Blobs and curves: object-based colocalisation for plant cells
Carl J. Nelson A , Patrick Duckney B , Timothy J. Hawkins B , Michael J. Deeks C , P. Philippe Laissue D , Patrick J. Hussey B and Boguslaw Obara A E
+ Author Affiliations
- Author Affiliations
A School of Engineering and Computing Sciences, Durham University, Durham DH13LE, UK.
B School of Biological and Biomedical Sciences, Durham University, Durham DH13LE, UK.
C College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4SB, UK.
D School of Biological Sciences, University of Essex, Colchester CO4 3SQ, UK.
E Corresponding author. Email: boguslaw.obara@dur.ac.uk
This paper originates from a presentation at the Second International Workshop on Image Analysis Methods for Plant Science, University of Nottingham, 2–3 September 2013.
Functional Plant Biology 42(5) 471-485 https://doi.org/10.1071/FP14047
Submitted: 4 March 2014 Accepted: 21 July 2014 Published: 22 September 2014
Abstract
Blobs and curves occur everywhere in plant bioimaging: from signals of fluorescence-labelled proteins, through cytoskeletal structures, nuclei staining and cell extensions such as root hairs. Here we look at the problem of colocalisation of blobs with blobs (protein-protein colocalisation) and blobs with curves (organelle-cytoskeleton colocalisation). This article demonstrates a clear quantitative alternative to pixel-based colocalisation methods and, using object-based methods, can quantify not only the level of colocalisation but also the distance between objects. Included in this report are computational algorithms, biological experiments and guidance for those looking to increase their use of computationally-based and quantified analysis of bioimages.
Additional keywords: actin-binding proteins, bioimage informatics, fluorescence microscopy, image analysis, mitochondrial trafficking, plant science.
References
Allan C, Burel J-M, Moore J, Blackburn C, Linkert M, Loynton S, MacDonald D, Moore WJ, Neves C, Patterson A, Porter M, Tarkowska A, Loranger B, Avondo J, Lagerstedt I, Linias L, Leo S, Hands K, Hay RT, Patwardhan A, Best C, Kleywegt GJ, Zanetti G, Swedlow JR (2012) OMERO: flexible, model-driven data management for experimental biology. Nature Methods 9, 245–253.| OMERO: flexible, model-driven data management for experimental biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivV2nsrw%3D&md5=26c459ab36c184850a19cf882502fcffCAS | 22373911PubMed |
Avisar D, Abu-Abied M, Belausov E, Sadot E, Hawes C, Sparkes IA (2009) A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles. Plant Physiology 150, 700–709.
| A comparative study of the involvement of 17 Arabidopsis myosin family members on the motility of Golgi and other organelles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsleitL4%3D&md5=866c7dc9b7f00c122d648e155091a825CAS | 19369591PubMed |
Babaloukas G, Tentolouris N, Liatis S, Sklavounou A, Perrea D (2011) Evaluation of three methods for retrospective correction of vignetting on medical microscopy images utilising two open source software tools. Journal of Microscopy 244, 320–324.
| Evaluation of three methods for retrospective correction of vignetting on medical microscopy images utilising two open source software tools.Crossref | GoogleScholarGoogle Scholar | 21950542PubMed |
Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. The Plant Journal 52, 570–582.
| Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtl2jur7P&md5=268c01a290c4b4584934013a6f79b0ccCAS | 17764500PubMed |
Brunkard JO, Runkel AM, Zambryski PC (2013) Plasmodesmata dynamics are coordinated by intracellular signalling pathways. Current Opinion in Plant Biology 16, 614–620.
| Plasmodesmata dynamics are coordinated by intracellular signalling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlektb3L&md5=57ac5448c4381c8530204c84adaefb53CAS | 23978390PubMed |
Cai G, Faleri C, Del Casino C, Emons A, Cresti M (2011) Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiology 155, 1169–1190.
| Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXksFOrt7o%3D&md5=96f072bfe7f4f38b857de2ccc6e27b61CAS | 21205616PubMed |
Cardona A, Tomancak P (2012) Current challenges in open-source bioimage informatics. Nature Methods 9, 661–665.
| Current challenges in open-source bioimage informatics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntb7O&md5=cb93ee2adea220175c573a25c82fb8b8CAS | 22743770PubMed |
Carpenter AE, Kamentsky L, Eliceiri KW (2012) A call for bioimaging software usability. Nature Methods 9, 666–670.
| A call for bioimaging software usability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKnt73P&md5=53c0c337602ee111b73e73bf3dcd2e66CAS | 22743771PubMed |
Cheung AY, Wu H (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annual Review of Plant Biology 59, 547–572.
