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KCH Kinesin Drives Nuclear Transport and Cytoskeletal Coalescence for Tip Cell Growth

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KCH Kinesin Drives Nuclear Transport and Cytoskeletal Coalescence for Tip Cell Growth bioRxiv preprint doi: https://doi.org/10.1101/308775; this version posted April 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. KCH kinesin drives nuclear transport and cytoskeletal coalescence for tip cell growth Moé Yamada and Gohta Goshima# Division of Biological Science, Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8602, Japan #[email protected] Long-distance transport along including organelles, proteins, and RNA, microtubules (MTs) is critical for are transported to their appropriate intracellular organisation. In animals, positions where they specifically function in antagonistic motor proteins kinesin response to internal and external signals. (plus end-directed) and dynein (minus Although it had been believed that plants end-directed) drive cargo transport. In predominantly utilize actin and myosin to land plants, however, the identity of move cellular components, recent studies motors responsible for transport is have uncovered the prevalence of poorly understood, as genes encoding microtubule (MT)-dependent transport as cytoplasmic dynein are missing. How well (Kong et al., 2015; Miki et al., 2015; other functions of dynein are brought Nakaoka et al., 2015; Zhu et al., 2015; about in plants also remains unknown. Yamada et al., 2017). However, a unique Here, we show that a subclass of the feature of plant motor systems is that the kinesin-14 family, KCH—which can also genes encoding cytoplasmic dynein, the bind actin—drives MT minus sole MT minus end-directed transporter in end-directed nuclear transport in the animals, have been lost during plant moss Physcomitrella patens. When all evolution. Moreover, dynein function is not four KCH genes were deleted, the limited to cargo transport, as a variety of nucleus was not maintained in the cell fundamental cellular processes requires centre but was translocated to the dynein, such as MT-based force apical end of protonemal cells. In the generation at the cortex (Grill and Hyman, knockout (KO) line, apical cell tip 2005; Gonczy, 2008; McNally, 2013), growth was also severely suppressed. MT-MT crosslinking (Ferenz et al., 2009; KCH was localised on MTs, including at Tanenbaum et al., 2013), and MT-actin the MT focal point near the tip where crosslinking (Grabham et al., 2007; Perlson MT plus ends coalesced with actin et al., 2013; Coles and Bradke, 2015). filaments. MT focus was not persistent However, how plants execute these in KCH KO lines, whereas actin functions without dynein remains destabilisation also disrupted the focus unanswered. despite KCH remaining on unfocused The moss Physcomitrella patens is an MTs. Functions of nuclear transport emerging model plant of cell and and tip growth were distinct, as a developmental biology, in part due to the truncated KCH construct restored applicability of homologous recombination nuclear transport activity but not tip and high-resolution live imaging (Cove, growth retardation of the KO line. Thus, 2005; Cove et al., 2006; Vidali and our study identified KCH as a Bezanilla, 2012). The protonemal apical long-distance retrograde transporter as cell of P. patens is an excellent system to well as a cytoskeletal crosslinker, study MT-based transport. MTs are reminiscent of the versatile animal predominantly aligned along the cell dynein. longitudinal axis with a characteristic overall polarity depending on cell cycle INTRODUCTION stage (illustrated in Figure 2A). Nucleus, chloroplasts, and newly formed MTs have Intracellular transport is a critical been identified as cargo that is transported cellular mechanism for cell organisation in on MT tracks in protonemal cells, wherein eukaryotic cells. Many cellular components, nuclear movement was shown to be 1 bioRxiv preprint doi: https://doi.org/10.1101/308775; this version posted April 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. independent of actin (Miki et al., 2015; et al., 2017). KAC/KCA is a class V Nakaoka et al., 2015; Yamada et al., 2017). kinesin-14 that no longer possesses MT Using this model system, kinesin-ARK affinity but has acquired an actin-binding (armadillo repeat-containing kinesin) was region and regulates actin-dependent first identified as a plus end-directed chloroplast photo-relocation movement nuclear transporter; upon RNAi knockdown and anchorage to the plasma membrane of this plant-specific, plus end-directed (Suetsugu et al., 2010; Suetsugu et al., motor protein, the nucleus migrated 2012). Class III kinesin-14 is localised to towards the cell centre after cell division as the spindle in moss but appears to have normal but then moved back to the cell lost MT-based motor activity (Miki et al., plate, i.e. the