vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/VJ20.590vavilov-2486Research ArticleМОЛЕКУЛЯРНЫЕ МАРКЕРЫ В ГЕНЕТИКЕ И СЕЛЕКЦИИBIOINFORMATICS AND SYSTEM BIOLOGYPlantLayout - программное средство для моделирования распределения веществ в тканях различной структурыPlantLayout pipeline to model tissue patterninghttps://orcid.org/0000-0003-3804-2049СавинаМ. С.SavinaM. S.

Новосибирск

Novosibirsk

savinams1991@gmail.comhttps://orcid.org/0000-0003-3438-0147МироноваВ. В.MironovaV. V.

Новосибирск

Novosibirsk

Федеральный исследовательский центр Институт цитологии и генетики, Сибирское отделение Российской академии наукРоссияInstitute of Cytology and Genetics, Siberian Branch of the Russian Academy of SciencesRussian FederationФедеральный исследовательский центр Институт цитологии и генетики, Сибирское отделение Российской академии наук; Новосибирский национальный исследовательский государственный университетРоссияInstitute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences; Novosibirsk State UniversityRussian Federation202018032020241102107Copyright © Савина М.С., Миронова В.В., 20202020Савина М.С., Миронова В.В.Savina M.S., Mironova V.V.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/2486

Для изучения механизмов, лежащих в основе формирования паттернов развития в тканях, необходим анализ динамики распределения регуляторов во времени и пространстве в тканях сложной структуры. Наибольшее значение это имеет в случае регуляторов развития (морфогенов), которые распределены в ткани неравномерно, образуя максимумы и градиенты, и регулируют клеточные процессы по-разному в зависимости от дозы. Настоящая работа посвящена описанию программного средства PlantLayout на языке MATLAB, которое облегчает исследование формирования распределений регуляторов в тканях различного строения. С его помощью можно построить двумерную структурную модель ткани, внедрить ее в математическую модель, описанную в терминах обычных дифференциальных уравнений, выполнить численные расчеты модели и визуализировать полученные результаты - всё на одной платформе. В результате можно изучать динамику работы генных сетей и изменения концентрации регуляторов в каждой клетке клеточного ансамбля, воспроизводящего строение реальной ткани. Исследуемые генные сети могут различаться для разных типов клеток. Одной из задач, которую решает PlantLayout в полуавтоматическом режиме, является определение ориентации клеточной стенки, что имеет значение в случае присутствия в ткани поляризованных клеток. Кроме того, PlantLayout позволяет автоматически определять другие качественные и количественные характеристики клеток и клеточных стенок, такие как длина и ширина клеточных стенок, площадь сечения и периметр клеток, которые могут помочь в моделировании паттернов распределения регуляторов развития, а также список соседних клеток для каждой клетки. В данной работе продемонстрирована эффективность разработанного программного средства PlantLayout применительно к моделированию распределения фитогормона ауксина в кончике корня растения.

To study the mechanisms underlying developmental pattern formation in a tissue, one needs to analyze the dynamics of the regulators in time and space across the tissue of a specific architecture. This problem is essential for the developmental regulators (morphogens) that distribute over the tissues anisotropically, forming there maxima and gradients and guiding cellular processes in a dose-dependent manner. Here we present the PlantLayout pipeline for MATLAB software, which facilitates the computational studies of tissue patterning. With its help, one can build a structural model of a two-dimensional tissue, embed it into a mathematical model in ODEs, perform numerical simulations, and visualize the obtained results - everything on the same platform. As a result, one can study the concentration dynamics of developmental regulators over the cell layout reconstructed from the real tissue. PlantLayout allows studying the dynamics and the output of gene networks guided by the developmental regulator in specific cells. The gene networks could be different for different cell types. One of the obstacles that PlantLayout removes semi-automatically is the determination of the cell wall orientation which is relevant when cells in the tissue have a polarity. Additionally, PlantLayout allows automatically extracting other quantitative and qualitative features of the cells and the cell walls, which might help in the modeling of a developmental pattern, such as the length and the width of the cell walls, the set of the neighboring cells, cell volume and cell perimeter. We demonstrate PlantLayout performance on the model of phytohormone auxin distribution over the plant root tip.

