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Asymmetric cell division in plants: mechanisms of symmetry breaking and cell fate determination

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Abstract

Asymmetric cell division is a fundamental mechanism that generates cell diversity while maintaining self-renewing stem cell populations in multicellular organisms. Both intrinsic and extrinsic mechanisms underpin symmetry breaking and differential daughter cell fate determination in animals and plants. The emerging picture suggests that plants deal with the problem of symmetry breaking using unique cell polarity proteins, mobile transcription factors, and cell wall components to influence asymmetric divisions and cell fate. There is a clear role for altered auxin distribution and signaling in distinguishing two daughter cells and an emerging role for epigenetic modifications through chromatin remodelers and DNA methylation in plant cell differentiation. The importance of asymmetric cell division in determining final plant form provides the impetus for its study in the areas of both basic and applied science.

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References

  1. Knoblich JA (2010) Asymmetric cell division: recent developments and their implications for tumour biology. Nat Rev Mol Cell Biol 11:849–860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Florian MC, Geiger H (2010) Concise review: polarity in stem cells, disease, and aging. Stem Cells 28:1623–1629

    Article  PubMed  PubMed Central  Google Scholar 

  3. Abrash EB, Bergmann DC (2009) Asymmetric cell divisions: a view from plant development. Dev Cell 16:783–796

    Article  CAS  PubMed  Google Scholar 

  4. Tameshige T, Hirakawa Y, Torii KU, Uchida N (2015) Cell walls as a stage for intercellular communication regulating shoot meristem development. Frontiers in plant science. 6:324

    Article  PubMed  PubMed Central  Google Scholar 

  5. Gonczy P (2008) Mechanisms of asymmetric cell division: flies and worms pave the way. Nat Rev Mol Cell Biol 9:355–366

    Article  PubMed  CAS  Google Scholar 

  6. Goldstein B, Macara IG (2007) The PAR proteins: fundamental players in animal cell polarization. Dev Cell 13:609–622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Noatynska A, Gotta M (2012) Cell polarity and asymmetric cell division: the C. elegans early embryo. Essays Biochem 53:1–14

    Article  CAS  PubMed  Google Scholar 

  8. Marston DJ, Goldstein B (2006) Symmetry breaking in C. elegans: another gift from the sperm. Dev Cell 11:273–274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Schubert CM, Lin R, de Vries CJ, Plasterk RH, Priess JR (2000) MEX-5 and MEX-6 function to establish soma/germline asymmetry in early C. elegans embryos. Mol Cell 5:671–682

    Article  CAS  PubMed  Google Scholar 

  10. DeRenzo C, Reese KJ, Seydoux G (2003) Exclusion of germ plasm proteins from somatic lineages by cullin-dependent degradation. Nature 424:685–689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Andersson ER, Sandberg R, Lendahl U (2011) Notch signaling: simplicity in design, versatility in function. Development 138:3593–3612

    Article  CAS  PubMed  Google Scholar 

  12. Rhyu MS, Jan LY, Jan YN (1994) Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76:477–491

    Article  CAS  PubMed  Google Scholar 

  13. Frise E, Knoblich JA, Younger-Shepherd S, Jan LY, Jan YN (1996) The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc Natl Acad Sci USA 93:11925–11932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dong Z, Yang N, Yeo SY, Chitnis A, Guo S (2012) Intralineage directional Notch signaling regulates self-renewal and differentiation of asymmetrically dividing radial glia. Neuron 74:65–78

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Coumailleau F, Furthauer M, Knoblich JA, Gonzalez-Gaitan M (2009) Directional Delta and Notch trafficking in Sara endosomes during asymmetric cell division. Nature 458:1051–1055

    Article  CAS  PubMed  Google Scholar 

  16. Montagne C, Gonzalez-Gaitan M (2014) Sara endosomes and the asymmetric division of intestinal stem cells. Development 141:2014–2023

    Article  CAS  PubMed  Google Scholar 

  17. Kressmann S, Campos C, Castanon I, Furthauer M, Gonzalez-Gaitan M (2015) Directional Notch trafficking in Sara endosomes during asymmetric cell division in the spinal cord. Nat Cell Biol 17:333–339

    Article  CAS  PubMed  Google Scholar 

  18. Derivery E, Seum C, Daeden A, Loubery S, Holtzer L, Julicher F, Gonzalez-Gaitan M (2015) Polarized endosome dynamics by spindle asymmetry during asymmetric cell division. Nature 528:280–285

