protoplasma 249:169–175

    Article  CAS  Google Scholar 

  • Zerzour R, Kroeger J, Geitmann A (2009) Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties. Dev Biol 334:437–446

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Feng J, Wu J, Wang X (2010) BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth. Planta 231:1323–1334

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We want to sincerely thank Mr. Massimo Guarnieri (Department of Life Sciences, University of Siena) for his help in the analysis of sucrose by HPLC. We also thank the staff of the Botanical Garden of Siena University for cultivating tobacco plants.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Life Sciences, University of Siena, Via Mattioli 4, 53100, Siena, Italy

    Giovanni Biagini, Claudia Faleri, Mauro Cresti & Giampiero Cai

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  1. Giovanni Biagini
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  2. Claudia Faleri
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  3. Mauro Cresti
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  4. Giampiero Cai
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Corresponding author

Correspondence to Giampiero Cai.

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Communicated by Scott D. Russell.

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Biagini, G., Faleri, C., Cresti, M. et al. Sucrose concentration in the growth medium affects the cell wall composition of tobacco pollen tubes. Plant Reprod 27, 129–144 (2014). https://doi.org/10.1007/s00497-014-0246-y

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  • DOI: https://doi.org/10.1007/s00497-014-0246-y

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