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植物驱动蛋白: 从微管阵列到生理活动调控

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  • 广州大学生命科学学院, 分子遗传与进化创新研究中心, 广州 510006

收稿日期: 2022-01-12

  录用日期: 2022-02-25

  网络出版日期: 2022-02-25

基金资助

国家自然科学基金(32072084)

Plant Kinesin: from Microtubule Arrays to Physiological Regulation

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  • Innovative Center of Molecular Genetics and Evolution, School of Life Sciences, Guangzhou University, Guangzhou 510006, China

Received date: 2022-01-12

  Accepted date: 2022-02-25

  Online published: 2022-02-25

摘要

驱动蛋白(kinesin)是以微管为轨道的分子马达, 其催化ATP水解为ADP, 将贮藏在ATP分子中的化学能高效地转化为机械能, 在细胞形态建成、细胞分裂、细胞运动、胞内物质运输和信号转导等多种生命活动中发挥重要作用。对植物驱动蛋白的研究落后于动物和真菌, 其原因不仅由于植物进化出独有的驱动蛋白家族, 而且其家族成员数量远多于动物驱动蛋白。该文主要总结了驱动蛋白在微管阵列动态组织, 包括周质微管和有丝分裂早前期微管带、纺锤体及成膜体中的角色和功能, 以及其对植物生理活动的调控作用。同时对重要经济作物大豆(Glycine max)中的驱动蛋白进行了系统分析、分类及功能预测, 发现大豆驱动蛋白数量庞大。结合公共数据库中大豆转录组数据, 对部分大豆驱动蛋白进行功能预测, 以期对大豆及其它作物驱动蛋白功能研究提供线索和启示。

本文引用格式

王韫慧, 王一帆, 蔺佳雨, 李金红, 姚士恩, 冯湘池, 曹振林, 王俊, 李美娜 . 植物驱动蛋白: 从微管阵列到生理活动调控[J]. 植物学报, 2022 , 57(3) : 358 -374 . DOI: 10.11983/CBB22007

Abstract

Kinesins are molecular motors that move along microtubules tracks, catalyze the hydrolysis of ATP to ADP, convert the chemical energy stored in ATP molecules into a mechanical force efficiently, and play important roles in various life activities such as cell morphogenesis, cell division, cell movement, intracellular transport, and signal transduction. Plant kinesin research lag behind that of animals and fungi, not only because plants have evolved a unique kinesin family, but also have more members than that of animals. Here we summarize the most recent advancements made towards understanding kinesin functions in the dynamic organization of microtubule arrays, including cortical microtubules and mitotic pre-prophase band, spindle apparatus and phragmoplast, and the regulation of plant physiological activities. We also performed a systematic analysis, classification and functional prediction of kinesins in soybean, the important cash crop, and found that the numbers of soybean kinesins are largely expanded. Taking advantage of the soybean transcriptome data in the public database, the functions of some soybean kinesins were predicted, to provide some clues for the study of kinesin functions in soybean and other crops.

