Mechanical Stimuli Modulate Lateral Root Organogenesis1[W][OA]

Unlike mammals, whose development is limited to a short temporal window, plants produce organs de novo throughout their lifetime in order to adapt their architecture to the prevailing environmental conditions. The production of lateral roots represents one example of such postembryonic organogenesis. An endogenous developmental program likely imposes an ordered arrangement on the position of new lateral roots. However, environmental stimuli such as nutrient levels also affect the patterning of lateral root production. In addition, we have found that mechanical forces can act as one of the triggers that entrain lateral root production to the environment of the Arabidopsis (Arabidopsis thaliana) plant. We observed that physical bending of the root recruited new lateral root formation to the convex side of the resultant bend. Transient bending of 20 s was sufficient to elicit this developmental program. Such bending triggered a Ca2+ transient within the pericycle, and blocking this change in Ca2+ also blocked recruitment of new lateral root production to the curved region of the root. The initial establishment of the mechanically induced lateral root primordium was independent of an auxin supply from the shoot and was not disrupted by mutants in a suite of auxin transporters and receptor/response elements. These results suggest that Ca2+ may be acting to translate the mechanical forces inherent in growth to a developmental response in roots.

[1]  Simon Gilroy,et al.  Ca2+ Regulates Reactive Oxygen Species Production and pH during Mechanosensing in Arabidopsis Roots[C][W] , 2009, The Plant Cell Online.

[2]  Klaus Palme,et al.  Mechanical induction of lateral root initiation in Arabidopsis thaliana , 2008, Proceedings of the National Academy of Sciences.

[3]  Christophe Godin,et al.  An Auxin Transport-Based Model of Root Branching in Arabidopsis thaliana , 2008, PloS one.

[4]  M. Mattson,et al.  Superoxide Flashes in Single Mitochondria , 2008, Cell.

[5]  S. Gilroy,et al.  Imaging of the Yellow Cameleon 3.6 Indicator Reveals That Elevations in Cytosolic Ca2+ Follow Oscillating Increases in Growth in Root Hairs of Arabidopsis1[W][OA] , 2008, Plant Physiology.

[6]  J. G. Dubrovsky,et al.  Auxin acts as a local morphogenetic trigger to specify lateral root founder cells , 2008, Proceedings of the National Academy of Sciences.

[7]  Simon Gilroy,et al.  Touch Sensing and Thigmotropism , 2008 .

[8]  Daniel R. Lewis,et al.  Mutations in Arabidopsis Multidrug Resistance-Like ABC Transporters Separate the Roles of Acropetal and Basipetal Auxin Transport in Lateral Root Development[W][OA] , 2007, The Plant Cell Online.

[9]  Joel s. Brown,et al.  Roots in space: a spatially explicit model for below-ground competition in plants , 2007, Proceedings of the Royal Society B: Biological Sciences.

[10]  Michal Sharon,et al.  Mechanism of auxin perception by the TIR1 ubiquitin ligase , 2007, Nature.

[11]  Tom Beeckman,et al.  Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis , 2007, Development.

[12]  G. Sandberg,et al.  AXR4 Is Required for Localization of the Auxin Influx Facilitator AUX1 , 2006, Science.

[13]  D. Inzé,et al.  Lateral Root Initiation or the Birth of a New Meristem , 2006, Plant Molecular Biology.

[14]  Masashi Yamada,et al.  Plant development is regulated by a family of auxin receptor F box proteins. , 2005, Developmental cell.

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

[16]  A. Miyawaki,et al.  Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[17]  S. Ritchie,et al.  The calcium-dependent protein kinase HvCDPK1 mediates the gibberellic acid response of the barley aleurone through regulation of vacuolar function. , 2004, The Plant journal : for cell and molecular biology.

[18]  N. Holbrook,et al.  Root-Gel Interactions and the Root Waving Behavior of Arabidopsis1[w] , 2004, Plant Physiology.

[19]  Julian I Schroeder,et al.  Reactive Oxygen Species Activation of Plant Ca2+ Channels. A Signaling Mechanism in Polar Growth, Hormone Transduction, Stress Signaling, and Hypothetically Mechanotransduction1 , 2004, Plant Physiology.

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

[21]  M. Evans,et al.  Gravity-regulated differential auxin transport from columella to lateral root cap cells , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Simon Gilroy,et al.  Touch modulates gravity sensing to regulate the growth of primary roots of Arabidopsis thaliana. , 2003, The Plant journal : for cell and molecular biology.

[23]  G. Sandberg,et al.  AUX1 Promotes Lateral Root Formation by Facilitating Indole-3-Acetic Acid Distribution between Sink and Source Tissues in the Arabidopsis Seedling , 2002, The Plant Cell Online.

[24]  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.

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

[26]  J. Kiss.  Mechanisms of the Early Phases of Plant Gravitropism , 2000, Critical reviews in plant sciences.

[27]  E. Spalding,et al.  Nonselective Block by La3+ of Arabidopsis Ion Channels Involved in Signal Transduction , 1998, The Journal of Membrane Biology.

[28]  M. Estelle,et al.  The TIR1 protein of Arabidopsis functions in auxin response and is related to human SKP2 and yeast grr1p. , 1998, Genes & development.

[29]  S. Gilroy,et al.  Cytoplasmic free calcium distributions during the development of root hairs of Arabidopsis thaliana. , 1997, The Plant journal : for cell and molecular biology.

[30]  D. Soll,et al.  A novel root gravitropism mutant of Arabidopsis thaliana exhibiting altered auxin physiology. , 1995, Physiologia plantarum.

[31]  M. Estelle,et al.  The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. , 1995, The Plant journal : for cell and molecular biology.

[32]  F. J. Pierce,et al.  The pattern of secondary root formation in curving roots of Arabidopsis thaliana (L.) Heynh. , 1989, Plant, cell & environment.

[33]  R. Scott Russell,et al.  Effects of Mechanical Impedance on Root Growth in Barley (Hordeum vulgare L.) III. OBSERVATIONS ON THE MECHANISM OF RESPONSE , 1980 .

[34]  Michael J. Goss,et al.  Effects of Mechanical Impedance on Root Growth in Barley, Hordeum vulgare L.II. EFFECTS ON CELL DEVELOPMENT IN SEMINAL ROOTS , 1977 .

[35]  Broome,et al.  Literature cited , 1924, A Guide to the Carnivores of Central America.

[36]  Corresponding authors. , 2008 .

[37]  M. Lucas,et al.  Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. , 2008, Journal of experimental botany.

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

[39]  E. Blancaflor,et al.  Mapping the functional roles of cap cells in the response of Arabidopsis primary roots to gravity. , 1998, Plant physiology.