Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004960.

Lateral root formation can be divided into two major phases: pericycle activation and meristem establishment. In Arabidopsis, the first lateral root initiation event is spatially and temporally asynchronous and involves a limited number of cells in the xylem pericycle. To study the molecular regulation during pericycle activation, we developed a lateral root–inducible system. Successive treatments with an auxin transport inhibitor and exogenous auxin were used to prevent the first formative divisions and then to activate the entire pericycle. Our morphological and molecular data show that, in this inducible system, xylem pericycle activation was synchronized and enhanced to cover the entire length of the root. The results also indicate that the inducible system can be considered a novel in planta system for the study of synchronized cell cycle reactivation. In addition, the expression patterns of Kip-Related Protein2 (KRP2) in the pericycle and its ectopic expression data revealed that the cyclin-dependent kinase inhibitor plays a significant role in the regulation of lateral root initiation. KRP2 appears to regulate early lateral root initiation by blocking the G1-to-S transition and to be regulated transcriptionally by auxin.

[1]  D. Inzé,et al.  Two Arabidopsis cyclin promoters mediate distinctive transcriptional oscillation in synchronized tobacco BY-2 cells. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[2]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[3]  D. Inzé,et al.  Transcript profiling of early lateral root initiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Murray,et al.  The role and regulation of D-type cyclins in the plant cell cycle , 2000, Plant Molecular Biology.

[5]  Franky R. G. Terras,et al.  Functional Analysis of Cyclin-Dependent Kinase Inhibitors of Arabidopsis , 2001, The Plant Cell Online.

[6]  C. Gutiérrez,et al.  A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. , 2001, The Plant journal : for cell and molecular biology.

[7]  M. Menges,et al.  Synchronous Arabidopsis suspension cultures for analysis of cell-cycle gene activity. , 2002, The Plant journal : for cell and molecular biology.

[8]  D. Inzé,et al.  Analysis of cell division parameters and cell cycle gene expression during the cultivation of Arabidopsis thaliana cell suspensions. , 2001, Journal of experimental botany.

[9]  T. Beeckman,et al.  Embedding Thin Plant Specimens for Oriented Sectioning , 2000, Biotechnic & histochemistry : official publication of the Biological Stain Commission.

[10]  H. Nusbaum,et al.  Formation of lateral root meristems is a two-stage process. , 1995, Development.

[11]  Hong Wang,et al.  Expression of the plant cyclin-dependent kinase inhibitor ICK1 affects cell division, plant growth and morphology. , 2000, The Plant journal : for cell and molecular biology.

[12]  S. Kosugi,et al.  Interaction of the Arabidopsis E2F and DP Proteins Confers Their Concomitant Nuclear Translocation and Transactivation , 2002, Plant Physiology.

[13]  S. Avanzi,et al.  Cytochemical Analyses on Cellular Differentiation in the Root Tip of Allium Cepa , 1970 .

[14]  J. Malamy,et al.  Environmental regulation of lateral root initiation in Arabidopsis. , 2001, Plant physiology.

[15]  C. Scheuring,et al.  A molecular marker for lateral root initiation: The RSI-1 gene of tomato (Lycopersicon esculentum Mill) is activated in early lateral root primordia , 1994, Molecular and General Genetics MGG.

[16]  P. Genschik,et al.  Cell Cycle – Dependent Proteolysis in Plants : Identification of the Destruction Box Pathway and Metaphase Arrest Produced by the Proteasome Inhibitor MG 132 , 1998 .

[17]  D. Chriqui Induction de prolifération des cellules prérhizogènes: auxine et polyamines , 1985 .

[18]  D. Inzé,et al.  Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa–DPa transcription factor , 2002, The EMBO journal.

[19]  D. Inzé,et al.  Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana , 2000, Planta.

[20]  A. Müller,et al.  Indole-3-acetic acid is synthesized from L-tryptophan in roots of Arabidopsis thaliana , 1998, Planta.

[21]  D. Inzé,et al.  Developmental expression of the Arabidopsis thaliana CycA2;1 gene , 2000, Planta.

