To Divide and to Rule; Regulating Cell Division in Roots During Post-embryonic Growth

  • Luis Sanz
  • James A. H. Murray
  • Walter DewitteEmail author
Part of the Progress in Botany book series (BOTANY, volume 73)


Post-embryonic cell proliferation allows for the development of an extensive root system. Recent genetic analysis in Arabidopsis thaliana has revealed several mechanisms involved cell proliferation control during root development, including hormone signaling and regulatory loops. Furthermore, cell division responds to changes in redox status induced by environmental stresses, and we explore putative connections to the pathways that regulate cell proliferation.


Lateral Root Reactive Nitrogen Species Lateral Root Formation Quiescent Center Root Apical Meristem 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors are indebted to Jeroen Nieuwland (University of Cardiff) for the illustrations.


  1. Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092PubMedGoogle Scholar
  2. Achard P, Renou JP, Berthome R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Curr Biol 18:656–660PubMedGoogle Scholar
  3. 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 119:109–120PubMedGoogle Scholar
  4. Aroca R, Amodeo G, Fernandez-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol 137:341–353PubMedGoogle Scholar
  5. Arrigo AP (1999) Gene expression and the thiol redox state. Free Radic Biol Med 27:936–944PubMedGoogle Scholar
  6. Arrigoni O, De Tullio MC (2002) Ascorbic acid: much more than just an antioxidant. Biochim Biophys Acta 1569:1–9PubMedGoogle Scholar
  7. Banhegyi G, Braun L, Csala M, Puskas F, Mandl J (1997) Ascorbate metabolism and its regulation in animals. Free Radic Biol Med 23:793–803PubMedGoogle Scholar
  8. Barroco RM, Peres A, Droual AM, De Veylder L, Nguyenle SL, De Wolf J, Mironov V, Peerbolte R, Beemster GT, Inze D, Broekaert WF, Frankard V (2006) The cyclin-dependent kinase inhibitor Orysa;KRP1 plays an important role in seed development of rice. Plant Physiol 142:1053–1064PubMedGoogle Scholar
  9. Bashandy T, Meyer Y, Reichheld JP (2011a) Redox regulation of auxin signaling and plant development in Arabidopsis. Plant Signal Behav 6:117–119PubMedGoogle Scholar
  10. Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld JP (2011b) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391Google Scholar
  11. Beeckman T, Burssens S, Inze D (2001) The peri-cell-cycle in Arabidopsis. J Exp Bot 52:403–411PubMedGoogle Scholar
  12. Bemis SM, Torii KU (2007) Autonomy of cell proliferation and developmental programs during Arabidopsis aboveground organ morphogenesis. Dev Biol 304:367–381PubMedGoogle Scholar
  13. Borghi L, Gutzat R, Futterer J, Laizet Y, Hennig L, Gruissem W (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811PubMedGoogle Scholar
  14. Boudolf V, Vlieghe K, Beemster GT, Magyar Z, Torres Acosta JA, Maes S, Van Der Schueren E, Inze D, De Veylder L (2004) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2Fa-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16:2683–2692PubMedGoogle Scholar
  15. Boudolf V, Lammens T, Boruc J, Van Leene J, Van Den Daele H, Maes S, Van Isterdael G, Russinova E, Kondorosi E, Witters E, De Jaeger G, Inze D, De Veylder L (2009) CDKB1;1 forms a functional complex with CYCA2;3 to suppress endocycle onset. Plant Physiol 150:1482–1493PubMedGoogle Scholar
  16. 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 14:867–876PubMedGoogle Scholar
  17. Brightman AO, Barr R, Crane FL, Morre DJ (1988) Auxin-stimulated NADH oxidase purified from plasma membrane of soybean. Plant Physiol 86:1264–1269PubMedGoogle Scholar