参考文献

[1] 沈锦波, 姜里文 (2018). 中国科学家在植物细胞骨架研究领域取得突破性进展. 植物学报 53, 741-744.
[2] 岳剑茹, 赫云建, 邱天麒, 郭南南, 韩雪萍, 王显玲 (2021). 植物微管骨架参与下胚轴伸长调节机制研究进展. 植物学报 56, 363-371.
[3] Albertsen MC, Palmer RG (1979). A comparative light- and electron-microscopic study of microsporogenesis in male sterile (MS1) and male fertile soybeans (Glycine max (L.) Merr.). Am J Bot 66, 253-265.
[4] Ambrose JC, Cyr R (2007). The kinesin ATK5 functions in early spindle assembly in Arabidopsis. Plant Cell 19, 226- 236.
[5] Ambrose JC, Li WX, Marcus A, Ma H, Cyr R (2005). A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol Biol Cell 16, 1584-1592.
[6] Asada T, Kuriyama R, Shibaoka H (1997). TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J Cell Sci 110, 179-189.
[7] Bannigan A, Scheible WR, Lukowitz W, Fagerstrom C, Wadsworth P, Somerville C, Baskin TI (2007). A conserved role for kinesin-5 in plant mitosis. J Cell Sci 120, 2819-2827.
[8] Bieling P, Telley IA, Surrey T (2010). A minimal midzone protein module controls formation and length of antiparallel microtubule overlaps. Cell 142, 420-432.
[9] Blancaflor EB (2013). Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am J Bot 100, 143-152.
[10] Brady ST (1985). A novel brain ATPase with properties expected for the fast axonal transport motor. Nature 317, 73-75.
[11] Brim CA, Young MF (1971). Inheritance of a male-sterile character in soybeans. Crop Sci 11, 564-566.
[12] Buschmann H, Dols J, Kopischke S, Pen?a EJ, Andrade- Navarro MA, Heinlein M, Szymanski DB, Zachgo S, Doonan JH, Lloyd CW (2015). Arabidopsis KCBP interacts with AIR9 but stays in the cortical division zone throughout mitosis via its MyTH4-FERM domain. J Cell Sci 128, 2033-2046.
[13] Chandrasekaran G, Tátrai P, Gergely F (2015). Hitting the brakes: targeting microtubule motors in cancer. Br J Cancer 113, 693-698.
[14] Chen CB, Marcus A, Li WX, Hu Y, Calzada JPV, Grossniklaus U, Cyr JR, Ma H (2002). The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129, 2401-2409.
[15] Dawe RK, Lowry EG, Gent JI, Stitzer MC, Swentowsky KW, Higgins DM, Ross-Ibarra J, Wallace JG, Kanizay LB, Alabady M, Qiu WH, Tseng KF, Wang N, Gao Z, Birchler JA, Harkess AE, Hodges AL, Hiatt EN (2018). A kinesin-14 motor activates neocentromeres to promote meiotic drive in maize. Cell 173, 839-850.
[16] de Cuevas M, Tao T, Goldstein LSB (1992). Evidence that the stalk of Drosophila kinesin heavy chain is an α-helical coiled coil. J Cell Biol 116, 957-965.
[17] de Keijzer J, Kieft H, Ketelaar T, Goshima G, Janson ME (2017). Shortening of microtubule overlap regions defines membrane delivery sites during plant cytokinesis. Curr Biol 27, 514-520.
[18] Desai A, Verma S, Mitchison TJ, Walczak CE (1999). Kin I kinesins are microtubule-destabilizing enzymes. Cell 96, 69-78.
[19] Duroc Y, Lemhemdi A, Larchevêque C, Hurel A, Cuacos M, Cromer L, Horlow C, Armstrong SJ, Chelysheva L, Mercier R (2014). The kinesin AtPSS1 promotes synapsis and is required for proper crossover distribution in meiosis. PLoS Genet 10, e1004674.
[20] Eng RC, Wasteneys GO (2014). The microtubule plus-end tracking protein ARMADILLO-REPEAT KINESIN 1 promotes microtubule catastrophe in Arabidopsis. Plant Cell 26, 3372-3386.
[21] Fang XL, Sun XY, Yang XD, Li Q, Lin CJ, Xu J, Gong WJ, Wang YF, Liu L, Zhao LM, Liu BH, Qin J, Zhang MC, Zhang CB, Kong FJ, Li MN (2021). MS1 is essential for male fertility by regulating the microsporocyte cell plate expansion in soybean. Sci China Life Sci 64, 1533-1545.
[22] Frey N, Klotz J, Nick P (2009). Dynamic bridges—a calponin-domain kinesin from rice links actin filaments and microtubules in both cycling and non-cycling cells. Plant Cell Physiol 50, 1493-1506.
[23] Fu Y, Li H, Yang ZB (2002). The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14, 777-794.
[24] Ganguly A, DeMott L, Zhu CM, McClosky DD, Anderson CT, Dixit R (2018). Importin-β directly regulates the motor activity and turnover of a Kinesin-4. Dev Cell 44, 642-651.
