The secret to life is being different: Asymmetric divisions in plant development

Current Opinion in Plant Biology

Volumn 13, Issue 6, 2010, Pages 661-669

  Paciorek, Tomasz ^a   Bergmann, Dominique C ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DIVISION; CELL POLARITY; CYTOLOGY; CYTOSKELETON; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; PHYSIOLOGY; PLANT; REVIEW;

CELL DIVISION; CELL POLARITY; CYTOSKELETON; PLANTS;

EID: 78649635772     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2010.09.016     Document Type: Review

References (83)

1. Willemsen V., Bauch M., Bennett T., Campilho A., Wolkenfelt H., Xu J., Haseloff J., Scheres B. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 2008, 6:913-922.
2. Mylona P., Linstead P., Martienssen R., Dolan L. SCHIZORIZA controls an asymmetric cell division and restricts epidermal identity in the Arabidopsis root. Development 2002, 18:4327-4334.
3. Di Laurenzio L., Wysocka-Diller J., Malamy J.E., Pysh L., Helariutta Y., Freshour G., Hahn M.G., Feldmann K.A., Benfey P.N. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 1996, 3:423-433.
4. MacAlister C.A., Ohashi-Ito K., Bergmann D.C. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 2007, 7127:537-540.
5. Pillitteri L.J., Sloan D.B., Bogenschutz N.L., Torii K.U. Termination of asymmetric cell division and differentiation of stomata. Nature 2007, 7127:501-505.
6. Pernas M., Ryan E., Dolan L. SCHIZORIZA controls tissue system complexity in plants. Curr Biol 2010, 9:818-823.
7. ten Hove C.A., Willemsen V., de Vries W.J., van Dijken A., Scheres B., Heidstra R. SCHIZORIZA encodes a nuclear factor regulating asymmetry of stem cell divisions in the Arabidopsis root. Curr Biol 2010, 5:452-457.
8. Cartwright H.N., Humphries J.A., Smith L.G. PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 2009, 5914:649-651.
9. Hara K., Kajita R., Torii K.U., Bergmann D.C., Kakimoto T. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 2007, 14:1720-1725.
10. Nadeau J.A., Sack F.D. Control of stomatal distribution on the Arabidopsis leaf surface. Science 2002, 5573:1697-1700.
11. Nakajima K., Sena G., Nawy T., Benfey P.N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 2001, 6853:307-311.
12. Etchells J.P., Turner S.R. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 2010, 5:767-774.
13. Petricka J.J., Van Norman J.M., Benfey P.N. Symmetry breaking in plants: molecular mechanisms regulating asymmetric cell divisions in Arabidopsis. Cold Spring Harb Perspect Biol 2009, 5:a000497.
14. Abrash E.B., Bergmann D.C. Asymmetric cell divisions: a view from plant development. Dev Cell 2009, 6:783-796.
15. Muller S., Wright A.J., Smith L.G. Division plane control in plants: new players in the band. Trends Cell Biol 2009, 4:180-188.
16. Onsum M.D., Rao C.V. Calling heads from tails: the role of mathematical modeling in understanding cell polarization. Curr Opin Cell Biol 2009, 1:74-81.
17. Irazoqui J.E., Gladfelter A.S., Lew D.J. Scaffold-mediated symmetry breaking by Cdc42p. Nat Cell Biol 2003, 12:1062-1070.
18. Kozubowski L., Saito K., Johnson J.M., Howell A.S., Zyla T.R., Lew D.J. Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr Biol 2008, 22:1719-1726.
19. Marston D.J., Goldstein B. Symmetry breaking in C. elegans: another gift from the sperm. Dev Cell 2006, 3:273-274.
20. Jenkins N., Saam J.R., Mango S.E. CYK-4/GAP provides a localized cue to initiate anteroposterior polarity upon fertilization. Science 2006, 5791:1298-1301.
21. Hable W.E., Kropf D.L. Sperm entry induces polarity in fucoid zygotes. Development 2000, 3:493-501.
22. Bayer M., Nawy T., Giglione C., Galli M., Meinnel T., Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 2009, 5920:1485-1488.
23. Hunt L., Gray J.E. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 2009, 10:864-869.
24. Hara K., Yokoo T., Kajita R., Onishi T., Yahata S., Peterson K.M., Torii K.U., Kakimoto T. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 2009, 6:1019-1031.
25. Rychel A.L., Peterson K.M., Torii K.U. Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. J Plant Res 2010, 123:275-280.
26. Carlsbecker A., Lee J.Y., Roberts C.J., Dettmer J., Lehesranta S., Zhou J., Lindgren O., Moreno-Risueno M.A., Vaten A., Thitamadee S., et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 7296:316-321.
27. Cui H., Levesque M.P., Vernoux T., Jung J.W., Paquette A.J., Gallagher K.L., Wang J.Y., Blilou I., Scheres B., Benfey P.N. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 2007, 5823:421-425.