  18. Brioudes F, Thierry AM, Chambrier P, Mollereau B, Bendahmane M (2010) Translationally controlled tumor protein is a conserved mitotic growth integrator in animals and plants. Proc Natl Acad Sci USA 107:16384–16389PubMedGoogle Scholar
  19. Burssens S, de Almeida EJ, Beeckman T, Richard C, Shaul O, Ferreira P, Van Montagu M, Inze D (2000) Developmental expression of the Arabidopsis thaliana CycA2;1 gene. Planta 211:623–631PubMedGoogle Scholar
  20. Casimiro I, Beeckman T, Graham N, Bhalerao R, Zhang H, Casero P, Sandberg G, Bennett MJ (2003) Dissecting Arabidopsis lateral root development. Trends Plant Sci 8:165–171PubMedGoogle Scholar
  21. Cheng JC, Seeley KA, Sung ZR (1995) RML1 and RML2, Arabidopsis genes required for cell proliferation at the root tip. Plant Physiol 107:365–376PubMedGoogle Scholar
  22. Cheng NH, Liu JZ, Liu X, Wu Q, Thompson SM, Lin J, Chang J, Whitham SA, Park S, Cohen JD, Hirschi KD (2011) Arabidopsis monothiol glutaredoxin, AtGRXS17, is critical for temperature-dependent postembryonic growth and development via modulating auxin response. J Biol Chem 286(23):20398–20406PubMedGoogle Scholar
  23. Churchman ML, Brown ML, Kato N, Kirik V, Hulskamp M, Inze D, De Veylder L, Walker JD, Zheng Z, Oppenheimer DG, Gwin T, Churchman J, Larkin JC (2006) SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell 18:3145–3157PubMedGoogle Scholar
  24. 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 316:421–425PubMedGoogle Scholar
  25. De Rybel B, Vassileva V, Parizot B, Demeulenaere M, Grunewald W, Audenaert D, Van Campenhout J, Overvoorde P, Jansen L, Vanneste S, Moller B, Wilson M, Holman T, Van Isterdael G, Brunoud G, Vuylsteke M, Vernoux T, De Veylder L, Inze D, Weijers D, Bennett MJ, Beeckman T (2010) A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr Biol 20:1697–1706PubMedGoogle Scholar
  26. De Schutter K, Joubes J, Cools T, Verkest A, Corellou F, Babiychuk E, Van Der Schueren E, Beeckman T, Kushnir S, Inze D, De Veylder L (2007) Arabidopsis WEE1 kinase controls cell cycle arrest in response to activation of the DNA integrity checkpoint. Plant Cell 19:211–225PubMedGoogle Scholar
  27. De Smet I, Lau S, Voss U, Vanneste S, Benjamins R, Rademacher EH, Schlereth A, De Rybel B, Vassileva V, Grunewald W, Naudts M, Levesque MP, Ehrismann JS, InzÕ D, Luschnig C, Benfey PN, Weijers D, Van Montagu MC, Bennett MJ, Jürgens G, Beeckman T (2010) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Proc Natl Acad Sci USA 107(6):2705–2710Google Scholar
  28. De Smet I, Tetsumura T, De Rybel B, Frey NF, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inze D, Bennett MJ, Beeckman T (2007) Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690PubMedGoogle Scholar
  29. De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jurgens G, Ingram GC, Inze D, Benfey PN, Beeckman T (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597PubMedGoogle Scholar
  30. De Tullio MC, Arrigoni O (2003) The ascorbic acid system in seeds: to protect and to serve. Seed Sci Res 13:249–260Google Scholar
  31. De Tullio MC, Jiang K, Feldman LJ (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol Biochem 48:328–336PubMedGoogle Scholar
  32. De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inze D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668PubMedGoogle Scholar
  33. Den Boer B, Murray JA (2000) Triggering the cell cycle in plants. Trends Cell Biol 10:245–250Google Scholar
  34. Dewitte W, Murray JA (2003) The plant cell cycle. Annu Rev Plant Biol 54:235–264PubMedGoogle Scholar
  35. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92PubMedGoogle Scholar
  36. Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray JA (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104:14537–14542PubMedGoogle Scholar