[25] Ganguly A, Zhu CM, Chen WZ, Dixit R (2020). FRA1 kinesin modulates the lateral stability of cortical microtubules through cellulose synthase-microtubule uncoupling proteins. Plant Cell 32, 2508-2524.
[26] Gicking AM, Wang P, Liu C, Mickolajczyk KJ, Guo LJ, Hancock WO, Qiu WH (2019). The orphan kinesin PAKRP2 achieves processive motility via a noncanonical stepping mechanism. Biophys J 116, 1270-1281.
[27] Hamada T (2014). Microtubule organization and microtubule-associated proteins in plant cells. Int Rev Cel Mol Biol 312, 1-52.
[28] Hedden P, Phillips AL (2000). Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5, 523- 530.
[29] Herrmann A, Livanos P, Zimmermann S, Berendzen K, Rohr L, Lipka E, Müller S (2021). KINESIN-12E regulates metaphase spindle flux and helps control spindle size in Arabidopsis. Plant Cell 33, 27-43.
[30] Higgins DM, Nannas NJ, Dawe RK (2016). The maize divergent spindle-1 (dv1) gene encodes a Kinesin-14A motor protein required for meiotic spindle pole organization. Front Plant Sci 7, 1277.
[31] Hiwatashi Y, Obara M, Sato Y, Fujita T, Murata T, Hasebe M (2008). Kinesins are indispensable for interdigitation of phragmoplast microtubules in the Moss Physcomitrella pa-tens. Plant Cell 20, 3094-3106.
[32] Hiwatashi Y, Sato Y, Doonan JH (2014). Kinesins have a dual function in organizing microtubules during both tip growth and cytokinesis in Physcomitrella patens. Plant Cell 26, 1256-1266.
[33] Ho CMK, Hotta T, Guo FL, Roberson RW, Lee YRJ, Liu B (2011). Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated pro- tein MAP65-3 in Arabidopsis. Plant Cell 23, 2909-2923.
[34] Hu CK, Coughlin M, Field CM, Mitchison TJ (2011). KIF4 regulates midzone length during cytokinesis. Curr Biol 21, 815-824.
[35] Huang YC, Wang HH, Huang X, Wang Q, Wang JC, An D, Li JQ, Wang WQ, Wu YR (2019). Maize VKS1 regulates mitosis and cytokinesis during early endosperm development. Plant Cell 31, 1238-1256.
[36] Itoh R, Fujiwara M, Yoshida S (2001). Kinesin-related proteins with a mitochondrial targeting signal. Plant Physiol 127, 724-726.
[37] Iwata S, Morikawa M, Takei Y, Hirokawa N (2020). An activity-dependent local transport regulation via degradation and synthesis of KIF17 underlying cognitive flexibility. Sci Adv 6, eabc8355.
[38] Jones MA, Raymond MJ, Smirnoff N (2006). Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis. Plant J 45, 83-100.
[39] Kadota A, Yamada N, Suetsugu N, Hirose M, Saito C, Shoda K, Ichikawa S, Kagawa T, Nakano A, Wada M (2009). Short actin-based mechanism for light-directed chloroplast movement in Arabidopsis. Proc Natl Acad Sci USA 106, 13106-13111.
[40] Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002). Chloroplast avoidance movement reduces photodamage in plants. Nature 420, 829-832.
[41] Kong ZS, Ioki M, Braybrook S, Li SD, Ye ZH, Lee YRJ, Hotta T, Chang A, Tian J, Wang GD, Liu B (2015). Kinesin-4 functions in vesicular transport on cortical micro- tubules and regulates cell wall mechanics during cell elongation in plants. Mol Plant 8, 1011-1023.
[42] Lane J, Allan V (1998). Microtubule-based membrane movement. Biochim Biophys Acta 1376, 27-55.
[43] Lawrence CJ, Dawe RK, Christie KR, Cleveland DW, Dawson SC, Endow SA, Goldstein LSB, Goodson HV, Hirokawa N, Howard J, Malmberg RL, McIntosh JR, Miki H, Mitchison TJ, Okada Y, Reddy ASN, Saxton WM, Schliwa M, Scholey JM, Vale RD, Walczak CE, Wordeman L (2004). A standardized kinesin nomenclature. J Cell Biol 167, 19-22.
[44] Lee YRJ, Giang HM, Liu B (2001). A novel plant kinesin-related protein specifically associates with the phragmoplast organelles. Plant Cell 13, 2427-2439.
[45] Lee YRJ, Li Y, Liu B (2007). Two Arabidopsis phragmoplast-associated kinesins play a critical role in cytokinesis during male gametogenesis. Plant Cell 19, 2595-2605.
[46] Lee YRJ, Liu B (2000). Identification of a phragmoplast- associated kinesin-related protein in higher plants. Curr Biol 10, 797-800.
[47] Lee YRJ, Liu B (2004). Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136, 3877-3883.
