MorphoGraphX: A platform for quantifying morphogenesis in 4D

eLife

Volumn 4, Issue MAY, 2015, Pages 1-20

  de Reuille, Pierre Barbier ^a   Routier Kierzkowska, Anne Lise ^b   Kierzkowski, Daniel ^b   Bassel, George W ^c   Schüpbach, Thierry ^d   Tauriello, Gerardo ^e   Bajpai, Namrata ^b   Strauss, Sören ^b   Weber, Alain ^a   Kiss, Annamaria ^f,g   Burian, Agata ^a,h   Hofhuis, Hugo ^b   Sapala, Aleksandra ^b   Lipowczan, Marcin ^h   Heimlicher, Maria B ⁱ   Robinson, Sarah ^a   Bayer, Emmanuelle M ^j   Basler, Konrad ⁱ   Koumoutsakos, Petros ^e   Roeder, Adrienne H K ^k   Aegerter Wilmsen, Tinri ⁱ   Nakayama, Naomi ^a,l   Tsiantis, Miltos ^b   Hay, Angela ^b   Kwiatkowska, Dorota ^h   Xenarios, Ioannis ^d   Kuhlemeier, Cris ^a   Smith, Richard S ^a,b   more..

^a UNIVERSITY OF BERN   (Switzerland)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^e ETH ZURICH   (Switzerland)

^f UNIVERSITÉ DE LYON   (France)

^g Laboratoire Joliot Curie   (France)

^h UNIVERSITY OF SILESIA   (Poland)

ⁱ Institute of Pharmaceutical Sciences   (Switzerland)

^j UNIVERSITÉ DE BORDEAUX   (France)

^k School of Integrative Plant Sciences   (United States)

^l UNIVERSITY OF EDINBURGH   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANISOTROPY; ARTICLE; CELL EXPANSION; CELL FUSION; CELL PROLIFERATION; CELL SHAPE; CELL SIZE; COMPUTER GRAPHICS; COMPUTER PROGRAM; CONTROLLED STUDY; GENE EXPRESSION; GROWTH RATE; IMAGE ANALYSIS; IMAGE PROCESSING; MAGNETIC RESONANCE ANGIOGRAPHY; MORPHOGENESIS; NONHUMAN; PROTEIN EXPRESSION; PROTEOMICS; SIGNAL PROCESSING; THREE DIMENSIONAL IMAGING; TIME LAPSE IMAGING; VALIDATION PROCESS; ALGORITHM; ANIMAL; ARABIDOPSIS; CASSIA; CONFOCAL MICROSCOPY; DEVICES; DROSOPHILA MELANOGASTER; FLOWER; FRUIT; GENETICS; GROWTH, DEVELOPMENT AND AGING; MICROTUBULE; PLANT DEVELOPMENT; PROCEDURES; SOFTWARE; STATISTICS AND NUMERICAL DATA; TOMATO; ULTRASTRUCTURE;

ALGORITHMS; ANIMALS; ANISOTROPY; ARABIDOPSIS; CASSIA; CELL PROLIFERATION; CELL SHAPE; DROSOPHILA MELANOGASTER; FLOWERS; FRUIT; GENE EXPRESSION; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; LYCOPERSICON ESCULENTUM; MICROSCOPY, CONFOCAL; MICROTUBULES; MORPHOGENESIS; PLANT DEVELOPMENT; SOFTWARE; TIME-LAPSE IMAGING;

EID: 84930640355     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05864     Document Type: Article

References (68)