  37. Dhondt S, Coppens F, De Winter F, Swarup K, Merks RM, Inze D, Bennett MJ, Beemster GT (2010) SHORT-ROOT and SCARECROW regulate leaf growth in Arabidopsis by stimulating S-phase progression of the cell cycle. Plant Physiol 154:1183–1195PubMedGoogle Scholar
  38. Dietz KJ (2008) Redox signal integration: from stimulus to networks and genes. Physiol Plant 133:459–468PubMedGoogle Scholar
  39. Dietz KJ, Pfannschmidt T (2011) Novel regulators in photosynthetic redox control of plant metabolism and gene expression. Plant Physiol 155:1477–1485PubMedGoogle Scholar
  40. Dolan L (2009) Meristems: the root of stem cell regulation. Curr Biol 19:459–460Google Scholar
  41. Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA 105:8790–8794PubMedGoogle Scholar
  42. Elo A, Immanen J, Nieminen K, Helariutta Y (2009) Stem cell function during plant vascular development. Semin Cell Dev Biol 20:1097–1106PubMedGoogle Scholar
  43. Erfurth I, Cromer L, Jolivet S, Girard C, Horlow C, Sun Y, To JP, Berchowitz LE, Copenhaver GP, Mercier R (2010) The cyclin-A CYCA1;2/TAM is required for the meiosis I to meiosis II transition and cooperates with OSD1 for the prophase to first meiotic division transition. PLoS Genet 6:e1000989PubMedGoogle Scholar
  44. Etchells JP, Turner SR (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137:767–774PubMedGoogle Scholar
  45. Feldman LJ, Torrey JG (1977) Nuclear changes associated with cellular dedifferentiation in pea root cortical cells cultured in vitro. J Cell Sci 28:87–105PubMedGoogle Scholar
  46. Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559PubMedGoogle Scholar
  47. Ferreira PC, Hemerly AS, Engler JD, van Montagu M, Engler G, Inze D (1994) Developmental expression of the Arabidopsis cyclin gene CYC1At. Plant Cell 6:1763–1774PubMedGoogle Scholar
  48. Filomeni G, Rotilio G, Ciriolo MR (2002) Cell signalling and the glutathione redox system. Biochem Pharmacol 64:1057–1064PubMedGoogle Scholar
  49. Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743PubMedGoogle Scholar
  50. Gagne JM, Song SK, Clark SE (2008) POLTERGEIST and PLL1 are required for stem cell function with potential roles in cell asymmetry and auxin signaling. Commun Integr Biol 1:53–55PubMedGoogle Scholar
  51. 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 449:1053–1057PubMedGoogle Scholar
  52. Geldner N, Denervaud-Tendon V, Hyman DL, Mayer U, Stierhof YD, Chory J (2009) Rapid, combinatorial analysis of membrane compartments in intact plants with a multicolor marker set. Plant J 59:169–178PubMedGoogle Scholar
  53. Gonzalez-Garcia MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E, Cano-Delgado AI (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138:849–859PubMedGoogle Scholar
  54. Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 449:1008–1013PubMedGoogle Scholar
  55. Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S (2011) Brassinosteroid perception in the epidermis controls root meristem size. Development 138:839–848PubMedGoogle Scholar
  56. Heiber I, Stroher E, Raatz B, Busse I, Kahmann U, Bevan MW, Dietz KJ, Baier M (2007) The redox imbalanced mutants of Arabidopsis differentiate signaling pathways for redox regulation of chloroplast antioxidant enzymes. Plant Physiol 143:1774–1788PubMedGoogle Scholar
  57. Heidstra R, Welch D, Scheres B (2004) Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev 18:1964–1969PubMedGoogle Scholar
  58. Helariutta Y (2007) Cell siganlling during vascular morphogenesis. Biochem Soc Trans 35:152–155PubMedGoogle Scholar
  59. 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 101:555–567PubMedGoogle Scholar
  60. Himanen K, Boucheron E, Vanneste S, de Almeida EJ, Inze D, Beeckman T (2002) Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351PubMedGoogle Scholar
