Application of Texture Measures to Study Effect of B Chromosomes on the 3D Architecture of Plant Chromatin — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
Application of Texture Measures to Study Effect of B Chromosomes on the 3D Architecture of Plant Chromatin
Department of Plant Anatomy and Cytology, Faculty of Biology and Protection of Environment, University of Silesia, Jagiellonska, Poland
,
Department of Plant Anatomy and Cytology, Faculty of Biology and Protection of Environment, University of Silesia, Jagiellonska, Poland
,
Royal College of Surgeons in Ireland, St Stephens Green, Ireland; 3Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa, Poland
1 Department of Plant Anatomy and Cytology, Faculty of Biology and Protection of Environment, University of Silesia, Jagiellonska, Poland
2 Department of Plant Anatomy and Cytology, Faculty of Biology and Protection of Environment, University of Silesia, Jagiellonska, Poland
3 Royal College of Surgeons in Ireland, St Stephens Green, Ireland; 3Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa, Poland
Background: Supernumerary chromosomes (B) comprise optional complement to basic (A) chromosome set. The presence of B-chromosomes may significantly reduce plant vigor and fertility. Potentially active genes constitute only small fraction of DNA of these chromosomes indicating that these effects are mediated by epigenetic mechanisms. One example is down-regulation of rDNA genes and condensation of their respective chromatin regions (demonstrated in squashed preparations using 2D microscopy). It may be postulated that the presence of B chromosomes leads to more extensive changes of local chromatin structure. Verification of hypothesis requires studying 3D spatial architecture of intact nuclei in tissue. Results: An image processing algorithm was developed and applied for isolation (from the confocal datasets) of regions corresponding to single nuclei. The nuclei were segmented using iterative global thresholding followed by growing and merging of regions belonging to different nuclei. The result of segmentation was verified by a human observer. Chromatin architecture was characterized quantitatively using global fluorescence intensity distribution measures (mean, variance) and local intensity distribution parameters (haraclick features, wavelet energy, run- length features). The sets of parameters corresponding to populations of nuclei with different number of B-chromo- somes were subjected to discriminate analysis. The distinct parameters were then correlated with depth in tissue at which a given nucleus was positioned. Conclusions: Combination of light microscopy with dedicated image processing and analysis framework made it possible to study chromatin architecture in nuclei containing various number of B chromosomes. These data indicate that alterations of 3D chromatin distribution occur globally in the interphase nuclei in the presence of Bs. The changes occur at the spatial scale comparable with the resolution limit of light microscopy and at larger distances.
A. Muntzing, “Accesory Chromosomes,” Accessory Chromosomes, Vol. 8, 1974, pp. 243-266. doi:10.1146/annurev.ge.08.120174.001331
J. P. M. Camacho, T. F. Sharbel and L. Beukeboom, “B-Chromosome Evolution,” Philosophical Transactions B, Vol. 355, No. 1394, 2000, pp. 163-178. doi:10.1098/rstb.2000.0556
R. N. Jones, “Tansley Review No. 85; B Chromosomes in Plants,” New Phytologist, Vol. 131, No. 4, 1995, pp. 411-434. doi:10.1111/j.1469-8137.1995.tb03079.x
E. L. Maistro, C. Oliveira and F. Foresti, “Cytogenetic Analysis of A- and B-Chromosomes of Prochilodus lineatus (Teleostei, Prochilodontidae) Using Different Restriction Enzyme Banding and Staining Methods,” Genetica, Vol. 108, No. 2, 2000, pp. 119-125. doi:10.1023/A:1004063031965
V. A. Trifonov, P. L. Perelman, S.-I. Kawada, M. A. Iwasa, S. I. Oda and A. S. Graphodatsky, “Complex structure of B-Chromosomes in Two Mammalian Species, Apodemus peninsulae (Rodentia) and Nyctereutes procyonoides (Carnivora),” Chromosome Research, Vol. 10, No. 2, 2002, pp. 109-116. doi:10.1023/A:1014940800901
A. G. Burgov, T. V. Karamyshera, E. A. Perepelov, E. A. Elisaphenko, D. N. Rubtsov, E. Warcha?owska-?liwa, H. Tatsuta and N. B. Rubsov, “DNA Content of the B Chromosomes in Grasshop per Podisma kanoi Storozh. (Orthoptera, Acrididae),” Chromosome Research, Vol. 15, No. 3, 2007, pp. 315-325.
