Electron tomography of cryo-immobilized plant tissue: A novel approach to studying 3d macromolecular architecture of mature plant cell walls in situ

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Sarkar, Purbasha ^b   Bosneaga, Elena ^a,b   Yap, Edgar G ^b   Das, Jyotirmoy ^a   Tsai, Wen Ting ^b   Cabal, Angelo ^a   Neuhaus, Erica ^b   Maji, Dolonchampa ^a   Kumar, Shailabh ^a   Joo, Michael ^b   Yakovlev, Sergey ^b   Csencsits, Roseann ^b   Yu, Zeyun ^c   Bajaj, Chandrajit ^d   Downing, Kenneth H ^b   Auer, Manfred ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^c University of Wisconsin Milwaukee   (United States)

^d University of Texas at Austin   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RESIN; CELLULOSE;

ARABIDOPSIS THALIANA; ARTICLE; CELL WALL; CONTROLLED STUDY; CYTOARCHITECTURE; ELECTRON TOMOGRAPHY; FREEZE DRYING; FROZEN SECTION; HIGH PRESSURE FREEZING; IMAGE ANALYSIS; IMAGE QUALITY; IMMOBILIZATION; LOW TEMPERATURE PROCEDURES; MOLECULAR IMAGING; NONHUMAN; PLANT CELL; PLANT TISSUE; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; RESIN EMBEDDING; ROOM TEMPERATURE; SELF PRESSURIZED RAPID FREEZING; THREE DIMENSIONAL IMAGING; TRANSMISSION ELECTRON MICROSCOPY; ARABIDOPSIS; CRYOPRESERVATION; CYTOLOGY; GENETICS; HISTOLOGY; IMMOBILIZED CELL; METABOLISM; MUTATION; PROCEDURES; TEMPERATURE; ULTRAMICROTOMY; ULTRASTRUCTURE;

ARABIDOPSIS; CELL WALL; CELLS, IMMOBILIZED; CELLULOSE; CRYOPRESERVATION; CRYOULTRAMICROTOMY; ELECTRON MICROSCOPE TOMOGRAPHY; FREEZE SUBSTITUTION; IMAGING, THREE-DIMENSIONAL; MUTATION; TEMPERATURE; TISSUE EMBEDDING;

EID: 84929940071     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0106928     Document Type: Article

References (87)