[22]  P. Genschik,et al.  Cell Cycle–Dependent Proteolysis in Plants: Identification of the Destruction Box Pathway and Metaphase Arrest Produced by the Proteasome Inhibitor MG132 , 1998, Plant Cell.

[23]  D. Inzé,et al.  Effect of auxin, cytokinin, and sucrose on cell cycle gene expression in Arabidopsis thaliana cell suspension cultures , 2002, Plant Cell, Tissue and Organ Culture.

[24]  Spatial pattern of cdc2 expression in relation to meristem activity and cell proliferation during plant development. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Inzé,et al.  Characterization of two distinct DP‐related genes from Arabidopsis thaliana 1 , 2000, FEBS letters.

[26]  D. Inzé,et al.  The peri-cell-cycle in Arabidopsis. , 2001, Journal of experimental botany.

[27]  D. Inzé,et al.  cdc2a expression in Arabidopsis is linked with competence for cell division. , 1993, The Plant cell.

[28]  W. Crosby,et al.  A plant cyclin-dependent kinase inhibitor gene , 1997, Nature.

[29]  D. Inzé,et al.  CDK-related protein kinases in plants , 2000, Plant Molecular Biology.

[30]  P. Benfey,et al.  Organization and cell differentiation in lateral roots of Arabidopsis thaliana. , 1997, Development.

[31]  Travis W. Banks,et al.  Identification of an SCF ubiquitin-ligase complex required for auxin response in Arabidopsis thaliana. , 1999, Genes & development.

[32]  D. Inzé,et al.  Cyclin-Dependent Kinases and Cell Division in Plants—The Nexus , 1999, Plant Cell.

[33]  D. Inzé,et al.  Auxin Transport Promotes Arabidopsis Lateral Root Initiation , 2001, Plant Cell.

[34]  D. Inzé,et al.  Chemical inhibitors: a tool for plant cell cycle studies , 2000, FEBS letters.

[35]  K. Ljung,et al.  Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. , 2002, The Plant journal : for cell and molecular biology.

[36]  G. Fink,et al.  A pathway for lateral root formation in Arabidopsis thaliana. , 1995, Genes & development.

[37]  Hong Wang,et al.  ICK1, a cyclin-dependent protein kinase inhibitor from Arabidopsis thaliana interacts with both Cdc2a and CycD3, and its expression is induced by abscisic acid. , 1998, The Plant journal : for cell and molecular biology.

[38]  J. Murray,et al.  A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. , 1995, The Plant cell.

[39]  M. Van Montagu,et al.  In situ hybridization to mRNA of Arabidopsis tissue sections. , 2001, Methods.

[40]  D. Inzé,et al.  Developmental expression of the arabidopsis cyclin gene cyc1At. , 1994, The Plant cell.

[41]  D. Inzé,et al.  Identification of novel cyclin-dependent kinases interacting with the CKS1 protein of Arabidopsis. , 2001, Journal of experimental botany.

[42]  P. Colowit,et al.  Experimental Studies on Lateral Root Formation in Radish Seedling Roots: II. Analysis of the Dose-Response to Exogenous Auxin. , 1988, Plant physiology.

[43]  Ottoline Leyser,et al.  An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root , 1999, Cell.

[44]  D. Inzé,et al.  Three discrete classes of Arabidopsis cyclins are expressed during different intervals of the cell cycle. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[45]  E. Coen,et al.  Patterns of cell division revealed by transcriptional regulation of genes during the cell cycle in plants. , 1994, The EMBO journal.

[46]  P. Beer-Romero,et al.  Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. , 1995, Science.

[47]  D. Inzé,et al.  Characterization and classification of plant cyclin sequences related to A- and B-type cyclins , 1998 .

[48]  M. Van Montagu,et al.  Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Inzé,et al.  When plant cells decide to divide. , 2001, Trends in plant science.

[50]  M. Durham,et al.  Experimental Studies on Lateral Root Formation in Radish Seedling Roots. I. General Methods, Developmental Stages, and Spontaneous Formation of Laterals , 1982, Botanical Gazette.

[51]  N. Segil,et al.  p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. , 1999, Development.

[52]  F. Skoog,et al.  A revised medium for rapid growth and bio assays with tobacco tissue cultures , 1962 .