Skip to main content
SpringerLink
Log in

Future Directions in Advanced Mycological Microscopy

  • Chapter
  • First Online:
Advanced Microscopy in Mycology

Part of the book series: Fungal Biology ((FUNGBIO))

Abstract

The field of mycology is poised to exploit the many recent advances in microscopic tools and instrumentation for cell biology. This chapter first outlines the latest developments in biosensors that will prove useful for targeting specific events in the context of single fungal cells, mycelia, or fungal-plant systems. Next, we focus on microscopic methods, in particular electron based, capable of generating three-dimensional (3D) data at single-molecule resolution. Combining the capabilities of any of the powerful microscopy platforms discussed in this volume (Chaps. 1–7) leads to correlative microscopy which vastly expands the range of image scale and data complexity. This sophisticated approach combines data collected separately or simultaneously from individual or hybrid microscopes, respectively, offering complementary internal and external spatial, structural, biochemical, and biophysical information on one sample. Finally, we review the recent select advances in imaging technology that we believe hold special promise to glean new insights from the inner working of fungal cells with unprecedented spatial and temporal resolutions.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    Airy disk refers to the diffraction pattern of concentric circles surrounding a bright central spot created from a focused lens (Abbé 1873). The diameter of the first-order central Airy disc, objective lens dependent, is 1 A.U. The LSCM pinhole is typically set to an optimal signal-to-noise and resolution at ~ 1 A.U. Smaller pinholes (i.e., 0.2 A.U.) theoretically provide better resolution at the expense of signal-to-noise in a traditional LSCM setup (Chap. 1).

References

  • Abbé E (1873) Über einen neuen Beleuchtungsapparat am Mikroskop. Arch mikrosk Anat 9:469–480

    Article  Google Scholar 

  • Agronskaia AV, Valentijn JA, van Driel LF, Schneijdenberg CT, Humbel BM, van Bergen en Henegouwen PM, Verkleij AJ, Koster AJ, Gerritsen HC (2008) Integrated fluorescence and transmission electron microscopy. J Struct Biol 164:183–189

    Article  CAS  PubMed  Google Scholar 

  • Akerboom J, Chen T-W, Wardill TJ, Tian L, Marvin JS, Mutlu S, Caldero NC, Esposti F, Borghuis BG, Richard Sun XR, Gordus A, Orger MB, Portugues R, Engert F, Macklin JJ, Filosa A, Aggarwal A, Kerr RA, Takagi R, Kracun S, Shigetomi E, Khakh BS, Baier H, Lagnado L, Wang SS-H, Bargmann CI, Kimmel BE, Jayaraman V, Svoboda K, Kim DS, Schreiter ER, Looger LL (2012) Optimization of a GCaMP calcium indicator for neural activity imaging. J Neurosci 32:13819–13840

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ando T, Uchihashi T, Kodera N (2013) High-speed AFM and applications to biomolecular systems. Annu Rev Biophys 42:393–414

    Article  CAS  PubMed  Google Scholar 

  • Andrews JS, Rolfe SA, Huang WE, Scholes JD, Banwart SA (2010) Biofilm formation in environmental bacteria is influenced by different macromolecules depending on genus and species. Environ Microbiol 12:2496–2507

    Article  CAS  PubMed  Google Scholar 

  • Bacia K, Schwille P (2003) A dynamic view of cellular processes by in vivo fluorescence auto- and cross-correlation spectroscopy. Methods 29:74–85

    Article  CAS  PubMed  Google Scholar 

  • Baddeley D, Cannell MB, Soeller C (2011) Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil. Nano Res 4:589–598

    Article  CAS  Google Scholar 

  • Bechtel HA, Muller EA, Olmon RL, Martin MC, Raschke MB (2014) Ultrabroadband infrared nanospectroscopic imaging. Proc Natl Acad Sci U S A 111:7191–7196

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, Lukyanov S (2006) Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 3:281–286

    Article  CAS  PubMed  Google Scholar 

  • Berweger S, Nguyen DM, Muller EA, Bechtel HA, Perkins TT, Raschke MB (2013) Nano-chemical infrared imaging of membrane proteins in lipid bilayers. J Am Chem Soc 135:18292–18295