1. Ragauskas AJ, Nagy M, Kim DH, Eckert CA, Hallett JP, et al. (2006) From wood to fuels: Integrating biofuels and pulp production. Industrial Biotechnol 2: 55-65.
2. McCann MC, Carpita NC (2008) Designing the deconstruction of plant cell walls. Curr Opin Plant Biol 11: 314-320.
3. Pauly M, Keegstra K (2008) Cell-wall carbohydrates and their modification as a resource for biofuels. Plant J 54: 559-568.
4. Sticklen MB (2008) Plant genetic engineering for biofuel production: Towards affordable cellulosic ethanol. Genetics 9: 433-443.
5. Mosier N, Wyman C, Dale B, Elander R, Lee YY, et al. (2005) Features of promising technologies for pretreatment of lignocellulosic biomass. Biores Tech 96: 673-686.
6. Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, et al. (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315: 804-807.
7. Banerjee G, Scott-Craig JS, Walton JD (2010) Improving enzymes for biomass conversion: A basic research perspective. Bioenerg Res 3: 82-92.
8. Elkins JG, Raman B, Keller M (2010) Engineered microbial systems for enhanced conversion of lignocellulosic biomass. Curr Opin Biotech 21: 657- 662.
9. Yuan JS, Tiller KH, Al-Ahmad H, Stewart NR, Stewart CN Jr. (2008) Plants to power: bioenergy to fuel the future. Trends Plant Sci 13: 421-429.
10. Xin Z, Watanabe N, Lam E (2011) Improving efficiency of cellulosic fermentation via genetic engineering to create "smart plants" for biofuel production. In: Buckeridge, MS, Goldman, GH, editors. Routes to cellulosic ethanol. New York: Springer. 181-197.
11. Popper ZA (2008) Evolution and diversity of green plant cell walls. Curr Opin Plant Biol 11: 286-292.
12. Sarkar P, Bosneaga E, Auer M (2009) Plant cell walls throughout evolution: Towards a molecular understanding of their design principles. J Exp Bot 60: 3615-3635.
13. Keegstra K (2010) Plant cell walls. Plant Physiol 154: 483-486.
14. Lee KJ, Marcus SE, Knox JP (2011) Cell wall biology: perspectives from cell wall imaging. Mol Plant 4: 212-219.
15. Leroux O (2012) Collenchyma: A versatile mechanical tissue with dynamic cell walls. Ann Bot 110: 1083-1098.
16. Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant cell walls. New York: Garland Science. 1-42.
17. Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci 3: 204.
18. Ohad I, Danon D (1964) On the dimensions of cellulose microfibrils. J Cell Biol 22: 302-305.
19. Frey-Wyssling A (1968) The ultrastructure of wood. Wood Sci Technol 2: 73- 83.
20. Heyn AN (1969) The elementary fibril and supermolecular structure of cellulose in soft wood fiber. J Ultrast Res 26: 52-68.
21. Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, et al. (2004) Toward a systems approach to understanding plant cell walls. Science 306: 2206-2211.
22. Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6: 850- 861.
23. Ding S-Y, Himmel ME (2006) The maize primary cell wall microfibril: A new model derived from direct visualization. J Agric Food Chem 54: 597-606.
24. Newman RH, Hill SJ, Harris PJ (2013) Wide-Angle x-ray scattering and solidstate nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. Plant Phys 163: 1558-1567.
25. Thomas LH, Forsyth VT, Sturcová A, Kennedy CJ, May RP, et al. (2013) Structure of cellulose microfibrils in primary cell walls from collenchyma. Plant Physiol 161: 465-476.
26. Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22: 53-78.
27. Taylor NG (2008) Cellulose biosynthesis and deposition in higher plants. New Phytol 178: 239-252.
28. Scheller HV, Ulvskov P (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263- 289.
29. McCann MC, Roberts K (1991) Architecture of the primary cell wall. In CW Lloyd, editor. The cytoskeletal basis of plant growth and form. London: Academica Press. 109-129.
30. Rose JKC, Bennett AB (1999) Cooperative disassembly of the cellulosexyloglucan network of plant cell walls: parallels between cell expansion and fruit ripening. Trends Plant Sci 4: 176-183.
31. Park YB, Cosgrove DJ (2012) A revised architecture of primary cell walls based on biomechanical changes induced by substrate-specific endoglucanases. Plant Physiol 158: 1933-1943.
32. Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38: 109-124.
33. Baskin TI, Meekes HTHM, Liang BM, Sharp RE (1999) Regulation of growth anisotropy in well-watered and water-stressed maize roots. II. Role of cortical microtubules and cellulose microfibrils. Plant Physiol 119: 681-692.