nucleus showed an abnormal 2014; Jonsson et al., 2015). The class IV minus end-directed motility (Figure 2A; Miki kinesin-14 TBK has a weak MT motor et al., 2015). It was also revealed that the activity and localises to cortical MTs yet its non-processive, minus end-directed KCBP cellular function is unknown (Goto and (kinesin-like calmodulin-binding protein)—a Asada, 2007; Jonsson et al., 2015). Class member of the kinesin-14 protein II kinesin-14 genes form a large clade in family—is required for minus end-directed the plant kinesin family, where 9 out of 61 A. nuclear transport. In the absence of KCBP, thaliana kinesin genes are classified into the nucleus could not move to the cell this clade (Figure 1A) and multiple activities centre immediately after cell division, i.e. and cellular functions have been reported. minus end-directed motility was inhibited Kinesin14-II possesses the calponin (Figure 2A; Yamada et al., 2017). Although homology (CH) domain in its a single dimeric KCBP cannot take multiple amino-terminal region followed by steps along the MT (non-processive), dimerisation and motor domains (hereafter clustered motors exhibit processive motility called KCH, which stands for kinesin with in vitro and in vivo; thus, multiple KCBP CH domain; Figure 1B). Adjacent to the motors associated with the nuclear surface motor domain, there exists an can transport the nucleus towards MT uncharacterised C-terminal extension in minus ends (Jonsson et al., 2015; Yamada this subfamily that is not found in ATK or et al., 2017). However, nuclear transport KCBP (Preuss et al., 2004; Frey et al., function of KCBP is limited during the latest 2009; Shen et al., 2012). Mutant analyses stage of cell division, as KCBP is no longer have uncovered divergent functions of necessary for maintaining central KCH, such as cell size regulation positioning of the nucleus during (OsKCH1; Frey et al., 2010), mitochondrial interphase. It is plausible that an additional respiration (Arabidopsis KP1; (Yang et al., minus end-directed motor protein that 2011)), and cell-to-cell movement of a antagonises kinesin-ARK and possibly transcription factor (Arabidopsis KinG; other plus end-directed kinesins is Spiegelman et al., 2018). However, the expressed in moss cells. complete picture of KCH function has not Minus end-directed kinesin-14 is been elucidated, since loss-of-function duplicated uniquely in the land plant analysis using complete null mutants has lineage and constitutes six subfamilies; in not been conducted for this highly Arabidopsis, it is the most expanded family duplicated gene subfamily in flowering among the kinesin superfamily (Zhu and plants. In contrast, P. patens possesses Dixit, 2011; Shen et al., 2012). KCBP only four KCH genes that are highly belongs to class VI of kinesin-14 and homologous (Figure 1A; red), suggesting transports not only the nucleus but also that they redundantly exhibit basal chloroplasts in moss (Yamada et al., 2017). functions of this kinesin subfamily. In Arabidopsis, the cytoskeletal In this study, we generated a plant with organisation of the trichome cell is a complete deletion of the KCH gene of P. defective in kcbp mutants, suggesting an patens, and provide evidence that KCH additional function to nuclear/chloroplast drives minus end-directed nuclear transport (Tian et al., 2015). The class I transport. Furthermore, KCH contributes to kinesin-14 ATK (HSET/XCTK2/Ncd) cell tip growth likely via crosslinking MTs at conserved in animals, is essential for the apical tip. These two functions are mitotic spindle coalescence, and drives distinct, as a KCH fragment that lacks the minus end-directed transport of newly unusual C-terminal extension fulfils the formed MTs along other MTs in the moss function of nuclear transport but not tip cytoplasm (Ambrose et al., 2005; Yamada growth. In contrast, the CH domain, which 2 bioRxiv preprint doi: https://doi.org/10.1101/308775; this version posted April 26, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC 4.0 International license. has been assumed to be the cargo (i.e. KO line. Unlike the KCBP KO line, sister actin) binding site, was not required for nuclei moved towards the cell centre after either function. We propose that plant KCH chromosome segregation, indicating that is a versatile cargo transporter that also minus end-directed motility during fulfils other MT-based functions, analogous telophase was not impaired in the absence to the dynein motor in animals. of KCH (Figure 2B, Movie 1). However, unlike the control cells that maintained RESULTS cell-centre positioning of the nucleus during tip growth, the nucleus did not stop moving Complete KCH deletion affects moss at the cell centre but migrated further growth and morphology towards the cell tip (apical cell) or moved The expression database (http:// back towards the cell plate (subapical cell).
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