M. Delgado, L. Moraiscecilio, N. Neves, R. N. Jones and W. Viegas, “The Influence of B Chromosomes on rDNA Organization in Rye Interphase Nuclei,” Chromosome Research, Vol. 3, No. 8, 1995, pp. 487-491. doi:10.1007/BF00713963
M. Delgado, A. Caperta, T. Ribeiro, W. Viegas, R. N. Jones and L. Morais-Cecilio, “Different Numbers of Rye B Chromosomes Induce Identical Compaction Changes in Distinct A Chromosome Domains,” Cytogenetic and Genome Research, Vol. 106, No. 2-4, 2004, pp. 320-324. doi:10.1159/000079306
L. Morais-Cecilio, M. Delgado, R. N. Jones and W. Viegas, “Modification of Wheat rDNA Loci by the Rye B Chromosomes, a Chromatin Organization Model,” Chromosome Research, Vol. 8, No. 2-4, 2000, pp. 341-351. doi:10.1023/A:1009291714371
J. Maluszynska and D. Schweizer, “Ribosomal RNA Genes in B Chromosomes of Crepis capillaries Detected by Non-Radioactive in Situ Hybridization,” Heredity, Vol. 62, 1989, pp. 59-65. doi:10.1038/hdy.1989.8
M. Gonzalez-Sanchez, M. Chiavarino, G. Jimenez, S. Manzanera, M. Rosato and M. J. Puertas, “The Parasitic Effects of Rye B Chromosomes Might Be Beneficial in the Long Term,” Cytogenetic and Genome Research, Vol. 106, No. 2-4, 2004, pp. 386-393. doi:10.1159/000079316
R. N. Jones, “B-Chromosome Systems in Flowering Plants and Animal Species,” International Review of Cytology, Vol. 40, 1975, pp. 1-100. doi:10.1016/S0074-7696(08)60951-1
C. R. Leach, A. Houben and J. N. Tinnis, “The B Chromosomes in Brachycome,” Cytogenetic and Genome Research, Vol. 106, No. 2-4, 2004, pp. 199-209. doi:10.1159/000079288
R. T. Grant-Downton and G. Dickinson, “Epigenetics and Its Implications for Plant Biology. 1. The Epigenetic Network in Plants,” Annals of Botany, Vol. 96, No. 7, 2005, pp. 1143-1164. doi:10.1093/aob/mci273
P. Fransz, W. Soppe and I. Shubert, “Heterochromatin in Interphase Nuclei of Arabidopsis thaliana,” Chromosome Research, Vol. 11, No. 3, 2004, pp. 227-240. doi:10.1023/A:1022835825899
P. Fransz, R. van Hoopen and F. Tessadori, “Composition and Formation of Heterochromatin in Arabidopsis thaliana,” Chromosome Research, Vol. 14, No. 1, 2006, pp. 71-82. doi:10.1007/s10577-005-1022-5
N. Dillon, “Heterochromatin structure and function,” Biology of the Cell, Vol. 96, No. 8, 2004, pp. 631-637. doi:10.1016/j.biolcel.2004.06.003
J. A. Fahrner and S. B. Baylin, “Heterochromatin: Stable and Unstable Invasions Home and Abroad,” Genes & Development, Vol. 17, No. 15, 2003, pp. 1805-1812. doi:10.1101/gad.1123303
M. J. Puertas, “Nature and Evolution of B Chromosomes in Plants: A Non-Coding but Information Rich Part of Plant Genomes,” Cytogenetic and Genome Research, Vol. 296, No. 1-4, 2002, pp. 198-205. doi:10.1159/000063047
M. V. Boland, M. K. Markey and R. F. Murphy, “Automated Recognition of Patterns Characteristic of Subcellular Structures in Fluorescence Microscopy Images,” Cytometry, Vol. 33, No. 3, 1998, pp. 366-375. doi:10.1002/(SICI)1097-0320(19981101)33:3 3.0.CO;2-R
K. Huang, J. Lin, J. A. Gajnak and R. F. Murphy, “Image Content-Based Retrieval and Automated Interpretation of Fluorescence Microscope Images via the Protein Subcellular Location Image Database,” Proceedings of 2002 IEEE International Symposiums on Biomedical Imaging (ISBI 2002), 2002, pp. 325-328. doi:10.1109/ISBI.2002.1029259
A. Huisman, L. S. Ploeger, H. F. J. Dullens, N. Poulin, W. E. Grizzle and P. J. van Diest, “Development of 3D Chromatin Texture Analysis Using Confocal Laser Scanning Microscopy,” Cellular Oncology, Vol. 27, No. 5-6, 2005, pp. 335-345.
K. C. Strasters, A. W. M. Smenlders, M. Buijs, A. B. Houtsmuller, H. T. M. van der Voort and N. N. Nanninga, “A 3-D Model for Chromatin Organization of G1 and G2 Populations from Quantitative Confocal Image Analysis,” Cytometry, Vol. 27, No. 3, 1997, pp. 201-212. doi:10.1002/(SICI)1097-0320(19970301)27:3 3.0.CO;2-H
G. Van de Wouwer, B. Weyn, P. Scheunders, W. Jacob, E. van Marck and D. van Dyck, “Wavelets as Chromatin Texture Description for Automated Identification of Neoplastic Nuclei,” Journal of Microscopy, Vol. 197, No. 1, 2000, pp. 25-35. doi:10.1046/j.1365-2818.2000.00594.x
S. Yatouji, F. Liautaud-Roger and J. Dufer, “Nuclear Chromatin Texture and Sensitivity to DNase I in Human Leukaemic CEM Cells Incubated with Nanomolar Okadaic Acid,” Cell Proliferation, Vol. 33, No. 1, 2000, pp. 51-62. doi:10.1046/j.1365-2184.2000.00163.x
S. Abraham, I. H. Ames and H. H. Smith, “Autoradiagraphic Studies of DNA Synthesis in the B Chromosomes of Crepis capillaries,” Journal of Heredity, Vol. 59, No. 5, 1968, pp. 297-299.
