Regeneration in plants and animals: dedifferentiation, transdifferentiation, or just differentiation?

The textbooks and literature of plant biology indicate that plant cells are totipotent, and that regeneration occurs via dedifferentiation, by which the cell and its descendents recapitulate earlier stages of development. However, recent work on the generation of callus, a presumed undifferentiated or dedifferentiated and disorganized cellular mass, indicates that the cells of callus are neither, and that callus forms predominantly from a pre-existing population of stem cells. Recent work in animal regeneration, for example in salamander limbs, also indicates that previous assumptions about the extent of dedifferentiation and pluripotency in animals are in need of critical reassessment. We review here some of these data, compare plant and animal regeneration, and argue that the importance of dedifferentiation and plasticity in regenerating systems is due for reevaluation.

[1]  D. Jones,et al.  Stem cells and the niche: a dynamic duo. , 2010, Cell stem cell.

[2]  E. Tanaka,et al.  Ectoderm to Mesoderm Lineage Switching During Axolotl Tail Regeneration , 2002, Science.

[3]  M. Nabors Introduction to Botany , 2003 .

[4]  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.

[5]  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.

[6]  Kenneth D. Birnbaum,et al.  Slicing across Kingdoms: Regeneration in Plants and Animals , 2008, Cell.

[7]  R. de Rosa,et al.  Hydra, a niche for cell and developmental plasticity. , 2006, Seminars in cell & developmental biology.

[8]  Tom Beeckman,et al.  Cytokinins Act Directly on Lateral Root Founder Cells to Inhibit Root Initiation[W] , 2007, The Plant Cell Online.

[9]  F M Watt,et al.  Out of Eden: stem cells and their niches. , 2000, Science.

[10]  A. Kuroiwa,et al.  Lens formation by pigmented epithelial cell reaggregate from dorsal iris implanted into limb blastema in the adult newt , 1999, Development, growth & differentiation.

[11]  K. Agata,et al.  Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians , 2010, Development, growth & differentiation.

[12]  Z. Vondráková Laimer, M., Rücker, W. (ed.): Plant Tissue Culture. 100 Years Since Gottlieb Haberlandt. , 2003, Photosynthetica.

[13]  Thomas Vierbuchen,et al.  Direct conversion of fibroblasts to functional neurons by defined factors , 2010, Nature.

[14]  Anoop Kumar,et al.  Plasticity and reprogramming of differentiated cells in amphibian regeneration , 2002, Nature Reviews Molecular Cell Biology.

[15]  P. Tsonis,et al.  Oocyte‐type linker histone B4 is required for transdifferentiation of somatic cells in vivo , 2010, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[16]  S. Abe,et al.  Differentiation of lens-like structures from newt iris epithelial cells in vitro. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Elly M. Tanaka,et al.  Cells keep a memory of their tissue origin during axolotl limb regeneration , 2009, Nature.

[18]  E. Hay Electron microscopic observations of muscle dedifferentiation in regenerating amblystoma limbs , 1959 .

[19]  Hans Clevers,et al.  Coexistence of Quiescent and Active Adult Stem Cells in Mammals , 2010, Science.

[20]  J. Slack,et al.  Regeneration of neural crest derivatives in the Xenopus tadpole tail , 2007, BMC Developmental Biology.

[21]  J. Slack,et al.  Cell lineage tracing during Xenopus tail regeneration , 2004, Development.

[22]  P. V. Ammirato,et al.  Growth and Development of Totipotent CellsSome Problems, Procedures, and Perspectives , 1970 .

[23]  S. Howell,et al.  Developmental steps in acquiring competence for shoot development in Arabidopsis tissue culture , 2007, Planta.

[24]  Jim Haseloff,et al.  Marking cell lineages in living tissues. , 2005, The Plant journal : for cell and molecular biology.

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

[26]  J. C. Belmonte,et al.  Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation , 2010, Nature.

[27]  L. Laplaze,et al.  GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. , 2005, Journal of experimental botany.

[28]  S. Odelberg,et al.  Unraveling the Molecular Basis for Regenerative Cellular Plasticity , 2004, PLoS biology.

[29]  Douglas A. Melton,et al.  In vivo reprogramming of adult pancreatic exocrine cells to β-cells , 2008, Nature.

