Real-time tracking of root hair nucleus morphodynamics using a microfluidic approach.
Arabidopsis
/ cytology
Arabidopsis Proteins
/ genetics
Cell Nucleus
/ physiology
Lab-On-A-Chip Devices
Membrane Proteins
/ genetics
Microfluidics
/ instrumentation
Microscopy, Confocal
/ methods
Microtubule-Associated Proteins
/ genetics
Nuclear Proteins
/ genetics
Plant Cells
Plant Roots
/ cytology
Plants, Genetically Modified
Time-Lapse Imaging
Arabidopsis thaliana
live cell imaging
microfluidics
nucleus
root hair
single cell
technical advance
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
10 2021
10 2021
Historique:
revised:
06
09
2021
received:
08
06
2021
accepted:
13
09
2021
pubmed:
26
9
2021
medline:
27
1
2022
entrez:
25
9
2021
Statut:
ppublish
Résumé
Root hairs (RHs) are tubular extensions of root epidermal cells that favour nutrient uptake and microbe interactions. RHs show a fast apical growth, constituting a unique single cell model system for analysing cellular morphodynamics. In this context, live cell imaging using microfluidics recently developed to analyze root development is appealing, although high-resolution imaging is still lacking to enable an investigation of the accurate spatiotemporal morphodynamics of organelles. Here, we provide a powerful coverslip based microfluidic device (CMD) that enables us to capture high resolution confocal imaging of Arabidopsis RH development with real-time monitoring of nuclear movement and shape changes. To validate the setup, we confirmed the typical RH growth rates and the mean nuclear positioning previously reported with classical methods. Moreover, to illustrate the possibilities offered by the CMD, we have compared the real-time variations in the circularity, area and aspect ratio of nuclei moving in growing and mature RHs. Interestingly, we observed higher aspect ratios in the nuclei of mature RHs, correlating with higher speeds of nuclear migration. This observation opens the way for further investigations of the effect of mechanical constraints on nuclear shape changes during RH growth and nuclear migration and its role in RH and plant development.
Substances chimiques
Arabidopsis Proteins
0
Membrane Proteins
0
Microtubule-Associated Proteins
0
Nuclear Proteins
0
SUN2 protein, Arabidopsis
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
303-313Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Agudelo, C.G., Sanati, A., Ghanbari, M., Packirisamy, M. & Geitmann, A. (2012) A microfluidic platform for the investigation of elongation growth in pollen tubes. Journal of Micromechanics and Microengineering, 22, 115009. https://doi.org/10.1088/0960-1317/22/11/115009
Almonacid, M., Jord, A.A., El Hayek, S., Othmani, A., Coulpier, F., Lemoine, S. et al. (2019) Active fluctuations of the nuclear envelope shape the transcriptional dynamics in oocytes. Developmental Cell, 51, 147-157.
Aufrecht, J.A., Ryan, J.M., Hasim, S., Allison, D.P., Nebenführ, A., Doktycz, M.J. et al. (2017) Imaging the root hair morphology of Arabidopsis seedlings in a two-layer microfluidic platform. Journal of Visualized Experiments: Jove, 126. https://doi.org/10.3791/55971
Balakrishnan, S., Raju, S.R., Barua, A. & Ananthasuresh, G.K. (2020) Predicting the tension in actin cytoskeleton from the nucleus shape. bioRxiv. https://www.biorxiv.org/content/early/2020/08/29/2020.08.28.272435
Bouhedda, F., Cubi, R., Baudrey, S. & Ryckelynck, M. (2021) μIVC-Seq: a method for ultrahigh-throughput development and functional characterization of small RNAs. Methods in Molecular Biology, 2300, 203-237.
Brechenmacher, L., Nguyen, T.H.N., Hixson, K., Libault, M., Aldrich, J., Pasa Tolic, L. et al. (2012) Identification of soybean proteins from a single cell type: the root hair. Proteomics, 12, 3365-3373.
Brochhausen, L., Maisch, J. & Nick, P. (2016) Break of symmetry in regenerating tobacco protoplasts is independent of nuclear positioning. Journal of Integrative Plant Biology, 58, 799-812.
Busch, W., Moore, B.T., Martsberger, B., Mace, D.L., Twigg, R.W., Jung, J. et al. (2012) A microfluidic device and computational platform for high-throughput live imaging of gene expression. Nature Methods, 9, 1101-1106.
Camilleri, C., Azimzadeh, J., Pastuglia, M., Bellini, C., Grandjean, O. & Bouchez, D. (2002) The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. The Plant Cell, 14, 833-845.
Chu, F.Y., Haley, S.C. & Zidovska, A. (2017) On the origin of shape fluctuations of the cell nucleus. Proceedings of the National Academy of Sciences of the United States of America, 114, 10338-10343.
Chytilova, E., Macas, J., Sliwinska, E., Rafelski, S.M., Lambert, G.M. & Galbraith, D.W. (2000) Nuclear dynamics in Arabidopsis thaliana. Molecular Biology of the Cell, 11, 2733-2741.
