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The Arabidopsis kinesin gene AtKin-1 plays a role in the nuclear division process during megagametogenesis

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Abstract

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Atkin - 1 , the only Kinesin-1 member of Arabidopsis thaliana , plays a role during female gametogenesis through regulation of nuclear division cycles.

Abstract

Kinesins are microtubule-dependent motor proteins found in eukaryotic organisms. They constitute a superfamily that can be further classified into at least 14 families. In the Kinesin-1 family, members from animal and fungi play roles in long-distance transport of organelles and vesicles. Although Kinesin-1-like sequences have been identified in higher plants, little is known about their function in plant cells, other than in a recently identified Kinesin-1-like protein in a rice pollen semi-sterile mutant. In this study, the gene encoding the only Kinesin-1 member in Arabidopsis, AtKin-1 was found to be specifically expressed in ovules and anthers. AtKin-1 loss-of-function mutants showed substantially aborted ovules in siliques, and this finding was supported by complementation testing. Reciprocal crossing between mutant and wild-type plants indicated that a defect in AtKin-1 results in partially aborted megagametophytes, with no observable effects on pollen fertility. Further observation of ovule development in the mutant pistils indicated that the enlargement of the megaspore was blocked and nuclear division arrested at the one-nucleate stage during embryo sac formation. Our data suggest that AtKin-1 plays a role in the nuclear division cycles during megagametogenesis.

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References

  • Arimoto M, Koushika SP, Choudhary BC, Li C, Matsumoto K, Hisamoto N (2011) The Caenorhabditis elegans JIP3 protein UNC-16 functions as an adaptor to link kinesin-1 with cytoplasmic dynein. J Neurosci 31(6):2216–2224. doi:10.1523/JNEUROSCI.2653-10.2011

    Article  PubMed  CAS  Google Scholar 

  • Barton NR, Goldstein LS (1996) Going mobile: microtubule motors and chromosome segregation. Proc Natl Acad Sci USA 93(5):1735–1742

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cai G, Cresti M (2012) Are kinesins required for organelle trafficking in plant cells? Front Plant Sci 3:170. doi:10.3389/fpls.2012.00170

    Article  PubMed Central  PubMed  Google Scholar 

  • Cai G, Romagnoli S, Moscatelli A, Ovidi E, Gambellini G, Tiezzi A, Cresti M (2000) Identification and characterization of a novel microtubule-based motor associated with membranous organelles in tobacco pollen tubes. Plant Cell 12(9):1719–1736

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Carson JH, Worboys K, Ainger K, Barbarese E (1997) Translocation of myelin basic protein mRNA in oligodendrocytes requires microtubules and kinesin. Cell Motil Cytoskelet 38(4):318–328. doi:10.1002/(SICI)1097-0169(1997)38:4<318::AID-CM2>3.0.CO;2-#

    Google Scholar 

  • Chen C, Marcus A, Li W, Hu Y, Calzada JP, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129(10):2401–2409

    PubMed  CAS  Google Scholar 

  • Christensen CA, King EJ, Jordan JR, Drews GN (1997) Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex Plant Reprod 10(1):49–64. doi:10.1007/s004970050067

    Article  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  PubMed  CAS  Google Scholar 

  • De Veylder L, Joubes J, Inze D (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6(6):536–543

    Article  PubMed  Google Scholar 

  • Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264

    Article  PubMed  CAS  Google Scholar 

  • Diefenbach RJ, Mackay JP, Armati PJ, Cunningham AL (1998) The C-terminal region of the stalk domain of ubiquitous human kinesin heavy chain contains the binding site for kinesin light chain. Biochem 37(47):16663–16670

    Article  CAS  Google Scholar 

  • Drews GN, Lee D, Christensen CA (1998) Genetic analysis of female gametophyte development and function. Plant Cell 10(1):5–17

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ebel C, Mariconti L, Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429(6993):776–780

    Article  PubMed  CAS  Google Scholar 

  • Goldstein LS, Philp AV (1999) The road less traveled: emerging principles of kinesin motor utilization. Annu Rev Cell Dev Biol 15:141–183. doi:10.1146/annurev.cellbio.15.1.141

    Article  PubMed  CAS  Google Scholar 

  • Grossniklaus U, Schneitz K (1998) The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol 9(2):227–238

    Article  PubMed  CAS  Google Scholar 

  • Helin K (1998) Regulation of cell proliferation by the E2F transcription factors. Curr Opin Genet Dev 8(1):28–35