    Article  CAS  PubMed  Google Scholar 

  19. Morrison SJ, Spradling AC (2008) Stem cells and niches: mechanisms that promote stem cell maintenance throughout life. Cell 132:598–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Gattazzo F, Urciuolo A, Bonaldo P (2014) Extracellular matrix: a dynamic microenvironment for stem cell niche. Biochim Biophys Acta 1840:2506–2519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Losick VP, Morris LX, Fox DT, Spradling A (2011) Drosophila stem cell niches: a decade of discovery suggests a unified view of stem cell regulation. Dev Cell 21:159–171

    Article  CAS  PubMed  Google Scholar 

  22. Fuchs E, Tumbar T, Guasch G (2004) Socializing with the neighbors: stem cells and their niche. Cell 116:769–778

    Article  CAS  PubMed  Google Scholar 

  23. Song X, Zhu CH, Doan C, Xie T (2002) Germline stem cells anchored by adherens junctions in the Drosophila ovary niches. Science 296:1855–1857

    Article  CAS  PubMed  Google Scholar 

  24. Song X, Wong MD, Kawase E, Xi R, Ding BC, McCarthy JJ, Xie T (2004) Bmp signals from niche cells directly repress transcription of a differentiation-promoting gene, bag of marbles, in germline stem cells in the Drosophila ovary. Development 131:1353–1364

    Article  CAS  PubMed  Google Scholar 

  25. Kawase E, Wong MD, Ding BC, Xie T (2004) Gbb/Bmp signaling is essential for maintaining germline stem cells and for repressing bam transcription in the Drosophila testis. Development 131:1365–1375

    Article  CAS  PubMed  Google Scholar 

  26. Chen D, McKearin D (2003) Dpp signaling silences bam transcription directly to establish asymmetric divisions of germline stem cells. Curr Biol 13:1786–1791

    Article  CAS  PubMed  Google Scholar 

  27. Wang X, Harris RE, Bayston LJ, Ashe HL (2008) Type IV collagens regulate BMP signalling in Drosophila. Nature 455:72–77

    Article  CAS  PubMed  Google Scholar 

  28. Akiyama T, Kamimura K, Firkus C, Takeo S, Shimmi O, Nakato H (2008) Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev Biol 313:408–419

    Article  CAS  PubMed  Google Scholar 

  29. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT (2007) Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 315:518–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wang X, Tsai JW, Imai JH, Lian WN, Vallee RB, Shi SH (2009) Asymmetric centrosome inheritance maintains neural progenitors in the neocortex. Nature 461:947–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Januschke J, Llamazares S, Reina J, Gonzalez C (2011) Drosophila neuroblasts retain the daughter centrosome. Nat Commun 2:243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Salzmann V, Chen C, Chiang CY, Tiyaboonchai A, Mayer M, Yamashita YM (2014) Centrosome-dependent asymmetric inheritance of the midbody ring in Drosophila germline stem cell division. Mol Biol Cell 25:267–275

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Yadlapalli S, Yamashita YM (2013) Chromosome-specific nonrandom sister chromatid segregation during stem-cell division. Nature 498:251–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Chen CT, Ettinger AW, Huttner WB, Doxsey SJ (2013) Resurrecting remnants: the lives of post-mitotic midbodies. Trends Cell Biol 23:118–128

    Article  CAS  PubMed  Google Scholar 

  35. Agromayor M, Martin-Serrano J (2013) Knowing when to cut and run: mechanisms that control cytokinetic abscission. Trends Cell Biol 23:433–441

    Article  CAS  PubMed  Google Scholar 

  36. Bringmann H, Hyman AA (2005) A cytokinesis furrow is positioned by two consecutive signals. Nature 436:731–734

    Article  CAS  PubMed  Google Scholar 

  37. Burgess DR, Chang F (2005) Site selection for the cleavage furrow at cytokinesis. Trends Cell Biol 15:156–162

    Article  CAS  PubMed  Google Scholar 

  38. Tran V, Lim C, Xie J, Chen X (2012) Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science 338:679–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Xie J, Wooten M, Tran V, Chen BC, Pozmanter C, Simbolon C, Betzig E, Chen X (2015) Histone H3 threonine phosphorylation regulates asymmetric histone inheritance in the Drosophila male germline. Cell 163:920–933

    Article  CAS  PubMed  Google Scholar 

  40. Fichelson P, Moch C, Ivanovitch K, Martin C, Sidor CM, Lepesant JA, Bellaiche Y, Huynh JR (2009) Live-imaging of single stem cells within their niche reveals that a U3snoRNP component segregates asymmetrically and is required for self-renewal in Drosophila. Nat Cell Biol 11:685–693