  61. Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008) Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA 105:15208–15213PubMedGoogle Scholar
  62. Hirakawa Y, Kondo Y, Fukuda H (2010a) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629PubMedGoogle Scholar
  63. Hirakawa Y, Kondo Y, Fukuda H (2010b) Regulation of vascular development by CLE peptide-receptor systems. J Integr Plant Biol 52:8–16PubMedGoogle Scholar
  64. Inze D, De Veylder L (2006) Cell cycle regulation in plant development. Annu Rev Genet 40:77–105PubMedGoogle Scholar
  65. Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21:2284–2297PubMedGoogle Scholar
  66. Ishida T, Adachi S, Yoshimura M, Shimizu K, Umeda M, Sugimoto K (2010) Auxin modulates the transition from the mitotic cycle to the endocycle in Arabidopsis. Development 137:63–71PubMedGoogle Scholar
  67. Ito M (2000) Factors controlling cyclin B expression. Plant Mol Biol 43:677–690PubMedGoogle Scholar
  68. Jakoby MJ, Weinl C, Pusch S, Kuijt SJ, Merkle T, Dissmeyer N, Schnittger A (2006) Analysis of the subcellular localization, function, and proteolytic control of the Arabidopsis cyclin-dependent kinase inhibitor ICK1/KRP1. Plant Physiol 141:1293–1305PubMedGoogle Scholar
  69. Jasinski S, Riou-Khamlichi C, Roche O, Perennes C, Bergounioux C, Glab N (2002) The CDK inhibitor NtKIS1a is involved in plant development, endoreduplication and restores normal development of cyclin D3; 1-overexpressing plants. J Cell Sci 115:973–982PubMedGoogle Scholar
  70. Jasinski S, Saraiva L, Perennes C, Domenichini S, Stevens R, Raynaud C, Bergounioux C, Glab N (2003) NtKIS2, a novel tobacco cyclin-dependet kinase inhibitor is differentially expressed during the cell cycle and plant development. Plant Physiol Biochem 41:503–676Google Scholar
  71. Jiang K, Feldman LJ (2003) Root meristem establishment and maintenanace: the role of auxin. J Plant Growth Regul 21:432–440Google Scholar
  72. Jiang K, Meng YL, Feldman LJ (2003) Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment. Development 130:1429–1438PubMedGoogle Scholar
  73. Jiang K, Schwarzer C, Lally E, Zhang S, Ruzin S, Machen T, Remington SJ, Feldman L (2006) Expression and characterization of a redox-sensing green fluorescent protein (reduction-oxidation-sensitive green fluorescent protein) in Arabidopsis. Plant Physiol 141:397–403PubMedGoogle Scholar
  74. Jiang C, Gao X, Liao L, Harberd NP, Fu X (2007) Phosphate starvation root architecture and anthocyanin accumulation responses are modulated by the gibberellin-DELLA signaling pathway in Arabidopsis. Plant Physiol 145:1460–1470PubMedGoogle Scholar
  75. Jiang K, Zhu T, Diao Z, Huang H, Feldman LJ (2010) The maize root stem cell niche: a partnership between two sister cell populations. Planta 231:411–424PubMedGoogle Scholar
  76. Johnston AJ, Gruissem W (2009) Gametophyte differentiation and imprinting control in plants: crosstalk between RBR and chromatin. Commun Integr Biol 2:144–146PubMedGoogle Scholar
  77. Johnston AJ, Kirioukhova O, Barrell PJ, Rutten T, Moore JM, Baskar R, Grossniklaus U, Gruissem W (2010) Dosage-sensitive function of retinoblastoma related and convergent epigenetic control are required during the Arabidopsis life cycle. PLoS Genet 6:e1000988PubMedGoogle Scholar
  78. Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126:1055–1060PubMedGoogle Scholar
  79. Kang J, Mizukami Y, Wang H, Fowke L, Dengler NG (2007) Modification of cell proliferation patterns alters leaf vein architecture in Arabidopsis thaliana. Planta 226:1207–1218PubMedGoogle Scholar
  80. Kawano T (2003) Roles of the reactive oxygen species-generating peroxidase reactions in plant defense and growth induction. Plant Cell Rep 21:829–837PubMedGoogle Scholar