математическое моделированиеобработка изображенийполярностьморфогенпаттернmathematical modelingimage analysispolaritymorphogenpatternThe work was supported by RFBR 18-34-00485 and the project 0324-2019-0040-С-01 from the Russian State BudgetReferencesBand L.R., Wells D.M., Fozard J.A., Ghetiu T., French A.P., Pound M.P., Wilson M.H., Yu L., Li W., Hijazi H.I., Oh J. Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell. 2014;26(3):862-875.Band L.R., Wells D.M., Fozard J.A., Ghetiu T., French A.P., Pound M.P., Wilson M.H., Yu L., Li W., Hijazi H.I., Oh J. Systems analysis of auxin transport in the Arabidopsis root apex. Plant Cell. 2014;26(3):862-875.Bellomo N., Carbonaro B. Toward a mathematical theory of living systems focusing on developmental biology and evolution: a review and perspectives. Phys. Life Rev. 2011;8(1):1-8.Bellomo N., Carbonaro B. Toward a mathematical theory of living systems focusing on developmental biology and evolution: a review and perspectives. Phys. Life Rev. 2011;8(1):1-8.Brunel G., Borianne P., Subsol G., Jaeger M., Caraglio Y. Automatic characterization of the cell organization in light microscopic images of wood: application to the identification of the cell file. Proc. of the 4th Int. Symp. on Plant Growth Modeling, Simulation, Visualization and Applications. IEEE. 2012;58-65.Brunel G., Borianne P., Subsol G., Jaeger M., Caraglio Y. Automatic characterization of the cell organization in light microscopic images of wood: application to the identification of the cell file. Proc. of the 4th Int. Symp. on Plant Growth Modeling, Simulation, Visualization and Applications. IEEE. 2012;58-65.Cerutti G., Ali O., Godin C. DRACO-STEM: an automatic tool to generate high-quality 3D meshes of shoot apical meristem tissue at cell resolution. Front. Plant Sci. 2017;8:353. de Reuille P.B., Routier-Kierzkowska A.L., Kierzkowski D., Bas-sel G.W., Schupbach T., Tauriello G., Bajpai N., Strauss S., Weber A., Kiss A., Burian A. MorphoGraphX: a platform for quantifying morphogenesis in 4D. Elife. 2015;4:e05864.Cerutti G., Ali O., Godin C. DRACO-STEM: an automatic tool to generate high-quality 3D meshes of shoot apical meristem tissue at cell resolution. Front. Plant Sci. 2017;8:353. de Reuille P.B., Routier-Kierzkowska A.L., Kierzkowski D., Bas-sel G.W., Schupbach T., Tauriello G., Bajpai N., Strauss S., Weber A., Kiss A., Burian A. MorphoGraphX: a platform for quantifying morphogenesis in 4D. Elife. 2015;4:e05864.Eckardt N.A. A useful model of auxin transport in the root apex. Plant Cell. 2014;26:843.Eckardt N.A. A useful model of auxin transport in the root apex. Plant Cell. 2014;26:843.Economou A.D., Ohazama A., Porntaveetus T., Sharpe P.T., Kondo S., Basson M.A., Gritli-Linde A., Cobourne M.T., Green J.B. Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat. Genet. 2012;44(3):348.Economou A.D., Ohazama A., Porntaveetus T., Sharpe P.T., Kondo S., Basson M.A., Gritli-Linde A., Cobourne M.T., Green J.B. Periodic stripe formation by a Turing mechanism operating at growth zones in the mammalian palate. Nat. Genet. 2012;44(3):348.Federici F., Dupuy L., Laplaze L., Heisler M., Haseloff J. Integrated genetic and computation methods for in planta cytometry. Nat. Methods. 2012;9(5):483.Federici F., Dupuy L., Laplaze L., Heisler M., Haseloff J. Integrated genetic and computation methods for in planta cytometry. Nat. Methods. 