[30]  H. Street,et al.  Plant tissue and cell culture , 1977 .

[31]  T. Rando,et al.  Stem Cell Review Series: Aging of the skeletal muscle stem cell niche , 2008, Aging cell.

[32]  L. Laurens,et al.  Pluripotency of Arabidopsis xylem pericycle underlies shoot regeneration from root and hypocotyl explants grown in vitro. , 2009, The Plant journal : for cell and molecular biology.

[33]  H. Fukaki,et al.  Hormone interactions during lateral root formation , 2009, Plant Molecular Biology.

[34]  S. Yamanaka,et al.  Induction of Pluripotent Stem Cells from Mouse Embryonic and Adult Fibroblast Cultures by Defined Factors , 2006, Cell.

[35]  T. Bosch,et al.  The Hydra polyp: Nothing but an active stem cell community , 2009, Development, growth & differentiation.

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

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

[38]  Elliot M Meyerowitz,et al.  Pattern formation during de novo assembly of the Arabidopsis shoot meristem , 2007, Development.

[39]  Robert Passier,et al.  Getting to the heart of the matter: direct reprogramming to cardiomyocytes. , 2010, Cell stem cell.

[40]  A. Saghatelyan,et al.  De-routing neuronal precursors in the adult brain to sites of injury: Role of the vasculature , 2010, Neuropharmacology.

[41]  Ryan M. Anderson,et al.  Primary contribution to zebrafish heart regeneration by gata4+ cardiomyocytes , 2010, Nature.

[42]  E. Hay,et al.  Origin of the blastema in regenerating limbs of the newt Triturus viridescens. An autoradiographic study using tritiated thymidine to follow cell proliferation and migration. , 1961, Developmental biology.

[43]  R. Gautheret Plant tissue culture: the history , 2003 .

[44]  W. H. Lewis,et al.  Behavior of cross striated muscle in tissue cultures , 1917 .

[45]  J. Slack,et al.  Control of muscle regeneration in the Xenopus tadpole tail by Pax7 , 2006, Development.

[46]  E. G. Butler The effects of X‐radiation on the regeneration of the fore limb of Amblystoma larvae , 1933 .

[47]  J. Clarke,et al.  In vivo imaging indicates muscle fiber dedifferentiation is a major contributor to the regenerating tail blastema. , 2001, Developmental biology.

[48]  S. Odelberg,et al.  Dedifferentiation of Mammalian Myotubes Induced by msx1 , 2000, Cell.

[49]  H. Yamamoto,et al.  Expression of Msx genes in regenerating and developing limbs of axolotl. , 1998, The Journal of experimental zoology.

[50]  J. Martinou,et al.  Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. , 2009, Developmental cell.

[51]  E. Laurenti,et al.  Balancing dormant and self-renewing hematopoietic stem cells. , 2009, Current opinion in genetics & development.

[52]  K. Poss,et al.  Advances in understanding tissue regenerative capacity and mechanisms in animals , 2010, Nature Reviews Genetics.

[53]  Francis S. Kim,et al.  Systemic signals regulate ageing and rejuvenation of blood stem cell niches , 2010, Nature.

[54]  T. Steeves,et al.  Patterns in plant development: Subject index , 1972 .

[55]  Yuval Dor,et al.  Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. , 2004, Nature.

[56]  T. Okada,et al.  Differentiation of lens tissue from the progeny of chick retinal pigment cells cultured in vitro: a demonstration of a switch of cell types in clonal cell culture. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. Reyer,et al.  Stimulation of lens regeneration from the newt dorsal iris when implanted into the blastema of the regenerating limb. , 1973, Developmental biology.

[58]  A. Parent,et al.  Vasculature Guides Migrating Neuronal Precursors in the Adult Mammalian Forebrain via Brain-Derived Neurotrophic Factor Signaling , 2009, The Journal of Neuroscience.

[59]  Peter H. Raven,et al.  Biology of plants , 1976 .

[60]  Masaki Ieda,et al.  Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. , 2010, Cell.

[61]  P. Reddien,et al.  Planarian regeneration involves distinct stem cell responses to wounds and tissue absence. , 2010, Developmental biology.

[62]  Douglas A. Melton,et al.  Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation , 2004, Nature.