KATANIN is a well-studied microtubule severing protein affecting microtubule organization and dynamic properties in higher plants. By regulating mitotic and cytokinetic and cortical microtubule arrays it is involved in the progression of cell division and cell division plane orientation. KATANIN is also involved in cell elongation and morphogenesis during plant growth. In this way KATANIN plays critical roles in diverse plant developmental processes including the development of pollen, embryo, seed, meristem, root, hypocotyl, cotyledon, leaf, shoot, and silique. KATANIN-dependent microtubule regulation seems to be under the control of plant hormones. This minireview provides an overview on available KATANIN mutants and discusses advances in our understanding of KATANIN biological roles in plants.

Department of Cell Biology Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Czechia

Zobrazit více v PubMed

Achard P., Cheng H., De Grauwe L., Decat J., Schoutteten H., Moritz T., et al. . (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91–94. 10.1126/science.1118642 PubMed DOI

Anderson P., Kedersha N. (2008). Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 33, 141–150. 10.1016/j.tibs.2007.12.003 PubMed DOI

Bailey M. E., Sackett D. L., Ross J. L. (2015). Katanin severing and binding microtubules are inhibited by tubulin carboxy tails. Biophys. J. 109, 2546–2561. 10.1016/j.bpj.2015.11.011 PubMed DOI PMC

Bichet A., Desnos T., Turner S., Grandjean O., Höfte H. (2001). BOTERO1 is required for normal orientation of cortical microtubules and anisotropic cell expansion in Arabidopsis. Plant J. 25, 137–148. 10.1046/j.1365-313x.2001.00946.x PubMed DOI

Bouquin T., Mattsson O., Naested H., Foster R., Mundy J. (2003). The Arabidopsis lue1 mutant defines a katanin p60 ortholog involved in hormonal control of microtubule orientation during cell growth. J. Cell. Sci. 116, 791–801. 10.1242/jcs.00274 PubMed DOI

Brodersen P., Sakvarelidze-Achard L., Bruun-Rasmussen M., Dunoyer P., Yamamoto Y. Y., Sieburth L., et al. . (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190. 10.1126/science.1159151 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, 807–827. 10.1105/tpc.13.4.807 PubMed DOI PMC

Burk D. H., Ye Z.-H. (2002). Alteration of oriented deposition of cellulose microfibrils by mutation of a katanin-like microtubule-severing protein. Plant Cell 14, 2145–2160. 10.1105/tpc.003947 PubMed DOI PMC

Buschmann H., Fabri C. O., Hauptmann M., Hutzler P., Laux T., Lloyd C. W., et al. . (2004). Helical growth of the Arabidopsis mutant tortifolia1 reveals a plant-specific microtubule-associated protein. Curr. Biol. 14, 1515–1521. 10.1016/j.cub.2004.08.033 PubMed DOI

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

Davis L. J., Odde D. J., Block S. M., Gross S. P. (2002). The importance of lattice defects in katanin-mediated microtubule severing in vitro. Biophys. J. 82, 2916–2927. 10.1016/S0006-3495(02)75632-4 PubMed DOI PMC

Deinum E. E., Tindemans S. H., Lindeboom J. J., Mulder B. M. (2017). How selective severing by katanin promotes order in the plant cortical microtubule array. Proc. Natl. Acad. Sci. U.S.A. 114, 6942–6947. 10.1073/pnas.1702650114 PubMed DOI PMC

Díaz-Valencia J. D., Morelli M. M., Bailey M., Zhang D., Sharp D. J., Ross J. L. (2011). Drosophila katanin-60 depolymerizes and severs at microtubule defects. Biophys. J. 100, 2440–2449. 10.1016/j.bpj.2011.03.062 PubMed DOI PMC

Eckert T., Le D. T., Link S., Friedmann L., Woehlke G. (2012). Spastin's microtubule-binding properties and comparison to katanin. PLoS ONE 7:e50161. 10.1371/journal.pone.0050161 PubMed DOI PMC

Fu X., Richards D. E., Ait-Ali T., Hynes L. W., Ougham H., Peng J., et al. . (2002). Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14, 3191–3200. 10.1105/tpc.006197 PubMed DOI PMC

Gardiner J. (2014). Movement disorders, 2nd Edn, in Use of Arabidopsis to Model Hereditary Spastic Paraplegia and Other Movement Disorders, ed LeDoux M. (Amsterdam: Elsevier Publishers; ), 1136–1142.