    Google Scholar 

  • Bhat B, Vantomme A, Yost D et al (2015a) Oxidative stress and metabolic perturbations in Escherichia coli exposed to sublethal levels of 2,4-dichlorophenoxyacetic acid. Chemosphere 135:453–461

    Google Scholar 

  • Bhat B, McGrath D et al (2015b) Rhizobium leguminosarum bv. viciae 3841 adapts to 2,4-dichlorophenoxyacetic acid with “auxin-like” morphological changes, cell envelope remodeling and upregulation of central metabolic pathways. PLoS ONE 10:e0123813

    Google Scholar 

  • Bourett TM, Czymmek KJ, Howard RJ (1998) An improved method for affinity probe localization in whole cells of filamentous fungi. Fungal Genet Biol 24:3–13

    Google Scholar 

  • Braunsmann C, Seifert J, Rheinlaender J, Schäffer TE (2014) High-speed force mapping on living cells with a small cantilever atomic force microscope. Rev Sci Instrum 85:073703

    Article  PubMed  Google Scholar 

  • Caplan J, Niethammer M, Taylor II RM II, Czymmek KJ (2011) The power of correlative microscopy: multi-modal, multi-scale, multi-dimensional. Curr Opin Struct Biol 21:686–693

    Google Scholar 

  • Chacko JV, Canale C, Harke B, Diaspro A (2013a) Sub-diffraction nano manipulation using STED AFM. PLoS ONE 8:e66608

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chacko JV, Zanacchi FC, Diaspro A (2013b) Probing cytoskeletal structures by coupling optical superresolution and AFM techniques for a correlative approach. Cytoskeleton 70:729–740

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chacko JV, Harke B, Canale C, Diaspro A (2014) Cellular level nanomanipulation using atomic force microscope aided with superresolution imaging. J Biomed Opt 19:105003

    Article  PubMed  Google Scholar 

  • Chakravarty R, Goel S, Cai W (2014) Nanobody: the “Magic Bullet” for molecular imaging? Theranostics 4:386–398

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chang WT, Yang YC, Lu HH, Li IL, Liau I (2010) Spatiotemporal characterization of phagocytic NADPH oxidase and oxidative destruction of intraphagosomal organisms in vivo using autofluorescence imaging and Raman microspectroscopy. J Am Chem Soc 132:1744–1745

    Article  CAS  PubMed  Google Scholar 

  • Czymmek KJ, Bourett TM, Dezwaan TM, Sweigard JA, Howard RJ (2002) Utility of cytoplasmic fluorescent proteins for live-cell imaging of Magnaporthe grisea in planta. Mycologia 94:280–289

    Article  PubMed  Google Scholar 

  • Czymmek KJ, Bourett TM, Howard RJ (2004) Fluorescent protein probes in fungi. In: Savidge T, Charalabos P (Imaging Meds) Methods in microbiology (microbial imaging), vol 34. Academic Press, New York, pp 27–32

    Google Scholar 

  • Czymmek KJ, Bourett TM, Shao Y, Dezwaan TM, Sweigard JA, Howard RJ (2005) Live-cell imaging of tubulin in the filamentous fungus Magnaporthe grisea treated with anti-microtubule and anti-microfilament agents. Protoplasma 225:23–32

    Article  CAS  PubMed  Google Scholar 

  • Denk W, Horstmann H (2004) Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2:e329

    Google Scholar 

  • den Hoedt SV, Effting APJ, Haring MT (2014) The SECOM platform: an integrated CLEM solution. Microsc Microanal 20(Supp 3):1006–1007

    Google Scholar 

  • Efimov AE, Tonevitsky AG, Dittrich M, Matsko NB (2007) Atomic force microscope (AFM) combined with the ultramicrotome: a novel device for the serial section tomography and AFM/TEM complementary structural analysis of biological and polymer samples. J Microsc 226:207–217