J. Juchimiuk and J. Maluszynska, “Transformed Roots of Crepis capillaries—A Sensitive System for the Evaluation of the Clastogenicity of Abiotic Agents,” Mutation Research, Vol. 565, No. 2, 2005, pp. 129-138. doi:10.1016/j.mrgentox.2004.10.016
P. F. Ambros, M. A. Matzke and A. J. M. Matzke, “Detection of a 17 kb Unique Sequence (T-DNA) in Plant Chromosome by in Situ Hybridization,” Chromosoma, Vol. 94, No. 1, 1986, pp. 11-18. doi:10.1007/BF00293525
J. Maluszynska, “The Effect of B Chromosomes and T-DNA on Chromosomal Variation in Callus Cells and Regenerated Roots of Crepis capillaris,” Plant Cell Tissue Organ Cult, Vol. 50, No. 2, 1997, pp. 113-118. doi:10.1023/A:1005727529303
N. Otsu, “A Threshold Selection Method from Gray-Level Histograms,” IEEE Transactions on Systems, Man and Cybernetics, Vol. 9, No. 1, 1979, pp. 62-66. doi:10.1109/TSMC.1979.4310076
M. Sezgin and B. Sankur, “Survey over Image Thresholding Techniques and Quantitative Performance Evaluation,” Journal of Electronic Imaging, Vol. 13, No. 1, 2004, pp. 146-165. doi:10.1117/1.1631315
C. J. S. Ferro, “Scale and Texture in Digital Image Classification,” Ph.D. Desideration, Eberly Collage of Arts and Sciences at West Virginia University, 2003.
M. Tuceryan and A. K. Jain, “Texture Analysis. The Handbook of Pattern Recognition and Computer Vision (2nd Edition),” World Scientific Publishing C., 1998, pp. 207-248.
D. H. Xu, A. Kurani, J. D. Furst and D. S. Raicu, “Run-Length Encoding for Volumetric Texture,” The 4th IASTED International Conference on Visualization, Imaging, and Image Processing, Marbella, 2004.
L. Breiman, J. Friedman, R. Olshen and C. Stone, “Classification and Regression Trees,” 1st Edition, Chapman & Hall, 1984.
Z. Darzynkiewicz, M. R. Melamed, T. Lindmo and M. R. Mendelsohn (Eds.), “Flow Cytometry and Sorting,” Wiley-Liss Inc., New York, 1990, pp. 315-340.
T. A. Larsen, D. S. Goodsell, D. Cascio, K. Grzeskowiak and R. E. Dickerson, “The Structure of DAPI Bound to DNA,” Journal of Biomolecular Structure and Dynamics, Vol. 7, No. 3, 1989, pp. 477-491. doi:10.1080/07391102.1989.10508505
G. Manzini, M. L. Barcellona, M. Avitabile and F. Quadrifoglio, “Interaction of Diamidino-2-phenylindole (DAPI) with Natural and Synthetic Nucleic Acids,” Nucleic Acids Research, Vol. 11, No. 24, 1983, pp. 8861-8876. doi:10.1093/nar/11.24.8861
D. Schweizer, “Reverse Fluorescent Chromosome Banding with Chromomycin and DAPI,” Chromosoma, Vol. 58, No. 4, 1976, pp. 307-324. doi:10.1007/BF00292840
M. S. Lin, D. E. Comings and O. S. Alfi, “Optical Studies of the Interaction of 4’-6’-Diamidino-2-phenylindole with DNA and Metaphase Chromosomes,” Chromosoma, Vol. 60, No. 1, 1977, pp. 15-25. doi:10.1007/BF00330407
A. Houben, D. Demidov, D. Gernand, A. Meister, C. R. Leach and I. Schubert, “Methylation of Histone H3 in Euchromatin of Plant Chromosomes Depends on Basic Nuclear DNA Content,” Plant Journal, Vol. 33, No. 6, 2003, pp. 967-973. doi:10.1046/j.1365-313X.2003.01681.x
J. Maluszynska, “B Chromosomes of Crepis capillaris (L.) Waller. In Vivo and in Vitro,” Ph.D. desideration, University of Vienna, 1990.
M. D. Sacristan, “Karyotypic Changes in Callus Cultures from Haploid and Diploid Plants of Crepis capillaris L., Wallr,” Chromosoma, Vol. 33, No. 3, 1971, pp. 273-283. doi:10.1007/BF00284945