Girard C., Chelysheva L., Choinard S., Froger N., Macaisne N., Lemhemdi A., et al. (2015). AAA-ATPase FIDGETIN-LIKE 1 and Helicase FANCM antagonize meiotic crossovers by distinct mechanisms. PLoS Genet. 11:e1005369 10.1371/journal.pgen.1005369 PubMed DOI PMC

Gosh D., Dasgupta D., Guha A. (2012). Models, regulations, and functions of microtubule severing by katanin. ISRN Mol. Biol. 2012:596289 10.5402/2012/596289 PubMed DOI PMC

Gu Y., Deng Z., Paredez A. R., DeBolt S., Wang Z. Y., Somerville C. (2008). Prefoldin 6 is required for normal microtubule dynamics and organization in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 105, 18064–18069. 10.1073/pnas.0808652105 PubMed DOI PMC

Gutierrez-Beltran E., Moschou P. N., Smertenko A. P., Bozhkov P. V. (2015). Tudor staphylococcal nuclease links formation of stress granules and processing bodies with mRNA catabolism in Arabidopsis. Plant Cell 27, 926–943. 10.1105/tpc.114.134494 PubMed DOI PMC

Hartman J. J., Mahr J., McNally K., Okawa K., Iwamatsu A., Thomas S., et al. . (1998). Katanin, a microtubule-severing protein, is a novel AAA ATPase that targets to the centrosome using a WD40-containing subunit. Cell 93, 277–287. 10.1016/S0092-8674(00)81578-0 PubMed DOI

Hartman J. J., Vale R. D. (1999). Microtubule disassembly by ATP-dependent oligomerization of the AAA enzyme katanin. Science 286, 782–785. 10.1126/science.286.5440.782 PubMed DOI

Jiang K., Rezabkova L., Hua S., Liu Q., Capitani G., Maarten A. F., et al. (2017). Microtubule minus-end regulation at spindle poles by an ASPM–katanin complex. Nat. Cell Biol. 19, 480–492. 10.1038/ncb3511 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

Komis G., Luptovčiak I., Ovečka M., Samakovli D., Šamajová O., Šamaj J. (2017). Katanin effects on dynamics of cortical microtubules and mitotic arrays in Arabidopsis thaliana revealed by advanced live-cell imaging. Front. Plant Sci. 8:866. 10.3389/fpls.2017.00866 PubMed DOI PMC

Komorisono M., Ueguchi-Tanaka M., Aichi I., Hasegawa Y., Ashikari M., Kitano H., et al. . (2005). Analysis of the rice mutant dwarf and gladius leaf 1. Aberrant katanin-mediated microtubule organization causes up-regulation of gibberellin biosynthetic genes independently of gibberellin signaling. Plant Physiol. 138, 1982–1993. 10.1104/pp.105.062968 PubMed DOI PMC

Lacroix B., van Dijk J., Gold N. D., Guizetti J., Aldrian-Herrada G., Rogowski K., et al. . (2010). Tubulin polyglutamylation stimulates spastin-mediated microtubule severing. J. Cell Biol. 189, 945–954. 10.1083/jcb.201001024 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 342:1245533. 10.1126/science.1245533 PubMed DOI

Locascio A., Blázquez M. A., Alabadí D. (2013). Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr. Biol. 23, 804–809. 10.1016/j.cub.2013.03.053 PubMed DOI

Loughlin R., Wilbur J. D., McNally F. J., Nédélecm 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 H., Feuerbach F., Kunert K., Grandbastien M.-A., Caboche M. (1995). RNA-mediated transposition of the tobacco retrotransposon Tnt1 in Arabidopsis thaliana. EMBO J. 14, 2364–2373. PubMed PMC

