1932

Abstract

A major challenge in developmental biology is unraveling the precise regulation of plant stem cell maintenance and the transition to a fully differentiated cell. In this review, we highlight major themes coordinating the acquisition of cell identity and subsequent differentiation in plants. Plant cells are immobile and establish position-dependent cell lineages that rely heavily on external cues. Central players are the hormones auxin and cytokinin, which balance cell division and differentiation during organogenesis. Transcription factors and miRNAs, many of which are mobile in plants, establish gene regulatory networks that communicate cell position and fate. Small peptide signaling also provides positional cues as new cell types emerge from stem cell division and progress through differentiation. These pathways recruit similar players for patterning different organs, emphasizing the modular nature of gene regulatory networks. Finally, we speculate on the outstanding questions in the field and discuss how they may be addressed by emerging technologies.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100617-062459
2018-10-06
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/34/1/annurev-cellbio-100617-062459.html?itemId=/content/journals/10.1146/annurev-cellbio-100617-062459&mimeType=html&fmt=ahah

Literature Cited

  1. Aichinger E, Villar CBR, Di Mambro R, Sabatini S, Köhler C 2011. The CHD3 chromatin remodeler PICKLE and polycomb group proteins antagonistically regulate meristem activity in the Arabidopsis root. Plant Cell 23:31047–60
    [Google Scholar]
  2. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I et al. 2004. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:1109–20
    [Google Scholar]
  3. Aukerman MJ 2003. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell Online 15:112730–41
    [Google Scholar]
  4. Balkunde R, Kitagawa M, Xu XM, Wang J, Jackson D 2017. SHOOT MERISTEMLESS trafficking controls axillary meristem formation, meristem size and organ boundaries in Arabidopsis. . Plant J 90:3435–46
    [Google Scholar]
  5. Bao N, Lye K-W, Barton MK 2004. MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Dev. Cell 7:5653–62
    [Google Scholar]
  6. Benfey PN, Linstead PJ, Roberts K, Schiefelbein JW, Hauser MT, Aeschbacher RA 1993. Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. Development 119:157–70
    [Google Scholar]
  7. Birnbaum K, Jung JW, Wang JY, Lambert GM, Hirst JA et al. 2005. Cell type–specific expression profiling in plants via cell sorting of protoplasts from fluorescent reporter lines. Nat. Methods 2:8615–19
    [Google Scholar]
  8. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I et al. 2005. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:702139–44
    [Google Scholar]
  9. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J et al. 2007. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:5851801–6
    [Google Scholar]
  10. Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R 2000. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:5479617–19
    [Google Scholar]
  11. Caggiano MP, Yu X, Bhatia N, Larsson A, Ram H et al. 2017. Cell type boundaries organize plant development. eLife 6:e27421
    [Google Scholar]
  12. Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:7296316–21
    [Google Scholar]
  13. Causier B, Ashworth M, Guo W, Davies B 2012. The TOPLESS interactome: a framework for gene repression in Arabidopsis. . Plant Physiol 158:1423–38
    [Google Scholar]
  14. Cederholm HM, Iyer-Pascuzzi AS, Benfey PN 2012. Patterning the primary root in Arabidopsis. Wiley Interdiscip. Rev. Dev. Biol 1:5675–91
    [Google Scholar]
  15. Chandler JW, Werr W 2015. Cytokinin-auxin crosstalk in cell type specification. Trends Plant Sci 20:5291–300
    [Google Scholar]
  16. Chickarmane VS, Gordon SP, Tarr PT, Heisler MG, Meyerowitz EM 2012. Cytokinin signaling as a positional cue for patterning the apical-basal axis of the growing Arabidopsis shoot meristem. PNAS 109:104002–7
    [Google Scholar]
  17. Clark NM, Hinde E, Winter CM, Fisher AP, Crosti G 2016. Tracking transcription factor mobility and interaction in Arabidopsis roots with fluorescence correlation spectroscopy. eLife 5:e14770
    [Google Scholar]