28. Alassimone J., Naseer S., Geldner N. A developmental framework for endodermal differentiation and polarity. Proc Natl Acad Sci U S A 2010, 11:5214-5219.
29. Zahner J.E., Harkins H.A., Pringle J.R. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae. Mol Cell Biol 1996, 4:1857-1870.
30. Harkins H.A., Page N., Schenkman L.R., De Virgilio C., Shaw S., Bussey H., Pringle J.R. Bud8p and Bud9p, proteins that may mark the sites for bipolar budding in yeast. Mol Biol Cell 2001, 8:2497-2518.
31. Chant J. cell polarity in yeast. Annu Rev Cell Dev Biol 1999, 1:365-391.
32. Schott D., Huffaker T., Bretscher A. Microfilaments and microtubules: the news from yeast. Curr Opin Microbiol 2002, 6:564-574.
33. Goldstein B., Macara I.G. The PAR proteins: fundamental players in animal cell polarization. Dev Cell 2007, 5:609-622.
34. Macara I.G., Mili S. Polarity and differential inheritance-universal attributes of life?. Cell 2008, 5:801-812.
35. Neumuller R.A., Knoblich J.A. Dividing cellular asymmetry: asymmetric cell division and its implications for stem cells and cancer. Genes Dev 2009, 23:2675-2699.
36. Rappaport R. Establishment of the mechanism of cytokinesis in animal cells. Int Rev Cytol 1986, 245-281.
37. Zhao L., Sack F.D. Ultrastructure of stomatal development in Arabidopsis (Brassicaceae) leaves. Am J Bot 1999, 7:929.
38. Galatis B. Microtubules and guard-cell morphogenesis in Zea mays L. J Cell Sci 1980, 1:211-244.
39. Scheres B., Benfey P.N. Asymmetric cell division in plants. Annu Rev Plant Physiol Plant Mol Biol 1999, 505-537.
40. Kropf D.L., Bisgrove S.R., Hable W.E. Establishing a growth axis in fucoid algae. Trends Plant Sci 1999, 12:490-494.
41. Panteris E., Apostolakos P., Galatis B. Cytoskeletal asymmetry in Zea mays subsidiary cell mother cells: a monopolar prophase microtubule half-spindle anchors the nucleus to its polar position. Cell Motil Cytoskeleton 2006, 11:696-709.
42. Oh S.A., Pal M.D., Park S.K., Johnson J.A., Twell D. The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germline establishment. J Exp Bot 2010, 4:969-981.
43. Lucas J.R., Nadeau J.A., Sack F.D. Microtubule arrays and Arabidopsis stomatal development. J Exp Bot 2006, 1:71-79.
44. Nebenfuhr A., Frohlick J.A., Staehelin L.A. Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 2000, 1:135-152.
45. Gallagher K., Smith L. Discordia mutations specifically misorient asymmetric cell divisions during development of the maize leaf epidermis. Development 1999, 20:4623-4633.
46. Twell D., Park S.K., Hawkins T.J., Schubert D., Schmidt R., Smertenko A., Hussey P.J. MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol 2002, 9:711-714.
47. Jurgens G., Grebe M., Steinmann T. Establishment of cell polarity during early plant development. Curr Opin Cell Biol 1997, 6:849-852.
48. Mansfield S.G., Briaty L.G. Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 1991, 69:461-476.
49. Qin Y., Zhao J. Localization of arabinogalactan proteins in egg cells, zygotes, and two-celled proembryos and effects of beta-d-glucosyl Yariv reagent on egg cell fertilization and zygote division in Nicotiana tabacum L. J Exp Bot 2006, 9:2061-2074.
50. Dong J., MacAlister C.A., Bergmann D.C. BASL controls asymmetric cell division in Arabidopsis. Cell 2009, 7:1320-1330.
51. Cowan C.R., Hyman A.A. Asymmetric cell division in C. elegans: cortical polarity and spindle positioning. Annu Rev Cell Dev Biol 2004, 427-453.
52. Wright A.J., Gallagher K., Smith L.G. Discordia1 and alternative discordia1 function redundantly at the cortical division site to promote preprophase band formation and orient division planes in maize. Plant Cell 2009, 21:234-247.
53. Camilleri C., Azimzadeh J., Pastuglia M., Bellini C., Grandjean O., Bouchez D. The Arabidopsis TONNEAU2 gene encodes a putative novel protein phosphatase 2A regulatory subunit essential for the control of the cortical cytoskeleton. Plant Cell 2002, 4:833-845.
54. Cutler S.R., Ehrhardt D.W. Polarized cytokinesis in vacuolate cells of Arabidopsis. Proc Natl Acad Sci U S A 2002, 5:2812-2817.
55. Park S.K., Howden R., Twell D. The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 1998, 19:3789-3799.
56. Guseman J.M., Lee J.S., Bogenschutz N.L., Peterson K.M., Virata R.E., Xie B., Kanaoka M.M., Hong Z., Torii K.U. Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8). Development 2010, 10:1731-1741.