[48] Lee YRJ, Qiu WH, Liu B (2015). Kinesin motors in plants: from subcellular dynamics to motility regulation. Curr Opin Plant Biol 28, 120-126.
[49] Li J, Jia JF, Qian Q, Yun YY, Zhang C, Xiao J, Du C, Luo W, Zou GX, Chen ML, Huang YQ, Feng YQ, Cheng ZK, 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, 628-640.
[50] Li YF, Deng ZG, Kamisugi Y, Chen ZR, Wang JJ, Han X, Wei YX, He H, Terzaghi W, Cove DJ, Cuming AC, Chen HD (2021). A minus-end directed kinesin motor directs gravitropism in Physcomitrella patens. Nat Commun 12, 4470.
[51] Malcos JL, Cyr RJ (2011). An ungrouped plant kinesin accumulates at the preprophase band in a cell cycle- dependent manner. Cytoskeleton 68, 247-258.
[52] Marcus AI, Li W, Ma H, Cyr RJ (2003). A kinesin mutant with an atypical bipolar spindle undergoes normal mitosis. Mol Biol Cell 14, 1717-1726.
[53] McFarlane HE, Döring A, Persson S (2014). The cell biology of cellulose synthesis. Annu Rev Plant Biol 65, 69-94.
[54] Miki H, Okada Y, Hirokawa N (2005). Analysis of the kinesin superfamily: insights into structure and function. Trends Cell Biol 15, 467-476.
[55] Mineyuki Y (1999). The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187, 1-49.
[56] Moschou PN, Gutierrez-Beltran E, Bozhkov PV, Smertenko A (2016). Separase promotes microtubule polymerization by activating CENP-E-related kinesin Kin7. Dev Cell 37, 350-361.
[57] Moschou PN, Smertenko AP, Minina EA, Fukada K, Savenkov EI, Robert S, Hussey PJ, Bozhkov PV (2013). The caspase-related protease separase (EXTRA SPINDLE POLES) regulates cell polarity and cytokinesis in Arabidopsis. Plant Cell 25, 2171-2186.
[58] Müller S, Han SC, Smith LG (2006). Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 16, 888-894.
[59] Myers SM, Collins I (2016). Recent findings and future directions for interpolar mitotic kinesin inhibitors in cancer therapy. Future Med Chem 8, 463-489.
[60] Nakamura M, Toyota M, Tasaka M, Morita MT (2011). An Arabidopsis E3 ligase, SHOOT GRAVITROPISM 9, modu- lates the interaction between statoliths and F-actin in gravity sensing. Plant Cell 23, 1830-1848.
[61] Nebenführ A, Dixit R (2018). Kinesins and myosins: molecular motors that coordinate cellular functions in plants. Annu Rev Plant Biol 69, 329-361.
[62] Ni CZ, Wang HQ, Xu T, Qu Z, Liu GQ (2005). AtKP1, a kinesin-like protein, mainly localizes to mitochondria in Arabidopsis thaliana. Cell Res 15, 725-733.
[63] Nishihama R, Ishikawa M, Araki S, Soyano T, Asada T, Machida Y (2001). The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. Genes Dev 15, 352-363.
[64] 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, 87-99.
[65] 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, 4439- 4450.
[66] Oh SA, Allen T, Kim GJ, Sidorova A, Borg M, Park SK, Twell D (2012). Arabidopsis fused kinase and the Kinesin-12 subfamily constitute a signaling module required for phragmoplast expansion. Plant J 72, 308-319.
[67] Oh SA, Bourdon V, Das 'Pal M, Dickinson H, Twell D (2008). Arabidopsis kinesins HINKEL and TETRASPORE act redundantly to control cell plate expansion during cytokinesis in the male gametophyte. Mol Plant 1, 794-799.
[68] Olszewski N, Sun TP, Gubler F (2002). Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14, S61-S80.
[69] Pan RQ, Lee YRJ, Liu B (2004). Localization of two homologous Arabidopsis kinesin-related proteins in the phragmoplast. Planta 220, 156-164.
[70] Preuss ML, Kovar DR, Lee YRJ, Staiger CJ, Delmer DP, Liu B (2004). A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol 136, 3945-3955.
[71] Rath O, Kozielski F (2012). Kinesins and cancer. Nat Rev Cancer 12, 527-539.
[72] Sasabe M, Machida Y (2012). Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton 69, 913-918.
[73] Song Y, Li G, Nowak J, Zhang XQ, Xu DB, Yang XJ, Huang GQ, Liang WQ, Yang LT, Wang CH, Bulone V, Nikoloski Z, Hu JP, Persson S, Zhang DB (2019). The rice actin-binding protein RMD regulates light-dependent shoot gravitropism. Plant Physiol 181, 630-644.
[74] Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jürgens 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, 153-158.
