A turanose-insensitive mutant suggests a role for WOX5 in auxin homeostasis in Arabidopsis thaliana.

Sugars acting as signalling molecules regulate many developmental processes in plants, including lateral and adventitious root production. Turanose, a non-metabolizable sucrose analogue, profoundly affects the growth pattern of Arabidopsis seedlings. Turanose-treated seedlings are characterized by a very short primary root and a short hypocotyl showing the production of adventitious roots. A turanose-insensitive (tin) mutant was identified and characterized. Because of a T-DNA insertion and a chromosomal translocation, tin expresses a chimeric form of WOX5, a gene known to be expressed in the root quiescent centre. The tin mutation can be complemented by overexpression of WOX5, suggesting it is a loss-of-function mutant. We found that WOX5 is both turanose- and auxin-inducible. Moreover, turanose insensitivity is associated with altered auxin homeostasis, as demonstrated by the constitutive activation of indole acetic acid (IAA) conjugation and SUPERROOT2 expression in tin. On the basis of turanose effects on wild-type seedlings and the tin molecular and hormonal phenotype, we propose a role for WOX5 in the root apical meristem as a negative trigger of IAA homeostatic mechanisms allowing the maintenance of a restricted area of auxin maximum, which is required for a correct root-formation pattern.

[1]  P. Naur,et al.  Arabidopsis mutants in the C-S lyase of glucosinolate biosynthesis establish a critical role for indole-3-acetaldoxime in auxin homeostasis. , 2004, The Plant journal : for cell and molecular biology.

[2]  R C Atkinson,et al.  Environmental regulation. , 1980, Science.

[3]  R. Jefferson Assaying chimeric genes in plants: The GUS gene fusion system , 1987, Plant Molecular Biology Reporter.

[4]  D. Inzé,et al.  Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. , 1995, The Plant cell.

[5]  F. Tax,et al.  T-DNA-associated duplication/translocations in Arabidopsis. Implications for mutant analysis and functional genomics. , 2001, Plant physiology.

[6]  G. Sandberg,et al.  Dissecting Arabidopsis lateral root development. , 2003, Trends in plant science.

[7]  N. Mitsukawa,et al.  Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. , 1995, The Plant journal : for cell and molecular biology.

[8]  T. Roitsch,et al.  Metabolizable and Non-Metabolizable Sugars Activate Different Signal Transduction Pathways in Tomato1 , 2002, Plant Physiology.

[9]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.

[10]  T. Boller,et al.  Trehalose induces the ADP-glucose pyrophosphorylase gene, ApL3, and starch synthesis in Arabidopsis. , 2000, Plant physiology.

[11]  U. Roessner,et al.  The sucrose analog palatinose leads to a stimulation of sucrose degradation and starch synthesis when supplied to discs of growing potato tubers. , 2001, Plant physiology.

[12]  P. León,et al.  Hexokinase as a sugar sensor in higher plants. , 1997, The Plant cell.

[13]  D. Inzé,et al.  Auxin regulation of cell cycle and its role during lateral root initiation , 2005 .

[14]  Mariusz Kowalczyk,et al.  Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana , 2002, Plant Molecular Biology.

[15]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[16]  S. Klosterman,et al.  Plant HMG proteins bearing the AT-hook motif , 2002 .

[17]  D. Shasha,et al.  A Gene Expression Map of the Arabidopsis Root , 2003, Science.

[18]  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.

[19]  Masashi Yamada,et al.  Sites and Regulation of Auxin Biosynthesis in Arabidopsis Roots , 2005, The Plant Cell Online.

[20]  D. Ware,et al.  Seed and molecular resources for Arabidopsis. , 2000, Plant physiology.

[21]  G. Horiguchi,et al.  Mutations in a gene for plastid ribosomal protein S6-like protein reveal a novel developmental process required for the correct organization of lateral root meristem in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[22]  M. Caboche,et al.  Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. , 1998, The Plant journal : for cell and molecular biology.

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

[24]  K. Sato-Nara,et al.  Sugar-induced adventitious roots in Arabidopsis seedlings , 2003, Journal of Plant Research.

[25]  A. Ray,et al.  Pollen tube guidance by the female gametophyte. , 1997, Development.

[26]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[27]  T. Laux,et al.  Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana , 2004, Development.

[28]  L. Campisi,et al.  Generation of enhancer trap lines in Arabidopsis and characterization of expression patterns in the inflorescence. , 1999, The Plant journal : for cell and molecular biology.

[29]  S. Delrot,et al.  Affinity purification of sucrose binding proteins from the plant plasma membrane. , 1994, Biochimica et biophysica acta.

[30]  J. Ward,et al.  Substrate Specificity of the Arabidopsis thaliana Sucrose Transporter AtSUC2* , 2003, Journal of Biological Chemistry.

[31]  K. Ljung,et al.  The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[32]  K. Koch,et al.  Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. , 2004, Current opinion in plant biology.

[33]  M. Matsuoka,et al.  Isolation and characterization of a rice WUSCHEL-type homeobox gene that is specifically expressed in the central cells of a quiescent center in the root apical meristem. , 2003, The Plant journal : for cell and molecular biology.

[34]  N. Ceccarelli,et al.  Endogenous auxins and embryogenesis in Phaseolus coccineus , 2001 .

[35]  C Camilleri,et al.  Major chromosomal rearrangements induced by T-DNA transformation in Arabidopsis. , 1998, Genetics.

[36]  S. Gibson,et al.  Control of plant development and gene expression by sugar signaling. , 2005, Current opinion in plant biology.

[37]  J. Malamy,et al.  Intrinsic and environmental response pathways that regulate root system architecture. , 2005, Plant, cell & environment.

[38]  Stuart A. Casson,et al.  Genes and signalling in root development , 2003 .

[39]  S. Delrot,et al.  Stimulation of sugar exit from leaf tissues ofVicia faba L. , 1988, Planta.

[40]  P. Perata,et al.  Sugar Repression of a Gibberellin-Dependent Signaling Pathway in Barley Embryos. , 1997, The Plant cell.

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

[42]  P. Perata,et al.  Glucose and disaccharide-sensing mechanisms modulate the expression of alpha-amylase in barley embryos. , 2000, Plant physiology.

[43]  S. Clough,et al.  Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. , 1998, The Plant journal : for cell and molecular biology.

[44]  Linda A. Castle,et al.  Genetic and molecular characterization of embryonic mutants identified following seed transformation in Arabidopsis , 1993, Molecular and General Genetics MGG.

[45]  F. Tognoni,et al.  Quantification of ethylene losses in different container-seal systems and comparison of biotic and abiotic contributions to ethylene accumulation in cultured tissues , 1992 .

[46]  Klaus Palme,et al.  AtPIN4 Mediates Sink-Driven Auxin Gradients and Root Patterning in Arabidopsis , 2002, Cell.

[47]  M. Schmitt,et al.  Sugar Transport into Protoplasts Isolated from Developing Soybean Cotyledons : II. Sucrose Transport Kinetics, Selectivity, and Modeling Studies. , 1984, Plant physiology.

[48]  J. Lee,et al.  Derepression of the activity of genetically engineered heat shock factor causes constitutive synthesis of heat shock proteins and increased thermotolerance in transgenic Arabidopsis. , 1995, The Plant journal : for cell and molecular biology.