Abstract
Key message
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.
Similar content being viewed by others
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
Barton NR, Goldstein LS (1996) Going mobile: microtubule motors and chromosome segregation. Proc Natl Acad Sci USA 93(5):1735–1742
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
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
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-#
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
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
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743
De Veylder L, Joubes J, Inze D (2003) Plant cell cycle transitions. Curr Opin Plant Biol 6(6):536–543
Dewitte W, Murray JAH (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264
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
Drews GN, Lee D, Christensen CA (1998) Genetic analysis of female gametophyte development and function. Plant Cell 10(1):5–17
Ebel C, Mariconti L, Gruissem W (2004) Plant retinoblastoma homologues control nuclear proliferation in the female gametophyte. Nature 429(6993):776–780
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
Grossniklaus U, Schneitz K (1998) The molecular and genetic basis of ovule and megagametophyte development. Semin Cell Dev Biol 9(2):227–238
Helin K (1998) Regulation of cell proliferation by the E2F transcription factors. Curr Opin Genet Dev 8(1):28–35
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
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
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
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
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
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
Lavia P, Jansen-Durr P (1999) E2F target genes and cell-cycle checkpoint control. BioEssays 21(3):221–230
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
Lee YR, Liu B (2000) Identification of a phragmoplast-associated kinesin-related protein in higher plants. Curr Biol 10:797–800
Lee YR, Giang H, Liu B (2001) A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13:2427–2439
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
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
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
Liu J, Qu LJ (2008) Meiotic and mitotic cell cycle mutants involved in gametophyte development in Arabidopsis. Mol Plant 1(4):564–574
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
Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252(5009):1162–1164
Mansfield SG, Briarty LG, Erni S (1991) Early embryogenesis in Arabidopsis thaliana. I. The mature embryo sac. Can J Bot 69:14
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
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
Miki H, Okada Y, Hirokawa N (2005) Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15(9):467–476
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
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
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
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
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
Reddy AS (2001) Molecular motors and their functions in plants. Int Rev Cytol 204:97–178
Reddy A (2005) Molecular motors in plant cells. Enclyopedia Mol Cell Bio Mol Med 8:461–494
Reddy A, Day I (2000) The role of the cytoskeleton and a molecular motor in trichome morphogenesis. Trends Plant Sci 5:503–505
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
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
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
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
Shi DQ, Yang WC (2011) Ovule development in Arabidopsis: progress and challenge. Curr Opin Plant Biol 14(1):74–80
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
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
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
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
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
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
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
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
Suetsugu N, Dolja VV, Wada M (2010a) Why have chloroplasts developed a unique motility system? Plant signal behav 5(10):1190–1196
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
Sundaresan V, Alandete-Saez M (2010) Pattern formation in miniature: the female gametophyte of flowering plants. Development 137(2):179–189
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
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
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
Vale RD (2003) The molecular motor toolbox for intracellular transport. Cell 112(4):467–480
Vale R, Fletterick R (1997) The design plan of kinesin motors. Annu Rev Cell Dev Biol 13:745–777
Vale R, Reese T, Sheetz M (1985a) Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42:39–50
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
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
Yang WC, Sundaresan V (2000) Genetics of gametophyte biogenesis in Arabidopsis. Curr Opin Plant Biol 3(1):53–57
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
Yang WC, Shi DQ, Chen YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108
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
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
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
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
Acknowledgments
This study was supported by the National Natural Science Foundation of China (Grant No. 308702288).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Schmit.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-014-1594-7