    Article  CAS  PubMed  Google Scholar 

  • Faas FG, Bárcena M, Agronskaia AV, Gerritsen HC, Moscicka KB, Diebolder CA, van Driel LF, Limpens RW, Bos E, Ravelli RB, Koning RI, Koster AJ (2013) Localization of fluorescently labeled structures in frozen-hydrated samples using integrated light electron microscopy. J Struct Biol 181:283–290

    Article  CAS  PubMed  Google Scholar 

  • Frommer WB, Davidson MW, Campbell RE (2009) Genetically encoded biosensors based on engineered fluorescent proteins. Chem Soc Rev 38:2833–2841

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gamble RC, West PG (1994) Scanning force microscope with integrated optics and cantilever mount. US Patent # 5291775 A, March 8

    Google Scholar 

  • Handschuh S, Baeumler N, Schwaha T, Ruthensteiner B (2013) A correlative approach for combining microCT, light and transmission electron microscopy in a single 3D scenario. Front Zool 10:44. doi:10.1186/1742-9994-10-44

    Article  PubMed Central  PubMed  Google Scholar 

  • Harke B, Chacko JV, Haschke H, Canale C, Diaspro A (2012) A novel nanoscopic tool by combining AFM with STED microscopy. Opt Nanoscopy 1:3

    Article  Google Scholar 

  • Harris SD, Read ND, Roberson RW, Shaw B, Seiler S, Plamann M, Momany M (2005) Spitzenkörper meets polarisome: microscopy, genetics, and genomics converge. Eukaryot Cell 4:225–229

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hayworth KJ, Morgan JL, Schalek R, Berger DR, Hildebrand DGC, Lichtman JW (2014) Imaging ATUM ultrathin section libraries with WaferMapper: a multi-scale approach to EM reconstruction of neural circuits. Front Neural Circuits 8:1–18

    Article  Google Scholar 

  • Helmstaedter M, Briggman KL, Denk W (2008) 3D structural imaging of the brain with photons and electrons. Curr Opin Neurobiol 18:633–407

    Google Scholar 

  • Hickey PC, Swift SR, Roca MG, Read ND (2004) Live-cell imaging of filamentous fungi using vital fluorescent dyes and confocal microscopy. In: Savidge T, Charalabos P (eds) Methods in microbiology (microbial imaging), vol 34. Academic Press, New York, pp  63–87

    Google Scholar 

  • Hillenbrand R, Knoll B, Keilmann F (2001) Pure optical contrast in scattering-type scanning near-field microscopy. J Microsc 202:77–83

    Article  CAS  PubMed  Google Scholar 

  • Hohmann-Marriott MF, Uchida M, van de Meene AML, Garret M, Hjelm BE, Kokoori S, Roberson RW (2006) Application of electron tomography to fungal ultrastructure studies. New Phytol 172:208–220

    Article  PubMed  Google Scholar 

  • Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY Dostmann WRG (2001) Spatiotemporal dynamics of guanosine 3′,5′-cyclic monophosphate revealed by genetically encoded, fluorescent indicator. Proc Natl Acad Sci U S A 98:2437–2442

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Howard RJ, Aist JR (1979) Hyphal tip cell ultrastructure of the fungus Fusarium:improved preservation by freeze-substitution. J Ultrastruct Res. 66: 224-234

    Article  CAS  PubMed  Google Scholar 

  • Hughes L, Hawes C, Monteith S, Vaughan S (2014) Serial block face scanning electron microscopy—the future of cell ultrastructure imaging. Protoplasma 251:395–401

    Article  PubMed  Google Scholar 

  • Igarashi K, Uchihashi T, Koivula A, Wada M, Kimura S, Penttilä M, Ando T, Samejima M (2012) Visualization of cellobiohydrolase I from Trichoderma reesei moving on crystalline cellulose using high-speed atomic force microscopy. Methods Enzymol 510:169–182

    Article  CAS  PubMed  Google Scholar 

  • Imamura H, Nhat KP, Togawa H, Saito K, Iino R, Kato-Yamada Y, Nagai T, Noji H (2009) Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. Proc Natl Acad Sci U S A 106:15651–15656

