Natural genetic variation in Arabidopsis identifies BREVIS RADIX , a novel regulator of cell proliferation and elongation in the root

Mutant analysis has been tremendously successful in deciphering the genetics of plant development. However, less is known about the molecular basis of morphological variation within species, which is caused by naturally occurring alleles. In this study, we succeeded in isolating a novel regulator of root growth by exploiting natural genetic variation in the model plant Arabidopsis. Quantitative trait locus analysis of a cross between isogenized accessions revealed that a single locus is responsible for approximately 80% of the variance of the observed difference in root length. This gene, named BREVIS RADIX (BRX), controls the extent of cell proliferation and elongation in the growth zone of the root tip. We isolated BRX by positional cloning. BRX is a member of a small group of highly conserved genes, the BRX gene family, which is only found in multicellular plants. Analyses of Arabidopsis single and double mutants suggest that BRX is the only gene of this family with a role in root development. The BRX protein is nuclear localized and activates transcription in a heterologous yeast system, indicating that BRX family proteins represent a novel class of transcription factors. Thus, we have identified a novel regulatory factor controlling quantitative aspects of root growth.

[1]  P. Benfey,et al.  Conditional root expansion mutants of Arabidopsis. , 1995, Development.

[2]  A. Brice,et al.  A QTL for flowering time in Arabidopsis reveals a novel allele of CRY2 , 2002, Nature Genetics.

[3]  M. C. Grant,et al.  EVOLUTIONARY SIGNIFICANCE OF LOCAL GENETIC DIFFERENTIATION IN PLANTS , 1996 .

[4]  H. Leyser,et al.  Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[5]  M Koornneef,et al.  Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. , 2000, Trends in plant science.

[6]  J. Reed,et al.  Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. , 1999, Development.

[7]  P. Benfey,et al.  Intercellular movement of the putative transcription factor SHR in root patterning , 2001, Nature.

[8]  J. Chory,et al.  Natural variation in light sensitivity of Arabidopsis , 2001, Nature Genetics.

[9]  S. Sabatini,et al.  SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. , 2003, Genes & development.

[10]  J. Guardiola.  Plant hormones. Physiology, biochemistry and molecular biology , 1996 .

[11]  D. Inzé,et al.  Cell cycle: the key to plant growth control? , 2003, Trends in plant science.

[12]  P. Benfey,et al.  The SCARECROW Gene Regulates an Asymmetric Cell Division That Is Essential for Generating the Radial Organization of the Arabidopsis Root , 1996, Cell.

[13]  D. Inzé,et al.  Molecular Markers and Cell Cycle Inhibitors Show the Importance of Cell Cycle Progression in Nematode-Induced Galls and Syncytia , 1999, The Plant Cell.

[14]  D. Inzé,et al.  CKS1At overexpression in Arabidopsis thaliana inhibits growth by reducing meristem size and inhibiting cell-cycle progression. , 2001, The Plant journal : for cell and molecular biology.

[15]  T. Baskin,et al.  Stunted plant 1 mediates effects of cytokinin, but not of auxin, on cell division and expansion in the root of Arabidopsis. , 2000, Plant physiology.

[16]  J. Murray,et al.  Cyclin D control of growth rate in plants , 2022 .

[17]  C. Turnbull,et al.  Micrografting techniques for testing long-distance signalling in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[18]  C. Lamb,et al.  Control of root growth and development by cyclin expression , 1996, Nature.

[19]  X. Deng,et al.  HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain , 2000, The EMBO journal.

[20]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

[21]  P. Benfey,et al.  Root development in Arabidopsis: four mutants with dramatically altered root morphogenesis. , 1993, Development.

[22]  R. Amasino,et al.  Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. , 2000, Science.

[23]  T. Baskin,et al.  Analysis of cell division and elongation underlying the developmental acceleration of root growth in Arabidopsis thaliana. , 1998, Plant physiology.

[24]  Gabriel Ciobanu,et al.  Molecular interaction , 2002, Theor. Comput. Sci..

[25]  J. Thornton,et al.  An overview of the structures of protein-DNA complexes , 2000, Genome Biology.

[26]  Xing Wang Deng,et al.  Molecular interaction between COP1 and HY5 defines a regulatory switch for light control of Arabidopsis development. , 1998, Molecular cell.

[27]  Detlef Weigel,et al.  Large-scale identification of single-feature polymorphisms in complex genomes. , 2003, Genome research.

[28]  Xiangdong Fu,et al.  Auxin promotes Arabidopsis root growth by modulating gibberellin response , 2003, Nature.

[29]  Claudia van den Berg,et al.  Short-range control of cell differentiation in the Arabidopsis root meristem , 1997, Nature.

[30]  Justin O Borevitz,et al.  The Impact of Genomics on the Study of Natural Variation in Arabidopsis , 2003, Plant Physiology.

[31]  B. Scheres,et al.  Root-Specific CLE19 Overexpression and the sol1/2 Suppressors Implicate a CLV-like Pathway in the Control of Arabidopsis Root Meristem Maintenance , 2003, Current Biology.

[32]  T. Mitchell-Olds,et al.  Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. , 2003, Genome research.

[33]  T. Mitchell-Olds,et al.  Establishment of a high-efficiency SNP-based framework marker set for Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

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

[35]  A. Weig,et al.  The complete set of genes encoding major intrinsic proteins in Arabidopsis provides a framework for a new nomenclature for major intrinsic proteins in plants. , 2001, Plant physiology.

[36]  Philip N Benfey,et al.  The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling , 2000, Cell.

[37]  Rüdiger Simon,et al.  Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis , 2003, Development Genes and Evolution.

[38]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[39]  Luis Herrera-Estrella,et al.  Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System1 , 2002, Plant Physiology.

[40]  Gerrit T.S. Beemster,et al.  Variation in Growth Rate between Arabidopsis Ecotypes Is Correlated with Cell Division and A-Type Cyclin-Dependent Kinase Activity1 , 2002, Plant Physiology.

[41]  B. Forde,et al.  An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. , 1998, Science.

[42]  O. Leyser.  Molecular genetics of auxin signaling. , 2002, Annual review of plant biology.

[43]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

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

[45]  C. Beveridge,et al.  MAX4 and RMS1 are orthologous dioxygenase-like genes that regulate shoot branching in Arabidopsis and pea. , 2003, Genes & development.

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

[47]  Valérie Laucou,et al.  Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014928 , 2003, The Plant Cell Online.