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Tube Growth of Solanum Chacoense

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Tube Growth of Solanum Chacoense Planta (2005) 220: 582–592 DOI 10.1007/s00425-004-1368-5 ORIGINAL ARTICLE Elodie Parre Æ Anja Geitmann Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense Received: 23 March 2004 / Accepted: 20 July 2004 / Published online: 21 September 2004 Ó Springer-Verlag 2004 Abstract The cell wall is one of the structural key players ical approach provides new insights concerning the regulating pollen tube growth, since plant cell expansion mechanics of pollen tube growth and the architecture of depends on an interplay between intracellular driving living plant cells. forces and the controlled yielding of the cell wall. Pectin is the main cell wall component at the growing pollen Keywords Cell expansion Æ Cell wall Æ tube apex. We therefore assessed its role in pollen tube Cytomechanics Æ Pectin Æ Pollen tube Æ Tip growth growth and cytomechanics using the enzymes pectinase and pectin methyl esterase (PME). Pectinase activity was Abbreviation PME: Pectin methyl esterase able to stimulate pollen germination and tube growth at moderate concentrations whereas higher concentrations caused apical swelling or bursting in Solanum chacoense Bitt. pollen tubes. This is consistent with a modification of the physical properties of the cell wall affecting its extensibility and thus the growth rate, as well as its Introduction capacity to withstand turgor. To prove that the enzyme- induced effects were due to the altered cell wall Pollen tubes are fast-growing cells exhibiting tip growth. mechanics, we subjected pollen tubes to micro-indenta- In flowering plants, pollen grains germinate on a tion experiments. We observed that cellular stiffness was receptive stigma and send pollen tubes down the style reduced and visco-elasticity increased in the presence of toward the ovary. This allows the delivery of the sperm pectinase. These are the first mechanical data that con- cells to the ovules in order to perform fertilization. The firm the influence of the amount of pectins in the pollen growth process in pollen tubes is confined to the dome- tube cell wall on the physical parameters characterizing shaped apex and occurs in one direction only (Derksen overall cellular architecture. Cytomechanical data were 1996; Hepler et al. 2001). Since the pollen tube grows also obtained to analyze the role of the degree of pectin rapidly and over long distances, the production of the methyl-esterification, which is known to exhibit a gra- cell wall, its composition and the configuration of its dient along the pollen tube axis. This feature has fre- components are important features that regulate the quently been suggested to result in a gradient of the behavior of pollen tube growth, and thus the fertilization physical properties characterizing the cell wall and our process (Taylor 1997). data provide, for the first time, mechanical support for In general, plant cell growth is driven by internal this concept. The gradient in cell wall composition from turgor pressure and restricted by the ability of the cell apical esterified to distal de-esterified pectins seems to be wall to extend under this pressure. To what extent this correlated with an increase in the degree of cell wall equilibrium between turgor and cell wall determines the rigidity and a decrease of visco-elasticity. Our mechan- rate of tip growth in cells exhibiting polar elongation, such as pollen tubes, root hairs or fungal hyphae, has been subject of vivid discussion (Money and Hill 1997, E. Parre Æ A. Geitmann (&) and references therein). The importance of additional Institut de Recherche en Biologie Ve´ge´tale, De´partement factors such as the putative propulsion force of the de Sciences Biologiques, Universite´de Montre´al, 4101, cytoskeletal elements and the regulation of insertion of Rue Sherbrooke Est, Montre´al, Que´bec, H1X 2B2, Canada E-mail: [email protected] new cell wall material is still largely unknown for tip- Tel.: +1-514-8728492 growing cells in general and for pollen tubes in partic- Fax: +1-514-8729406 ular. There seems to be no doubt, however, that the 583 force counteracting the internal driving force is provided outer withstanding forces in this cellular system; (ii) our by the cell wall. Even though the structure of the pollen data revealed that both the amount and the configura- tube cell wall has been described in detail, few ap- tion of pectins are key factors determining the physical proaches have been made to assess its mechanics in a properties of the apical cell wall, thus controlling pollen quantitative manner since Green (1969) stated that tip tube growth. growth is regulated by the tip-to-flank gradient in the rate of wall surface expansion. In the pollen tube cell wall, two or three layers can be distinguished depending on the plant