  81. Kerk N, Feldman LJ (1995) A biochemical model for the initiation an maintenance of the quiescent centr: implications for organization of root meristems. Development 121:2825–2833Google Scholar
  82. Kerk NM, Jiang K, Feldman LJ (2000) Auxin metabolism in the root apical meristem. Plant Physiol 122:925–932PubMedGoogle Scholar
  83. Kisu Y, Harada Y, Goto M, Esaka M (1997) Cloning of the pumpkin ascorbate oxidase gene and analysis of a cis-acting region involved in induction by auxin. Plant Cell Physiol 38:631–637PubMedGoogle Scholar
  84. Kondo Y, Hirakawa Y, Kieber JJ, Fukuda H (2010) CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant Cell Physiol 52:37–48PubMedGoogle Scholar
  85. Kornet N, Scheres B (2009) Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21:1070–1079PubMedGoogle Scholar
  86. Laskowski M, Grieneisen VA, Hofhuis H, Hove CA, Hogeweg P, Maree AF, Scheres B (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol 6:e307PubMedGoogle Scholar
  87. Lee SH, Singh AP, Chung GC, Ahn SJ, Noh EK, Steudle E (2004) Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport of nutrients. Physiol Plant 120:413–420PubMedGoogle Scholar
  88. Liso R, De Tullio MC, Ciraci S, Balestrini R, La Rocca N, Bruno L, Chiappetta A, Bitonti MB, Bonfante P, Arrigoni O (2004) Localization of ascorbic acid, ascorbic acid oxidase, and glutathione in roots of Cucurbita maxima L. J Exp Bot 55:2589–2597PubMedGoogle Scholar
  89. Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287PubMedGoogle Scholar
  90. Magyar Z, De Veylder L, Atanassova A, Bako L, Inze D, Bogre L (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17:2527–2541PubMedGoogle Scholar
  91. Mahonen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Tormakangas K, Ikeda Y, Oka A, Kakimoto T, Helariutta Y (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311:94–98PubMedGoogle Scholar
  92. Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci USA 105:20027–20031PubMedGoogle Scholar
  93. May MJ, Vernoux T, Sanchez-Fernandez R, Van Montagu M, Inze D (1998) Evidence for posttranscriptional activation of gamma-glutamylcysteine synthetase during plant stress responses. Proc Natl Acad Sci USA 95:12049–12054PubMedGoogle Scholar
  94. Menges M, Murray JA (2002) Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. Plant J 30:203–212PubMedGoogle Scholar
  95. Menges M, de Jager SM, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566PubMedGoogle Scholar
  96. Menges M, Pavesi G, Morandini P, Bogre L, Murray JA (2007) Genomic organization and evolutionary conservation of plant D-type cyclins. Plant Physiol 145:1558–1576PubMedGoogle Scholar
  97. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN (2010) Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329:1306–1311PubMedGoogle Scholar
  98. Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S (2010) The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 20:1138–1143PubMedGoogle Scholar
  99. Nakagami H, Kawamura K, Sugisaka K, Sekine M, Shinmyo A (2002) Phosphorylation of retinoblastoma-related protein by the cyclin D/cyclin-dependent kinase complex is activated at the G1/S-phase transition in tobacco. Plant Cell 14:1847–1857PubMedGoogle Scholar
  100. Nakajima K, Sena G, Nawy T, Benfey PN (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature 413:307–311PubMedGoogle Scholar
  101. Nieuwland J, Maughan S, Dewitte W, Scofield S, Sanz L, Murray JA (2009) The D-type cyclin CYCD4;1 modulates lateral root density in Arabidopsis by affecting the basal meristem region. Proc Natl Acad Sci USA 106:22528–22533PubMedGoogle Scholar
  102. Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850PubMedGoogle Scholar