    Article  CAS  PubMed  Google Scholar 

  41. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796–815

    Article  Google Scholar 

  42. Pillitteri LJ, Peterson KM, Horst RJ, Torii KU (2011) Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell 23:3260–3275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Zhang Y, Wang P, Shao W, Zhu JK, Dong J (2015) The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. Dev Cell 33:136–149

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  44. Dong J, MacAlister CA, Bergmann DC (2009) BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–1330

    Article  PubMed  PubMed Central  Google Scholar 

  45. Silva PA, Ul-Rehman R, Rato C, Di Sansebastiano GP, Malho R (2010) Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. BMC Plant Biol 10:179

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Krecek P, Skupa P, Libus J, Naramoto S, Tejos R, Friml J, Zazimalova E (2009) The PIN-FORMED (PIN) protein family of auxin transporters. Genome Biol 10:249

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Frank MJ, Smith LG (2002) A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr Biol 12:849–853

    Article  CAS  PubMed  Google Scholar 

  48. Cartwright HN, Humphries JA, Smith LG (2009) PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 323:649–651

    Article  CAS  PubMed  Google Scholar 

  49. Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Pillitteri LJ, Dong J (2013) Stomatal development in Arabidopsis. Arabidopsis Book 11:e0162

    Article  PubMed  PubMed Central  Google Scholar 

  51. Liu T, Ohashi-Ito K, Bergmann DC (2009) Orthologs of Arabidopsis thaliana stomatal bHLH genes and regulation of stomatal development in grasses. Development 136:2265–2276

    Article  CAS  PubMed  Google Scholar 

  52. MacAlister CA, Bergmann DC (2011) Sequence and function of basic helix-loop-helix proteins required for stomatal development in Arabidopsis are deeply conserved in land plants. Evol Dev 13:182–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhang X, Facette M, Humphries JA, Shen Z, Park Y, Sutimantanapi D, Sylvester AW, Briggs SP, Smith LG (2012) Identification of PAN2 by quantitative proteomics as a leucine-rich repeat-receptor-like kinase acting upstream of PAN1 to polarize cell division in maize. Plant Cell 24:4577–4589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Sutimantanapi D, Pater D, Smith LG (2014) Divergent roles for maize PAN1 and PAN2 receptor-like proteins in cytokinesis and cell morphogenesis. Plant Physiol 164:1905–1917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Facettte MR, Park Y, Sutimantanapi D, Luo A, Cartwright HN, Yang B, Bennett EJ, Sylvester AW, Smith LG (2015) The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize. Nat Plants 1:1–8

    Google Scholar 

  56. Geisler MJ, Deppong DO, Nadeau JA, Sack FD (2003) Stomatal neighbor cell polarity and division in Arabidopsis. Planta 216:571–579

    CAS  PubMed  Google Scholar 

  57. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293

    Article  CAS  PubMed  Google Scholar 

  58. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031

    Article  CAS  PubMed  Google Scholar 

  59. Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 19:864–869

    Article  CAS  PubMed  Google Scholar 

  60. Jewaria PK, Hara T, Tanaka H, Kondo T, Betsuyaku S, Sawa S, Sakagami Y, Aimoto S, Kakimoto T (2013) Differential effects of the peptides Stomagen, EPF1 and EPF2 on activation of MAP kinase MPK6 and the SPCH protein level. Plant Cell Physiol 54:1253–1262

    Article  CAS  PubMed  Google Scholar 

  61. Lee JS, Hnilova M, Maes M, Lin YC, Putarjunan A, Han SK, Avila J, Torii KU (2015) Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522:439–443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. MacAlister CA, Ohashi-Ito K, Bergmann DC (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–540

    Article  CAS  PubMed  Google Scholar 

  63. Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116

    Article  CAS  PubMed  Google Scholar 

  64. Meng X, Wang H, He Y, Liu Y, Walker JC, Torii KU, Zhang S (2012) A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell 24:4948–4960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Smekalova V, Luptovciak I, Komis G, Samajova O, Ovecka M, Doskocilova A, Takac T, Vadovic P, Novak O, Pechan T, Ziemann A, Kosutova P, Samaj J (2014) Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation. New Phytol 203:1175–1193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Merouane A, Rey-Villamizar N, Lu Y, Liadi I, Romain G, Lu J, Singh H, Cooper LJ, Varadarajan N, Roysam B (2015) Automated profiling of individual cell-cell interactions from high-throughput time-lapse imaging microscopy in nanowell grids (TIMING). Bioinformatics 31:3189–3197 (Oxford, England)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Tang F, Lao K, Surani MA (2011) Development and applications of single-cell transcriptome analysis. Nat Methods 8:S6–S11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kania U, Fendrych M, Friml J (2014) Polar delivery in plants; commonalities and differences to animal epithelial cells. Open Biology 4:140017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Scheres B (2007) Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 8:345–354

