Katanin Effects on Dynamics of Cortical Microtubules and Mitotic Arrays in Arabidopsis thaliana Revealed by Advanced Live-Cell Imaging
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
28596780
PubMed Central
PMC5443160
DOI
10.3389/fpls.2017.00866
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, cell division, interphase, katanin, live imaging, microtubules, preprophase band, super resolution microscopy,
- Publikační typ
- časopisecké články MeSH
Katanin is the only microtubule severing protein identified in plants so far. Previous studies have documented its role in regulating cortical microtubule organization during cell growth and morphogenesis. Although, some cell division defects are reported in KATANIN mutants, it is not clear whether or how katanin activity may affect microtubule dynamics in interphase cells, as well as the progression of mitosis and cytokinesis and the orientation of cell division plane (CDP). For this reason, we characterized microtubule organization and dynamics in growing and dividing cotyledon cells of Arabidopsis ktn1-2 mutant devoid of KATANIN 1 activity. In interphase epidermal cells of ktn1-2 cortical microtubules exhibited aberrant and largely isotropic organization, reduced bundling and showed excessive branched microtubule formation. End-wise microtubule dynamics were not much affected, although a significantly slower rate of microtubule growth was measured in the ktn1-2 mutant where microtubule severing was completely abolished. KATANIN 1 depletion also brought about significant changes in preprophase microtubule band (PPB) organization and dynamics. In this case, many PPBs exhibited unisided organization and splayed appearance while in most cases they were broader than those of wild type cells. By recording PPB maturation, it was observed that PPBs in the mutant narrowed at a much slower pace compared to those in Col-0. The form of the mitotic spindle and the phragmoplast was not much affected in ktn1-2, however, the dynamics of both processes showed significant differences compared to wild type. In general, both mitosis and cytokinesis were considerably delayed in the mutant. Additionally, the mitotic spindle and the phragmoplast exhibited extensive rotational motions with the equatorial plane of the spindle being essentially uncoupled from the division plane set by the PPB. However, at the onset of its formation the phragmoplast undergoes rotational motion rectifying the expansion of the cell plate to match the original cell division plane. Conclusively, KATANIN 1 contributes to microtubule dynamics during interphase, regulates PPB formation and maturation and is involved in the positioning of the mitotic spindle and the phragmoplast.
Zobrazit více v PubMed
Azimzadeh J., Nacry P., Christodoulidou A., Drevensek S., Camilleri C., Amiour N., et al. . (2008). Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20, 2146–2159. 10.1105/tpc.107.056812 PubMed DOI PMC
Beck M., Komis G., Müller J., Menzel D., Samaj J. (2010). Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell 22, 755–771. 10.1105/tpc.109.071746 PubMed DOI PMC
Beck M., Komis G., Ziemann A., Menzel D., Samaj J. (2011). Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol. 189, 1069–1083. 10.1111/j.1469-8137.2010.03565.x PubMed DOI
Blancaflor E. B., Hasenstein K. H. (1993). Organization of cortical microtubules in graviresponding maize roots. Planta 191, 231–237. PubMed
Blancaflor E. B., Hasenstein K. H. (1995a). Growth and microtubule orientation of Zea mays roots subjected to osmotic stress. Int. J. Plant Sci. 156, 774–783. 10.1086/297301 PubMed DOI