Dolan, L., Duckett, C.M., Grierson, C., Linstead, P., Schneider, K., Lawson, E. et al. (1994) Clonal relationships and cell patterning in the root epidermis of Arabidopsis. Development, 120, 2465-2474.
Dorland, Y.L., Cornelissen, A.S., Kuijk, C., Tol, S., Hoogenboezem, M., van Buul, J.D. et al. (2019) Nuclear shape, protrusive behaviour and in vivo retention of human bone marrow mesenchymal stromal cells is controlled by Lamin-A/C expression. Scientific Reports, 9, 1-15.
Fal, K., Korsbo, N., Alonso-Serra, J., Teles, J., Liu, M., Refahi, Y. et al. (2021) Tissue folding at the organ-meristem boundary results in nuclear compression and chromatin compaction. Proceedings of the National Academy of Sciences USA, 118. https://doi.org/10.1073/pnas.2017859118
Fendrych, M., Akhmanova, M., Merrin, J., Glanc, M., Hagihara, S., Takahashi, K. et al. (2018) Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nature Plants, 4, 453-459.
Goswami, R., Asnacios, A., Hamant, O. & Chabouté, M.E. (2020) Is the plant nucleus a mechanical rheostat? Current Opinion in Plant Biology, 57, 155-163. https://doi.org/10.1016/j.pbi.2020.09.001
Goswami, R., Asnacios, A., Milani, P., Graindorge, S., Houlné, G., Mutterer, J. et al. (2020) Mechanical shielding in plant nuclei. Current Biology, 30, 2013-2025.
Goto, C., Tamura, K., Nishimaki, S., Maruyama, D. & Hara-Nishimura, I. (2020) The nuclear envelope protein KAKU4 determines the migration order of the vegetative nucleus and sperm cells in pollen tubes. Journal of Experimental Botany, 71, 6273-6281.
Graumann, K., Runions, J. & Evans, D.E. (2010) Characterization of SUN-domain proteins at the higher plant nuclear envelope. The Plant Journal, 61, 134-144.
Grierson, C., Nielsen, E., Ketelaarc, T. & Schiefelbein, J. (2014) Root hairs. The Arabidopsis Book, American Society of Plant Biologists, 12, 1-25. https://doi.org/10.1199/tab.0172
Griffis, A.H.N., Groves, N.R., Zhou, X. & Meier, I. (2014) Nuclei in motion: movement and positioning of plant nuclei in development, signaling, symbiosis, and disease. Frontiers in Plant Science, 5, 1-7.
Guichard, M., Garcia, B., de Olalla, E., Stanley, C.E. & Grossmann, G. (2020) Microfluidic systems for plant root imaging. Methods in Cell Biology, 160, 381-404.
Hepler, P.K., Vidali, L. & Cheung, A.Y. (2001) Polarized cell growth in higher plants. Annual Review of Cell and Developmental Biology, 17, 159-187.
Jiang, H., Xu, Z., Aluru, M.R. & Dong, L. (2014) Plant chip for high-throughput phenotyping of Arabidopsis. Lab on a chip, 14, 1281-1293.
Jones, M.A., Shen, J.-J., Fu, Y., Li, H., Yang, Z. & Grierson, C.S. (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. The Plant Cell, 14, 763-776.
Kang, E., Zheng, M., Zhang, Y., Yuan, M., Yalovsky, S., Zhu, L. et al. (2017) The microtubule-associated protein MAP18 affects ROP2 GTPase activity during root hair growth. Plant Physiology, 174, 202-222.
Ketelaar, T., Faivre-Moskalenko, C., Esseling, J.J., Ruijter, N.C.A.D., Grierson, C.S., Dogterom, M. et al. (2002) Positioning of nuclei in Arabidopsis root hairs: an actin-regulated process of tip growth. The Plant Cell, 14, 2941-2955.
Krupinski, P., Bozorg, B., Larsson, A., Pietra, S., Grebe, M. & Jönsson, H. (2016) A model analysis of mechanisms for radial microtubular patterns at root hair initiation sites. Frontiers in Plant Science, 7, https://doi.org/10.3389/fpls.2016.01560
Lan, P., Li, W., Lin, W.D., Santi, S. & Schmidt, W. (2013) Mapping gene activity of Arabidopsis root hairs. Genome Biology, 14(R67), 1-20.
Landrein, B., Kiss, A., Sassi, M., Chauvet, A., Das, P., Cortizo, M. et al. (2015) Mechanical stress contributes to the expression of the STM homeobox gene in Arabidopsis shoot meristems. Elife, 4, e07811.
Li, W. & Lan, P. (2015) Re-analysis of RNA-seq transcriptome data reveals new aspects of gene activity in Arabidopsis root hairs. Frontiers in Plant Science, 6, 421.
Libault, M., Farmer, A., Brechenmacher, L., Drnevich, J., Langley, R.J., Bilgin, D.D. et al. (2010) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiology, 152, 541-552.
Lockhart, J.A. (1965) An analysis of irreversible plant cell elongation. Journal of Theoretical Biology, 8, 264-275.
Massalha, H., Korenblum, E., Malitsky, S., Shapiro, O.H. & Aharoni, A. (2017) Live imaging of root-bacteria interactions in a microfluidics setup. Proceedings of the National Academy of Sciences of the United States of America, 114, 4549-4554.
