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2012 Second Harmonic Generation Imaging of the Deep Shade Plant Journal of Microscopy, Vol. 248, Pt 3 2012, pp. 234–244 doi: 10.1111/j.1365-2818.2012.03668.x Received 4 April 2012; accepted 28 August 2012 Second harmonic generation imaging of the deep shade plant Selaginella erythropus using multifunctional two-photon laser scanning microscopy A.H. RESHAK∗,† & C.-R. SHEUE‡ ∗School of Complex Systems, FFPW, CENAKVA, University of South Bohemia in CB, Nove Hrady 37333, Czech Republic †School of Material Engineering, Malaysia University of Perlis, P.O Box 77, d/a Pejabat Pos Besar, 01007 Kangar, Perlis, Malaysia ‡Department of Life Sciences, National Chung Hsing University, 250, Kuo Kuang Rd, Taichung 402, Taiwan Key words. Chloroplast, multifunctional two-photon laser scanning microscopy (MF-2PLSM), second harmonic generation (SHG), Selaginella erythropus, two-photon excitation fluorescence (TPEF). Summary SHG is known to leave no energy deposition on the interacting matter because of the SHG virtual energy conservation Background: Multifunctional two-photon laser scanning characteristic. microscopy provides attractive advantages over conventional two-photon laser scanning microscopy. For the first time, simultaneous measurement of the second harmonic Introduction generation (SHG) signals in the forward and backward directions and two photon excitation fluorescence were Nonlinear optical effects, such as two-photon (Denk et al., achieved from the deep shade plant Selaginella erythropus. 1990) and three-photon (Wokosin et al., 1996; Maiti et al., Results: These measurements show that the S. erythropus 1997; Schrader et al., 1997; Tuer et al., 2008) fluorescence, leaves produce high SHG signals in both directions and significantly improve depth resolution and reduce the the SHG signals strongly depend on the laser’s status of background noise. Nonlinear optical techniques have been polarization and the orientation of the dipole moment in used to develop a new generation of optical microscopes with the molecules that interact with the laser light. The novelty novel capabilities. These new capabilities include the ability of this work is (1) uncovering the unusual structure of to use near-infrared light to induce absorption and enhance S. erythropus leaves, including diverse chloroplasts, various fluorescence from fluorophores that absorb in the ultraviolet cell types and micromophology, which are consistent with region. Other capabilities of nonlinear microscopes include observations from general electron microscopy; and (2) using improving spatial and temporal resolution without the use of the multifunctional two-photon laser scanning microscopy pinholes or slits for spatial filtering, improving signal strength by combining three platforms of laser scanning microscopy, for deeper penetration into thick and highly scattering tissue fluorescence microscopy, harmonic generation microscopy and confining photobleaching to the focal volume (Denk and polarizing microscopy for detecting the SHG signals in et al., 1990). The invention of nonlinear laser microscopy the forward and backward directions, as well as two photon has opened new opportunities for noninvasive examination of excitation fluorescence. the structure and functioning of living cells and tissues (Denk Conclusions: With the multifunctional two-photon laser et al., 1990). scanning microscopy, one can use noninvasive SHG imaging Among different multiphoton implementations (Zumbusch to reveal the true architecture of the sample, without et al., 1999; Zipfel et al., 2003), second harmonic generation photodamage or photobleaching, by utilizing the fact that the (SHG) imaging (Roth & Freund, 1980; Freund et al., 1986; Campagnola et al., 2001; Yeh et al., 2002; Campagnola Correspondence to: A. H. Reshak, Tel: +420 777729583; fax: +420–386 361255; & Lowe, 2003; Cox et al., 2003) is particularly suitable e-mail:[email protected];andC.R.Sheue,Tel/fax:+886422857395;e-mail: for investigating noncentrosymmetric structures. SHG is a [email protected] nonlinear optical process that occurs only at the focal point of C 2012 The Authors Journal of Microscopy C 2012 Royal Microscopical Society SECOND HARMONIC GENERATION IMAGING 235 a laser beam (Shen, 1989). The application of SHG imaging is investigated by means of the multifunctional-two-photon of cellular structure and functioning is quite new and notable laser scanning microscopy (MF-2PLSM), which the first (Campagnola & Loew, 2003). Advances in mode-locked lasers author established by combining three platforms of laser [instead of a continuous wave, mode-locked lasers, which emit scanning microscopy: fluorescence microscopy, harmonic short pulses in the range of nanoseconds to femtoseconds (fs)] generation microscopy and polarizing microscopy. MF- makes