34. MacKinnon IM, Sturcova A, Sugimoto-Shirasu K, His I, McCann MC, Jarvis MC (2006) Cell-wall structure and anisotropy in procuste, a cellulose synthase mutant of Arabidopsis thaliana. Planta 224: 438-448.
35. Verbelen JP, Kerstens S (2000) Polarization confocal microscopy and congo red fluorescence: A simple and rapid method to determine the mean cellulose fibril orientation in plants. J Microscopy 198: 101-107.
36. Anderson CT, Carroll A, Akhmetova L, Somerville C (2010) Real-Time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol 152: 787-796.
37. Preston RD, Nicolai E, et al. (1948) An electron microscope study of cellulose in the wall of Valonia ventricosa. Nature 162: 665-667.
38. McCann MC, Wells B, Roberts K (1990) Direct visualization of cross-links in the primary plant cell wall. J Cell Sci 96: 323-334.
39. Fujino T, Itoh T (1994) Architecture of the cell wall of a green alga, Oocystis apiculata Protoplasma 180: 39-48.
40. Fujino T, Sone Y, Mitsuishi Y, Itoh T (2000) Characterization of cross-links between cellulose microfibrils, and their occurrence during elongation growth in pea epicotyl. Plant Cell Physiol 41: 486-494.
41. Roland J C, Vian B, Reis D (1975) Observations with cytochemistry and ultracryotomy on the fine structure of the expanding walls in actively eleongating plant cells. J Cell Sci 19: 239-259.
42. Sugimoto K, Williamson RE, Wasteneys GO (2000) New techniques enable comparative analysis of microtubule orientation, wall texture, and growth rate in intact roots of Arabidopsis. Plant Physiol 124: 1493-1506.
43. Thimm JC, Burritt DJ, Ducker WA, Melton LD (2000) Celery (Apium graveolens L.) parenchyma cell walls examined by atomic force microscopy: effect of dehydration on cellulose microfibrils. Planta 212: 25-32.
44. Davies LM, Harris PJ (2003) Atomic force microscopy of microfibrils in primary cell walls. Planta 217: 283-289.
45. Ding SY, Liu YS, Zeng Y, Himmel ME, Baker JO, et al. (2012) How does plant cell wall nanoscale architecture correlate with enzymatic digestibility? Science 338: 1055-1060.
46. Radotic K, Roduit C, Simonovic J, Hornitschek P, Fankhauser C, et al. (2012) Atomic force microscopy stiffness tomography on living Arabidopsis thaliana cells reveals the mechanical properties of surface and deep cell-wall layers during growth. Biophys J 103: 386-394.
47. Lucic V, Forster F, Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74: 833-865.
48. McIntosh R, Nicastro D, Mastronarde D (2005) New views of cells in 3D: An introduction to electron tomography. Trends Cell Biol 15: 43-51.
49. Xu P, Donaldson LA, Gergely ZR, Staehelin LA (2006) Dual-Axis electron tomography: A new approach for investigating the spatial organization of wood cellulose microfibrils. Wood Sci Technol 41: 101-116.
50. Xu P, Liu H, Donaldson LA, Zhang Y (2011) Mechanical performance and cellulose microfibrils in wood with high S2 microfibril angles. J Mat Sci 46: 534- 540.
51. Chundawat SPS, Donohoe BS, da Costa Sousa L, Elder T, Agarwal UP, et al. (2011) Multi-scale visualization and characterization of lignocellulosic plant cell wall deconstruction during thermochemical pretreatment. Energy Environ Sci 4: 973.
52. Ciesielski PN, Matthews JF, Tucker MP, Beckham GT, Crowley MF, et al. (2013) Electron tomography of pretreated biomass informs atomic modeling of cellulose microfibrils. ACS Nano 7: 8011-8019.
53. McDonald KL, Auer M (2006) High-pressure freezing, cellular tomography, and structural cell biology. Biotechniques 41: 137-143.
54. Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, et al. (2001) COBRA encodes a putative GPI-Anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Develop 15: 1115-1127.
55. Roudier F, Fernandez AG, Fujita M, Himmelspach R, Borner GH, et al. (2005) COBRA, an Arabidopsis extracellular glycosyl-phosphatidyl inositol-Anchored protein, specifically controls highly anisotropic expansion through its involvement in cellulose microfibril orientation. Plant Cell 17: 1749-1763.
56. Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, et al. (2010) Identification of a cellulose synthase-Associated protein required for cellulose biosynthesis. Proc Natl Acad Sci USA 107: 12866-12871.
57. Leunissen JL, Yi H (2009) Self-pressurized rapid freezing (SPRF): A novel cryofixation method for specimen preparation in electron microscopy. J Microscopy 235: 25-35.
