Externally imposed electric field enhances plant root tip regeneration

Abstract In plants, shoot and root regeneration can be induced in the distinctive conditions of tissue culture (in vitro) but is also observed in intact individuals (in planta) recovering from tissue damage. Roots, for example, can regenerate their fully excised meristems in planta, even in mutants with impaired apical stem cell niches. Unfortunately, to date a comprehensive understanding of regeneration in plants is still missing. Here, we provide evidence that an imposed electric field can perturb apical root regeneration in Arabidopsis. Crucially, we explored both spatial and temporal competences of the stump to respond to electrical stimulation, by varying respectively the position of the cut and the time interval between excision and stimulation. Our data indicate that a brief pulse of an electric field parallel to the root is sufficient to increase by up to two‐fold the probability of its regeneration, and to perturb the local distribution of the hormone auxin, as well as cell division regulation. Remarkably, the orientation of the root towards the anode or the cathode is shown to play a role.

[1]  E. J. Lund Electrical Control of Organic Polarity in the Egg of Fucus , 1923, Botanical Gazette.

[2]  E. J. Lund Experimental control of organic polarity by the electric current. IV. The quantitative relations between current density, orientation, and inhibition of regeneration , 1924 .

[3]  E. J. Lund Experimental control of organic polarity by the electric current. V. The nature of the control of organic polarity by the electric current , 1925 .

[4]  C. Miller,et al.  Chemical regulation of growth and organ formation in plant tissues cultured in vitro. , 1957, Symposia of the Society for Experimental Biology.

[5]  James Joseph Biundo,et al.  Analysis of Contingency Tables , 1969 .

[6]  B. Novak,et al.  Orientation ofFucus egg polarity by electric a. c. and d. c. fields , 1973, Biophysik.

[7]  Stephen D. Smith EFFECTS OF ELECTRODE PLACEMENT ON STIMULATION OF ADULT FROG LIMB REGENERATION * , 1974, Annals of the New York Academy of Sciences.

[8]  P. Barlow Recovery of Geotropism after Removal of the Root Cap , 1974 .

[9]  H. Peng,et al.  Polarization of fucoid eggs by steady electrical fields. , 1976, Developmental biology.

[10]  R. Nuccitelli,et al.  Electrical controls of development. , 1977, Annual review of biophysics and bioengineering.

[11]  D. Francis REGENERATION OF MERISTEMATIC ACTIVITY FOLLOWING DECAPITATION OF THE ROOT TIP OF VICIA FABA L. , 1978 .

[12]  A. Goldsworthy,et al.  Electrical Control of Shoot Regeneration in Plant Tissue Cultures , 1985, Bio/Technology.

[13]  E. Kinney Primer of Biostatistics , 1987 .

[14]  T. Jones,et al.  Pea root regeneration after tip excisions at different levels: polarity of new growth , 1988 .

[15]  M. Evans,et al.  Electrotropism of maize roots. Role of the root cap and relationship to gravitropism. , 1990, Plant physiology.

[16]  M. Weisenseel,et al.  DC-Electric Fields Affect the Growth Direction and StatocytePolarity of Root Tips (Lepidium sativum) , 1991 .

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

[18]  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.

[19]  Stimulation of tobacco shoot regeneration by alternating weak electric field , 1998 .

[20]  P. Doerner,et al.  Technical advance: spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. , 1999, The Plant journal : for cell and molecular biology.

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

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

[23]  E. Meyerowitz,et al.  Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana , 2004, Development.

[24]  B. Scheres,et al.  Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. , 2004, Genes & development.

[25]  D. Morris The influence of small direct electric currents on the transport of auxin in intact plants , 1980, Planta.

[26]  L. Feldman The de novo origin of the quiescent center regenerating root apices of Zea mays , 2004, Planta.

[27]  Min Zhao,et al.  Controlling cell behavior electrically: current views and future potential. , 2005, Physiological reviews.

[28]  Per Capita,et al.  About the authors , 1995, Machine Vision and Applications.

[29]  Michael Sauer,et al.  A Molecular Framework for Plant Regeneration , 2006, Science.

[30]  B. Zagórska-Marek,et al.  Influence of a weak DC electric field on root meristem architecture. , 2007, Annals of botany.

[31]  Michael Levin,et al.  Large-scale biophysics: ion flows and regeneration. , 2007, Trends in cell biology.

[32]  J. Botto,et al.  The plant cell , 2007, Plant Molecular Biology Reporter.

[33]  Renze Heidstra,et al.  Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation , 2007, Current Biology.

[34]  G. Sena,et al.  Organ regeneration does not require a functional stem cell niche in plants , 2008, Nature.

[35]  Elliot M Meyerowitz,et al.  Arabidopsis regeneration from multiple tissues occurs via a root development pathway. , 2010, Developmental cell.

[36]  Chongsheng He,et al.  Reprogramming of H3K27me3 Is Critical for Acquisition of Pluripotency from Cultured Arabidopsis Tissues , 2012, PLoS genetics.

[37]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[38]  Paul T Tarr,et al.  A Robust and Sensitive Synthetic Sensor to Monitor the Transcriptional Output of the Cytokinin Signaling Network in Planta1[C][W][OA] , 2013, Plant Physiology.

[39]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[40]  Nicolas Minc,et al.  Electrochemical control of cell and tissue polarity. , 2014, Annual review of cell and developmental biology.

[41]  Hai Huang,et al.  WOX11 and 12 Are Involved in the First-Step Cell Fate Transition during de Novo Root Organogenesis in Arabidopsis[W] , 2014, Plant Cell.

[42]  E. Meyerowitz,et al.  PLETHORA Genes Control Regeneration by a Two-Step Mechanism , 2015, Current Biology.

[43]  Teva Vernoux,et al.  Reporters for sensitive and quantitative measurement of auxin response , 2015, Nature Methods.

[44]  J. Kieber,et al.  The Yin-Yang of Hormones: Cytokinin and Auxin Interactions in Plant Development , 2015, Plant Cell.

[45]  S. Sabatini,et al.  Plant hormone cross-talk: the pivot of root growth. , 2015, Journal of experimental botany.

[46]  Adam P. Fisher,et al.  Uncovering the networks involved in stem cell maintenance and asymmetric cell division in the Arabidopsis root. , 2016, Current opinion in plant biology.