  103. Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67PubMedGoogle Scholar
  104. Oakenfull EA, Riou-Khamlichi C, Murray JA (2002) Plant D-type cyclins and the control of G1 progression. Philos Trans R Soc Lond B Biol Sci 357:749–760PubMedGoogle Scholar
  105. Oliveira RA, Nasmyth K (2010) Getting through anaphase: splitting the sisters and beyond. Biochem Soc Trans 38:1639–1644PubMedGoogle Scholar
  106. Peres A, Churchman ML, Hariharan S, Himanen K, Verkest A, Vandepoele K, Magyar Z, Hatzfeld Y, Van Der Schueren E, Beemster GT, Frankard V, Larkin JC, Inze D, De Veylder L (2007) Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J Biol Chem 282:25588–25596PubMedGoogle Scholar
  107. Peret B, De Rybel B, Casimiro I, Benkova E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends Plant Sci 14:399–408PubMedGoogle Scholar
  108. Pernas M, Ryan E, Dolan L (2010) SCHIZORIZA controls tissue system complexity in plants. Curr Biol 20:818–823PubMedGoogle Scholar
  109. Petersson SV, Johansson AI, Kowalczyk M, Makoveychuk A, Wang JY, Moritz T, Grebe M, Benfey PN, Sandberg G, Ljung K (2009) An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 21:1659–1668PubMedGoogle Scholar
  110. Pfeiffer W, Hoftberger M (2001) Oxidative burst in Chenopodium rubrum suspension cells: induction by auxin and osmotic changes. Physiol Plant 111:144–150Google Scholar
  111. Pignocchi C, Foyer CH (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Curr Opin Plant Biol 6:379–389PubMedGoogle Scholar
  112. Pignocchi C, Fletcher JM, Wilkinson JE, Barnes JD, Foyer CH (2003) The function of ascorbate oxidase in tobacco. Plant Physiol 132:1631–1641PubMedGoogle Scholar
  113. Planchais S, Perennes C, Glab N, Mironov V, Inze D, Bergounioux C (2002) Characterization of cis-acting element involved in cell cycle phase-independent activation of Arath;CycB1;1 transcription and identification of putative regulatory proteins. Plant Mol Biol 50:111–127PubMedGoogle Scholar
  114. Potters G, De Gara L, Asard H, Horemans N (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiol Biochem 40:537–548Google Scholar
  115. Potters G, Horemans N, Bellone S, Caubergs RJ, Trost P, Guisez Y, Asard H (2004) Dehydroascorbate influences the plant cell cycle through a glutathione-independent reduction mechanism. Plant Physiol 134:1479–1487PubMedGoogle Scholar
  116. Potters G, Pasternak TP, Guisez Y, Palme KJ, Jansen MA (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105PubMedGoogle Scholar
  117. Qi R, John PC (2007) Expression of genomic AtCYCD2;1 in Arabidopsis induces cell division at smaller cell sizes: implications for the control of plant growth. Plant Physiol 144:1587–1597PubMedGoogle Scholar
  118. Reichheld JP, Vernoux T, Lardon F, van Montagu M, Inze D (1999) Specific checkpoints regulate plant cell cycle progression in response to oxidative stress. Plant J 17:647–656Google Scholar
  119. Renaudin JP, Colasanti J, Rime H, Yuan Z, Sundaresan V (1994) Cloning of four cyclins from maize indicates that higher plants have three structurally distinct groups of mitotic cyclins. Proc Natl Acad Sci USA 91:7375–7379PubMedGoogle Scholar
  120. Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JA (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544PubMedGoogle Scholar
  121. Sanchez-Calderon L, Lopez-Bucio J, Chacon-Lopez A, Cruz-Ramirez A, Nieto-Jacobo F, Dubrovsky JG, Herrera-Estrella L (2005) Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. Plant Cell Physiol 46:174–184PubMedGoogle Scholar
  122. Sanchez-Fernandez R, Fricker M, Corben LB, White NS, Sheard N, Leaver CJ, Van Montagu M, Inze D, May MJ (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proc Natl Acad Sci USA 94:2745–2750PubMedGoogle Scholar