| Structural and signaling networks for the polar cell growth machinery in pollen tubes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsbY%3D&md5=8cbe774a07c828c018b1b9a66491831bCAS | 18444907PubMed |
Cho BH, Cao-Berg I, Bakal JA, Murphy RF (2012) OMERO.searcher: content-based image search for microscope images. Nature Methods 9, 633–634.
| OMERO.searcher: content-based image search for microscope images.Crossref | GoogleScholarGoogle Scholar | 22743762PubMed |
Cobb JN, Declerck G, Greenberg A, Clark R, McCouch S (2013) Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype–phenotype relationships and its relevance to crop improvement. Theoretical and Applied Genetics 126, 867–887.
| Next-generation phenotyping: requirements and strategies for enhancing our understanding of genotype–phenotype relationships and its relevance to crop improvement.Crossref | GoogleScholarGoogle Scholar | 23471459PubMed |
Deeks MJ, Calcutt JR, Ingle EKS, Hawkins TJ, Chapman S, Richardson AC, Mentlak DA, Dixon MR, Cartwright F, Smertenko AP, Oparka K, Hussey PJ (2012) A superfamily of actin-binding proteins at the actin–membrane nexus of higher plants. Current Biology 22, 1595–1600.
| A superfamily of actin-binding proteins at the actin–membrane nexus of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFahtrnM&md5=8d9ac5b074e91d632d99531a44765f3dCAS | 22840520PubMed |
Dhondt S, Van Haerenborgh D, Van Cauwenbergh C, Merks RMHH, Philips W, Beemster GTSS, Inzé D (2012) Quantitative analysis of venation patterns of Arabidopsis leaves by supervised image analysis. The Plant Journal 69, 553–563.
| Quantitative analysis of venation patterns of Arabidopsis leaves by supervised image analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XislemtL0%3D&md5=982102c4049b19ececd3c13dd6fbed13CAS | 21955023PubMed |
Eliceiri KW, Berthold MR, Goldberg IG, Ibáñez L, Manjunath BS, Martone ME, Murphy RF, Peng H, Plant AL, Roysam B, Stuurman N, Swedlow JR, Tomancak P, Carpenter AE (2012) Biological imaging software tools. Nature Methods 9, 697–710.
| Biological imaging software tools.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKnur7F&md5=a38b481552b56501dbd300d3e08f5d09CAS | 22743775PubMed |
Fichtl A, Sailer M, Brenner RE, Schmidt V, Walther P, Lück S, Joos H (2011) Statistical analysis of the intermediate filament network in cells of mesenchymal lineage by greyvalue-oriented image segmentation. Computational Statistics 28, 139–160.
Gelasca ED, Obara B, Fedorov D, Kvilekval K, Manjunath BS (2009) A biosegmentation benchmark for evaluation of bioimage analysis methods. BMC Bioinformatics 10, 368
| A biosegmentation benchmark for evaluation of bioimage analysis methods.Crossref | GoogleScholarGoogle Scholar |
Goff SA, Vaughn M, McKay S, Lyons E, Stapleton AE, Gessler D, Matasci N, Wang L, Hanlon M, Lenards A, Muir A, Merchant N, Lowry S, Mock S, Helmke M, Kubach A, Narro M, Hopkins N, Micklos D, Hilgert U, Gonzales M, Jordan C, Skidmore E, Dooley R, Cazes J, McLay R, Lu Z, Pasternak S, Koesterke L, Piel WH, Grene R, Noutsos C, Gendler K, Feng X, Tang C, Lent M, Kim S-J, Kvilekval K, Manjunath BS, Tannen V, Stamatakis A, Sanderson M, Welch SM, Cranston KA, Soltis P, Soltis D, O’Meara B, Ane C, Brutnell T, Kleibenstein DJ, White JW, Leebens-Mack J, Donoghue MJ, Spalding EP, Vision TJ, Myers CR, Lowenthal D, Enquist BJ, Boyle B, Akoglu A, Andrews G, Ram S, Ware D, Stein L, Stanzione D (2011) The iPlant Collaborative: Cyberinfrastructure for plant biology. Frontiers in Plant Science 2, 34
| The iPlant Collaborative: Cyberinfrastructure for plant biology.Crossref | GoogleScholarGoogle Scholar | 22645531PubMed |
Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annual Review of Cell and Developmental Biology 17, 159–187.
| Polarized cell growth in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXos1OmsLs%3D&md5=969e908eb0acb0cdb14a0d8eae9dc0a0CAS | 11687487PubMed |
Kleine-Vehn J, Wabnik K, Martinière A, Łangowski Ł, Willig K, Naramoto S, Friml J (2011) Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Molecular Systems Biology 7, 540
| Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane.Crossref | GoogleScholarGoogle Scholar | 22027551PubMed |
Kuhn WH (1955) The Hungarian method for the assignment problem. Naval Research Logistics Quarterly 2, 83–97.