    Article  CAS  PubMed  Google Scholar 

  70. Bennett T, van den Toorn A, Sanchez-Perez GF, Campilho A, Willemsen V, Snel B, Scheres B (2010) SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 22:640–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Willemsen V, Bauch M, Bennett T, Campilho A, Wolkenfelt H, Xu J, Haseloff J, Scheres B (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 15:913–922

    Article  CAS  PubMed  Google Scholar 

  72. Koizumi K, Wu S, MacRae-Crerar A, Gallagher KL (2011) An essential protein that interacts with endosomes and promotes movement of the SHORT-ROOT transcription factor. Curr Biol 21:1559–1564

    Article  CAS  PubMed  Google Scholar 

  73. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN (2007) An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:421–425

    Article  CAS  PubMed  Google Scholar 

  74. Bennett T, van den Toorn A, Willemsen V, Scheres B (2014) Precise control of plant stem cell activity through parallel regulatory inputs. Development 141:4055–4064

    Article  CAS  PubMed  Google Scholar 

  75. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814

    Article  CAS  PubMed  Google Scholar 

  76. Stahl Y, Grabowski S, Bleckmann A, Kuhnemuth R, Weidtkamp-Peters S, Pinto KG, Kirschner GK, Schmid JB, Wink RH, Hulsewede A, Felekyan S, Seidel CA, Simon R (2013) Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr Biol 23:362–371

    Article  CAS  PubMed  Google Scholar 

  77. Kinoshita A, ten Hove CA, Tabata R, Yamada M, Shimizu N, Ishida T, Yamaguchi K, Shigenobu S, Takebayashi Y, Iuchi S, Kobayashi M, Kurata T, Wada T, Seo M, Hasebe M, Blilou I, Fukuda H, Scheres B, Heidstra R, Kamiya Y, Sawa S (2015) A plant U-box protein, PUB4, regulates asymmetric cell division and cell proliferation in the root meristem. Development 142:444–453

    Article  CAS  PubMed  Google Scholar 

  78. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  Google Scholar 

  79. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:1053–1057

    Article  CAS  PubMed  Google Scholar 

  80. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN (1996) The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:423–433

    Article  PubMed  Google Scholar 

  81. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN (2000) The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:555–567

    Article  CAS  PubMed  Google Scholar 

  82. Wysocka-Diller JW, Helariutta Y, Fukaki H, Malamy JE, Benfey PN (2000) Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development 127:595–603

    CAS  PubMed  Google Scholar 

  83. Long Y, Goedhart J, Schneijderberg M, Terpstra I, Shimotohno A, Bouchet BP, Akhmanova A, Gadella TW Jr, Heidstra R, Scheres B, Blilou I (2015) SCARECROW-LIKE23 and SCARECROW jointly specify endodermal cell fate but distinctly control SHORT-ROOT movement. Plant J 84:773–784

    Article  CAS  PubMed  Google Scholar 

  84. Koizumi K, Hayashi T, Wu S, Gallagher KL (2012) The SHORT-ROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue. Proc Natl Acad Sci USA 109:13010–13015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B (2007) Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev 21:2196–2204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JA, Benfey PN (2010) Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:128–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D (2010) MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–916

    Article  CAS  PubMed  Google Scholar 

  88. Crawford BC, Sewell J, Golembeski G, Roshan C, Long JA, Yanofsky MF (2015) Plant development. Genetic control of distal stem cell fate within root and embryonic meristems. Science 347:655–659

    Article  CAS  PubMed  Google Scholar 

  89. Han X, Kumar D, Chen H, Wu S, Kim JY (2014) Transcription factor-mediated cell-to-cell signalling in plants. J Exp Bot 65:1737–1749

    Article  CAS  PubMed  Google Scholar 

  90. Hannapel DJ (2013) A perspective on photoperiodic phloem-mobile signals that control development. Front Plant Sci 4:295