    Article  PubMed  CAS  Google Scholar 

  • Hirokawa N, Takemura R (2005) Molecular motors and mechanisms of directional transport in neurons. Nat Rev Neurosci 6(3):201–214. doi:10.1038/nrn1624

    Article  PubMed  CAS  Google Scholar 

  • Hulskamp M, Parekh NS, Grini P, Schneitz K, Zimmermann I, Lolle SJ, Pruitt RE (1997) The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Dev Biol 187(1):114–124. doi:10.1006/dbio.1997.8554

    Article  PubMed  CAS  Google Scholar 

  • Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon A-F, Weissenbach J, Quetier F, Wincker P, French-Italian Public Consortium for Grapevine Genome C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467

    Article  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907

    PubMed Central  PubMed  CAS  Google Scholar 

  • Kmieciak M, Simpson CG, Lewandowska D, Brown JWS, Jarmolowski A (2002) Cloning and characterization of two subunits of Arabidopsis thaliana nuclear cap-binding complex. Gene 283(1–2):171–183

    Article  PubMed  CAS  Google Scholar 

  • Kwee HS, Sundaresan V (2003) The NOMEGA gene required for female gametophyte development encodes the putative APC6/CDC16 component of the anaphase promoting complex in Arabidopsis. Plant J 36(6):853–866

    Article  PubMed  CAS  Google Scholar 

  • Lavia P, Jansen-Durr P (1999) E2F target genes and cell-cycle checkpoint control. BioEssays 21(3):221–230

    Article  PubMed  CAS  Google Scholar 

  • Lawrence C, Dawe R, Christie K, Cleveland D, Dawson S, Endow S, Goldstein L, Goodson H, Hirokawa N, Howard J, Malmberg R, Mclntosh J, Miki H, Mitchison T, Okada Y, Reddy A, Saxton W, Schliwa M, Scholey J, Vale R, Walczak C, Wordeman L (2004) A standardized kinesin nomenclature. J Cell Biol 167:19–22

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lee YR, Liu B (2000) Identification of a phragmoplast-associated kinesin-related protein in higher plants. Curr Biol 10:797–800

    Article  PubMed  CAS  Google Scholar 

  • Lee YR, Giang H, Liu B (2001) A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13:2427–2439

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Leopold PL, McDowall AW, Pfister KK, Bloom GS, Brady ST (1992) Association of kinesin with characterized membrane-bounded organelles. Cell Motil Cytoskelet 23(1):19–33. doi:10.1002/cm.970230104

    Article  CAS  Google Scholar 

  • Li N, Yuan L, Liu N, Shi D, Li X, Tang Z, Liu J, Sundaresan V, Yang W-C (2009) SLOW WALKER2, a NOC1/MAK21 homologue, is essential for coordinated cell cycle progression during female gametophyte development in Arabidopsis. Plant Physiol 151(3):1486–1497

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li J, Jiang J, Qian Q, Xu Y, Zhang C, Xiao J, Du C, Luo W, Zou G, Chen M, Huang Y, Feng Y, Cheng Z, Yuan M, Chong K (2011) Mutation of rice BC12/GDD1, which encodes a kinesin-like protein that binds to a GA biosynthesis gene promoter, leads to dwarfism with impaired cell elongation. Plant Cell 23(2):628–640. doi:10.1105/tpc.110.081901

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Liu J, Qu LJ (2008) Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol Plant 1(4):564–574

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Cyr R, Palevitz B (1996) A kinesin-like protein, KatAp, in the cells of Arabidopsis and other plants. Plant Cell 8:119–132

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252(5009):1162–1164

    Article  PubMed  CAS  Google Scholar 

  • Mansfield SG, Briarty LG, Erni S (1991) Early embryogenesis in Arabidopsis thaliana. I. The mature embryo sac. Can J Bot 69:14

    Google Scholar 

  • Marcus AI, Li W, Ma H, Cyr RJ (2003) A kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol Biol Cell 14(4):1717–1726. doi:10.1091/mbc.E02-09-0586

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D (2002) The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 277(12):9911–9919

    Article  PubMed  CAS  Google Scholar 

  • Miki H, Okada Y, Hirokawa N (2005) Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15(9):467–476

    Article  PubMed  CAS  Google Scholar 

  • Moore JM, Calzada JP, Gagliano W, Grossniklaus U (1997) Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol 62:35–47