| The Hungarian method for the assignment problem.Crossref | GoogleScholarGoogle Scholar |
Kvilekval K, Fedorov D, Obara B, Singh A, Manjunath BS (2010) Bisque: a platform for bioimage analysis and management. Bioinformatics 26, 544–552.
| Bisque: a platform for bioimage analysis and management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvF2qu7g%3D&md5=58dc7e712afcbc77b4cf0e33e139d9a8CAS | 20031971PubMed |
Lachmanovich E, Shvartsman DE, Malka Y, Botvin C, Henis YI, Weiss AM (2003) Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immunofluorescence co-patching studies. Journal of Microscopy 212, 122–131.
| Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immunofluorescence co-patching studies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srltFWhsw%3D%3D&md5=e152ca1e34907e691800a2ad8d195656CAS | 14629561PubMed |
Lichius A, Goryachev AB, Fricker MD, Obara B, Castro-Longoria E, Read ND (2014) Functional divergence of RAC1 and CDC42 small GTPases during cell fusion in Neurospora crassa. Journal of Cell Science in press.
Ljosa V, Sokolnicki KL, Carpenter AE (2013) Annotated high-throughput microscopy image sets for validation. Nature Methods 9, 1179–1180.
Lobet G, Draye X, Périlleux C (2013) An online database for plant image analysis software tools. Plant Methods 9, 38
| An online database for plant image analysis software tools.Crossref | GoogleScholarGoogle Scholar | 24107223PubMed |
Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA (1992) Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. Journal of Cell Science 103, 857–862.
Moscatelli A, Idilli AL, Rodighiero S, Caccianiga M (2012) Inhibition of actin polymerisation by low concentration Latrunculin B affects endocytosis and alters exocytosis in shank and tip of tobacco pollen tubes. Plant Biology 14, 770–782.
| Inhibition of actin polymerisation by low concentration Latrunculin B affects endocytosis and alters exocytosis in shank and tip of tobacco pollen tubes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKjsbzK&md5=e4baba50ef0d3387f73bac48e859fe15CAS |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. 15, 473–497.
| A revised medium for rapid growth and bio assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=727f2209935a898d7e76484915aa5b8dCAS |
Nyquist H (1928) Certain topics in telegraph transmission theory. Transactions of the American Institute of Electrical Engineers 47, 617–644.
| Certain topics in telegraph transmission theory.Crossref | GoogleScholarGoogle Scholar |
Obara B, Grau V, Fricker MD (2012) A bioimage informatics approach to automatically extract complex fungal networks. Bioinformatics 28, 2374–2381.
| A bioimage informatics approach to automatically extract complex fungal networks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlanurfO&md5=2fb058c29dde1e084a4de8c5ad4fe772CAS | 22743223PubMed |
Obara B, Jabeen A, Fernandez N, Laissue PP (2013) A novel method for quantified, superresolved, three-dimensional colocalisation of isotropic, fluorescent particles. Histochemistry and Cell Biology 139, 391–402.
| A novel method for quantified, superresolved, three-dimensional colocalisation of isotropic, fluorescent particles.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXis1Wltbk%3D&md5=e393b1d6e66a07cbdc565ae3d17d925cCAS | 23381680PubMed |
Obata B, Byun J, Fedorov D, Manjunath BS (2008). Automatic nuclei detection and dataflow in BISQUIK system. In ‘Workshop on bioimage informatics: biological imaging, computer vision and data mining’. Santa Barbara.
Pound MP, French AP, Wells DM, Bennett MJ, Pridmore TP (2012) CellSeT: novel software to extract and analyze structured networks of plant cells from confocal images. The Plant Cell 24, 1353–1361.
| CellSeT: novel software to extract and analyze structured networks of plant cells from confocal images.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XoslCrt7g%3D&md5=58c4caac9ab4ff346748d1903b9c968cCAS | 22474181PubMed |
Pridmore TP, French AP, Pound MP (2012) What lies beneath: underlying assumptions in bioimage analysis. Trends in Plant Science 17, 688–692.
| What lies beneath: underlying assumptions in bioimage analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1aktLfI&md5=66b91315adc1e06082e6d63a9b0e4b57CAS | 22902890PubMed |
Rajaram S, Pavie B, Hac NEF, Altschuler SJ, Wu LF (2012) SimuCell : a flexible framework for creating synthetic microscopy images. Nature Methods 9, 634–635.