    PubMed  PubMed Central  Google Scholar 

  91. Ueda M, Laux T (2012) The origin of the plant body axis. Curr Opin Plant Biol 15:578–584

    Article  PubMed  Google Scholar 

  92. Zhang Z, Laux T (2011) The asymmetric division of the Arabidopsis zygote: from cell polarity to an embryo axis. Sex Plant Reprod 24:161–169

    Article  CAS  PubMed  Google Scholar 

  93. De Smet I, Lau S, Mayer U, Jurgens G (2010) Embryogenesis–the humble beginnings of plant life. Plant J 61:959–970

    Article  PubMed  CAS  Google Scholar 

  94. Petricka JJ, Van Norman JM, Benfey PN (2009) Symmetry breaking in plants: molecular mechanisms regulating asymmetric cell divisions in Arabidopsis. Cold Spring Harb Perspect Biol 1:a000497

    Article  PubMed  PubMed Central  Google Scholar 

  95. Lukowitz W, Roeder A, Parmenter D, Somerville C (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116:109–119

    Article  CAS  PubMed  Google Scholar 

  96. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 19:63–73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:1485–1488

    Article  CAS  PubMed  Google Scholar 

  98. Costa LM, Marshall E, Tesfaye M, Silverstein KA, Mori M, Umetsu Y, Otterbach SL, Papareddy R, Dickinson HG, Boutiller K, VandenBosch KA, Ohki S, Gutierrez-Marcos JF (2014) Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344:168–172

    Article  CAS  PubMed  Google Scholar 

  99. Jeong S, Palmer TM, Lukowitz W (2011) The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 21:1268–1276

    Article  CAS  PubMed  Google Scholar 

  100. Jeong S, Bayer M, Lukowitz W (2011) Taking the very first steps: from polarity to axial domains in the early Arabidopsis embryo. J Exp Bot 62:1687–1697

    Article  CAS  PubMed  Google Scholar 

  101. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 14:867–876

    Article  CAS  PubMed  Google Scholar 

  102. Ueda M, Zhang Z, Laux T (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20:264–270

    Article  CAS  PubMed  Google Scholar 

  103. Wu X, Chory J, Weigel D (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev Biol 309:306–316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131:657–668

    Article  CAS  PubMed  Google Scholar 

  105. Gancz D, Gilboa L (2013) Hormonal control of stem cell systems. Annu Rev Cell Dev Biol 29:137–162

    Article  CAS  PubMed  Google Scholar 

  106. Zhao Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Kieffer M, Neve J, Kepinski S (2010) Defining auxin response contexts in plant development. Curr Opin Plant Biol 13:12–20

    Article  CAS  PubMed  Google Scholar 

  108. Petrasek J, Friml J (2009) Auxin transport routes in plant development. Development 136:2675–2688

    Article  CAS  PubMed  Google Scholar 

  109. Moller B, Weijers D (2009) Auxin control of embryo patterning. Cold Spring Harb Perspect Biol 1:a001545

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  110. Tucker MR, Laux T (2007) Connecting the paths in plant stem cell regulation. Trends Cell Biol 17:403–410

    Article  CAS  PubMed  Google Scholar 

  111. Terpstra I, Heidstra R (2009) Stem cells: the root of all cells. Semin Cell Dev Biol 20:1089–1096

    Article  CAS  PubMed  Google Scholar 

  112. Aichinger E, Kornet N, Friedrich T, Laux T (2012) Plant stem cell niches. Annu Rev Plant Biol 63:615–636

    Article  CAS  PubMed  Google Scholar 

  113. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D, Jurgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602

    Article  CAS  PubMed  Google Scholar 

  114. Paponov IA, Teale WD, Trebar M, Blilou I, Palme K (2005) The PIN auxin efflux facilitators: evolutionary and functional perspectives. Trends Plant Sci 10:170–177

    Article  CAS  PubMed  Google Scholar 

  115. Swarup R, Peret B (2012) AUX/LAX family of auxin influx carriers-an overview. Front Plant Sci 3:225

    Article  PubMed  PubMed Central  Google Scholar 

  116. Geisler M, Murphy AS (2006) The ABC of auxin transport: the role of p-glycoproteins in plant development. FEBS Lett 580:1094–1102

    Article  CAS  PubMed  Google Scholar 

  117. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–153

    Article  CAS  PubMed  Google Scholar 

  118. Berleth T, Jurgens G (1993) The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118:575–587

    Google Scholar 

  119. Hamann T, Mayer U, Jurgens G (1999) The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development 126:1387–1395