Meier, I., Griffis, A.H., Groves, N.R. & Wagner, A. (2016) Regulation of nuclear shape and size in plants. Current Opinion in Cell Biology, 40, 114-123.
Misra, C.S., Santos, M.R., Rafael-Fernandes, M., Martins, N.P., Monteiro, M. & Becker, J.D. (2019) Transcriptomics of Arabidopsis sperm cells at single-cell resolution. Plant Reproduction, 32, 29-38.
Newman-Griffis, A.H., del Cerro, P., Charpentier, M. & Meier, I. (2019) Medicago LINC complexes function in nuclear morphology, nuclear movement, and root nodule symbiosis. Plant Physiology, 179, 491-506.
Parashar, A. & Pandey, S. (2011) Plant-in-chip: microfluidic system for studying root growth and pathogenic interactions in Arabidopsis. Applied Physics Letters, 98, https://doi.org/10.1063/1.3604788
Petricka, J.J., Schauer, M.A., Megraw, M., Breakfield, N.W., Thompson, J.W., Georgiev, S. et al. (2012) The protein expression landscape of the Arabidopsis root. Proceedings of the National Academy of Sciences of the United States of America, 109, 6811-6818.
Qiao, Z., Pingault, L., Zogli, P., Langevin, M., Rech, N., Farmer, A. et al. (2017) A comparative genomic and transcriptomic analysis at the level of isolated root hair cells reveals new conserved root hair regulatory elements. Plant Molecular Biology, 94, 641-655.
Ryu, K.H., Huang, L., Kang, H.M. & Schiefelbein, J. (2019) Single-cell RNA sequencing resolves molecular relationships among individual plant cells. Plant Physiology, 179, 1444-1456.
Satterlee, J.W., Strable, J. & Scanlon, M.J. (2021) Plant stem-cell organization and differentiation at single-cell resolution. Proceedings of the National Academy of Sciences of the United States of America, 117, 33689-33699.
Shibata, M., Breuer, C., Kawamura, A., Clark, N.M., Rymen, B., Braidwood, L. et al. (2018) GTL1 and DF1 regulate root hair growth through transcriptional repression of ROOT HAIR DEFECTIVE 6-LIKE 4 in Arabidopsis. Development, 145, https://doi.org/10.1242/dev.159707
Sieberer, B.J., Ketelaar, T., Esseling, J.J. & Emons, A.M.C. (2005) Microtubules guide root hair tip growth. New Phytologist, 167, 711-719.
Stanley, C.E., Shrivastava, J., Brugman, R., Heinzelmann, E., van Swaay, D. & Grossmann, G. (2018) Dual-flow-RootChip reveals local adaptations of roots towards environmental asymmetry at the physiological and genetic levels. New Phytologist, 217, 1357-1369.
Sun, L., Liu, L., Lin, X., Xia, Z., Cao, J., Xu, S. et al. (2021) Microfluidic devices for monitoring the root morphology of Arabidopsis thaliana in situ. Analytical Sciences, 37, 605-611.
Tamura, K., Iwabuchi, K., Fukao, Y., Kondo, M., Okamoto, K., Ueda, H. et al. (2013) Myosin XI-i links the nuclear membrane to the cytoskeleton to control nuclear movement and shape in Arabidopsis. Current Biology, 23, 1776-1781.
Van Bruaene, N., Joss, G., Thas, O. & Van Oostveldt, P. (2003) Four-dimensional imaging and computer-assisted track analysis of nuclear migration in root hairs of Arabidopsis thaliana. Journal of Microscopy, 211, 167-178.
Van Bruaene, N., Joss, G. & Van Oostveldt, P. (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiology, 136, 3905-3919.
Vassileva, V.N., Kouchi, H. & Ridge, R.W. (2005) Microtubule dynamics in living root hairs: transient slowing by lipochitin oligosaccharide nodulation signals. The Plant Cell, 17, 1777-1787.
Versaevel, M., Grevesse, T. & Gabriele, S. (2012) Spatial coordination between cell and nuclear shape within micropatterned endothelial cells. Nature Communications, 14, 1-11.
Volgger, M., Lang, I., Ovecka, M. & Lichtscheidl, I. (2010) Plasmolysis and cell wall deposition in wheat root hairs under osmotic stress. Protoplasma, 243, 51-62.
Wymer, C.L., Bibikova, T.N. & Gilroy, S. (1997) Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. The Plant Journal, 12, 427-439.
Yamada, M. & Goshima, G. (2018) The KCH kinesin drives nuclear transport and cytoskeletal coalescence to promote tip cell growth in Physcomitrella patens. The Plant Cell, 30, 1496-1510.
Yi, K., Menand, B., Bell, E. & Dolan, L. (2010) A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nature Genetics, 42, 264-267.
Zhang, S., Liu, J., Xue, X., Tan, K., Wang, C. & Su, H. (2019) The migration direction of hair cell nuclei is closely related to the perinuclear actin filaments in Arabidopsis. Biochemical and Biophysical Research Communications, 519, 783-789.