Comprehensive and quantitative analysis of intracellular structure polarization at the apical–basal axis in elongating Arabidopsis zygotes

A comprehensive and quantitative evaluation of multiple intracellular structures or proteins is a promising approach to provide a deeper understanding of and new insights into cellular polarity. In this study, we developed an image analysis pipeline to obtain intensity profiles of fluorescent probes along the apical–basal axis in elongating Arabidopsis thaliana zygotes based on two-photon live-cell imaging data. This technique showed the intracellular distribution of actin filaments, mitochondria, microtubules, and vacuolar membranes along the apical–basal axis in elongating zygotes from the onset of cell elongation to just before asymmetric cell division. Hierarchical cluster analysis of the quantitative data on intracellular distribution revealed that the zygote may be compartmentalized into two parts, with a boundary located 43.6% from the cell tip, immediately after fertilization. To explore the biological significance of this compartmentalization, we examined the positions of the asymmetric cell divisions from the dataset used in this distribution analysis. We found that the cell division plane was reproducibly inserted 20.5% from the cell tip. This position corresponded well with the midpoint of the compartmentalized apical region, suggesting a potential relationship between the zygote compartmentalization, which begins with cell elongation, and the position of the asymmetric cell division.

[1]  Moritaka Nakamura,et al.  Cell polarity linked to gravity sensing is generated by protein translocation from statoliths to the plasma membrane , 2023, bioRxiv.

[2]  Satoru Tsugawa,et al.  Coordinate Normalization of Live-Cell Imaging Data Reveals Growth Dynamics of the Arabidopsis Zygote. , 2023, Plant & cell physiology.

[3]  T. Higaki,et al.  Machine learning and feature analysis of the cortical microtubule organization of Arabidopsis cotyledon pavement cells , 2022, Protoplasma.

[4]  Andreas P. Cuny,et al.  Live cell microscopy: From image to insight , 2022, Biophysics reviews.

[5]  G. Goshima,et al.  Division site determination during asymmetric cell division in plants. , 2022, The Plant cell.

[6]  D. Weijers,et al.  Pole position: How plant cells polarize along the axes , 2021, The Plant cell.

[7]  Juan Dong,et al.  Establishing asymmetry: stomatal division and differentiation in plants. , 2021, The New phytologist.

[8]  T. Higashiyama,et al.  Dynamic Rearrangement and Directional Migration of Tubular Vacuoles are Required for the Asymmetric Division of the Arabidopsis Zygote. , 2021, Plant & cell physiology.

[9]  K. Torii.  Stomatal development in the context of epidermal tissues , 2021, Annals of botany.

[10]  T. Higashiyama,et al.  Mitochondrial dynamics and segregation during the asymmetric division of Arabidopsis zygotes , 2020, Quantitative Plant Biology.

[11]  K. Pogliano,et al.  Shaping an Endospore: Architectural Transformations During Bacillus subtilis Sporulation. , 2020, Annual review of microbiology.

[12]  Yusuke Kimata,et al.  Intracellular dynamics and transcriptional regulations in plant zygotes: a case study of Arabidopsis , 2020, Plant Reproduction.

[13]  Jonas Hartmann,et al.  An image-based data-driven analysis of cellular architecture in a developing tissue , 2020, bioRxiv.

[14]  F. Berger,et al.  New cues for body axis formation in plant embryos. , 2019, Current opinion in plant biology.

[15]  T. Higashiyama,et al.  Polar vacuolar distribution is essential for accurate asymmetric division of Arabidopsis zygotes , 2019, Proceedings of the National Academy of Sciences.

[16]  Charles Kervrann,et al.  A quantitative approach for analyzing the spatio-temporal distribution of 3D intracellular events in fluorescence microscopy , 2018, eLife.

[17]  T. Higashiyama,et al.  In Vitro Ovule Cultivation for Live-cell Imaging of Zygote Polarization and Embryo Patterning in Arabidopsis thaliana. , 2017, Journal of visualized experiments : JoVE.

[18]  D. Montell,et al.  Development and dynamics of cell polarity at a glance , 2017, Journal of Cell Science.

[19]  T. Laux,et al.  Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. , 2017, Genes & development.

[20]  Takumi Higaki,et al.  Cytoskeleton dynamics control the first asymmetric cell division in Arabidopsis zygote , 2016, Proceedings of the National Academy of Sciences.

[21]  Paul A. Wiggins,et al.  Genome-scale quantitative characterization of bacterial protein localization dynamics throughout the cell cycle , 2014, Molecular microbiology.

[22]  F. Berger,et al.  Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana , 2014, eLife.

[23]  S. Han,et al.  Homotypic vacuole fusion requires VTI11 and is regulated by phosphoinositides. , 2014, Molecular plant.

[24]  L. Vidali,et al.  Physcomitrella patens: a model for tip cell growth and differentiation. , 2012, Current opinion in plant biology.

[25]  T. Laux,et al.  The origin of the plant body axis. , 2012, Current opinion in plant biology.

[26]  Kerstin Pingel,et al.  50 Years of Image Analysis , 2012 .

[27]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[28]  T. Ueda,et al.  Statistical organelle dissection of Arabidopsis guard cells using image database LIPS , 2012, Scientific Reports.

[29]  G. Jürgens,et al.  Early embryogenesis in flowering plants: setting up the basic body pattern. , 2012, Annual review of plant biology.

[30]  A. Nakano,et al.  The occurrence of 'bulbs', a complex configuration of the vacuolar membrane, is affected by mutations of vacuolar SNARE and phospholipase in Arabidopsis. , 2011, The Plant journal : for cell and molecular biology.

[31]  Shohei Yamaoka,et al.  MIRO1 influences the morphology and intracellular distribution of mitochondria during embryonic cell division in Arabidopsis , 2011, Plant Cell Reports.

[32]  M. Galli,et al.  Paternal Control of Embryonic Patterning in Arabidopsis thaliana , 2009, Science.

[33]  W. Lukowitz,et al.  A MAPKK Kinase Gene Regulates Extra-Embryonic Cell Fate in Arabidopsis , 2004, Cell.

[34]  F. Sack,et al.  Stomatal Development in Arabidopsis , 2002, The arabidopsis book.

[35]  E. Liscum.  Faculty Opinions recommendation of Involvement of the vacuoles of the endodermis in the early process of shoot gravitropism in Arabidopsis. , 2002 .

[36]  M. Morita,et al.  SGR2, a Phospholipase-Like Protein, and ZIG/SGR4, a SNARE, Are Involved in the Shoot Gravitropism of Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010215. , 2002, The Plant Cell Online.

[37]  L. Breiman.  Random Forests , 2001, Encyclopedia of Machine Learning and Data Mining.

[38]  Daisuke Kurihara,et al.  Live-Cell Imaging of Zygotic Intracellular Structures and Early Embryo Pattern Formation in Arabidopsis thaliana. , 2020, Methods in molecular biology.

[39]  A. Hyman,et al.  The first cell cycle of the Caenorhabditis elegans embryo: spatial and temporal control of an asymmetric cell division. , 2011, Results and problems in cell differentiation.

[40]  Natsumaro Kutsuna,et al.  Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. , 2010, The Plant journal : for cell and molecular biology.

[41]  Andy Liaw,et al.  Classification and Regression by randomForest , 2007 .