    CAS  PubMed  Google Scholar 

  120. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–230

    Article  CAS  PubMed  Google Scholar 

  121. Mayer U, Buttner G, Jurgens G (1993) Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117:149–162

    Google Scholar 

  122. Busch M, Mayer U, Jurgens G (1996) Molecular analysis of the Arabidopsis pattern formation of gene GNOM: gene structure and intragenic complementation. Mol Gen Genet 250:681–691

    CAS  PubMed  Google Scholar 

  123. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–318

    Article  CAS  PubMed  Google Scholar 

  124. Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Heller M, Kammerer PW, Al-Nawas B, Luszpinski MA, Forch R, Brieger J (2015) The effect of extracellular matrix proteins on the cellular response of HUVECS and HOBS after covalent immobilization onto titanium. J Biomed Mater Res A. 103:2035–2044

    Article  CAS  PubMed  Google Scholar 

  126. Song SK, Hofhuis H, Lee MM, Clark SE (2008) Key divisions in the early Arabidopsis embryo require POL and PLL1 phosphatases to establish the root stem cell organizer and vascular axis. Dev Cell 15:98–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Meyer MR, Shah S, Zhang J, Rohrs H, Rao AG (2015) Evidence for intermolecular interactions between the intracellular domains of the Arabidopsis receptor-like kinase ACR4, its homologs and the Wox5 transcription factor. PLoS One 10:e0118861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Boyer F, Simon R (2015) Asymmetric cell divisions constructing Arabidopsis stem cell niches: the emerging role of protein phosphatases. Plant Biol (Stuttgart, Germany) 17:935–945

    Article  CAS  Google Scholar 

  129. Balcerowicz M, Hoecker U (2014) Auxin–a novel regulator of stomata differentiation. Trends Plant Sci 19:747–749

    Article  CAS  PubMed  Google Scholar 

  130. Le J, Liu XG, Yang KZ, Chen XL, Zou JJ, Wang HZ, Wang M, Vanneste S, Morita M, Tasaka M, Ding ZJ, Friml J, Beeckman T, Sack F (2014) Auxin transport and activity regulate stomatal patterning and development. Nat Commun 5:3090

    Article  PubMed  CAS  Google Scholar 

  131. Zhang JY, He SB, Li L, Yang HQ (2014) Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll. Proc Natl Acad Sci USA 111:E3015–E3023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012) Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos Trans R Soc Lond B Biol Sci 367:1461–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P, Smith RS, Weijers D (2014) Genetic control of plant development by overriding a geometric division rule. Dev Cell 29:75–87

    Article  CAS  PubMed  Google Scholar 

  134. Liao CY, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D (2015) Reporters for sensitive and quantitative measurement of auxin response. Nat Methods 12:207–210 (2 p following 210)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Keegstra K (2010) Plant cell walls. Plant Physiol 154:483–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Rasmussen CG, Humphries JA, Smith LG (2011) Determination of symmetric and asymmetric division planes in plant cells. Annu Rev Plant Biol 62:387–409

    Article  CAS  PubMed  Google Scholar 

  137. Lauffenburger DA, Horwitz AF (1996) Cell migration: a physically integrated molecular process. Cell 84:359–369

    Article  CAS  PubMed  Google Scholar 

  138. Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174:195–291

    Article  CAS  PubMed  Google Scholar 

  139. Qin Y, Zhao J (2006) 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 57:2061–2074

    Article  CAS  PubMed  Google Scholar 

  140. Herve C, Simeon A, Jam M, Cassin A, Johnson KL, Salmean AA, Willats WG, Doblin MS, Bacic A, Kloareg B (2015) Arabinogalactan proteins have deep roots in eukaryotes: identification of genes and epitopes in brown algae and their role in Fucus serratus embryo development. New Phytol 209:1428–1441

    Article  PubMed  CAS  Google Scholar 

  141. Geshi N, Johansen JN, Dilokpimol A, Rolland A, Belcram K, Verger S, Kotake T, Tsumuraya Y, Kaneko S, Tryfona T, Dupree P, Scheller HV, Hofte H, Mouille G (2013) A galactosyltransferase acting on arabinogalactan protein glycans is essential for embryo development in Arabidopsis. Plant J 76:128–137

    CAS  PubMed  Google Scholar 

  142. Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 153:403–419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M, Bogre L, Hussey PJ (2006) Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 119:3227–3237

    Article  CAS  PubMed  Google Scholar 

  144. Komis G, Illes P, Beck M, Samaj J (2011) Microtubules and mitogen-activated protein kinase signalling. Curr Opin Plant Biol 14:650–657