1. Aegerter-Wilmsen T, Heimlicher MB, Smith AC, de Reuille PB, Smith RS, Aegerter CM, Basler K. 2012. Integrating force-sensing and signaling pathways in a model for the regulation of wing imaginal disc size. Development 139: 3221-3231. doi: 10.1242/dev.082800.
2. Bassel GW, Stamm P, Mosca G, Barbier de Reuille P, Gibbs DJ, Winter R, Janka A, Holdsworth MJ, Smith RS. 2014. Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo. Proceedings of the National Academy of Sciences of USA 111:8685-8690. doi: 10.1073/pnas.1404616111.
3. Bayer E, Smith RS, Mandel T, Nakayama N, Sauer M, Prusinkiewicz P, Kuhlemeier C. 2009. Integration of transport-based models for phyllotaxis and midvein formation. Genes & Development 23:373-384. doi: 10.1101/gad.497009.
4. Bloomenthal J. 1988. Polygonization of implicit surfaces. Computer Aided Geometric Design 5:341-355. doi: 10.1016/0167-8396(88)90013-1.
5. Boudaoud A, Burian A, Borowska-Wykręt D, Uyttewaal M, Wrzalik R, Kwiatkowska D, Hamant O. 2014. FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nature Protocols 9:457-463. doi: 10.1038/nprot.2014.024.
6. Butler LC, Blanchard GB, Kabla AJ, Lawrence NJ, Welchman DP, Mahadevan L, Adams RJ, Sanson B. 2009. Cell shape changes indicate a role for extrinsic tensile forces in Drosophila germ-band extension. Nature Cell Biology 11:859-864. doi: 10.1038/ncb1894.
7. Chickarmane V, Roeder AH, Tarr PT, Cunha A, Tobin C, Meyerowitz EM. 2010.Computational morphodynamics: a modeling framework to understand plant growth. Annual Review of Plant Biology 61:65-87. doi: 10.1146/annurev-arplant-042809-112213.
8. Chitwood DH, Headland LR, Ranjan A, Martinez CC, Braybrook SA, Koenig DP, Kuhlemeier C, Smith RS, Sinha NR. 2012. Leaf asymmetry as a developmental constraint imposed by auxin-dependent phyllotactic patterning. The Plant Cell 24:2318-2327. doi: 10.1105/tpc.112.098798.
9. de Reuille PB, Bohn-Courseau I, Godin C, Traas J. 2005. A protocol to analyse cellular dynamics during plant development. The Plant Journal 44:1045-1053. doi: 10.1111/j.1365-313X.2005.02576.x.
10. De Rybel B, Möller B, Yoshida S, Grabowicz I, Barbier de Reuille P, Boeren S, Smith RS, Borst JW, Weijers D. 2013. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Developmental Cell 24:426-437. doi: 10.1016/j.devcel.2012.12.013.
11. Denk W, Horstmann H. 2004. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLOS Biology 2:e329. doi: 10.1371/journal.pbio.0020329.
12. Dumais J, Kwiatkowska D. 2002. Analysis of surface growth in shoot apices. The Plant Journal 31:229-241. doi: 10.1046/j.1365-313X.2001.01350.x.
13. Dumais J, Steele C. 2000. New evidence for the role of mechanical forces in the shoot apical meristem. Journal of Plant Growth Regulation 19:7-18. doi: 10.1007/s003440000003.
14. Elsner J, Michalski M, Kwiatkowska D. 2012. Spatiotemporal variation of leaf epidermal cell growth: a quantitative analysis of Arabidopsis thaliana wild-type and triple cyclinD3 mutant plants. Annals of Botany 109:897-910.doi: 10.1093/aob/mcs005.
15. Everitt C. 2001. Interactive order-independent transparency. 7NVIDIA.
16. Federici F, Dupuy L, Laplaze L, Heisler M, Haseloff J. 2012. Integrated genetic and computation methods for in planta cytometry. Nature Methods 9:483-485. doi: 10.1038/nmeth.1940.
17. Federl P, Prusinkiewicz P. 1999. Virtual laboratory: an interactive software environment for computer graphics. Proceedings of Computer Graphics International 93-100.