57. Muller S., Han S., Smith L.G. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 2006, 9:888-894.
58. Walker K.L., Muller S., Moss D., Ehrhardt D.W., Smith L.G. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr Biol 2007, 21:1827-1836.
59. Xu X.M., Zhao Q., Rodrigo-Peiris T., Brkljacic J., He C.S., Muller S., Meier I. RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc Natl Acad Sci U S A 2008, 47:18637-18642.
60. Pickett-Heaps J.D., Northcote D.H. Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J Cell Sci 1966, 1:109-120.
61. Borg M., Twell D. Life after meiosis: patterning the angiosperm male gametophyte. Biochem Soc Trans 2010, 2:577-582.
62. Gu Y., Vernoud V., Fu Y., Yang Z. ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot 2003, 380:93-101.
63. Jones M.A., Shen J.J., Fu Y., Li H., Yang Z., Grierson C.S. The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 2002, 4:763-776.
64. Wisniewska J., Xu J., Seifertova D., Brewer P.B., Ruzicka K., Blilou I., Rouquie D., Benkova E., Scheres B., Friml J. Polar PIN localization directs auxin flow in plants. Science 2006, 5775:883.
65. Takano J., Tanaka M., Toyoda A., Miwa K., Kasai K., Fuji K., Onouchi H., Naito S., Fujiwara T. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc Natl Acad Sci U S A 2010, 11:5220-5225.
66. Friml J., Yang X., Michniewicz M., Weijers D., Quint A., Tietz O., Benjamins R., Ouwerkerk P.B., Ljung K., Sandberg G., et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 2004, 5697:862-865.
67. Michniewicz M., Zago M.K., Abas L., Weijers D., Schweighofer A., Meskiene I., Heisler M.G., Ohno C., Zhang J., Huang F., et al. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 2007, 6:1044-1056.
68. Huang F., Kemel Zago M., Abas L., van Marion A., Galvan Ampudia C.S., Offringa R. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 2010, 22:1129-1142.
69. Galweiler L., Guan C., Muller A., Wisman E., Mendgen K., Yephremov A., Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 1998, 5397:2226-2230.
70. Benkova E., Michniewicz M., Sauer M., Teichmann T., Seifertova D., Jurgens G., Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 2003, 5:591-602.
71. Men S., Boutte Y., Ikeda Y., Li X., Palme K., Stierhof Y.D., Hartmann M.A., Moritz T., Grebe M. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat Cell Biol 2008, 2:237-244.
72. Friml J., Vieten A., Sauer M., Weijers D., Schwarz H., Hamann T., Offringa R., Jurgens G. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 2003, 6963:147-153.
73. Friml J., Wisniewska J., Benkova E., Mendgen K., Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 2002, 6873:806-809.
74. Takano J., Miwa K., Yuan L., von Wiren N., Fujiwara T. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc Natl Acad Sci U S A 2005, 34:12276-12281.
75. Dhonukshe P., Tanaka H., Goh T., Ebine K., Mahonen A.P., Prasad K., Blilou I., Geldner N., Xu J., Uemura T., et al. Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature 2008, 456:962-966.
76. Geldner N., Anders N., Wolters H., Keicher J., Kornberger W., Muller P., Delbarre A., Ueda T., Nakano A., Jurgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 2003, 2:219-230.
77. Kleine-Vehn J., Dhonukshe P., Sauer M., Brewer P.B., Wisniewska J., Paciorek T., Benkova E., Friml J. ARF GEF-dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr Biol 2008, 7:526-531.
78. Chen D., Ren Y., Deng Y., Zhao J. Auxin polar transport is essential for the development of zygote and embryo in Nicotiana tabacum L. and correlated with ABP1 and PM H+-ATPase activities. J Exp Bot 2010, 6:1853-1867.
79. Braun N., Wyrzykowska J., Muller P., David K., Couch D., Perrot-Rechenmann C., Fleming A.J. Conditional repression of AUXIN BINDING PROTEIN1 reveals that it coordinates cell division and cell expansion during postembryonic shoot development in Arabidopsis and tobacco. Plant Cell 2008, 20:2746-2762.
80. Mayer U., Buttner G., Jurgens G. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 1993, 117:149-162.
81. Polevoi V.V., Tarakhovskaia E.R., Maslov I., Polevoi A.V. Role of auxin in induction of polarity in zygotes of Fucus vesiculosus L. Ontogenez 2003, 6:432-437.
82. Geldner N., Denervaud-Tendon V., Hyman D.L., Mayer U., Stierhof Y.D., Chory J. Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 2009, 1:169-178.
83. Nelson B.K., Cai X., Nebenfuhr A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J 2007, 6:1126-1136.