    Article  CAS  PubMed  Google Scholar 

  145. Robinson S, Barbier de Reuille P, Chan J, Bergmann D, Prusinkiewicz P, Coen E (2011) Generation of spatial patterns through cell polarity switching. Science 333:1436–1440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Adrian J, Chang J, Ballenger CE, Bargmann BO, Alassimone J, Davies KA, Lau OS, Matos JL, Hachez C, Lanctot A, Vaten A, Birnbaum KD, Bergmann DC (2015) Transcriptome dynamics of the stomatal lineage: birth, amplification, and termination of a self-renewing population. Dev Cell 33:107–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Mattout A, Meshorer E (2010) Chromatin plasticity and genome organization in pluripotent embryonic stem cells. Curr Opin Cell Biol 22:334–341

    Article  CAS  PubMed  Google Scholar 

  148. Mattout A, Aaronson Y, Sailaja BS, Raghu Ram EV, Harikumar A, Mallm JP, Sim KH, Nissim-Rafinia M, Supper E, Singh PB, Sze SK, Gasser SM, Rippe K, Meshorer E (2015) Heterochromatin Protein 1beta (HP1beta) has distinct functions and distinct nuclear distribution in pluripotent versus differentiated cells. Genome Biol 16:213

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  149. Joffe B, Leonhardt H, Solovei I (2010) Differentiation and large scale spatial organization of the genome. Curr Opin Genet Dev 20:562–569

    Article  CAS  PubMed  Google Scholar 

  150. Apostolou E, Hochedlinger K (2013) Chromatin dynamics during cellular reprogramming. Nature 502:462–471

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Thorstensen T, Grini PE, Aalen RB (2011) SET domain proteins in plant development. Biochim Biophys Acta 1809:407–420

    Article  CAS  PubMed  Google Scholar 

  152. Yao X, Feng H, Yu Y, Dong A, Shen WH (2013) SDG2-mediated H3K4 methylation is required for proper Arabidopsis root growth and development. PLoS One 8:e56537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Pi L, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D, Hennig L, Groot E, Laux T (2015) Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev Cell 33:576–588

    Article  CAS  PubMed  Google Scholar 

  154. Zhang Y, Jiao Y, Liu Z, Zhu YX (2015) ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells. Nat Commun 6:6003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Farrona S, Hurtado L, Bowman JL, Reyes JC (2004) The Arabidopsis thaliana SNF2 homolog AtBRM controls shoot development and flowering. Development. 131:4965–4975

    Article  CAS  PubMed  Google Scholar 

  156. Yang S, Li C, Zhao L, Gao S, Lu J, Zhao M, Chen CY, Liu X, Luo M, Cui Y, Yang C, Wu K (2015) The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance. Plant Cell 27:1670–1680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Li C, Chen C, Gao L, Yang S, Nguyen V, Shi X, Siminovitch K, Kohalmi SE, Huang S, Wu K, Chen X, Cui Y (2015) The Arabidopsis SWI2/SNF2 chromatin remodeler BRAHMA regulates polycomb function during vegetative development and directly activates the flowering repressor gene SVP. PLoS Genet 11:e1004944

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  158. Desvoyes B, de Mendoza A, Ruiz-Trillo I, Gutierrez C (2014) Novel roles of plant RETINOBLASTOMA-RELATED (RBR) protein in cell proliferation and asymmetric cell division. J Exp Bot 65:2657–2666

    Article  CAS  PubMed  Google Scholar 

  159. Dahiya A, Wong S, Gonzalo S, Gavin M, Dean DC (2001) Linking the Rb and polycomb pathways. Mol Cell 8:557–569

    Article  CAS  PubMed  Google Scholar 

  160. Kotake Y, Cao R, Viatour P, Sage J, Zhang Y, Xiong Y (2007) pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev 21:49–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Kuwabara A, Gruissem W (2014) Arabidopsis RETINOBLASTOMA-RELATED and Polycomb group proteins: cooperation during plant cell differentiation and development. J Exp Bot 65:2667–2676

    Article  CAS  PubMed  Google Scholar 

  162. Johnston AJ, Matveeva E, Kirioukhova O, Grossniklaus U, Gruissem W (2008) A dynamic reciprocal RBR-PRC2 regulatory circuit controls Arabidopsis gametophyte development. Curr Biol 18:1680–1686