Luesse D. R., DeBlasio S. L., Hangarter R. P. (2010). Integration of Phot1, Phot2, and PhyB signalling in light-induced chloroplast movements. J. Exp. Bot. 61, 4387–4397. 10.1093/jxb/erq242 PubMed DOI PMC

Luo D., Oppenheimer D. G. (1999). Genetic control of trichome branch number in Arabidopsis: the roles of the FURCA loci. Development 126, 5547–5557. PubMed

Luptovciak I., Samakovli D., Komis G., Šamaj J. (2017). KATANIN 1 is essential for embryogenesis and seed formation in Arabidopsis. Front. Plant Sci. 8:728. 10.3389/fpls.2017.00728 PubMed DOI PMC

McClinton R. S., Chandler J. S., Callis J. (2001). cDNA isolation, characterization, and protein intracellular localization of a katanin-like p60 subunit from Arabidopsis thaliana. Protoplasma 216, 181–190. 10.1007/BF02673870 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

McNally K., Audhya A., Oegema K., McNally F. J. (2006). Katanin controls mitotic and meiotic spindle length. J. Cell Biol. 175, 881–891. 10.1083/jcb.200608117 PubMed DOI PMC

McNally K. P., Bazirgan O. A., McNally F. J. (2000). Two domains of p80 katanin regulate microtubule severing and spindle pole targeting by p60 katanin. J. Cell. Sci. 113(Pt 9), 1623–1633. PubMed

Meier C., Bouquin T., Nielsen M. E., Raventos D., Mattsson O., Rocher A., et al. . (2001). Gibberellin response mutants identified by luciferase imaging. Plant J. 25, 509–519. 10.1046/j.1365-313x.2001.00980.x PubMed DOI

Mollet S., Cougot N., Wilczynska A., Dautry F., Kress M., Bertrand E., et al. . (2008). Translationally repressed mRNA transiently cycles through stress granules during Stress. Mol. Biol. Cell 19, 4469–4479. 10.1091/mbc.E08-05-0499 PubMed DOI PMC

Nagawa S., Sawa S., Sato S., Kato T., Tabata S., Fukuda H. (2006). Gene trapping in Arabidopsis reveals genes involved in vascular development. Plant Cell Physiol. 47, 1394–1405. 10.1093/pcp/pcl009 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

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

Reed J. W., Elumalai R. P., Chory J. (1998). Suppressors of an Arabidopsis thaliana phyB mutation identify genes that control light signaling and hypocotyl elongation. Genetics 148, 1295–1310. PubMed PMC

Ren H., Dang X., Cai X., Yu P., Li Y., Zhang S., et al. . (2017). Spatio-temporal orientation of microtubules controls conical cell shape in Arabidopsis thaliana petals. PLoS Genet. 13:e1006851. 10.1371/journal.pgen.1006851 PubMed DOI PMC

Sampathkumar A., Krupinski P., Wightman R., Milani P., Berquand A., Boudaoud A., et al. . (2014). Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. Elife 3:e01967. 10.7554/eLife.01967 PubMed DOI PMC

Santner A., Estelle M. (2009). Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071–1078. 10.1038/nature08122 PubMed DOI

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

Schneider K., Wells B., Dolan L., Roberts K. (1997). Structural and genetic analysis of epidermal cell differentiation in Arabidopsis primary roots. Development 124, 1789–1798. PubMed

Smertenko A., Assaad F., Baluška F., Bezanilla M., Buschmann H., Drakakaki G., et al. . (2017). Plant cytokinesis: terminology for structures and processes. Trends Cell Biol. [Epub ahead of print]. 10.1016/j.tcb.2017.08.008 PubMed DOI

Soga K., Yamaguchi A., Kotake T., Wakabayashi K., Hoson T. (2010a). 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

Soga K., Yamaguchi A., Kotake T., Wakabayashi K., Hoson T. (2010b). Transient increase in the levels of γ-tubulin complex and katanin are responsible for reorientation by ethylene and hypergravity of cortical microtubules. Plant Signal. Behav. 5, 1480–1482. 10.4161/psb.5.11.13561 PubMed DOI PMC