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jun AD, Signo K, Yost CM, Dahms TES (2011) Atomic force microscopy of a ctpA mutant in Rhizobium leguminosarum reveals surface property defects linking ctpA function to biofilm formation. Microbiol 157:3049–3058

    Article  Google Scholar 

  • Jungmann R, Avendaño MS, Woehrstein JB, Dai M, Shih WM, Yin P (2014) Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat Methods 11:313–318

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaminskyj SGW, Dahms TES (2008) High spatial resolution surface imaging and analysis of fungal cells using SEM and AFM. Micron 39:349–361

    Article  CAS  PubMed  Google Scholar 

  • Kanemaru T, Hirata K, Takasu S, Isobe S, Mizuki K, Mataka S, Nakamura K (2009) A fluorescence scanning electron microscope Ultramicroscopy 109:344–349

    Article  CAS  PubMed  Google Scholar 

  • Kankanala P, Czymmek K, Valent B (2007) Roles for rice membrane dynamics and plasmodesmata during biotrophic invasion by the blast fungus. Plant Cell 19:706–724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kim H-S, Czymmek KJ, Patel A, Modla S, Nohe A, Duncan R, Gilroy S, Kang S (2012) Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca2+ signatures associated with polarized growth, development, and pathogenesis. Fungal Genet Biol 49:589–601

    Article  CAS  PubMed  Google Scholar 

  • Lal R, Arnsdorf MF (2010) Multidimensional atomic force microscopy for drug discovery: a versatile tool for defining targets, designing therapeutics and monitoring their efficacy. Life Sci 86:545–562

    Article  CAS  PubMed  Google Scholar 

  • Lausch V, Hermann P, Laue M, Bannert N (2014) Silicon nitride grids are compatible with correlative negative staining electron microscopy and tip-enhanced Raman spectroscopy for use in the detection of micro-organisms. J Appl Microbiol 116:1521–1530

    Article  CAS  PubMed  Google Scholar 

  • Le NC, Yokokawa R, Dao DV, Nguyen TD, Wells JC, Sugiyama S (2009) Versatile microfluidic total internal reflection (TIR)-based devices: application to microbeads velocity measurement and single molecule detection with upright and inverted microscope. Lab Chip 9:244–250

    Article  CAS  PubMed  Google Scholar 

  • Li H, Wang H, Huang D, Liang L, Gu Y, Liang C, Xu S, Xu W (2014) Note: Raman microspectroscopy integrated with fluorescence and dark field imaging. Rev Sci Instrum 85:056109

    Article  PubMed  Google Scholar 

  • Löschberger A, Franke C, Krohne G, van de Linde S, Sauer M (2014) Correlative super-resolution fluorescence and electron microscopy of the nuclear pore complex with molecular resolution. J Cell Sci 127:4351–4355

    Article  PubMed  Google Scholar 

  • Luo KQ, Yu VC, Pu Y, Chang DC (2001) Application of the fluorescence resonance energy transfer method for studying the dynamics of caspase-3 activation during UV-induced apoptosis in living HeLa cells. Biochem Biophys Res Commun 283:1054–1060

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Snook L, Kaminskyj S, Dahms TES (2005) Surface ultrastructure and elasticity in growing tips and mature regions of Aspergillus hyphae describe wall maturation. Microbiol 151:3679–3688

    Article  CAS  Google Scholar 

  • Ma H, Snook L, Tian C, Kaminskyj S, Dahms TES (2006) Fungal surface remodeling visualized by atomic force microscopy. Mycol Res 110:879–886

    Article  PubMed  Google Scholar 

  • Martell JD, Deerinck TJ, Sancak Y, Poulos TL, Mootha VK, Sosinsky GE, Ellisman MH, Ting AY (2012) Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat Biotechnol 30:1143–1148

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Micheva KD, Smith SJ (2007) Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55:25–36

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192–195

    Article  PubMed  Google Scholar 

  • Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882–887

    Article  CAS  PubMed  Google Scholar 

  • Modla S, Caplan JL, Czymmek KJ, Lee JY (2015) Localization of fluorescently tagged protein to plasmodesmata by correlative light and electron microscopy. Methods Mol Biol 1217:121–133