SHG imaging of cells possible, because lower intensities 2PLSM provides attractive advantages over conventional can be used (Reshak et al., 2009). Using chiral chromophores, fluorescence microscopy for revealing the true architecture chiral SHG imaging can be applied to otherwise impossible of the samples that can not produce autofluorescence without symmetric structures (Yan et al., 2006). labelling or staining, which might induce undesirable effects Second harmonic imaging microscopy (SHIM) is based on a in the living cell. Reconstruction of complementary images by nonlinear optical effect known as SHG (Barzda et al., 2004; eliminatingtheangledependenceofimages,whenusinglinear Barzda et al., 2005; Greenhalgh et al., 2006). SHIM has polarized laser, helps maximize the SHG signals and hence been established as a viable microscope imaging contrast improves the brightness and the sharpness of the features in mechanism for visualization of cell and tissue structure and SHG images of samples. This technique will provide biologists function. SHIM using SHG as a probe is shown to produce and medical researchers another useful visualization tool for high-resolution images of transparent biological specimens exploring the nature of living cells. (Campagnola & Loew, 2003). A second harmonic microscope The study organism, S. erythropus, is an unusual plant obtains contrasts from variations in a specimen’s ability growing in the low light understory of tropical rain forests. A to generate second harmonic light from the incident light giant chloroplast, termed a bizonoplast, was first discovered in whereasaconventionalopticalmicroscopeobtainsitscontrast this plant (Sheue et al., 2007). The bizonoplast is characterized by detecting variations in optical density, path length or by unique dimorphic ultrastructure differentiating the refractive index of the specimen. SHG requires intense laser chloroplast into upper and lower zones. However, the light to pass through a material with a noncentrosymmetric leaves (viz. microphyll) of S. erythropus also contain typical molecular structure (Reshak et al., 2009). Second harmonic chloroplasts. Novel patterns of silica bodies on leaf surface light emerging from SHG material is exactly half the of this plant have also been observed (Sheue et al., 2006). wavelength (frequency doubled) of the light entering the Baseline studies of the leaf structure of this plant from general material (Reshak et al., 2009). The alternative technique, electron microscopy contrast with MF-2PLSM, revealing the two-photon-excited fluorescence (TPEF) is also a two-photon advantages of these new nonlinear techniques to better process. TPEF involves some energy loss during relaxation understand this deep shade plant noninvasively. from the excited state, whereas SHG is energy conserving. Advances in the developments of SHIM have provided Material and methods researchers with novel means by which noninvasive visualization of nonbiological and biological specimens can be Laser sources and imaging system achieved with high penetration and high spatial resolution, and is known to leave no energy deposition on the interacting The schematic of the MF-2PLSM is shown in Figure 1. This matter because of SHIM’s virtual energy conservation MF-2PLSM consists of an inverted i-mic 2 microscope (Till- characteristic (Gao et al., 2006). That is, the emitted SHG Photonics, Grafelfing, Germany), equipped with Ti:sapphire photon energy is the same as the total absorbed excitation femtosecond laser with a tuning range of 690–820 nm. The photonenergy.Theinhomogeneityinherenttomostbiological laser is a Tsunami 3941-M3B pumped by a Millennia-V, specimen, and in particular, to the internal structure of 5W solid-state pump laser (Spectra-Physics, Mountain View, various cells, leads to high quality SHG images without CA, USA). The Tsunami laser was used to generate linearly any preconditioning such as labelling or staining that might polarized pulses at 810 nm, 20 mW and 100 fs pulse width induce undesirable effects in the living cell (Reshak, 2009). at frequency of 80 MHz, for fluorescence excitation and SHG. Historically, resolution in fluorescence optical microscopy has Thus, in general to maximize the signal (fluorescence emission been limited by the Rayleigh criterion. The Rayleigh criterion and SHG), short pulses should be used and average laser states that two images are just resolved when the principal power should be kept low to prevent heating of the sample maximum (of the Fraunhofer diffraction pattern) of one image as well as unwanted one-photon absorption and to reduce coincides with the first minimum of the other (Born & Wolf, the risk of highly nonlinear photodamage (Denk et al., 1995). 1980). Techniques with better resolution than the Rayleigh A beam
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