  18. Clark SE, Running MP, Meyerowitz EM 1995. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–67
    [Google Scholar]
  19. Clark SE, Williams RW, Meyerowitz EM 1997. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. . Cell 89:4575–85
    [Google Scholar]
  20. Couzigou J-M, Combier J-P 2016. Plant microRNAs: key regulators of root architecture and biotic interactions. New Phytol 212:122–35
    [Google Scholar]
  21. Cruz-Ramírez A, Díaz-Triviño S, Blilou I, Grieneisen VA, Sozzani R et al. 2012. A bistable circuit involving SCARECROW-RETINOBLASTOMA integrates cues to inform asymmetric stem cell division. Cell 150:51002–15
    [Google Scholar]
  22. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ et al. 2007. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 316:5823421–25
    [Google Scholar]
  23. Daum G, Medzihradszky A, Suzaki T, Lohmann JU 2014. A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis. . PNAS 111:4014619–24
    [Google Scholar]
  24. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W et al. 2008. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:5901594–97
    [Google Scholar]
  25. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R et al. 2007. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr. Biol. 17:8678–82
    [Google Scholar]
  26. Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M et al. 2008. A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:59061380–84
    [Google Scholar]
  27. Depuydt S, Rodriguez-Villalon A, Santuari L, Wyser-Rmili C, Ragni L, Hardtke CS 2013. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. PNAS 110:177074–79
    [Google Scholar]
  28. DeYoung BJ, Bickle KL, Schrage KJ, Muskett P, Patel K, Clark SE 2005. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. . Plant J 45:11–16
    [Google Scholar]
  29. DeYoung BJ, Clark SE 2008. BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:2895–904
    [Google Scholar]
  30. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y et al. 1996. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86:3423–33
    [Google Scholar]
  31. Di Mambro R, De Ruvo M, Pacifici E, Salvi E, Sozzani R et al. 2017. Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. PNAS 114:36E7641–49
    [Google Scholar]
  32. Ding Z, Friml J 2010. Auxin regulates distal stem cell differentiation in Arabidopsis roots. PNAS 107:2612046–51
    [Google Scholar]
  33. Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M et al. 2017. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355:6322280–84
    [Google Scholar]
  34. Dolzblasz A, Nardmann J, Clerici E, Causier B, van der Graaff E et al. 2016. Stem cell regulation by Arabidopsis WOX genes. Mol. Plant 9:71–41
    [Google Scholar]
  35. Drisch RC, Stahl Y 2015. Function and regulation of transcription factors involved in root apical meristem and stem cell maintenance. Front. Plant Sci. 6:505
    [Google Scholar]
  36. Efroni I, Birnbaum KD 2016. The potential of single-cell profiling in plants. Genome Biol 17:11–8
    [Google Scholar]
  37. Efroni I, Han S-K, Kim HJ, Wu M-F, Steiner E et al. 2013. Regulation of leaf maturation by chromatin-mediated modulation of cytokinin responses. Dev. Cell 24:4438–45
    [Google Scholar]
  38. Efroni I, Mello A, Nawy T, Ip P-L, Rahni R et al. 2016. Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell 165:71721–33
    [Google Scholar]
  39. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP et al. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr. Biol. 13:201768–74
    [Google Scholar]
  40. Feldmann KA, Marks MD 1986. Rapid and efficient regeneration of plants from explants of Arabidopsis thaliana. . Plant Sci 47:163–69
    [Google Scholar]
  41. Fernandez A, Drozdzecki A, Hoogewijs K, Nguyen A, Beeckman T et al. 2013. Transcriptional and functional classification of the GOLVEN/ROOT GROWTH FACTOR/CLE-like signaling peptides reveals their role in lateral root and hair formation. Plant Physiol 161:2954–70
    [Google Scholar]
  42. Fernandez A, Drozdzecki A, Hoogewijs K, Vassileva V, Madder A et al. 2015. The GLV6/RGF8/CLEL2 peptide regulates early pericycle divisions during lateral root initiation. J. Exp. Bot. 66:175245–56
    [Google Scholar]
  43. Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R et al. 2005. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17:92542–53