Blancaflor E. B., Hasenstein K. H. (1995b). Time course and auxin sensitivity of cortical microtubule reorientation in maize roots. Protoplasma 185, 72–82. 10.1007/BF01272755 PubMed DOI
Burk D. H., Liu B., Zhong R., Morrison W. H., Ye Z. H. (2001). A Katanin-like protein regulates normal cell wall biosynthesis and cell elongation. Plant Cell 13, 807–828. 10.1105/tpc.13.4.807 PubMed DOI PMC
Buschmann H., Chan J., Sanchez-Pulido L., Andrade-Navarro M. A., Doonan J. H., Lloyd C. W. (2006). Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr. Biol. 16, 1938–1943. 10.1016/j.cub.2006.08.028 PubMed DOI
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. Plant Cell 14, 833–845. 10.1105/tpc.010402 PubMed DOI PMC
Chen X., Grandont L., Li H., Hauschild R., Paque S., Abuzeineh A., et al. . (2014). Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules. Nature 516, 90–93. 10.1038/nature13889 PubMed DOI PMC
Dhonukshe P., Gadella T. W., Jr. (2003). Alteration of microtubule dynamic instability during preprophase band formation revealed by yellow fluorescent protein-CLIP170 microtubule plus-end labeling. Plant Cell 15, 597–611. 10.1105/tpc.008961 PubMed DOI PMC
Dovgalyuk A., Kalynyak T., Blume Y. B. (2003). Heavy metals have a different action from aluminium in disrupting microtubules in Allium cepa meristematic cells. Cell Biol. Int. 27, 193–195. 10.1016/S1065-6995(02)00334-7 PubMed DOI
Fishel E. A., Dixit R. (2013). Role of nucleation in cortical microtubule array organization: variations on a theme. Plant J. 75, 270–277. 10.1111/tpj.12166 PubMed DOI
Granger C., Cyr R. (2001). Use of abnormal preprophase bands to decipher division plane determination. J. Cell Sci. 114, 599–607. PubMed
Gunning B. E., Hardham A. R., Hughes J. E. (1978). Pre-prophase bands of microtubules in all categories of formative and proliferative cell division in Azolla roots. Planta 143, 145–160. 10.1007/BF00387786 PubMed DOI
Hamada T. (2014). Microtubule organization and microtubule-associated proteins in plant cells. Int. Rev. Cell Mol. Biol. 312, 1–52. 10.1016/B978-0-12-800178-3.00001-4 PubMed DOI
Higaki T., Kutsuna N., Sano T., Kondo N., Hasezawa S. (2010). 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. Plant J. 61, 156–165. 10.1111/j.1365-313X.2009.04032.x PubMed DOI
Janski N., Masoud K., Batzenschlager M., Herzog E., Evrard J. L., Houlne G., et al. . (2012). The GCP3-interacting proteins GIP1 and GIP2 are required for γ–tubulin complex protein localization, spindle integrity, and chromosomal stability. Plant Cell 24, 1171–1187. 10.1105/tpc.111.094904 PubMed DOI PMC
Karahara I., Suda J., Tahara H., Yokota E., Shimmen T., Misaki K., et al. . (2009). The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant J. 57, 819–831. 10.1111/j.1365-313X.2008.03725.x PubMed DOI
Kartasalo K., Pölönen R. P., Ojala M., Rasku J., Lekkala J., Aalto-Setälä K., et al. . (2015). CytoSpectre: a tool for spectral analysis of oriented structures on cellular and subcellular levels. BMC Bioinformatics 16:344. 10.1186/s12859-015-0782-y PubMed DOI PMC
Keech O., Pesquet E., Gutierrez L., Ahad A., Bellini C., Smith S. M., et al. . (2010). Leaf senescence is accompanied by an early disruption of the microtubule network in Arabidopsis. Plant Physiol. 154, 1710–1720. 10.1104/pp.110.163402 PubMed DOI PMC
Kojo K. H., Higaki T., Kutsuna N., Yoshida Y., Yasuhara H., Hasezawa S. (2013). Roles of cortical actin microfilament patterning in division plane orientation in plants. Plant Cell Physiol. 54, 1491–1503. 10.1093/pcp/pct093 PubMed DOI