[75] Suetsugu N, Yamada N, Kagawa T, Yonekura H, Uyeda TQP, Kadota A, Wada M (2010). Two kinesin-like proteins mediate actin-based chloroplast movement in Arabidopsis thaliana. Proc Natl Acad Sci USA 107, 8860-8865.
[76] Tian J, Han LB, Feng ZD, Wang GD, Liu WW, Ma YP, Yu YJ, Kong ZS (2015). Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin. eLife 4, e09351.
[77] Tseng KF, Wang P, Lee YRJ, Bowen J, Gicking AM, Guo LJ, Liu B, Qiu WH (2018). The preprophase band-associated Kinesin-14 OsKCH2 is a processive minus-end- directed microtubule motor. Nat Commun 9, 1067.
[78] Vale RD (2003). The molecular motor toolbox for intracellular transport. Cell 112, 467-480.
[79] Vale RD, Fletterick RJ (1997). The design plan of kinesin motors. Annu Rev Cell Dev Biol 13, 745-777.
[80] Vale RD, Reese TS, Sheetz MP (1985). Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42, 39-50.
[81] Walker KL, Müller S, Moss D, Ehrhardt DW, Smith LG (2007). Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 17, 1827- 1836.
[82] Wang HQ, Liu RJ, Wang JW, Wang P, Shen PWY, Liu GQ (2014). The Arabidopsis kinesin gene AtKin-1 plays a role in the nuclear division process during megagametogenesis. Plant Cell Rep 33, 819-828.
[83] Wick SM, Seagull RW, Osborn M, Weber K, Gunning BES (1981). Immunofluorescence microscopy of organized mic- rotubule arrays in structurally stabilized meristematic plant cells. J Cell Biol 89, 685-690.
[84] Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Müller S, Meier I (2008). RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc Natl Acad Sci USA 105, 18637-18642.
[85] Yamada M, Tanaka-Takiguchi Y, Hayashi M, Nishina M, Goshima G (2017). Multiple Kinesin-14 family members drive microtubule minus end-directed transport in plant cells. J Cell Biol 216, 1705-1714.
[86] Yang CY, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG (2003). TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34, 229- 240.
[87] Yang GH, Gao P, Zhang H, Huang SJ, Zheng ZL (2007). A mutation in MRH2 kinesin enhances the root hair tip growth defect caused by constitutively activated ROP2 small GTPase in Arabidopsis. PLoS One 2, e1074.
[88] 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, 1093-1106.
[89] Yin XL, Takei Y, Kido MA, Hirokawa N (2011). Molecular motor KIF17 is fundamental for memory and learning via differential support of synaptic NR2A/2B levels. Neuron 70, 310-325.
[90] Yuan M, Shaw PJ, Warn RM, Lloyd CW (1994). Dynamic reorientation of cortical microtubules, from transverse to longitudinal, in living plant cells. Proc Natl Acad Sci USA 91, 6050-6053.
[91] Zhang M, Zhang BC, Qian Q, Yu YC, Li R, Zhang JW, Liu XL, Zeng DL, Li JY, Zhou YH (2010). Brittle Culm 12, a dual-targeting Kinesin-4 protein, controls cell-cycle progression and wall properties in rice. Plant J 63, 312-328.
[92] Zhong RQ, Burk DH, Morrison III WH, Ye ZH (2002). A kinesin-like protein is essential for oriented deposition of cellulose microfibrils and cell wall strength. Plant Cell 14, 3101-3117.
[93] Zhou SR, Wang Y, Li WC, Zhao ZG, Ren YL, Wang Y, Gu SH, Lin QB, Wang D, Jiang L, Su N, Zhang X, Liu LL, Cheng ZJ, Lei CL, Wang JL, Guo XP, Wu FQ, Ikehashi H, Wang HY, Wan JM (2011). Pollen Semi-Sterility 1 encodes a kinesin-1-like protein important for male meiosis, anther dehiscence, and fertility in rice. Plant Cell 23, 111-129.
[94] Zhu CM, Dixit R (2012). Functions of the Arabidopsis kinesin superfamily of microtubule-based motor proteins. Protoplasma 249, 887-899.
[95] Zhu CM, Ganguly A, Baskin TI, McClosky DD, Anderson CT, Foster C, Meunier KA, Okamoto R, Berg H, Dixit R (2015). The Fragile Fiber 1 kinesin contributes to cortical microtubule-mediated trafficking of cell wall components. Plant Physiol 167, 780-792.
[96] Zou JJ, Zheng ZY, Xue S, Li HH, Wang YR, Le J (2016). The role of Arabidopsis Actin-Related Protein 3 in amyloplast sedimentation and polar auxin transport in root gravitropism. J Exp Bot 67, 5325-5337.
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