    [Google Scholar]
  44. Fletcher JC, Brand U, Running MP, Simon R, Meyerowitz EM 1999. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 283:54091911–14
    [Google Scholar]
  45. Gaillochet C, Lohmann JU 2015. The never-ending story: from pluripotency to plant developmental plasticity. Development 142:132237–49
    [Google Scholar]
  46. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I et al. 2007. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 449:71651053–57
    [Google Scholar]
  47. Gallagher KL, Paquette AJ, Nakajima K, Benfey PN 2004. Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 14:201847–51
    [Google Scholar]
  48. Galli M, Gallavotti A 2016. Expanding the regulatory network for meristem size in plants. Trends Genet 32:6372–83
    [Google Scholar]
  49. Gallois J-L, Nora FR, Mizukami Y, Sablowski R 2004. WUSCHEL induces shoot stem cell activity and developmental plasticity in the root meristem. Genes Dev 18:4375–80
    [Google Scholar]
  50. Geldner N 2013. The endodermis. Annu. Rev. Plant Biol. 64:531–58
    [Google Scholar]
  51. Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM 2009. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. PNAS 106:3816529–34
    [Google Scholar]
  52. Han P, Li Q, Zhu YX 2008. Mutation of Arabidopsis BARD1 causes meristem defects by failing to confine WUSCHEL expression to the organizing center. Plant Cell 20:61482–93
    [Google Scholar]
  53. Hantke SS, Carpenter R, Coen ES 1995. Expression of floricaula in single cell layers of periclinal chimeras activates downstream homeotic genes in all layers of floral meristems. Development 121:127–35
    [Google Scholar]
  54. Hara K, Kajita R, Torii KU, Bergmann DC, Kakimoto T 2007. The secretory peptide gene EPF1 enforces the stomatal one-cell-spacing rule. Genes Dev 21:141720–25
    [Google Scholar]
  55. Hara K, Yokoo T, Kajita R, Onishi T, Yahata S et al. 2009. Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:61019–31
    [Google Scholar]
  56. Hawker NP 2004. Roles for class III HD-Zip and KANADI genes in Arabidopsis root development. Plant Physiol 135:42261–70
    [Google Scholar]
  57. Heidstra R, Sabatini S 2014. Plant and animal stem cells: similar yet different. Nat. Rev. Mol. Cell Biol. 15:5301–12
    [Google Scholar]
  58. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J et al. 2000. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 101:5555–67
    [Google Scholar]
  59. Hirsch S, Oldroyd GED 2009. GRAS-domain transcription factors that regulate plant development. Plant Signal. Behav. 4:8698–700
    [Google Scholar]
  60. Hobe M, Müller R, Grünewald M, Brand U, Simon RD 2003. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev. Genes Evol 213:8371–81
    [Google Scholar]
  61. Horvitz HR, Herskowitz I 1992. Mechanisms of asymmetric cell division: Two Bs or not two Bs, that is the question. Cell 68:2237–55
    [Google Scholar]
  62. Huangfu D, Osafune K, Maehr R, Guo W, Eijkelenboom A et al. 2008. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat. Biotechnol. 26:111269–75
    [Google Scholar]
  63. Hunt L, Gray JE 2009. The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr. Biol. 19:10864–69
    [Google Scholar]
  64. Hwang I, Sheen J, Müller B 2012. Cytokinin signaling networks. Annu. Rev. Plant Biol. 63:353–80
    [Google Scholar]
  65. Ikeuchi M, Iwase A, Sugimoto K 2015. Control of plant cell differentiation by histone modification and DNA methylation. Curr. Opin. Plant Biol. 28:60–67
    [Google Scholar]
  66. Jackson D 2002. Double labeling of KNOTTED1 mRNA and protein reveals multiple potential sites of protein trafficking in the shoot apex. Plant Physiol 129:41423–29
    [Google Scholar]
  67. Jackson D, Veit B, Hake S 1994. Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development 120:2405–13
    [Google Scholar]
  68. Ji L, Liu X, Yan J, Wang W, Yumul RE et al. 2011. ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through two microRNAs in Arabidopsis. . PLOS Genet 7:3e1001358
    [Google Scholar]
  69. Katsir L, Davies KA, Bergmann DC, Laux T 2011. Peptide signaling in plant development. Curr. Biol. 21:9R356–64
    [Google Scholar]
  70. Keshishian EA, Rashotte AM 2015. Plant cytokinin signalling. Essays Biochem 58:013–27