Kojo K. H., Yasuhara H., Hasezawa S. (2014). Time-sequential observation of spindle and phragmoplast orientation in BY-2 cells with altered cortical actin microfilament patterning. Plant Signal. Behav. 9:e29579. 10.4161/psb.29579 PubMed DOI PMC
Komis G., Mistrik M., Samajová O., Doskočilová A., Ovečka M., Illés P., et al. . (2014). Dynamics and organization of cortical microtubules as revealed by superresolution structured illumination microscopy. Plant Physiol. 165, 129–148. 10.1104/pp.114.238477 PubMed DOI PMC
Komis G., Mistrik M., Šamajová O., Ovečka M., Bartek J., Šamaj J. (2015). Superresolution live imaging of plant cells using structured illumination microscopy. Nat. Protoc. 10, 1248–1263. 10.1038/nprot.2015.083 PubMed DOI
Krasylenko Y. A., Yemets A. I., Sheremet Y. A., Blume Y. B. (2012). Nitric oxide as a critical factor for perception of UV-B irradiation by microtubules in Arabidopsis. Physiol. Plant. 145, 505–515. 10.1111/j.1399-3054.2011.01530.x PubMed DOI
Lei L., Singh A., Bashline L., Li S., Yingling Y. G., Gu Y. (2015). CELLULOSE SYNTHASE INTERACTIVE1 is required for fast recycling of cellulose synthase complexes to the plasma membrane in Arabidopsis. Plant Cell 27, 2926–2940. 10.1105/tpc.15.00442 PubMed DOI PMC
Lin D., Cao L., Zhou Z., Zhu L., Ehrhardt D., Yang Z., et al. . (2013). Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr. Biol. 23, 290–297. 10.1016/j.cub.2013.01.022 PubMed DOI
Lindeboom J. J., Nakamura M., Hibbel A., Shundyak K., Gutierrez R., Ketelaar T., et al. . (2013). A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342:e1245533. 10.1126/science.1245533 PubMed DOI
Lipka E., Herrmann A., Mueller S. (2015). Mechanisms of plant cell division. Wiley Interdiscip. Rev. Dev. Biol. 4, 391–405. 10.1002/wdev.186 PubMed DOI
Liu T., Tian J., Wang G., Yu Y., Wang C., Ma Y., et al. . (2014). Augmin triggers microtubule-dependent microtubule nucleation in interphase plant cells. Curr. Biol. 24, 2708–2713. 10.1016/j.cub.2014.09.053 PubMed DOI
Loughlin R., Wilbur J. D., McNally F. J., Nédélec F. J., Heald R. (2011). Katanin contributes to interspecies spindle length scaling in Xenopus. Cell 147, 1397–1407. 10.1016/j.cell.2011.11.014 PubMed DOI PMC
Lucas J. R., Courtney S., Hassfurder M., Dhingra S., Bryant A., Shaw S. L. (2011). Microtubule-associated proteins MAP65-1 and MAP65-2 positively regulate axial cell growth in etiolated Arabidopsis hypocotyls. Plant Cell 23, 1889–1903. 10.1105/tpc.111.084970 PubMed DOI PMC
Lucas J. R., Shaw S. L. (2012). MAP65-1 and MAP65-2 promote cell proliferation and axial growth in Arabidopsis roots. Plant J. 71, 454–463. 10.1111/j.1365-313x.2012.05002.x PubMed DOI
Mace A., Wang W. (2015). Modelling the role of catastrophe, crossover and katanin-mediated severing in the self-organisation of plant cortical microtubules. IET Syst. Biol. 9, 277–284. 10.1049/iet-syb.2015.0022 PubMed DOI PMC
Marcus A. I., Dixit R., Cyr R. J. (2005). Narrowing of the preprophase microtubule band is not required for cell division plane determination in cultured plant cells. Protoplasma 226, 169–174. 10.1007/s00709-005-0119-1 PubMed DOI
McNally F. J., Vale R. D. (1993). Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75, 419–429. 10.1016/0092-8674(93)90377-3 PubMed DOI
Müller S., Han S., Smith L. G. (2006). Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr. Biol. 16, 888–894. 10.1016/j.cub.2006.03.034 PubMed DOI
Murata T., Sano T., Sasabe M., Nonaka S., Higashiyama T., Hasezawa S., et al. . (2013). Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat. Commun. 4:1967. 10.1038/ncomms2967 PubMed DOI PMC