58. Yakovlev S, Downing KH (2011) Freezing in sealed capillaries for preparation of frozen hydratedsections. J Microscopy 244: 235-247.
59. Yakovlev S, Luef B, Comolli LR, Downing KH (2010) Self Pressure Freezing of Caulobacter crescentus for the Preparation of Frozen Hydrated Sections. Microscopy Microanal 16: 860-861.
60. Han H-M, Huebinger J, Grabenbauer M (2012) Self-pressurized rapid freezing (SPRF) as a simple fixation method for cryo-electron microscopy of vitreous sections. J Struct Biol 178: 84-87.
61. Pierson J, Fernandez JJ, Bos E, Amini S, Gnaegi H, et al. (2010) Improving the technique of vitreous cryo-sectioning for cryo-electron tomography: electrostatic charging for section attachment and implementation of an anti-contamination glove box. J Struct Biol 169: 219-225.
62. Suloway C, Pulokas J, Fellmann D, Cheng A, Guerra F, et al. (2005) Automated molecular microscopy: The new Leginon system. J Struct Biol 151: 41-60.
63. Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152: 36-51.
64. Otegui MS, Mastronarde DN, Kang BH, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncytial-Type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13: 2033-2051.
65. Segui-Simarro JM, Austin JR, II, White EA, Staehelin LA (2004) Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16: 836-856.
66. Donohoe BS, Kang BH, Staehelin LA (2007) Identification and characterization of COPIa- and COPIb-Type vesicle classes associated with plant and algal Golgi. Proc Natl Acad Sci USA 104: 163-168.
67. Donohoe BS, Mogelsvang S, Staehelin LA (2006) Electron tomography of ER, Golgi and related membrane systems. Methods 39: 154-162.
68. Mastronarde DN (1997) Dual-Axis tomography: An approach with alignment methods that preserve resolution. J Struct Biol 120: 343-352.
69. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
70. Frangakis AS, Hegerl R (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135: 239- 250.
71. Fernandez JJ, Li S (2003) An improved algorithm for anisotropic nonlinear diffusion for denoising cryo-Tomograms. J Struct Biol 144: 152-161.
72. Yu Z, Bajaj C (2008) Computational approaches for automatic structural analysis of large biomolecular complexes. IEEE/ACM Trans Comput Biol Bioinform 5: 568-582.
73. Zhang Q, Bettadapura R, Bajaj C (2012) Macromolecular structure modeling from 3D EM using VolRover 2.0. Biopolymers 97: 709-731.
74. Bajaj CL, Pascucci V, Schikore DR (1997) The contour spectrum. In Proceedings of IEEE Visualization 1997, Phoenix, AZ, 167-173.
75. Németh G, Palágyi K (2011) Topology preserving parallel thinning algorithms. Int J Imag Syst Tech 21: 37-44.
76. Al-Amoudi A, Chang JJ, Leforestier A, McDowall A, Salamin LM, et al. (2004a) Cryo-electron microscopy of vitreous sections. EMBO J 23: 3583-3588.
77. Al-Amoudi A, Norlen LP, Dubochet J (2004b) Cryo-electron microscopy of vitreous sections of native biological cells and tissues. J Struct Biol 148: 131-135.
78. Eltsov M, Dubochet J (2005) Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J Bact 187: 8047-8054.
79. Resch GP, Brandstetter M, Pickl-Herk AM, Konigsmaier L, Wonesch VI, et al. (2011) Immersion freezing of biological specimens: rationale, principles, and instrumentation. Cold Spring Harbor protocols 2011: 778-782.
80. Dick-Perez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, et al. (2011) Structure and interactions of plant cell-wall polysaccharides by two- and threedimensional magic-Angle-spinning solid-state NMR. Biochem 50: 989-1000.
81. Humphrey E (2006) Microwave processing in a modern microscopy facilty. Microscopy Microanal 12: 194.
82. Hayat MA (2000) Principles and techniques of electron microscopy: Biological applications, Ed 4th. Cambridge: Cambridge University Press. pp. 4-84.
83. Krishnamurthy KV (1999) Methods in cell wall cytochemistry. Boca Raton: CRC Press. pp. 29-150.
84. El Mansouri NE, Yuan Q, Huang F (2011) Characterization of alkaline lignins for use in phenol-formaldehyde and epoxy resins. BioResources 6: 2647-2662.
85. McDonald KL, Webb RI (2011) Freeze substitution in 3 hours or less. J Microscopy 243: 227-233.
86. McDonald KL (2014) Out with the old and in with the new: rapid specimen preparation procedures for electron microscopy of sectioned biological material. Protoplasma 251: 429-448.
87. McDonald KL (2013) Rapid Embedding Methods into Epoxy and LR White Resins for Morphological and Immunological Analysis of Cryofixed Biological Specimens. Microsc Microanal 19: 1-12.