Stoppin-Mellet V., Gaillard J., Timmers T., Neumann E., Conway J., Vantard M. (2007). Arabidopsis katanin binds microtubules using a multimeric microtubule-binding domain. Plant Physiol. Biochem. 45, 867–877. 10.1016/j.plaphy.2007.09.005 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 favours bundling of cortical microtubules in plants. Plant J. 46, 1009–1017. 10.1111/j.1365-313X.2006.02761.x PubMed DOI

Sudo H., Baas P. W. (2010). Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J. Neurosci. 30, 7215–7226. 10.1523/JNEUROSCI.0048-10.2010 PubMed DOI PMC

Suetsugu N., Sato Y., Tsuboi H., Kasahara M., Imaizumi T., Kagawa T., et al. . (2012). The KAC family of kinesin-like proteins is essential for the association of chloroplasts with the plasma membrane in land plants. Plant Cell Physiol. 53, 1854–1865. 10.1093/pcp/pcs133 PubMed DOI

Suetsugu N., Yamada N., Kagawa T., Yonekura H., Uyeda T. Q., Kadota A., et al. . (2010). Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 107, 8860–8865. 10.1073/pnas.0912773107 PubMed DOI PMC

Takáč T., Šamajová O., Pechan T., Luptovčiak I., Šamaj J. (2017). Feedback microtubule control and microtubule-actin cross-talk in Arabidopsis revealed by integrative proteomic and cell biology analysis of KATANIN 1 mutants. Mol. Cell Proteomics 16, 1591–1609. 10.1074/mcp.M117.068015 PubMed DOI PMC

Trehin C., Schrempp S., Chauvet A., Berne-Dedieu A., Thierry A. M., Faure, et al. . (2013). QUIRKY interacts with STRUBBELIG and PAL OF QUIRKY to regulate cell growth anisotropy during Arabidopsis gynoecium development. Development 140, 4807–4817. 10.1242/dev.091868 PubMed DOI

Uyttewaal M., Burian A., Alim K., Landrein B., Borowska-Wykret 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

Valenstein M. L., Roll-Mecak A. (2016). Graded control of microtubule severing by tubulin glutamylation. Cell 164, 911–921. 10.1016/j.cell.2016.01.019 PubMed DOI PMC

Wan L., Wang X., Li S., Hu J., Huang W., Zhu Y. (2014). Overexpression of OsKTN80a, a katanin P80 ortholog, caused the repressed cell elongation and stalled cell division mediated by microtubule apparatus defects in primary root in Oryza sativa. J. Integr. Plant Biol. 56, 622–634. 10.1111/jipb.12170 PubMed DOI

Wang C., Liu W., Wang G., Li J., Dong L., Han L., et al. . (2017). KTN80 confers precision to microtubule severing by specific targeting of katanin complexes in plant cells. EMBO J. [Epub ahead of print]. 10.15252/embj.201796823 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

Zehr E., Szyk A., Piszczek G., Szczesna E., Zuo X., Roll-Mecak A. (2017). Katanin spiral and ring structures shed light on power stroke for microtubule severing. Nat. Struct. Mol. Biol. 24, 717–725. 10.1038/nsmb.3448 PubMed DOI PMC

Zhang Q., Fischel E., Bertoche T., Dixit R. (2013). Microtubule severing at crossover sites by katanin generates order cortical microtubular arrays in arabidopsis. Curr. Biol. 23, 2191–2195. 10.1016/j.cub.2013.09.018 PubMed DOI

Zhang Y., Iakovidis M., Costa S. (2016). Control of patterns of symmetric cell division in the epidermal and cortical tissues of the Arabidopsis root. Development 143, 978–982. 10.1242/dev.129502 PubMed DOI PMC

Silver Nanoparticles Alter Microtubule Arrangement, Dynamics and Stress Phytohormone Levels

Spatiotemporal Pattern of Ectopic Cell Divisions Contribute to Mis-Shaped Phenotype of Primary and Lateral Roots of katanin1 Mutant

Complementary Superresolution Visualization of Composite Plant Microtubule Organization and Dynamics

Recent Advances in the Cellular and Developmental Biology of Phospholipases in Plants