18. Fernandez R, Das P, Mirabet V, Moscardi E, Traas J, Verdeil JL, Malandain G, Godin C. 2010.Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution. Nature Methods 7:547-553. doi: 10.1038/nmeth.1472.
19. Goldfeather J, Interrante V. 2004. A Novel Cubic-Order Algorithm for Approximating Principal Direction Vectors. ACM Transactions on Graphics 23:1 45-63.
20. Goodall C, Green P. 1986. Quantitative analysis of surface growth. Botanical Gazette 147:1-15. doi: 10.1086/337562.
21. Grandjean O, Vernoux T, Laufs P, Belcram K, Mizukami Y, Traas J. 2004. In vivo analysis of cell division, cell growth, and differentiation at the shoot apical meristem in Arabidopsis. The Plant Cell 16:74-87. doi: 10.1105/tpc. 017962.
22. Green PB, Havelange A, Bernier G. 1991. Floral morphogenesis in Anagallis: scanning-electron-micrograph sequences from individual growing meristems before, during, and after the transition to flowering. Planta 185: 502-512. doi: 10.1007/BF00202959.
23. Hamant O, Heisler M, Jönsson H, Krupinski P, Uyttewaal M, Bokov P, Corson F, Sahlin P, Boudaoud A, Meyerowitz EM, Couder Y, Traas J. 2008. Developmental patterning by mechanical signals in Arabidopsis. Science 322: 1650-1655. doi: 10.1126/science.1165594.
24. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV, Long JA, Meyerowitz EM. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology 15:1899-1911. doi: 10.1016/j.cub.2005.09.052.
25. Heller E, Kumar KV, Grill SW, Fuchs E. 2014. Forces generated by cell intercalation tow epidermal sheets in mammalian tissue morphogenesis. Developmental Cell 28:617-632. doi: 10.1016/j.devcel.2014.02.011.
26. Jönsson H, Gruel J, Krupinski P, Troein C. 2012. On evaluating models in computational morphodynamics. Current Opinion in Plant Biology 15:103-110.doi: 10.1016/j.pbi.2011.09.007.
27. Jönsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E. 2006. An auxin-driven polarized transport model for phyllotaxis. Proceedings of the National Academy of Sciences of USA 103:1633-1638. doi: 10.1073/pnas. 0509839103.
28. Kennaway R, Coen E, Green A, Bangham A. 2011. Generation of diverse biological forms through combinatorial interactions between tissue polarity and growth. PLOS Computational Biology 7:e1002071. doi: 10.1371/journal. pcbi.1002071.
29. Kierzkowski D, Lenhard M, Smith R, Kuhlemeier C. 2013. Interaction between meristem tissue layers controls phyllotaxis. Developmental Cell 26:616-628. doi: 10.1016/j.devcel.2013.08.017.
30. Kierzkowski D, Nakayama N, Routier-Kierzkowska A-L, Weber A, Bayer E, Schorderet M, Reinhardt D, Kuhlemeier C, Smith RS. 2012. Elastic domains regulate growth and organogenesis in the plant shoot apical meristem. Science 335:1096-1099. doi: 10.1126/science.1213100.
31. Kondo S, Miura T. 2010.Reaction-diffusion model as a framework for understanding biological pattern formation. Science 329:1616-1620. doi: 10.1126/science.1179047.
32. Kuchen EE, Fox S, de Reuille PB, Kennaway R, Bensmihen S, Avondo J, Calder GM, Southam P, Robinson S Bangham A, Coen E. 2012. Generation of leaf shape through early patterns of growth and tissue polarity. Science 335:1092-1096. doi: 10.1126/science.1214678.
33. Kwiatkowska D. 2004. Surface growth at the reproductive shoot apex of Arabidopsis thaliana pin-formed 1 and wild type. Journal of Experimental Botany 55:1021-1032. doi: 10.1093/jxb/erh109.
