Cytoskeletal remodeling has a fundamental role, especially during transitional developmental stages when cells rapidly adopt new forms and roles, like gametogenesis, fertilization and concomitant embryogenesis and seed formation. KATANIN 1, a microtubule severing protein, fulfills a major regulatory mechanism of dynamic microtubule turnover in eukaryotes. Herein, we show that three well-established KATANIN 1 mutants, fra2, lue1 and ktn1-2 collectively display lower fertility and seed set in Arabidopsis. These lower fertility and seed set rates of fra2, lue1 and ktn1-2 mutants were correlated to abnormalities in the development of embryo proper and seed. Such phenotypes were rescued by transformation of mutants with functional pKTN1::GFP:KTN1 construct. This study significantly expands the already broad functional repertoire of KATANIN 1 and unravels its new role in embryo and seed development. Thus, KATANIN 1 significantly contributes to the fertility and proper embryo and seed formation in Arabidopsis.

Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University OlomoucOlomouc Czechia

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Abu-Abied M., Mordehaev I., Sunil Kumar G. B., Ophir R., Wasteneys G. O., Sadot E. (2015a). Analysis of microtubule-associated-proteins during IBA-mediated adventitious root induction reveals KATANIN dependent and independent alterations of expression patterns. PLoS ONE 10:e0143828 10.1371/journal.pone.0143828 PubMed DOI PMC

Abu-Abied M., Rogovoy Stelmakh O., Mordehaev I., Grumberg M., Elbaum R., Wasteneys G. O., et al. (2015b). Dissecting the contribution of microtubule behaviour in adventitious root induction. J. Exp. Bot. 66 2813–2824. 10.1093/jxb/erv097 PubMed DOI PMC

Albertson D. G. (1984). Formation of the first cleavage spindle in nematode embryos. Dev. Biol. 101 61–72. 10.1016/0012-1606(84)90117-9 PubMed DOI

Albertson D. G., Thomson J. N. (1993). Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosom. Res. 1 15–26. 10.1007/BF00710603 PubMed DOI

Beard S. M., Smitk R. B., Chan B. G., Mains P. E. (2016). Regulation of the MEI-1/MEI-2 microtubule-severing Katanin complex in early Caenorhabditis elegans development. G3 6 3257–3268. 10.1534/g3.116.031666 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. 10.1111/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

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

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

Joly N., Martino L., Gigant E., Dumont J., Pintard L. (2016). Microtubule-severing activity of AAA-ATPase Katanin is essential for female meiotic spindle assembly. Development 143 3604–3614. 10.1242/dev.140830 PubMed DOI

Jürgens G., Mayer U. (1994). “Arabidopsis,” in A Colour Atlas of Developing Embryos ed. Bard J. (London: Wolfe Publishing; ) 7–21.

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

Kemphues K. J., Wolf N., Wood W. B., Hirsh D. (1986). Two loci required for cytoplasmic organization in early embryos of Caenorhabditis elegans. Dev. Biol. 113 449–460. 10.1016/0012-1606(86)90180-6 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

McCarter J., Bartlett B., Dang T., Schedl T. (1999). On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205 111–128. 10.1006/dbio.1998.9109 PubMed DOI

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

Mukherjee S., Diaz Valencia J. D., Stewman S., Metz J., Monnier S., Rath U., et al. (2012). Human Fidgetin is a microtubule severing the enzyme and minus-end depolymerase that regulates mitosis. Cell Cycle 11 2359–2366. 10.4161/cc.20849 PubMed DOI PMC

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

O’Donnell L., O’Bryan M. K. (2014). Microtubules and spermatogenesis. Semin. Cell Dev. Biol. 30 45–54. 10.1016/j.semcdb.2014.01.003 PubMed DOI

O’Donnell L., Rhodes D., Smith S. J., Merriner D. J., Clark B. J., Borg C., et al. (2012). An essential role for katanin p80 and microtubule severing in male gamete production. PLoS Genet. 8:e1002698 10.1371/journal.pgen.1002698 PubMed DOI PMC

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

Qu J., Ye J., Geng Y. F., Sun Y. W., Gao S. Q., Zhang B. P., et al. (2012). Dissecting functions of KATANIN and WRINKLED1 in cotton fiber development by virus-induced gene silencing. Plant Physiol. 160 738–748.10.1104/pp.112.198564 PubMed DOI PMC

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

Russell S. D. (1993). The egg cell: development and role in fertilization and early embryogenesis. Plant Cell 5 1349–1359. 10.1105/tpc.5.10.1349 PubMed DOI PMC

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

Sornay E., Dewitte W., Murray J. A. H. (2016). Seed size plasticity in response to embryonic lethality conferred by ectopic CYCD activation is dependent on plant architecture. Plant Signal. Behav. 11:e1192741 10.1080/15592324.2016.1192741 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. (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

Tang E. I., Lee W. M., Cheng C. (2016). Coordination of actin- and microtubule-based cytoskeletons support transport of spermatids and residual bodies/phagosomes during spermatogenesis in the testis of the male rat. Endocrinology 157 1644–1659. 10.1210/en.2015-1962 PubMed DOI PMC

Tang E. I., Mruk D. D., Cheng C. Y. (2013). MAP/microtubule affinity-regulating kinases, microtubule dynamics, and spermatogenesis. J. Endocrinol. 217 R13–R23. 10.1530/JOE-12-0586 PubMed DOI PMC

ten Hove C. A., Lu K. J., Weijers D. (2015). Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142 420–430.10.1242/dev.111500 PubMed DOI

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

Webb M. C., Gunning B. E. S. (1994). Embryo sac development in Arabidopsis. II. The cytoskeleton during megagametogenesis. Sex. Plant Reprod. 7 153–163. 10.1007/BF00228488 DOI

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

Yang C.-Y., Spielman M., Coles J. P., Li Y., Ghelani S., Bourdon V., et al. (2003). TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J. 34 229–240. 10.1046/j.1365-313X.2003.01713.x PubMed DOI

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

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

Katanin: A Sword Cutting Microtubules for Cellular, Developmental, and Physiological Purposes

Feedback Microtubule Control and Microtubule-Actin Cross-talk in Arabidopsis Revealed by Integrative Proteomic and Cell Biology Analysis of KATANIN 1 Mutants