    [Google Scholar]
  71. Kidner CA, Martienssen RA 2004. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428:81–84
    [Google Scholar]
  72. Kidner C, Sundaresan V, Roberts K, Dolan L 2000. Clonal analysis of the Arabidopsis root confirms that position, not lineage, determines cell fate. Planta 211:2191–99
    [Google Scholar]
  73. Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C et al. 2006. Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:3560–73
    [Google Scholar]
  74. Kim I, Hempel FD, Sha K, Pfluger J, Zambryski PC 2002. Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. . Development 129:51261–72
    [Google Scholar]
  75. Kimelman D 2006. Mesoderm induction: from caps to chips. Nat. Rev. Genet. 7:5360–72
    [Google Scholar]
  76. Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S et al. 2010. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. . Development 137:244327–27
    [Google Scholar]
  77. Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T et al. 2006. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:5788845–48
    [Google Scholar]
  78. Kumpf RP, Shi C-L, Larrieu A, Stø IM, Butenko MA et al. 2013. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. PNAS 110:135235–40
    [Google Scholar]
  79. Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M et al. 2007. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:7128652–55
    [Google Scholar]
  80. Kwon CS, Chen C, Wagner D 2005. WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. . Genes Dev 19:8992–1003
    [Google Scholar]
  81. Laux T, Mayer KF, Berger J, Jurgens G 1996. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. . Development 122:187–96
    [Google Scholar]
  82. Le J, Liu X-G, Yang K-Z, Chen X-L, Zou J-J et al. 2014. Auxin transport and activity regulate stomatal patterning and development. Nat. Commun. 5:3090
    [Google Scholar]
  83. Lee JS, Hnilova M, Maes M, Lin Y-CL, Putarjunan A et al. 2015. Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522:7557439–43
    [Google Scholar]
  84. Leibfried A, To JPC, Busch W, Stehling S, Kehle A et al. 2005. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438:70711172–75
    [Google Scholar]
  85. Lenhard M, Laux T 2003. Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development 130:143163–73
    [Google Scholar]
  86. Li S, Yamada M, Han X, Ohler U, Benfey PN 2016. High-resolution expression map of the Arabidopsis root reveals alternative splicing and lincRNA regulation. Dev. Cell 39:4508–22
    [Google Scholar]
  87. Liao C-Y, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D 2015. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods 12:3207–10
    [Google Scholar]
  88. Lokerse AS, Weijers D 2009. Auxin enters the matrix—assembly of response machineries for specific outputs. Curr. Opin. Plant Biol. 12:5520–26
    [Google Scholar]
  89. Long JA, Moan EI, Medford JI, Barton MK 1996. A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. . Nature 379:656066–69
    [Google Scholar]
  90. Long JA, Ohno C, Smith ZR, Meyerowitz EM 2006. TOPLESS regulates apical embryonic fate in Arabidopsis. . Science 312:57791520–23
    [Google Scholar]
  91. Long Y, Smet W, Cruz-Ramírez A, Castelijns B, de Jonge W et al. 2015. Arabidopsis BIRD zinc finger proteins jointly stabilize tissue boundaries by confining the cell fate regulator SHORT-ROOT and contributing to fate specification. Plant Cell 27:41185–99
    [Google Scholar]
  92. Long Y, Stahl Y, Weidtkamp-Peters S, Postma M, Zhou W et al. 2017. In vivo FRET-FLIM reveals cell-type-specific protein interactions in Arabidopsis roots. Nature 548:766597–102
    [Google Scholar]
  93. Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L et al. 1995. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 270:52441980–83
    [Google Scholar]
  94. Mähönen AP, ten Tusscher K, Siligato R, Smetana O, Díaz-Triviño S et al. 2014. PLETHORA gradient formation mechanism separates auxin responses. Nature 515:7525125–29
    [Google Scholar]
  95. Malamy JE, Benfey PN 1997. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. . Development 124:133–44
    [Google Scholar]
  96. Matsubayashi Y 2014. Posttranslationally modified small-peptide signals in plants. Annu. Rev. Plant Biol. 65:385–413
    [Google Scholar]