34. Kwiatkowska D, Dumais J. 2003. Growth and morphogenesis at the vegetative shoot apex of Anagallis arvensis L. Journal of Experimental Botany 54:1585-1595. doi: 10.1093/jxb/erg166.
35. Kwiatkowska D, Routier-Kierzkowska AL. 2009. Morphogenesis at the inflorescence shoot apex of Anagallis arvensis: surface geometry and growth in comparison with the vegetative shoot. Journal of Experimental Botany 60:3407-3418. doi: 10.1093/jxb/erp176.
36. Lecuit T, Lenne PF. 2007. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nature Reviews Molecular Cell Biology 8:633-644. doi: 10.1038/nrm2222.
37. Levoy M. 1990. Efficient ray tracing of volume data. ACM Transactions on Graphics 9:245-261. doi: 10.1145/78964.78965.
38. Merks RM, Van de Peer Y, InzéD, Beemster GT. 2007. Canalization without flux sensors: a traveling-wave hypothesis. Trends in Plant Science 12:384-390. doi: 10.1016/j.tplants.2007.08.004.
39. Milde F, Tauriello G, Haberkern H, Koumoutsakos P. 2014. SEM++: a particle model of cellular growth, signaling and migration. Computational Particle Mechanics 1:211-227. doi: 10.1007/s40571-014-0017-4.
40. Mosaliganti KR, Noche RR, Xiong F, Swinburne IA, Megason SG. 2012. ACME: automated cell morphology extractor for comprehensive reconstruction of cell membranes. PLOS Computational Biology 8:e1002780. doi: 10.1371/journal.pcbi.1002780.
41. Nakayama N, Smith RS, Mandel T, Robinson S, Kimura S, Boudaoud A, Kuhlemeier C. 2012. Mechanical regulation of auxin-mediated growth. Current Biology 22:1468-1476. doi: 10.1016/j.cub.2012.06.050.
42. Peng H, Long F, Zhao T, Myers E. 2011. Proof-editing is the bottleneck of 3D neuron reconstruction: the problem and solutions. Neuroinformatics 9:103-105. doi: 10.1007/s12021-010-9090-x.
43. Peng H, Ruan Z, Long F, Simpson JH, Myers EW. 2010.V3D enables real-time 3D visualization and quantitative analysis of large-scale biological image data sets. Nature Biotechnology 28:348-353. doi: 10.1038/nbt.1612.
44. 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. doi: 10.1105/tpc.112. 096289.
45. Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM. 2004. Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131: 4225-4237. doi: 10.1242/dev.01261.
46. Routier-Kierzkowska AL, Kwiatkowska D. 2008. New stereoscopic reconstruction protocol for scanning electron microscope images and its application to in vivo replicas of the shoot apical meristem. Functional Plant Biology 35:1034-1046. doi: 10.1071/FP08047.
47. Routier-Kierzkowska AL, Weber A, Kochova P, Felekis D, Nelson BJ, Kuhlemeier C, Smith RS. 2012. Cellular force microscopy for in vivo measurements of plant tissue mechanics. Plant Physiology 158:1514-1522. doi: 10.1104/pp.111.191460.
48. Sampathkumar A, Krupinski P, Wightman R. 2014. Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3:e01967. doi: 10.7554/eLife.01967.
49. Santuari L, Scacchi E, Rodriguez-Villalon A, Salinas P, Dohmann EM, Brunoud G, Vernoux T, Smith RS, Hardtke CS. 2011. Positional information by differential endocytosis splits auxin response to drive Arabidopsis root meristem growth. Current Biology 21:1918-1923. doi: 10.1016/j.cub.2011.10.002.
50. Savaldi-Goldstein S, Peto C, Chory J. 2007. The epidermis both drives and restricts plant shoot growth. Nature 446:199-202. doi: 10.1038/nature05618.
51. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: an open-source platform for biological-image analysis. Nature Methods 9:676-682. doi: 10.1038/nmeth.2019.