    Article  CAS  PubMed  Google Scholar 

  • Monserrate A, Casado S, Flors C (2014) Correlative atomic force microscopy and localization-based super-resolution microscopy: revealing labelling and image reconstruction artefacts. Chem Phys Chem 15:647–650

    CAS  PubMed  Google Scholar 

  • Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A (2004) Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci, U S A 101:10554–10559

    Google Scholar 

  • Nagao E, Dvorak JA (1998) An integrated approach to the study of living cells by atomic force microscopy. J Microsc 191:8–19

    Google Scholar 

  • Narayan K, Danielson CM, Lagarec K, Lowekamp BC, Coffman P, Laquerre A, Phaneuf MW, Hope TJ, Subramaniam S (2014) Multi-resolution correlative focused ion beam scanning electron microscopy: applications to cell biology. J Struct Biol 185:278–284

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nelson: http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2958.2004.04066.x/abstract: Nelson G, Kozlova-Zwinderman O, Collis AJ, Knight MR, Fincham JRS, Stanger CP, Renwick A, Hessing JGM, Punt PJ, Van Den Hondel CAMJJ, Read, ND (2004) Calcium measurement in living filamentous fungi expressing codon-optimized aequorin. Mol Microbiol 52:1437–1450

  • Newman RH, Fosbrink MD, Zhang J (2011) Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Chem Rev 111:3614–3666

    Google Scholar 

  • Oestreicher Z, Taoka A, Fukumori Y (2015) A comparison of the surface nanostructure from two different types of gram-negative cells: Escherichia coli and Rhodobacter sphaeroides. Micron 72C:8–14

    Article  Google Scholar 

  • Okumoto S, Jones A, Frommer WB (2012) Quantitative imaging with fluorescent biosensors. Annu Rev Plant Biol 63:663–706

    Article  CAS  PubMed  Google Scholar 

  • Paslay LC, Falgout L, Savin DA, Heinhorst S, Cannon GC, Morgan SE (2013) Kinetics and control of self-assembly of ABH1 hydrophobin from the edible white button mushroom. Biomacromolecules 14:2283–2293

    Article  CAS  PubMed  Google Scholar 

  • Paul BC, El-Ganiny AM, Abbas M, Kaminskyj SGW, Dahms TES (2011) Quantifying the importance of galacto-furanose in Aspergillus nidulans hyphal wall surface organization by atomic force microscopy. Eukaryot Cell 10:646–653

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paul BC, Snook L, Ma H, Dahms TES (2013) High-resolution imaging and force spectroscopy of fungal hyphal cells by atomic force microscopy. In: Gupta VK, Tuohy MG, Ayyachamy M, Turner KM, O’Donovan A (eds) Laboratory protocols in fungal biology. Springer, USA

    Google Scholar 

  • Perkel JM (2014) Correlating Light and Electron Microscopy. BioTechniques 57:172–177

    Google Scholar 

  • Pertz O, Hodgson L, Klemke RL, Hahn KM (2006) Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440:1069–1072

    Article  CAS  PubMed  Google Scholar 

  • Planchon TA, Gao L, Milkie DE, Davidson MW, Galbraith JA, Galbrait CG, Betzig E (2011) Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination. Nat Methods 8:417–423

    Google Scholar 

  • Reuben S, Banas K, Banas A, Swarup S (2014) Combination of synchrotron radiation-based Fourier transforms infrared microspectroscopy and confocal laser scanning microscopy to understand spatial heterogeneity in aquatic multispecies biofilms. Water Res 64:123–133

    Google Scholar 

  • Reynaud EG, Peychl J, Huisken J, Tomancak P (2015) Guide to light-sheet microscopy for adventurous biologists. Nat Methods 12:30–34

    Google Scholar 

  • Ries J, Kaplan C, Platonova E, Eghlidi H, Ewers H (2012) A simple, versatile method for GFP-based super-resolution microscopy via nanobodies. Nat Methods 9:582–4

    Google Scholar 

  • Riquelme M, Roberson RW, McDaniel DP Bartnicki-Garcıa S (2002) The effects of ropy-1 mutation on cytoplasmic organization and intracellular motility in mature hyphae of Neurospora crassa. Fungal Genet Biol 37:171–179