    Article  CAS  PubMed  Google Scholar 

  163. Ohashi-Ito K, Bergmann DC (2006) Arabidopsis FAMA controls the final proliferation/differentiation switch during stomatal development. Plant Cell. 18:2493–2505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Matos JL, Lau OS, Hachez C, Cruz-Ramirez A, Scheres B, Bergmann DC (2014) Irreversible fate commitment in the Arabidopsis stomatal lineage requires a FAMA and RETINOBLASTOMA-RELATED module. eLife. doi:10.7554/eLife.03271

    Google Scholar 

  165. Lee E, Lucas JR, Goodrich J, Sack FD (2014) Arabidopsis guard cell integrity involves the epigenetic stabilization of the FLP and FAMA transcription factor genes. Plant J 78:566–577

    Article  CAS  PubMed  Google Scholar 

  166. Tricker PJ, Lopez CM, Gibbings G, Hadley P, Wilkinson MJ (2013) Transgenerational, dynamic methylation of stomata genes in response to low relative humidity. Int J Mol Sci 14:6674–6689

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Gong Z, Morales-Ruiz T, Ariza RR, Roldan-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111:803–814

    Article  CAS  PubMed  Google Scholar 

  168. Agius F, Kapoor A, Zhu JK (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc Natl Acad Sci USA 103:11796–11801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Yamamuro C, Miki D, Zheng Z, Ma J, Wang J, Yang Z, Dong J, Zhu JK (2014) Overproduction of stomatal lineage cells in Arabidopsis mutants defective in active DNA demethylation. Nat Commun 5:4062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Krogan NT, Hogan K, Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139:4180–4190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Ashtiyani RK, Moghaddam AM, Schubert V, Rutten T, Fuchs J, Demidov D, Blattner FR, Houben A (2011) AtHaspin phosphorylates histone H3 at threonine 3 during mitosis and contributes to embryonic patterning in Arabidopsis. Plant J 68:443–454

    Article  CAS  PubMed  Google Scholar 

  172. Muller S, Wright AJ, Smith LG (2009) Division plane control in plants: new players in the band. Trends Cell Biol 19:180–188

    Article  PubMed  CAS  Google Scholar 

  173. Van Damme D (2009) Division plane determination during plant somatic cytokinesis. Curr Opin Plant Biol 12:745–751

    Article  PubMed  CAS  Google Scholar 

  174. Van Damme D, Vanstraelen M, Geelen D (2007) Cortical division zone establishment in plant cells. Trends Plant Sci 12:458–464

    Article  PubMed  CAS  Google Scholar 

  175. Lipka E, Herrmann A, Mueller S (2015) Mechanisms of plant cell division. Wiley Interdiscip Rev Dev Biol 4:391–405

    Article  PubMed  Google Scholar 

  176. Rasmussen CG, Wright AJ, Muller S (2013) The role of the cytoskeleton and associated proteins in determination of the plant cell division plane. Plant J 75:258–269

    Article  CAS  PubMed  Google Scholar 

  177. Muller S, Jurgens G (2016) Plant cytokinesis-No ring, no constriction but centrifugal construction of the partitioning membrane. Semin Cell Dev Biol 53:10–18

    Article  PubMed  CAS  Google Scholar 

  178. Smith LG (2001) Plant cell division: building walls in the right places. Nat Rev Mol Cell Biol 2:33–39

    Article  CAS  PubMed  Google Scholar 

  179. Lloyd CW (1991) How does the cytoskeleton read the laws of geometry in aligning the division plane of plant cells? Development 113:55–65

    Google Scholar 

  180. Lau OS, Davies KA, Chang J, Adrian J, Rowe MH, Ballenger CE, Bergmann DC (2014) Direct roles of SPEECHLESS in the specification of stomatal self-renewing cells. Science 345:1605–1609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Biology, Western Washington University, Bellingham, WA, 98225, USA

    Lynn Jo Pillitteri

  2. Waksman Institute of Microbiology, Rutgers the State University of New Jersey, Piscataway, NJ, 08854, USA

    Xiaoyu Guo & Juan Dong

  3. Department of Plant Biology and Pathology, Rutgers the State University of New Jersey, New Brunswick, NJ, 08901, USA

    Juan Dong

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  1. Lynn Jo Pillitteri
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Pillitteri, L.J., Guo, X. & Dong, J. Asymmetric cell division in plants: mechanisms of symmetry breaking and cell fate determination. Cell. Mol. Life Sci. 73, 4213–4229 (2016). https://doi.org/10.1007/s00018-016-2290-2

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