52. Schmidt T, Pasternak T, Liu K, Blein T, Aubry-Hivet D, Dovzhenko A, Duerr J, Teale W, Ditengou FA, Burkhardt H Ronneberger O, Palme K. 2014. The iRoCS Toolbox - 3D analysis of the plant root apical meristem at cellular resolution. The Plant Journal 77:806-814. doi: 10.1111/tpj.12429.
53. Shani E, Ben-Gera H, Shleizer-Burko S, Burko Y, Weiss D, Ori N. 2010.Cytokinin regulates compound leaf development in tomato. The Plant Cell 22:3206-3217. doi: 10.1105/tpc.110.078253.
54. Sick S, Reinker S, Timmer J, Schlake T. 2006. WNT and DKK determine hair follicle spacing through a reactiondiffusion mechanism. Science 314:1447-1450. doi: 10.1126/science.1130088.
55. Smith C, Prusinkiewicz P, Samavati F. 2004. Local specification of surface subdivision algorithms. In: Pfaltz JL, Nagl M, Böhlen B, editors. Applications of graph transformations with industrial relevance. Springer-Verlag GmbH. p. 313-327Second International Workshop, AGTIVE 2003.
56. Sommer C, Strähle C, Köthe F, Hamprecht A. 2011. Ilastik: interactive learning and segmentation toolkit. p. 230-233Eighth IEEE international Symposium on Biomedical imaging (ISBI).
57. Steeves TA, Sussex IM. 1989. Patterns in plant development. Cambridge University Press.
58. Stoma S, Lucas M, Chopard J, Schaedel M, Traas J, Godin C. 2008. Flux-based transport enhancement as a plausible unifying mechanism for auxin transport in meristem development. PLOS Computational Biology 4: e1000207. doi: 10.1371/journal.pcbi.1000207.
59. TschumperléD. 2012. The CImg library. Cachan, France IPOL 2012 Meeting on Image Processing Libraries.
60. Ueda K, Matsuyama T, Hashimoto T. 1999. Visualization of microtubules in living cells of transgenic Arabidopsis thaliana. Protoplasma 206:201-206. doi: 10.1007/BF01279267.
61. Uyttewaal M, Burian A, Alim K, Landrein B, Borowska-Wykręt D, Dedieu A, Peaucelle A, Ludynia M, Traas J Boudaoud A, Kwiatkowska D, Hamant O. 2012. Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149:439-451. doi: 10.1016/j.cell.2012.02.048.
62. Varner VD, Voronov DA, Taber LA. 2010.Mechanics of head fold formation: investigating tissue-level forces during early development. Development 137:3801-3811. doi: 10.1242/dev.054387.
63. Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, Galinha C, Gan X, Hajheidari M, Hay A, Smith RS, Huijser P Bailey CD, Tsiantis M. 2014. Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343:780-783. doi: 10.1126/science.1248384.
64. Wabnik K, Robert HS, Smith RS, Friml J. 2013. Modeling framework for the establishment of the apical-basal embryonic axis in plants. Current Biology 23:2513-2518. doi: 10.1016/j.cub.2013.10.038.
65. Williams M, Green P. 1988. Sequential scanning electron microscopy of a growing plant meristem. Protoplasma 147:77-79. doi: 10.1007/BF01403879.
66. Wills G. 2012. Visualization toolkit software. Wiley Interdisciplinary Reviews: Computational Statistics 4:474-481. doi: 10.1002/wics.1224.
67. Yoo TS, Ackerman MJ, Lorensen WE, Schroeder W, Chalana V, Aylward S, Metaxas D, Whitaker R. 2002. Engineering and algorithm design for an image processing Api: a technical report on ITK-the insight toolkit. Studies in Health Technology and Informatics 85:586-592.
68. Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P, Smith RS, Weijers D. 2014. Genetic control of plant development by overriding a geometric division rule. Developmental Cell 29:75-87. doi: 10.1016/j.devcel. 2014.02.002.