Murata T., Sonobe S., Baskin T. I., Hyodo S., Hasezawa S., Nagata T., et al. . (2005). Microtubule-dependent microtubule nucleation based on recruitment of gamma-tubulin in higher plants. Nat. Cell Biol. 7, 961–968. 10.1038/ncb1306 PubMed DOI
Muratov A., Baulin V. A. (2015). Mechanism of dynamic reorientation of cortical microtubules due to mechanical stress. Biophys. Chem. 207, 82–89. 10.1016/j.bpc.2015.09.004 PubMed DOI
Nakamura M. (2015). Microtubule nucleating and severing enzymes for modifying microtubule array organization and cell morphogenesis in response to environmental cues. New Phytol. 205, 1022–1027. 10.1111/nph.12932 PubMed DOI
Nakamura M., Ehrhardt D. W., Hashimoto T. (2010). Microtubule and katanin-dependent dynamics of microtubule nucleation complexes in the acentrosomal Arabidopsis cortical array. Nat. Cell Biol. 12, 1064–1070. 10.1038/ncb2110 PubMed DOI
Nyporko A. Y., Demchuk O. N., Blume Y. B. (2003). Cold adaptation of plant microtubules: structural interpretation of primary sequence changes in a highly conserved region of alpha-tubulin. Cell Biol. Int. 27, 241–243. 10.1016/S1065-6995(02)00342-6 PubMed DOI
Panteris E., Adamakis I. D. (2012). Aberrant microtubule organization in dividing root cells of p60-katanin mutants. Plant Signal. Behav. 7, 16–18. 10.4161/psb.7.1.18358 PubMed DOI PMC
Panteris E., Adamakis I. D., Voulgari G., Papadopoulou G. (2011). A role for katanin in plant cell division: microtubule organization in dividing root cells of fra2 and lue1 Arabidopsis thaliana mutants. Cytoskeleton 68, 401–413. 10.1002/cm.20522 PubMed DOI
Paredez A. R., Somerville C. R., Ehrhardt D. W. (2006). Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312, 1491–1495. 10.1126/science.1126551 PubMed DOI
Pickett-Heaps J. D., Northcote D. H. (1966). Organisation of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J. Cell Sci. 1, 109–120. PubMed
Rasmussen C. G., Humphries J. A., Smith L. G. (2011). Determination of symmetric and asymmetric division planes in plant cells. Annu. Rev. Plant Biol. 62, 387–409. 10.1146/annurev-arplant-042110-103802 PubMed DOI
Roll-Mecak A., Vale R. D. (2005). The Drosophila homologue of the hereditary spastic paraplegia protein, spastin, severs and disassembles microtubules. Curr. Biol. 15, 650–655. 10.1016/j.cub.2005.02.029 PubMed DOI
Sasabe M., Kosetsu K., Hidaka M., Murase A., Machida Y. (2011). Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant Signal. Behav. 6, 743–747. 10.4161/psb.6.5.15146 PubMed DOI PMC
Sassi M., Ali O., Boudon F., Cloarec G., Abad U., Cellier C., et al. . (2014). An auxin-mediated shift toward growth isotropy promotes organ formation at the shoot meristem in Arabidopsis. Curr. Biol. 24, 2335–2342. 10.1016/j.cub.2014.08.036 PubMed DOI
Schaefer E., Belcram K., Uyttewaal M., Duroc Y., Goussot M., Legland D., et al. . (2017). The preprophase band of microtubules controls the robustness of division orientation in plants. Science 356, 186–189. 10.1126/science.aal3016 PubMed DOI
Shaw S. L., Kamyar R., Ehrhardt D. W. (2003). Sustained microtubule treadmilling in Arabidopsis cortical arrays. Science 300, 1715–1718. 10.1126/science.1083529 PubMed DOI
Soga K., Yamaguchi A., Kotake T., Wakabayashi K., Hoson T. (2010). 1-Aminocyclopropane-1-carboxylic acid ACC-induced reorientation of cortical microtubules is accompanied by a transient increase in the transcript levels of gamma-tubulin complex and katanin genes in azuki bean epicotyls. J. Plant Physiol. 167, 1165–1171. 10.1016/j.jplph.2010.04.001 PubMed DOI