    Article  CAS  PubMed  Google Scholar 

  • Sandercock JR (1987) A dynamic antivibration system. Proc SPIE 0732, 1st Intl Conf on Vibration Control in Optics and Metrology, 157. doi:10.1117/12.937916

    Google Scholar 

  • Sato M, Hida N, Ozawa T, Umezawa Y (2000) Fluorescent indicators for cyclic GMP based on cyclic GMP-dependent protein kinase Ialpha and green fluorescent proteins. Anal Chem 72:5918–5924

    Article  CAS  PubMed  Google Scholar 

  • Schleifenbaum A, Stier G, Gasch A, Sattler M, Schultz C (2004) Genetically encoded FRET probe for PKC activity based on pleckstrin. J Am Chem Soc 126:11786–11787

    Article  CAS  PubMed  Google Scholar 

  • Schulz O, Zhao Z, Ward A, Koenig M, Koberling F, Liu Y, Enderlein J, Yan H, Ros R (2013) Tip induced fluorescence quenching for nanometer optical and topographical resolution. Opt Nanoscopy 2:1

    Article  Google Scholar 

  • Shibafuji Y, Nakamura A, Uchihashi T, Sugimoto N, Fukuda S, Watanabe H, Samejima M, Ando T, Noji H, Koivula A, Igarashi K, Iino R (2014) Single-molecule imaging analysis of elementary reaction steps of Trichoderma reesei cellobiohydrolase I (Cel7A) hydrolyzing crystalline cellulose Iα and IIII. J Biol Chem 289:14056–14065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shibata M, Uchihashi T, Ando T, Yasuda R (2015) Long-tip high-speed atomic force microscopy for nanometer-scale imaging in live cells. Sci Rep 5:8724

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shu X, Lev-Ram V, Deerinck TK, Qi Y, Ramko EB, Davidson MW, Jin Y, Ellisman MH, Tserevelakis GJ, Soliman D, Omar M, Ntziachristos V (2014) Hybrid multiphoton and optoacoustic microscope. Opt Lett 39:1819–1822

    Article  Google Scholar 

  • Smith C (2012) Two microscopes are better than one. Nature 492:293–297

    Article  CAS  PubMed  Google Scholar 

  • Stemmer A (1995) A hybrid scanning force and light microscope for surface imaging and three-dimensional optical sectioning in differential interference contrast. J Microsc 178:28–36

    Article  CAS  PubMed  Google Scholar 

  • Subach FV, Subach OM, Gundorov IS, Morozova KS, Piatkevich KD, Cuervo AM, Verkhusha VV (2009) Monomeric fluorescent timers that change color from blue to red report on cellular trafficking. Nat Chem Biol 5:118–126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Terskikh A, Fradkov A, Ermakova G, Zaraisky A, Tan P, Kajava AV, Zhao X, Lukyanov S, Matz M, Kim S, Weissman I, Siebert P (2000) “Fluorescent Timer”: protein that changes color with time. Science 290:1585–1588

    Article  CAS  PubMed  Google Scholar 

  • Tsien RY (2011) A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol 9:e1001041

    Article  PubMed Central  PubMed  Google Scholar 

  • Tsutsui H, Karasawa S, Okamura Y, Miyawaki A (2008) Improving membrane voltage measurements using FRET with new fluorescent proteins. Nat Methods 7:683–685

    Article  Google Scholar 

  • van Manen HJ, Otto C (2007) Hybrid confocal Raman fluorescence microscopy on single cells using semiconductor quantum dots. Nano Lett 7:1631–1636

    Google Scholar 

  • Varnai P, Balla T (2007) Visualization and manipulation of phosphoinsitide dynamics in live cells using engineered protein dynamics. Eur J Physiol 455:69–82

    Article  CAS  Google Scholar 

  • Wei D, Jacobs S, Modla S, Zhang S, Young CL, Cirino R, Caplan J, Czymmek K (2012) High-resolution three-dimensional reconstruction of a whole yeast cell using focused-ion beam scanning electron microscopy. Biotechniques 53(1):41–48