  97. Matsuzaki Y, Ogawa-Ohnishi M, Mori A, Matsubayashi Y 2010. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. . Science 329:59951065–67
    [Google Scholar]
  98. Mayer KF, Schoof H, Haecker A, Lenhard M, Jurgens G, Laux T 1998. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:6805–15
    [Google Scholar]
  99. McConnell JR, Emery J, Eshed Y, Bao N, Bowman J, Barton MK 2001. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:6838709–13
    [Google Scholar]
  100. McHale NA 2004. MicroRNA-directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems. Plant Cell Online 16:71730–40
    [Google Scholar]
  101. Meng L, Buchanan BB, Feldman LJ, Luan S 2012. CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis. . PNAS 109:51760–65
    [Google Scholar]
  102. Meng WJ, Cheng ZJ, Sang YL, Zhang MM, Rong XF et al. 2017. Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell 29:61357–72
    [Google Scholar]
  103. Meng X, Chen X, Mang H, Liu C, Yu X et al. 2015. Differential function of Arabidopsis SERK family receptor-like kinases in stomatal patterning. Curr. Biol. 25:182361–72
    [Google Scholar]
  104. Moreno-Risueno MA, Sozzani R, Yardımcı GG, Petricka JJ, Vernoux T et al. 2015. Transcriptional control of tissue formation throughout root development. Science 350:6259426–30
    [Google Scholar]
  105. Morrison SJ, Shah NM, Anderson DJ 1997. Regulatory mechanisms in stem cell biology. Cell 88:3287–98
    [Google Scholar]
  106. Müller B, Sheen J 2008. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 453:71981094–97
    [Google Scholar]
  107. Muller R, Bleckmann A, Simon R 2008. The receptor kinase CORYNE of Arabidopsis transmits the stem cell–limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell Online 20:4934–46
    [Google Scholar]
  108. Nadeau JA, Sack FD 2003. Stomatal development: Cross talk puts mouths in place. Trends Plant Sci 8:6294–99
    [Google Scholar]
  109. Nakajima K, Sena G, Nawy T, Benfey PN 2001. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:6853307–11
    [Google Scholar]
  110. Nakayama T, Shinohara H, Tanaka M, Baba K, Ogawa-Ohnishi M, Matsubayashi Y 2017. A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science 355:6322284–86
    [Google Scholar]
  111. Nicolas WJ, Grison MS, Trépout S, Gaston A, Fouché M et al. 2017. Architecture and permeability of post-cytokinesis plasmodesmata lacking cytoplasmic sleeves. Nat. Plants 3:17082
    [Google Scholar]
  112. Nimchuk ZL 2017. CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop. PLOS Genet 13:3e1006681
    [Google Scholar]
  113. Nimchuk ZL, Tarr PT, Ohno C, Qu X, Meyerowitz EM 2011. Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Curr. Biol. 21:5345–52
    [Google Scholar]
  114. Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y 2008. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:5861294–94
    [Google Scholar]
  115. Ou Y, Lu X, Zi Q, Xun Q, Zhang J et al. 2016. RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. . Cell Res 26:6686–98
    [Google Scholar]
  116. Perales M, Rodriguez K, Snipes S, Yadav RK, Diaz-Mendoza M, Reddy GV 2016. Threshold-dependent transcriptional discrimination underlies stem cell homeostasis. PNAS 113:41E6298–306
    [Google Scholar]
  117. Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y et al. 2014. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. eLife 3:e03115
    [Google Scholar]
  118. Pi L, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D et al. 2015. Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev. Cell 33:5576–88
    [Google Scholar]
  119. Pillitteri LJ, Bogenschutz NL, Torii KU 2008. The bHLH protein, MUTE, controls differentiation of stomata and the hydathode pore in Arabidopsis. . Plant Cell Physiol 49:6934–43
    [Google Scholar]
  120. Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU 2007. Termination of asymmetric cell division and differentiation of stomata. Nature 445:7127501–5
    [Google Scholar]
  121. Pillitteri LJ, Torii KU 2012. Mechanisms of stomatal development. Annu. Rev. Plant Biol. 63:591–614
    [Google Scholar]
  122. Polyn S, Willems A, De Veylder L 2015. Cell cycle entry, maintenance, and exit during plant development. Curr. Opin. Plant Biol. 23:1–7
    [Google Scholar]
  123. Prigge MJ 2005. Class III homeodomain–leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 17:161–76