| SimuCell : a flexible framework for creating synthetic microscopy images.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVKntbbI&md5=4fc3c595e70f8e6ded50bb4aa87b3db2CAS | 22743763PubMed |
Roeder AHK, Chickarmane V, Cunha A, Obara B, Munjunath BS, Meyerowitz EM (2010) Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana. PLoS Biology 8, e1000367
| Variability in the control of cell division underlies sepal epidermal patterning in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Rolland-Lagan A-G, Amin M, Pakulska M (2009) Quantifying leaf venation patterns: two-dimensional maps. The Plant Journal 57, 195–205.
| Quantifying leaf venation patterns: two-dimensional maps.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFOiu7k%3D&md5=52f30fe0c3307617f825e4ca0dc4c1f3CAS | 18785998PubMed |
Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M (2007) Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant & Cell Physiology 48, 345–361.
| Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjsVCqsrc%3D&md5=a88333e42bde423fcccb140b9e215e81CAS |
Sappl PG, Heisler MG (2013) Live-imaging of plant development: latest approaches. Current Opinion in Plant Biology 16, 33–40.
| Live-imaging of plant development: latest approaches.Crossref | GoogleScholarGoogle Scholar | 23196271PubMed |
Sezgin M, Sankur B (2004) Survey over image thresholding techniques and quantitative performance evaluation. Journal of Electronic Imaging 13, 146–165.
| Survey over image thresholding techniques and quantitative performance evaluation.Crossref | GoogleScholarGoogle Scholar |
Shannon CE (1949) Communication in the presence of noise. Proceedings of the IRE 37, 10–21.
| Communication in the presence of noise.Crossref | GoogleScholarGoogle Scholar |
Shapiro LG, Stockman GC (2001). ‘Computer Vision.’ (Prentice Hall: Upper Saddle River, NJ, USA)
Simpson C, Thomas C, Findlay K, Bayer E, Maule AJ (2009) An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking. The Plant Cell 21, 581–594.
| An Arabidopsis GPI-anchor plasmodesmal neck protein with callose binding activity and potential to regulate cell-to-cell trafficking.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVKrt78%3D&md5=0551c13796c53363b7418598716a4eeeCAS | 19223515PubMed |
Sparkes IA, Teanby NA, Hawes C (2008) Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation. Journal of Experimental Botany 59, 2499–2512.
| Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnt1Sls7Y%3D&md5=ff75bfc12fec64fb4966577c4645d6f2CAS | 18503043PubMed |
Swedlow JR, Goldberg I, Brauner E, Sorger PK (2003) Informatics and quantitative analysis in bioimage informatics. Science 300, 100–102.
| Informatics and quantitative analysis in bioimage informatics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXis1CgtLg%3D&md5=fbd8390a1f5939412509f04c98d16f71CAS | 12677061PubMed |
Thomasson MS, Macnaughtan MA (2013) Microscopy basics and the study of actin–actin-binding protein interactions. Analytical Biochemistry 443, 156–165.
| Microscopy basics and the study of actin–actin-binding protein interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslCls7jM&md5=be25fbf0980a29c9b5c7260e10f276c0CAS | 24044992PubMed |
Van Gestel K, Kohler RH, Verbelen JP (2002) Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules. Journal of Experimental Botany 53, 659–667.
| Plant mitochondria move on F-actin, but their positioning in the cortical cytoplasm depends on both F-actin and microtubules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitlCks7w%3D&md5=827aca4047b90e3a3d40e43b5899fd13CAS | 11886885PubMed |
Yang Y, Li Y, Wu C (2013) Genomic resources for functional analyses of the rice genome. Current Opinion in Plant Biology 16, 157–163.
| Genomic resources for functional analyses of the rice genome.Crossref | GoogleScholarGoogle Scholar | 23571012PubMed |
Zheng M, Beck M, Muller J, Chen T, Wang X, Wang F, Wang Q, Wang Y, Baluska F, Logan DC, Šamaj J, Lin J (2009) Actin turnover is required for myosin-dependent mitochondrial movements in Arabidopsis root hairs. PLoS ONE 4, e5961
| Actin turnover is required for myosin-dependent mitochondrial movements in Arabidopsis root hairs.Crossref | GoogleScholarGoogle Scholar | 19536333PubMed |
Zheng M, Wang Q, Teng Y, Wang X, Wang F, Chen T, Samaj J, Logan DC (2010) The speed of mitochondrial movement is regulated by the cytoskeleton and myosin in Picea wilsonii pollen tubes. Planta 231, 779–791.
| The speed of mitochondrial movement is regulated by the cytoskeleton and myosin in Picea wilsonii pollen tubes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvV2gs78%3D&md5=96867451d896195e77bcde4a2ea1b5dcCAS | 20033230PubMed |
