Allometric scaling and proportion regulation in the freshwater planarian Schmidtea mediterranea

The regulation of scale and proportion in living organisms is an intriguing and enduring problem of biology. Regulatory mechanisms for controlling body size and proportion are clearly illustrated by the regeneration of missing body parts after amputation, in which the newly regenerated tissues ultimately attain a size that is anatomically congruent with the size of the rest of the organism. Understanding the molecular processes underpinning scaling would have deep consequences for our comprehension of tissue regeneration, developmental ontogeny, growth, and evolution. Although many theories have been put forward to explain this process, it is interesting that no satisfactory mechanistic explanation is currently available to explain scalar relationships. We chose to investigate the freshwater planarian, a commonly used model system for the study of metazoan regeneration, to delineate a strategy for the molecular dissection of scale and proportion mechanisms in metazoans. Here, we report on the cloning and discrete expression pattern of a novel planarian gene, which shares homology with the DEG/ENaC super‐family of sodium channels. We have named H.112.3c cintillo (“head ribbon” in Spanish) and present a strategy for using the expression of this gene to monitor scale and proportion regulation during regeneration, growth and degrowth in the freshwater planarian Schmidtea mediterranea. Developmental Dynamics 226:326–333, 2003.© 2003 Wiley‐Liss, Inc.

[1]  M. Chalfie,et al.  Regulation of Caenorhabditis elegans degenerin proteins by a putative extracellular domain , 1995, Current Biology.

[2]  A. Sánchez Alvarado,et al.  Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. , 2000, Developmental biology.

[3]  K. Agata,et al.  A planarian orthopedia homolog is specifically expressed in the branch region of both the mature and regenerating brain , 1997, Development, growth & differentiation.

[4]  Robert Brown.  On Size and Life , 1985, The Yale Journal of Biology and Medicine.

[5]  R. Farnesi,et al.  Dugesia lugubris s.l. auricles: research into the ultrastructure and on the functional efficiency. , 1980, Rivista di biologia.

[6]  E. Hafen,et al.  The Drosophila insulin/IGF receptor controls growth and size by modulating PtdInsP(3) levels. , 2002, Development.

[7]  Kazuho Ikeo,et al.  FGFR-related gene nou-darake restricts brain tissues to the head region of planarians , 2002, Nature.

[8]  K. Schmidt-Nielsen,et al.  Scaling, why is animal size so important? , 1984 .

[9]  M. Driscoll,et al.  In Vivo Structure–Function Analyses ofCaenorhabditis elegans MEC-4, a Candidate Mechanosensory Ion Channel Subunit , 2000, The Journal of Neuroscience.

[10]  E. Hafen,et al.  Drosophila S6 kinase: a regulator of cell size. , 1999, Science.

[11]  C. Pantin.  Problems of Relative Growth , 1932, Nature.

[12]  D'arcy W. Thompson,et al.  On Growth and Form , 1917, Nature.

[13]  James H. Brown,et al.  Effects of size and temperature on developmental time , 2002, Nature.

[14]  Peter G. Gillespie,et al.  Molecular basis of mechanosensory transduction , 2001, Nature.

[15]  A. Leroi,et al.  Increased or decreased levels of Caenorhabditis elegans lon-3, a gene encoding a collagen, cause reciprocal changes in body length. , 2002, Genetics.

[16]  Amos Maritan,et al.  Size and form in efficient transportation networks , 1999, Nature.

[17]  H. Nijhout,et al.  The development and evolution of exaggerated morphologies in insects. , 2000, Annual review of entomology.

[18]  Raul K. Suarez,et al.  Allometric cascade as a unifying principle of body mass effects on metabolism , 2002, Nature.

[19]  J. Baguñá,et al.  Quantitative analysis of cell types during growth, degrowth and regeneration in the planarians Dugesia mediterranea and Dugesia tigrina , 1981, Hydrobiologia.

[20]  L. Hennighausen,et al.  Conditional loss of PTEN leads to precocious development and neoplasia in the mammary gland. , 2002, Development.

[21]  T. H. Morgan,et al.  Experimental studies of the regeneration of Planaria maculata , 2015, Roux's archives of developmental biology.

[22]  A. Sánchez Alvarado,et al.  Double-stranded RNA specifically disrupts gene expression during planarian regeneration. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  W. R. Stahl,et al.  Scaling of respiratory variables in mammals. , 1967, Journal of applied physiology.

[24]  Phillip A. Newmark,et al.  Not your father's planarian: a classic model enters the era of functional genomics , 2002, Nature Reviews Genetics.

[25]  G. Morata,et al.  Minutes: mutants of drosophila autonomously affecting cell division rate. , 1975, Developmental biology.

[26]  D. Emlen,et al.  The developmental basis for allometry in insects. , 1999, Development.

[27]  T. Gojobori,et al.  Dissecting planarian central nervous system regeneration by the expression of neural‐specific genes , 2002, Development, growth & differentiation.

[28]  D P Corey,et al.  The molecules of mechanosensation. , 1997, Annual review of neuroscience.

[29]  F. Hainsworth.  Scaling: why is animal size so important? , 1985 .

[30]  J. F. Staples,et al.  Relationships between enzymatic flux capacities and metabolic flux rates: nonequilibrium reactions in muscle glycolysis. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  D. Emlen.  Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae) , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  N. Pierce.  Origin of Species , 1914, Nature.

[33]  J. Baguñá,et al.  The Fissiparous Race of the Planarian Dugesia Lugubris S.L. Found in Barcelona (Spain) Belongs to the Biotype G: Comparative Analysis of the Karyotypes , 1972 .

[34]  G. Morata,et al.  Developmental compartmentalisation of the wing disk of Drosophila. , 1973, Nature: New biology.

[35]  M. Driscoll,et al.  DEG/ENaC channels: A touchy superfamily that watches its salt , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[36]  James H. Brown,et al.  A General Model for the Origin of Allometric Scaling Laws in Biology , 1997, Science.

[37]  L. Vinci.  The notebooks of Leonardo da Vinci. , 1952 .

[38]  Sofia M. C. Robb,et al.  Identification of immunological reagents for use in the study of freshwater planarians by means of whole‐mount immunofluorescence and confocal microscopy , 2002, Genesis.

[39]  Phillip A. Newmark,et al.  The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration , 2002, Development.

[40]  C. Lehner,et al.  Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase. , 1997, Development.

[41]  S. Gilman,et al.  The notebooks of Leonardo da Vinci , 1978, Medical History.