  123. Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J, Wen B, Quelhas P, De Jager S, Titmus C, Campilho A, Ren H, Estelle M, Wang H, Murray JA (2011) The Arabidopsis D-type cyclin CYCD2;1 and the inhibitor ICK2/KRP2 modulate auxin-induced lateral root formation. Plant Cell 23:641–660PubMedGoogle Scholar
  124. Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakagami H, Scheible WR, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814PubMedGoogle Scholar
  125. Schafer FQ, Buettner GR (2001) Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212PubMedGoogle Scholar
  126. Schnittger A, Schobinger U, Stierhof YD, Hulskamp M (2002a) Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 12:415–420PubMedGoogle Scholar
  127. Schnittger A, Schobinger U, Bouyer D, Weinl C, Stierhof YD, Hulskamp M (2002b) Ectopic D-type cyclin expression induces not only DNA replication but also cell division in Arabidopsis trichomes. Proc Natl Acad Sci USA 99:6410–6415PubMedGoogle Scholar
  128. Schopfer P (2001) Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. Plant J 28:679–688PubMedGoogle Scholar
  129. Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828PubMedGoogle Scholar
  130. Serralbo O, Perez-Perez JM, Heidstra R, Scheres B (2006) Non-cell-autonomous rescue of anaphase-promoting complex function revealed by mosaic analysis of HOBBIT, an Arabidopsis CDC27 homolog. Proc Natl Acad Sci USA 103:13250–13255PubMedGoogle Scholar
  131. Shackelford RE, Kaufmann WK, Paules RS (2000) Oxidative stress and cell cycle checkpoint function. Free Radic Biol Med 28:1387–1404PubMedGoogle Scholar
  132. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminium. Plant Cell Rep 26:2027–2038PubMedGoogle Scholar
  133. Shen W (2002) The plant E2F-Rb pathway and epigenetic control. Trend Plant Sci 7:505–511Google Scholar
  134. 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 15:98–109PubMedGoogle Scholar
  135. 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 466:128–132PubMedGoogle Scholar
  136. Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914PubMedGoogle Scholar
  137. Takahama U (1996) Effects of fusicoccin and indole-3-acetic acid on the levels of ascorbic acid and dehydorascorbic acid in the apoplast during elongation of epicotyl segments of Vigna angularis. Physiol Plant 98:731–736Google Scholar
  138. Takahashi I, Kojima S, Sakaguchi N, Umeda-Hara C, Umeda M (2010) Two Arabidopsis cyclin A3s possess G1 cyclin-like features. Plant Cell Rep 29:307–315PubMedGoogle Scholar
  139. Tan X, Calderon-Villalobos LI, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645PubMedGoogle Scholar
  140. Ten Hove CA, Willemsen V, de Vries WJ, van Dijken A, Scheres B, Heidstra R (2010) SCHIZORIZA encodes a nuclear factor regulating asymmetry of stem cell divisions in the Arabidopsis root. Curr Biol 20:452–457PubMedGoogle Scholar
  141. Teotia S, Muthuswamy S, Lamb RS (2010) Radical-induced cell death1 and similar to RCD one1 and the stress-induced morphogenetic response. Plant Signal Behav 5:143–145PubMedGoogle Scholar
  142. Torres M (2010) ROS in biotic interactions. Physiol Plant 138:414–429PubMedGoogle Scholar
  143. Torres Acosta JA, Fowke LC, Wang H (2011) Analyses of phylogeny, evolution, conserved sequences and genome-wide expression of the ICK/KRP family of plant CDK inhibitors. Ann Bot 107(7):1141–1157PubMedGoogle Scholar
  144. Tyburski J, Krzeminski L, Tretyn A (2008) Exogenous auxin affects ascorbate metabolism in roots of tomato seedlings. Plant Growth Regul 54:203–215Google Scholar
  145. Tyburski J, Dunajska K, Tretyn A (2009) Reactive oxygen species localization in roots of Arabidopsis thaliana seedlings grown under phosphate deficiency. Plant Growth Regul 59:27–36Google Scholar