    Article  PubMed  CAS  Google Scholar 

  • Nishihama R, Soyano T, Ishikawa M, Araki S, Tanaka H, Asada T, Irie K, Ito M, Terada M, Banno H, Yamazaki Y, Machida Y (2002) Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 109(1):87–99

    Article  PubMed  CAS  Google Scholar 

  • Oda Y, Fukuda H (2013) Rho of plant GTPase signaling regulates the behavior of Arabidopsis Kinesin-13A to establish secondary cell wall patterns. Plant Cell 25(11):4439–4450. doi:10.1105/tpc.113.117853

    Article  PubMed  CAS  Google Scholar 

  • Pagnussat GC, Yu H-J, Ngo QA, Rajani S, Mayalagu S, Johnson CS, Capron A, Xie L-F, Ye D, Sundaresan V (2005) Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Dev 132(3):603–614

    Article  CAS  Google Scholar 

  • Quan L, Xiao R, Li W, Oh SA, Kong H, Ambrose JC, Malcos JL, Cyr R, Twell D, Ma H (2008) Functional divergence of the duplicated AtKIN14a and AtKIN14b genes: critical roles in Arabidopsis meiosis and gametophyte development. Plant J 53(6):1013–1026. doi:10.1111/j.1365-313X.2007.03391.x

    Article  PubMed  CAS  Google Scholar 

  • Reddy AS (2001) Molecular motors and their functions in plants. Int Rev Cytol 204:97–178

    Article  PubMed  CAS  Google Scholar 

  • Reddy A (2005) Molecular motors in plant cells. Enclyopedia Mol Cell Bio Mol Med 8:461–494

    Google Scholar 

  • Reddy A, Day I (2000) The role of the cytoskeleton and a molecular motor in trichome morphogenesis. Trends Plant Sci 5:503–505

    Article  PubMed  CAS  Google Scholar 

  • Reddy A, Day I (2001) Kinesins in the Arabidopsis genome: a comparative analysis among eukaryotes. BMC Genomics 2:2.1-2.13

  • Richardson D, Simmons M, Reddy A (2006) Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7(1):18

    Article  PubMed Central  PubMed  Google Scholar 

  • Romagnoli S, Cai G, Cresti M (2003) In vitro assays demonstrate that pollen tube organelles use kinesin-related motor proteins to move along microtubules. Plant Cell 15(1):251–269

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Romagnoli S, Cai G, Faleri C, Yokota E, Shimmen T, Cresti M (2007) Microtubule- and actin filament-dependent motors are distributed on pollen tube mitochondria and contribute differently to their movement. Plant Cell Physiol 48(2):345–361. doi:10.1093/pcp/pcm001

    Article  PubMed  CAS  Google Scholar 

  • Sawin KE, LeGuellec K, Philippe M, Mitchison TJ (1992) Mitotic spindle organization by a plus-end-directed microtubule motor. Nature 359(6395):540–543. doi:10.1038/359540a0

    Article  PubMed  CAS  Google Scholar 

  • Shi DQ, Yang WC (2011) Ovule development in Arabidopsis: progress and challenge. Curr Opin Plant Biol 14(1):74–80

    Article  PubMed  CAS  Google Scholar 

  • Shi DQ, Liu J, Xiang YH, Ye D, Sundaresan V, Yang WC (2005) SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell 17(8):2340–2354

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG (1997) TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124(13):2645–2657

    PubMed  CAS  Google Scholar 

  • Springer PS, McCombie WR, Sundaresan V, Martienssen RA (1995) Gene trap tagging of PROLIFERA, an essential MCM2-3-5-like gene in Arabidopsis. Science 268(5212):877–880

    Article  PubMed  CAS  Google Scholar 

  • Springer PS, Holding DR, Groover A, Yordan C, Martienssen RA (2000) The essential Mcm7 protein PROLIFERA is localized to the nucleus of dividing cells during the G(1) phase and is required maternally for early Arabidopsis development. Development 127(9):1815–1822

    PubMed  CAS  Google Scholar 

  • Steinberg G, Schliwa M (1995) The neurospora organelle motor: a distant relative of conventional kinesin with unconventional properties. Mol Biol Cell 6(11):1605–1618

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Steinberg G, Schliwa M, Lehmler C, Bolker M, Kahmann R, McIntosh JR (1998) Kinesin from the plant pathogenic fungus Ustilago maydis is involved in vacuole formation and cytoplasmic migration. J Cell Sci 111(Pt 15):2235–2246