Stoppin-Mellet V., Gaillard J., Vantard M. (2002). Functional evidence for in vitro microtubule severing by the plant katanin homologue. Biochem. J. 365, 337–342. 10.1042/bj20020689 PubMed DOI PMC
Stoppin-Mellet V., Gaillard J., Vantard M. (2006). Katanin's severing activity favors bundling of cortical microtubules in plants. Plant J. 46, 1009–1017. 10.1111/j.1365-313X.2006.02761.x PubMed DOI
Takeuchi M., Karahara I., Kajimura N., Takaoka A., Murata K., Misaki K., et al. . (2016). Single microfilaments mediate the early steps of microtubule bundling during preprophase band formation in onion cotyledon epidermal cells. Mol. Biol. Cell 27, 1809–1820. 10.1091/mbc.E15-12-0820 PubMed DOI PMC
Uyttewaal M., Burian A., Alim K., Landrein B., Borowska-Wykręt D., Dedieu A., et al. . (2012). Mechanical stress acts via katanin to amplify differences in growth rate between adjacent cells in Arabidopsis. Cell 149, 439–451. 10.1016/j.cell.2012.02.048 PubMed DOI
Van Damme D., Vanstraelen M., Geelen D. (2007). Cortical division zone establishment in plant cells. Trends Plant Sci. 12, 458–464. 10.1016/j.tplants.2007.08.011 PubMed DOI
Verde F., Dogterom M., Stelzer E., Karsenti E., Leibler S. (1992). Control of microtubule dynamics and length by cyclin A- and cyclin B-dependent kinases in Xenopus egg extracts. J. Cell Biol. 118, 1097–1108. 10.1083/jcb.118.5.1097 PubMed DOI PMC
Vos J. W., Dogterom M., Emons A. M. (2004). Microtubules become more dynamic but not shorter during preprophase band formation: a possible “search-and-capture” mechanism for microtubule translocation. Cell Motil. Cytoskeleton 57, 246–258. 10.1002/cm.10169 PubMed DOI
Walker K. L., Müller S., Moss D., Ehrhardt D. W., Smith L. G. (2007). Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr. Biol. 17, 1827–1836. 10.1016/j.cub.2007.09.063 PubMed DOI PMC
Webb M., Jouannic S., Foreman J., Linstead P., Dolan L. (2002). Cell specification in the Arabidopsis root epidermis requires the activity of ECTOPIC ROOT HAIR 3-a katanin-p60 protein. Development 129, 123–131. PubMed
Wightman R., Chomicki G., Kumar M., Carr P., Turner S. R. (2013). SPIRAL2 determines plant microtubule organization by modulating microtubule severing. Curr. Biol. 23, 1902–1907. 10.1016/j.cub.2013.07.061 PubMed DOI PMC
Wightman R., Turner S. R. (2007). Severing at sites of microtubule crossover contributes to microtubule alignment in cortical arrays. Plant J. 52, 742–751. 10.1111/j.1365-313X.2007.03271.x PubMed DOI
Wightman R., Turner S. R. (2008). A novel mechanism important for the alignment of microtubules. Plant Signal. Behav. 3, 238–239. 10.4161/psb.3.4.5140 PubMed DOI PMC
Xu X. M., Zhao Q., Rodrigo-Peiris T., Brkljacic J., He C. S., Müller S., et al. . (2008). RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc. Natl. Acad. Sci. U.S.A. 105, 18637–18642. 10.1073/pnas.0806157105 PubMed DOI PMC
Zhang D., Rogers G. C., Buster D. W., Sharp D. J. (2007). Three microtubule severing enzymes contribute to the “Pacman-flux” machinery that moves chromosomes. J. Cell Biol. 177, 231–242. 10.1083/jcb.200612011 PubMed DOI PMC
Zhang Q., Fishel E., Bertroche T., Dixit R. (2013). Microtubule severing at crossover sites by katanin generates ordered cortical microtubule arrays in Arabidopsis. Curr. Biol. 23, 2191–2195. 10.1016/j.cub.2013.09.018 PubMed DOI
Imaging plant cells and organs with light-sheet and super-resolution microscopy
Analysis of formin functions during cytokinesis using specific inhibitor SMIFH2
Phosphorylation of Plant Microtubule-Associated Proteins During Cell Division
Advances in Imaging Plant Cell Dynamics
Katanin: A Sword Cutting Microtubules for Cellular, Developmental, and Physiological Purposes