  146. Tyburski J, Dunajska K, Tretyn A (2010) A role for redox factors in shaping root architecture under phosphorus deficiency. Plant Signal Behav 5:64–66PubMedGoogle Scholar
  147. Ubeda-Tomas S, Federici F, Casimiro I, Beemster GT, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ (2009) Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 19:1194–1199PubMedGoogle Scholar
  148. 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 390:287–289PubMedGoogle Scholar
  149. Van Leene J, Hollunder J, Eeckhout D, Persiau G, Van De Slijke E, Stals H, Van Isterdael G, Verkest A, Neirynck S, Buffel Y, De Bodt S, Maere S, Laukens K, Pharazyn A, Ferreira PC, Eloy N, Renne C, Meyer C, Faure JD, Steinbrenner J, Beynon J, Larkin JC, Van de Peer Y, Hilson P, Kuiper M, De Veylder L, Van Onckelen H, Inze D, Witters E, De Jaeger G (2010) Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana. Mol Syst Biol 6:397PubMedGoogle Scholar
  150. Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D (2002) Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell 14:903–916PubMedGoogle Scholar
  151. Vanneste S, De Rybel B, Beemster GT, Ljung K, De Smet I, Van Isterdael G, Naudts M, Iida R, Gruissem W, Tasaka M, Inze D, Fukaki H, Beeckman T (2005) Cell cycle progression in the pericycle is not sufficient for SOLITARY ROOT/IAA14-mediated lateral root initiation in Arabidopsis thaliana. Plant Cell 17:3035–3050PubMedGoogle Scholar
  152. Verkest A, Manes CL, Vercruysse S, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inze D, De Veylder L (2005) The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes. Plant Cell 17:1723–1736PubMedGoogle Scholar
  153. Vernoux T, Wilson RC, Seeley KA, Reichheld JP, Muroy S, Brown S, Maughan SC, Cobbett CS, Van Montagu M, Inze D, May MJ, Sung ZR (2000) The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development. Plant Cell 12:97–110PubMedGoogle Scholar
  154. Wang H, Qi Q, Schorr P, Cutler AJ, Crosby WL, Fowke LC (1998) ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. Plant J 1:501–510Google Scholar
  155. Wang H, Zhou Y, Gilmer S, Whitwill S, Fowke LC (2000) Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. Plant J 24:613–623PubMedGoogle Scholar
  156. Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105:18625–18630PubMedGoogle Scholar
  157. Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349PubMedGoogle Scholar
  158. Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K, Blilou I, Rouquie D, Benkova E, Scheres B, Friml J (2006) Polar PIN localization directs auxin flow in plants. Science 312:883PubMedGoogle Scholar
  159. Wu S, Scheible WR, Schindelasch D, Van Den Daele H, De Veylder L, Baskin TI (2010) A conditional mutation in Arabidopsis thaliana separase induces chromosome non-disjunction, aberrant morphogenesis and cyclin B1;1 stability. Development 137:953–961PubMedGoogle Scholar
  160. Zhou Y, Fowke LC, Wang H (2002) Plant CDK inhibitors: studies of interactions with cell cycle regulators in the yeast two-hybrid system and functional comparisons in transgenic Arabidopsis plants. Plant Cell Rep 20:967–975Google Scholar
  161. Zhou Y, Wang H, Gilmer S, Whitwill S, Fowke LC (2003) Effects of co-expressing the plant CDK inhibitor ICK1 and D-type cyclin genes on plant growth, cell size and ploidy in Arabidopsis thaliana. Planta 216:604–613PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Luis Sanz
    • 1
  • James A. H. Murray
    • 2
  • Walter Dewitte
    • 2
    Email author
  1. 1.Centro Hispano Luso de Investigaciones AgrariasUniversidad de SalamancaSalamancaSpain
  2. 2.Cardiff School of BiosciencesUniversity of CardiffWalesUK

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