2012;9(5):483.Hong J.H., Savina M., Du J., Devendran A., Ramakanth K.K., Tian X., Sim W.S., Mironova V.V., Xu J. A sacrifice-forsurvival mechanism protects root stem cell niche from chilling stress. Cell. 2017; 170(1):102-113.Hong J.H., Savina M., Du J., Devendran A., Ramakanth K.K., Tian X., Sim W.S., Mironova V.V., Xu J. A sacrifice-forsurvival mechanism protects root stem cell niche from chilling stress. Cell. 2017; 170(1):102-113.Jonsson H., Heisler M.G., Shapiro B.E., Meyerowitz E.M., Mjols-ness E. An auxin-driven polarized transport model for phyllotaxis. Proc. Natl. Acad. Sci. USA. 2006;103(5):1633-1638.Jonsson H., Heisler M.G., Shapiro B.E., Meyerowitz E.M., Mjols-ness E. An auxin-driven polarized transport model for phyllotaxis. Proc. Natl. Acad. Sci. USA. 2006;103(5):1633-1638.Lacalli T.C. Modeling the Drosophila pair-rule pattern by reaction-diffusion: gap input and pattern control in a 4-morphogen system. J. Theor. Biol. 1990;144(2):171-194.Lacalli T.C. Modeling the Drosophila pair-rule pattern by reaction-diffusion: gap input and pattern control in a 4-morphogen system. J. Theor. Biol. 1990;144(2):171-194.Lewis J. Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr. Biology. 2003; 13(16):1398-1408.Lewis J. Autoinhibition with transcriptional delay: a simple mechanism for the zebrafish somitogenesis oscillator. Curr. Biology. 2003; 13(16):1398-1408.Likhoshvai V., Ratushny A. Generalized Hill function method for modeling molecular processes. J. Bioinform. Comput. Biol. 2007; 5(02b):521-531.Likhoshvai V., Ratushny A. Generalized Hill function method for modeling molecular processes. J. Bioinform. Comput. Biol. 2007; 5(02b):521-531.Lobet G., Draye X., Perilleux C. An online database for plant image analysis software tools. Plant Methods. 2013;9(1):38.Lobet G., Draye X., Perilleux C. An online database for plant image analysis software tools. Plant Methods. 2013;9(1):38.Merks R.M., Guravage M., Inze D., Beemster G.T. VirtualLeaf: an open-source framework for cell-based modeling of plant tissue growth and development. Plant Physiol. 2011;155(2):656-666.Merks R.M., Guravage M., Inze D., Beemster G.T. VirtualLeaf: an open-source framework for cell-based modeling of plant tissue growth and development. Plant Physiol. 2011;155(2):656-666.Mironova V.V., Omelyanchuk N.A., Novoselova E.S., Doroshkov A.V., Kazantsev F.V., Kochetov A.V., Kolchanov N.A., Mjolsness E., Likhoshvai V.A. Combined in silico/in vivo analysis of mechanisms providing for root apical meristem self-organization and maintenance. Ann. Bot. 2012;110(2):349-360.Mironova V.V., Omelyanchuk N.A., Novoselova E.S., Doroshkov A.V., Kazantsev F.V., Kochetov A.V., Kolchanov N.A., Mjolsness E., Likhoshvai V.A. Combined in silico/in vivo analysis of mechanisms providing for root apical meristem self-organization and maintenance. Ann. Bot. 2012;110(2):349-360.Pound M.P., French A.P., Wells D.M., Bennett M.J., Pridmore T.P. Cell Set: novel software to extract and analyze structured networks of plant cells from confocal images. Plant Cell. 2012;24(4):1353-1361.Pound M.P., French A.P., Wells D.M., Bennett M.J., Pridmore T.P. Cell Set: novel software to extract and analyze structured networks of plant cells from confocal images. Plant Cell. 2012;24(4):1353-1361.Pradal C., Dufour-Kowalski S., Boudon F., Fournier C., Godin C. OpenAlea: a visual programming and component-based software platform for plant modelling. Funct. Plant Biol. 2008;35(10): 751-760.Pradal C., Dufour-Kowalski S., Boudon F., Fournier C., Godin C. OpenAlea: a visual programming and component-based software platform for plant modelling. Funct. Plant Biol. 2008;35(10): 751-760.Raspopovic J., Marcon L., Russo L., Sharpe J. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science. 2014;345(6196):566-570.Raspopovic J., Marcon L., Russo L., Sharpe J. Digit patterning is controlled by a Bmp-Sox9-Wnt Turing network modulated by morphogen gradients. Science. 2014;345(6196):566-570.Schmidt T., Pasternak T., Liu K., Blein T., Aubry-Hivet D., Dovzhenko A., Duerr J., Teale W., Ditengou F.A., Burkhardt H., Ronneber-ger O. The iRoCS Toolbox - 3D analysis of the plant root apical meristem at cellular resolution. Plant J. 2014;77(5):806-814.Schmidt T., Pasternak T., Liu K., Blein T., Aubry-Hivet D., Dovzhenko A., Duerr J., Teale W., Ditengou F.A., Burkhardt H., Ronneber-ger O. The iRoCS Toolbox - 3D analysis of the plant root apical meristem at cellular resolution. Plant J. 2014;77(5):806-814.Shampine L.F., Reichelt M.W. The MATLAB ODE suite. SIAM J. Sci. Comput. 1997;18(1):1-22.Shampine L.F., Reichelt M.W. The MATLAB ODE suite. SIAM J. Sci. Comput. 1997;18(1):1-22.Shampine L.F., Reichelt M.W., Kierzenka J.A. Solving index-1 DAEs in MATLAB and Simulink. SIAM Rev. 1999;41(3):538-552.Shampine L.F., Reichelt M.W., Kierzenka J.A. Solving index-1 DAEs in MATLAB and Simulink. SIAM Rev. 1999;41(3):538-552.Shapiro B.E., Meyerowitz E., Mjolsness E. Using cellzilla for plant growth simulations at the cellular level. Front. Plant Sci. 2013;4:408.Shapiro B.E., Meyerowitz E., Mjolsness E. Using cellzilla for plant growth simulations at the cellular level. Front. Plant Sci. 2013;4:408.Shimojo H., Kageyama R. Oscillatory control of Deltalike1 in somi-togenesis and neurogenesis: a unified model for different oscillatory dynamics. Semin. Cell Dev. Biol. 2016;49:76-82.Shimojo H., Kageyama R. Oscillatory control of Deltalike1 in somi-togenesis and neurogenesis: a unified model for different oscillatory dynamics. Semin. Cell Dev. Biol. 2016;49:76-82.Smith R.S., Guyomarc’h S., Mandel T., Reinhardt D., Kuhlemeier C., Prusinkiewicz P. A plausible model of phyllotaxis. Proc. Natl. Acad. Sci. USA. 2006;103(5):1301-1306.Smith R.S., Guyomarc’h S., Mandel T., Reinhardt D., Kuhlemeier C., Prusinkiewicz P. A plausible model of phyllotaxis. Proc. Natl. Acad. Sci. USA. 2006;103(5):1301-1306.Tomlin C.J., Axelrod J.D. Biology by numbers: mathematical modelling in developmental biology. Nat. Rev. Genet. 2007;8(5):331.Tomlin C.J., Axelrod J.D. Biology by numbers: mathematical modelling in developmental biology. Nat. Rev. Genet. 2007;8(5):331.Turing A.M. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 1952;237:37-72.Turing A.M. The chemical basis of morphogenesis. Phil. Trans. R. Soc. Lond. B. Biol. Sci. 1952;237:37-72.Zubairova U.S., Verman P.Y., Oshchepkova P.A., Elsukova A.S., Doroshkov A.V. LSM-W2: laser scanning microscopy worker for wheat leaf surface morphology. BMC Syst. Biol. 2019;13(1):22.Zubairova U.S., Verman P.Y., Oshchepkova P.A., Elsukova A.S., Doroshkov A.V. LSM-W2: laser scanning microscopy worker for wheat leaf surface morphology. BMC Syst. Biol. 2019;13(1):22.

The authors declare that there are no conflicts of interest present.