    CAS  PubMed  Google Scholar 

  • Weisshart K (2014) The basic principle of airyscanning, pp 1–11. ZEISS

    Google Scholar 

  • Williams PA, Papadakis SJ, Flavo MR, Patel AM, Sinclair M, Seeger A, Hesler A, Taylor RM, Washburn S, Superfine R (2002) Controlled placement of an individual carbon nanotube onto a microelectromechanical structure. Appl Phys Lett 80:2574–2576

    Article  CAS  Google Scholar 

  • Wu J, Zheng G, Lee LM (2012) Optical imaging techniques in microfluidics and their applications. Lab Chip 12:3566–3575

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Gerard ALV, Huang BCB, Anderson DC, Payan DG, Luo Y (1998) Detection of programmed cell death using fluorescence energy transfer. Nucleic Acids Res 26:2034–2035

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Young CL, Raden DL, Caplan J, Czymmek K, Robinson AS (2012) Optimized cassettes for live-cell imaging of proteins and high-resolution in yeast. Yeast 29:119–136

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zaccolo M, De Giorgi F, Cho CY, Feng L, Knapp T, Negulescu PA, Taylor SS, Tsien RY Pozzan T (2000) A genetically encoded, fluorescent indicator for cyclic AMP in living cells. Nat Cell Biol 2:25–29

    Article  CAS  PubMed  Google Scholar 

  • Zanacchi FC, Lavagnino Z, Donnorso MP, Bue AD, Furia L, Faretta M, Diaspro A (2011) Live-cell 3D super-resolution imaging in thick biological samples. Nat Methods 8:1047–1049

    Article  CAS  Google Scholar 

  • Zhang C, Czymmek KJ, Shapiro AD (2003) Nitric oxide does not trigger early programmed cell death events but may contribute to cell-to-cell signaling governing progression of the Arabidopsis hypersensitive response. Mol Plant Microbe Interact 16:962–972

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Tian Y, Cai M, Wang F, Wu J, Gao J, Liu S, Jiang J, Jiang S, Wang H (2014) Studying the nucleated mammalian cell membrane by single molecule approaches. PLoS ONE 9:e91595

    Article  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

TESD thanks Spencer Zwarych for collecting the LM and AFM data, and Geremy Lague for photographing Supriya Bhat and the AFM setup shown in Fig. 8.3. Special thanks to Drs. Kathleen Gough, Catherine Liao, Hans Bechtel and Michael Martin and Susan Kaminskyj for the collaborative data collection, analysis and sample preparation for SINS at ALS (Berkeley), and to Dr. Gough for kindly preparing Fig. 8.4.

A very special thanks to Dr. Seogchan Kang and Dr. Hye-Seon Kim for permission to use the 3D super-resolution data, and Dr. Jeff Caplan and Dr. Carissa Young for their efforts and permission to use Airyscan and 3D FESEM/FIB images of yeast.

Author information

Authors and Affiliations

  1. North American Applications and Labs, Carl Zeiss Microscopy, LLC, One Zeiss Drive, 10594, Thornwood, NY, USA

    Dr. Kirk J. Czymmek PhD

  2. Department of Chemistry and Biochemistry, University of Regina, S4P 1N7, Regina, SK, Canada

    Dr. Prof. Tanya E. S. Dahms PhD

Authors
  1. Dr. Kirk J. Czymmek PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dr. Prof. Tanya E. S. Dahms PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Kirk J. Czymmek PhD or Tanya E. S. Dahms PhD .

Editor information

Editors and Affiliations

  1. University of Regina, Regina, Canada

    Tanya E. S. Dahms

  2. North American Applications and Labs, Carl Zeiss Microscopy, LLC, Thornwood, New York, USA

    Kirk J. Czymmek

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Czymmek, K., Dahms, T. (2015). Future Directions in Advanced Mycological Microscopy. In: Dahms, T., Czymmek, K. (eds) Advanced Microscopy in Mycology. Fungal Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-22437-4_8

Download citation

Publish with us

Policies and ethics

Search

Navigation