species and the Materials and methods method of investigation (Heslop-Harrison 1987; Steer and Steer 1989). It consists of a primary pecto-cellulosic Pollen tube growth layer and a secondary callosic wall. In the tip of the pollen tube, the cell wall lacks the callosic inner lining Solanum chacoense Bitt. plants were grown in the (Heslop-Harrison 1987), and thus pectins appear to be Montreal Botanical Garden greenhouses. Pollen was major component of the cell wall in this region crucial collected after dehiscence, dehydrated on anhydrous for cell expansion (Roggen and Stanley 1969;Lietal. calcium sulfate overnight and stored at À20°C. On the 1994, 1997, 2002; Derksen et al. 1995; Holdaway-Clarke day of use pollen was re-hydrated in a humid atmo- and Hepler 2003). sphere and cultivated in drops of liquid or solidified Immunocytochemical studies have shown that pectins medium. The latter was obtained by addition of 20 or located at the tip of the growing pollen tube are highly 40 mg mlÀ1 low-melting agarose (Type I-B Low EEO; esterified, while they are de-esterified in areas away from Sigma, St. Louis, MO, USA) or 10 mg mlÀ1Gel-Gro the tip (Li et al. 1994, 1995, 1997, 2002; Jauh and Lord (Gellan gum; gel strength twice as high as that of aga- 1996; Lennon and Lord 2000). This gradient in the de- rose; ICN Biochemicals, Aurora, OH, USA). The À1 gree of esterification is the result of the tip-focused growth medium contained 100 lgml H3BO3, À1 À1 growth process. The wall components are secreted at the 300 lgml Ca(NO3)2ÆH2O, 100 lgml KNO3, À1 À1 extreme apex as esterified pectin residues produced by 200 lgml MgSO4Æ7H2O, 50 lgml sucrose (Brew- the Golgi apparatus (Levy and Staehelin 1992; Haseg- baker and Kwack 1963). Various concentrations of awa et al. 1998). Upon arrival in the cell wall, they be- pectinase (0.2 units/mg solid; USB, Cleveland, OH, come increasingly de-esterified during maturation USA) or PME (238 units/mg solid; Sigma) were added through the activity of the enzyme pectin methyl-ester- at the start of germination (to assess the effect on ger- ase (PME; Kauss and Hassid 1967; Li et al. 1997; mination) or after 30 min of germination (to assess the Geitmann 1999). De-esterification permits Ca2+ ions to effect on elongation). Controls were performed by add- cross-link the acidic pectins to form a semi rigid pectate ing enzyme that had been denatured by boiling for gel (Jarvis 1984; Carpita and Gibeaut 1993), which is 10 min. Germination rate and pollen tube length were presumed to provide mechanical support for the distal assessed in the light microscope after 2 h incubation on areas of the elongating tube by altering the physical microscope slides. properties of the cell wall. Esterified and thus non-gel- ated pectins, which are present predominantly at the apex, are presumed to allow turgor-driven expansion of the tube (Morris et al. 1982; McNeil et al. 1984; Li et al. Fluorescence label 1994, 1997; Geitmann et al. 1995; Derksen 1996; Jauh and Lord 1996; Geitmann and Cresti 1998; Franklin- For immuno-fluorescence labeling, pollen tubes were Tong 1999; Geitmann 1999). However, no experimental fixed after 2 h germination in 30 mg mlÀ1 freshly evidence has been brought forward to show that the prepared formaldehyde in Pipes buffer (1 mM EGTA, physical properties of the cell wall at the apex are indeed 0.5 mM MgCl2, 50 mM Pipes) for 30 min. To allow different from those in the distal part of a growing pollen for quantitative comparison of fluorescence intensity, tube. A gradient of the cytomechanical properties along pollen tubes grown in solidified medium (Gel-Gro) the longitudinal pollen tube axis measured by micro- were resuspended by adding 0.1 M citrate buffer indentation of Papaver pollen tubes is consistent with (55 mM citric acid, 125 mM sodium citrate, pH 6) at this concept (Geitmann and Parre 2004), but whether or 30°C, to assure that the gel did not limit the access of not it is due to the physical properties of the cell wall or antibodies to the cells (liquid medium controls were in particular to those of the pectin component remains treated similarly). Subsequently, cells were incubated to be shown. with monoclonal antibodies JIM5 and JIM7 (gener- Here we provide mechanical data that support two ously provided by Dr. Paul Knox) diluted 1:50 in PBS longstanding hypotheses that hitherto were largely based buffer, followed by an incubation with goat anti-rat on circumstantial evidence: (i) we show that pollen tube IgG–Alexa Fluor 594 (diluted 1:100 in buffer; growth and germination are governed by physical Molecular Probes, Eugene, OR, USA) over night at properties of the apical cell wall, thus supporting the 4°C. JIM5 and JIM7 recognize homogalacturonans importance of an equilibrium between inner driving and with a low and a high degree of esterification, 584 respectively (VandenBosch et al.
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