    PubMed  CAS  Google Scholar 

  • Stevens R, Mariconti L, Rossignol P, Perennes C, Cella R, Bergounioux C (2002) Two E2F sites in the Arabidopsis MCM3 promoter have different roles in cell cycle activation and meristematic expression. J Biol Chem 277(36):32978–32984

    Article  PubMed  CAS  Google Scholar 

  • Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jurgens G, Mayer U (2002) The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr Biol 12(2):153–158

    Article  PubMed  CAS  Google Scholar 

  • Suetsugu N, Dolja VV, Wada M (2010a) Why have chloroplasts developed a unique motility system? Plant signal behav 5(10):1190–1196

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQ, Kadota A, Wada M (2010b) Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107(19):8860–8865. doi:10.1073/pnas.0912773107

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sundaresan V, Alandete-Saez M (2010) Pattern formation in miniature: the female gametophyte of flowering plants. Development 137(2):179–189

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tanaka H, Ishikawa M, Kitamura S, Takahashi Y, Soyano T, Machida C, Machida Y (2004) The AtNACK1/HINKEL and STUD/TETRASPORE/AtNACK2 genes, which encode functionally redundant kinesins, are essential for cytokinesis in Arabidopsis. Genes Cells 9(12):1199–1211. doi:10.1111/j.1365-2443.2004.00798.x

    Article  PubMed  CAS  Google Scholar 

  • Tiezzi A, Moscatelli A, Cai G, Bartalesi A, Cresti M (1992) An immunoreactive homolog of mammalian kinesin in Nicotiana tabacum pollen tubes. Cell Motil Cytoskelet 21(2):132–137. doi:10.1002/cm.970210206

    Article  CAS  Google Scholar 

  • Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112(4):467–480

    Article  PubMed  CAS  Google Scholar 

  • Vale R, Fletterick R (1997) The design plan of kinesin motors. Annu Rev Cell Dev Biol 13:745–777

    Article  PubMed  CAS  Google Scholar 

  • Vale R, Reese T, Sheetz M (1985a) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39–50

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vale RD, Schnapp BJ, Mitchison T, Steuer E, Reese TS, Sheetz MP (1985b) Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell 43(3 Pt 2):623–632

    Article  PubMed  CAS  Google Scholar 

  • Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster GTS, Gruissem W, Van de Peer Y, Inze D, De Veylder L (2005) Genome-wide identification of potential plant E2F target genes. Plant Physiol 139(1):316–328

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang WC, Sundaresan V (2000) Genetics of gametophyte biogenesis in Arabidopsis. Curr Opin Plant Biol 3(1):53–57

    Article  PubMed  CAS  Google Scholar 

  • Yang C, Spielman M, Coles J, Li Y, Ghelani S, Bourdon V, Brown R, Lemmon B, Scott R, Dickinson H (2003) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34:229–240

    Article  PubMed  CAS  Google Scholar 

  • Yang WC, Shi DQ, Chen YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108

    Article  PubMed  CAS  Google Scholar 

  • Yang XY, Chen ZW, Xu T, Qu Z, Pan XD, Qin XH, Ren DT, Liu GQ (2011) Arabidopsis kinesin KP1 specifically interacts with VDAC3, a mitochondrial protein, and regulates respiration during seed germination at low temperature. Plant Cell 23(3):1093–1106. doi:10.1105/tpc.110.082420

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhong R, Burk D, Morris W, Ye Z (2002) A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14:3101–3117

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhou S, Wang Y, Li W, Zhao Z, Ren Y, Wang Y, Gu S, Lin Q, Wang D, Jiang L, Su N, Zhang X, Liu L, Cheng Z, Lei C, Wang J, Guo X, Wu F, Ikehashi H, Wang H, Wan J (2011) Pollen semi-sterility1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23(1):111–129. doi:10.1105/tpc.109.073692

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhu C, Dixit R (2012) Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma 249(4):887–899. doi:10.1007/s00709-011-0343-9

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by the National Natural Science Foundation of China (Grant No. 308702288).

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The authors declare that they have no conflict of interest.

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Correspondence to Haiqing Wang.

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Wang, H., Liu, R., Wang, J. et al. The Arabidopsis kinesin gene AtKin-1 plays a role in the nuclear division process during megagametogenesis. Plant Cell Rep 33, 819–828 (2014). https://doi.org/10.1007/s00299-014-1594-7

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