    [Google Scholar]
  124. Rahni R, Efroni I, Birnbaum KD 2016. A case for distributed control of local stem cell behavior in plants. Dev. Cell 38:6635–42
    [Google Scholar]
  125. Raissig MT, Matos JL, Anleu Gil MX, Kornfeld A, Bettadapur A et al. 2017. Mobile MUTE specifies subsidiary cells to build physiologically improved grass stomata. Science 355:63301215–18
    [Google Scholar]
  126. Robards AW, Lucas WJ 1990. Plasmodesmata. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:369–419
    [Google Scholar]
  127. Rodriguez K, Perales M, Snipes S, Yadav RK, Diaz-Mendoza M, Reddy GV 2016. DNA-dependent homodimerization, sub-cellular partitioning, and protein destabilization control WUSCHEL levels and spatial patterning. PNAS 113:41E6307–15
    [Google Scholar]
  128. Rojo E 2002. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell 14:5969–77
    [Google Scholar]
  129. Rosspopoff O, Chelysheva L, Saffar J, Lecorgne L, Gey D et al. 2017. Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development. Development 144:71187–200
    [Google Scholar]
  130. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T et al. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:5463–72
    [Google Scholar]
  131. Sabatini S, Heidstra R, Wildwater M, Scheres B 2003. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17:3354–58
    [Google Scholar]
  132. Saibo NJM, Vriezen WH, Beemster GTS, Van Der Straeten D 2003. Growth and stomata development of Arabidopsis hypocotyls are controlled by gibberellins and modulated by ethylene and auxins. Plant J 33:6989–1000
    [Google Scholar]
  133. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T et al. 2007. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:7137811–14
    [Google Scholar]
  134. Schaller GE, Bishopp A, Kieber JJ 2015. The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:144–63
    [Google Scholar]
  135. Scheres B 2007. Stem-cell niches: nursery rhymes across kingdoms. Nat. Rev. Mol. Cell Biol. 8:5345–54
    [Google Scholar]
  136. Schoof H, Lenhard M, Haecker A, Mayer KF, Jurgens G, Laux T 2000. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:6635–44
    [Google Scholar]
  137. Schweitzer R, Shilo BZ 1997. A thousand and one roles for the Drosophila EGF receptor. Trends Genet 13:5191–96
    [Google Scholar]
  138. Sessions A, Yanofsky MF, Weigel D 2000. Cell-cell signaling and movement by the floral transcription factors LEAFY and APETALA1. Science 289:5480779–82
    [Google Scholar]
  139. Shimizu N, Ishida T, Yamada M, Shigenobu S, Tabata R et al. 2015. BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytol 208:41104–13
    [Google Scholar]
  140. Shinohara H, Mori A, Yasue N, Sumida K, Matsubayashi Y 2016. Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis. . PNAS 113:143897–902
    [Google Scholar]
  141. Skoog F, Miller CO 1957. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11:118–30
    [Google Scholar]
  142. Slane D, Kong J, Berendzen KW, Kilian J, Henschen A et al. 2014. Cell type–specific transcriptome analysis in the early Arabidopsis thaliana embryo. Development 141:244831–40
    [Google Scholar]
  143. Smith ZD, Sindhu C, Meissner A 2016. Molecular features of cellular reprogramming and development. Nat. Rev. Mol. Cell Biol. 17:31–16
    [Google Scholar]
  144. Song W, Liu L, Wang J, Wu Z, Zhang H et al. 2016. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Res 26:6674–85
    [Google Scholar]
  145. Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM et al. 2010. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 466:7302128–32
    [Google Scholar]
  146. Stahl Y, Grabowski S, Bleckmann A, Kühnemuth R, Weidtkamp-Peters S et al. 2013. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 23:5362–71
    [Google Scholar]
  147. Stahl Y, Wink RH, Ingram GC, Simon R 2009. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19:11909–14
    [Google Scholar]
  148. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT et al. 2005. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:2616–27
    [Google Scholar]
  149. Su YH, Zhang XS 2014. The hormonal control of regeneration in plants. Curr. Top. Dev. Biol. 108:35–69
    [Google Scholar]
  150. Szemenyei H, Hannon M, Long JA 2008. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:58681384–86
    [Google Scholar]
  151. Tameshige T, Okamoto S, Lee JS, Aida M, Tasaka M et al. 2016. A secreted peptide and its receptors shape the auxin response pattern and leaf margin morphogenesis. Curr. Biol. 26:182478–85
    [Google Scholar]
  152. Tian H, Wabnik K, Niu T, Li H, Yu Q et al. 2014. WOX5-IAA17 feedback circuit–mediated cellular auxin response is crucial for the patterning of root stem cell niches in Arabidopsis. Mol. . Plant 7:2277–89
    [Google Scholar]
  153. van den Berg C, Willemsen V, Hage W, Weisbeek P, Scheres B 1995. Cell fate in the Arabidopsis root meristem determined by directional signaling. Nature 378:655262–65
    [Google Scholar]
  154. van den Berg C, Willemsen V, Hendriks G, Weisbeek P, Scheres B 1997. Short-range control of cell differentiation in the Arabidopsis root meristem. Nature 390:6657287–89
    [Google Scholar]
  155. Vatén A, Dettmer J, Wu S, Stierhof Y-D, Miyashima S et al. 2011. Callose biosynthesis regulates symplastic trafficking during root development. Dev. Cell 21:61144–55
    [Google Scholar]
  156. Weijers D, Wagner D 2016. Transcriptional responses to the auxin hormone. Annu. Rev. Plant Biol. 67:539–74
    [Google Scholar]
  157. Wendrich JR, Möller BK, Li S, Saiga S, Sozzani R et al. 2017. Framework for gradual progression of cell ontogeny in the Arabidopsis root meristem. PNAS 114:42E8922–29
    [Google Scholar]
  158. Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T 2003. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:112532–50
    [Google Scholar]
  159. Williams L 2005. Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:163657–68
    [Google Scholar]
  160. Wu M-F, Yamaguchi N, Xiao J, Bargmann B, Estelle M et al. 2015. Auxin-regulated chromatin switch directs acquisition of flower primordium founder fate. eLife 4:e09269
    [Google Scholar]
  161. Wu S, Lee C-M, Hayashi T, Price S, Divol F et al. 2014. A plausible mechanism, based upon SHORT-ROOT movement, for regulating the number of cortex cell layers in roots. PNAS 111:4516184–89
    [Google Scholar]
  162. Xu XM, Wang J, Xuan Z, Goldshmidt A, Borrill PGM et al. 2011. Chaperonins facilitate KNOTTED1 cell-to-cell trafficking and stem cell function. Science 333:60461141–44
    [Google Scholar]
  163. Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV 2011. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes Dev 25:192025–30
    [Google Scholar]
  164. Yadav RK, Tavakkoli M, Reddy GV 2010. WUSCHEL mediates stem cell homeostasis by regulating stem cell number and patterns of cell division and differentiation of stem cell progenitors. Development 137:213581–89
    [Google Scholar]
  165. Yang S, Li C, Zhao L, Gao S, Lu J et al. 2015. The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance. Plant Cell 27:61670–80
    [Google Scholar]
  166. Zhang Y, Jiao Y, Liu Z, Zhu Y-X 2015. ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells. Nat. Commun 6:6003
    [Google Scholar]
  167. Zhang Z, Zhang X 2012. Argonautes compete for miR165/166 to regulate shoot apical meristem development. Curr. Opin. Plant Biol. 15:6652–58
    [Google Scholar]
  168. Zhao Z, Andersen SU, Ljung K, Dolezal K, Miotk A et al. 2010. Hormonal control of the shoot stem-cell niche. Nature 465:73011089–92
    [Google Scholar]
  169. Zhong R, Ye Z-H 2007. Regulation of HD-ZIP III genes by microRNA 165. Plant Signal. Behav 2:5351–53
    [Google Scholar]
  170. Zhou W, Wei L, Xu J, Zhai Q, Jiang H et al. 2010. Arabidopsis tyrosylprotein sulfotransferase acts in the auxin/PLETHORA pathway in regulating postembryonic maintenance of the root stem cell niche. Plant Cell 22:113692–709
    [Google Scholar]
  171. Zhou Y, Liu X, Engstrom EM, Nimchuk ZL, Pruneda-Paz JL et al. 2015. Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 517:7534377–80
    [Google Scholar]
  172. Zürcher E, Tavor-Deslex D, Lituiev D, Enkerli K, Tarr PT, Müller B 2013. A robust and sensitive synthetic sensor to monitor the transcriptional output of the cytokinin signaling network in planta. Plant Physiol 161:31066–75
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100617-062459
Loading
/content/journals/10.1146/annurev-cellbio-100617-062459
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error