The ‘root-brain’ hypothesis of Charles and Francis Darwin

This year celebrates the 200th aniversary of the birth of Charles Darwin, best known for his theory of evolution summarized in On the Origin of Species. Less well known is that, in the second half of his life, Darwin’s major scientific focus turned towards plants. He wrote several books on plants, the next-to-last of which, The Power of Movement of Plants, published together with his son Francis, opened plants to a new view. Here we amplify the final sentence of this book in which the Darwins proposed that: “It is hardly an exaggeration to say that the tip of the radicle thus endowed [with sensitivity] and having the power of directing the movements of the adjoining parts, acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense-organs, and directing the several movements.” This sentence conveys two important messages: first, that the root apex may be considered to be a ‘brain-like’ organ endowed with a sensitivity which controls its navigation through soil; second, that the root apex represents the anterior end of the plant body. In this article, we discuss both these statements.

[1]  R. Barer The Unity of Life , 1963, Nature.

[2]  P. Barlow REGENERATION OF THE CAP OF PRIMARY ROOTS OF ZEA MAYS , 1974 .

[3]  J. Heslop-Harrison Darwin and the Movement of Plants: A Retrospect , 1980 .

[4]  M. Evans,et al.  Induction of curvature in maize roots by calcium or by thigmostimulation: role of the postmitotic isodiametric growth zone. , 1992, Plant physiology.

[5]  A. Leopold,et al.  The contribution of the extracellular matrix to gravisensing in characean cells. , 1992, Journal of cell science.

[6]  M. Evans,et al.  The Role of the Distal Elongation Zone in the Response of Maize Roots to Auxin and Gravity , 1993, Plant physiology.

[7]  F. Baluška,et al.  Specialized Zones of Development in Roots: View from the Cellular Level , 1996, Plant physiology.

[8]  A. Leopold,et al.  The effect of the external medium on the gravitropic curvature of rice (Oryza sativa, Poaceae) roots. , 1997, American journal of botany.

[9]  M. Staves Cytoplasmic streaming and gravity sensing in Chara internodal cells , 1997, Planta.

[10]  F. Baluška,et al.  Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: a major developmental switch occurs in the postmitotic transition region. , 1997, European journal of cell biology.

[11]  F. Sack,et al.  Plastids and gravitropic sensing , 1997, Planta.

[12]  G. Bokoch,et al.  Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells , 1997, Current Biology.

[13]  F. Baluška,et al.  Actin cytoskeleton in plants: From transport networks to signaling networks , 1999, Microscopy research and technique.

[14]  M. Drew,et al.  Programmed cell death and aerenchyma formation in roots. , 2000, Trends in plant science.

[15]  Xiaowen Zhao,et al.  The role of root border cells in plant defense. , 2000, Trends in plant science.

[16]  F. Baluška,et al.  ACTIN AND MYOSIN VIII IN DEVELOPING ROOT APEX CELLS Development-and tissue-specific distributions with possible relevancefor diverse root cellfunctions , 2000 .

[17]  František Baluška,et al.  Actin: A Dynamic Framework for Multiple Plant Cell Functions , 2000, Developments in Plant and Soil Sciences.

[18]  F. Baluška,et al.  Actin‐Based Domains of the “Cell Periphery Complex” and their Associations with Polarized “Cell Bodies” in Higher Plants , 2000 .

[19]  F. Baluška,et al.  CYTOSKELETAL PERSPECTIVES ON ROOT GROWTH AND MORPHOGENESIS. , 2000, Annual review of plant physiology and plant molecular biology.

[20]  F. Baluška,et al.  A Polarity Crossroad in the Transition Growth Zone of Maize Root Apices: Cytoskeletal and Developmental Implications , 2001, Journal of Plant Growth Regulation.

[21]  Marcel Dicke,et al.  Chemical information transfer between wounded and unwounded plants: backing up the future , 2001 .

[22]  Klaus Palme,et al.  Auxin transport inhibitors block PIN1 cycling and vesicle trafficking , 2001, Nature.

[23]  F. Baluška,et al.  F-Actin-Dependent Endocytosis of Cell Wall Pectins in Meristematic Root Cells. Insights from Brefeldin A-Induced Compartments1 , 2002, Plant Physiology.

[24]  C. Ritzenthaler,et al.  Brefeldin A: Deciphering an Enigmatic Inhibitor of Secretion , 2002, Plant Physiology.

[25]  M. Evans,et al.  Root gravitropism in response to a signal originating outside of the cap , 2002, Planta.

[26]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

[27]  M. Evans,et al.  The Kinetics of Root Gravitropism: Dual Motors and Sensors , 2002, Journal of Plant Growth Regulation.

[28]  F. Baluška,et al.  The architecture of polarized cell growth: the unique status of elongating plant cells. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[29]  F. Baluška,et al.  Cytoskeleton-Plasma Membrane-Cell Wall Continuum in Plants. Emerging Links Revisited1 , 2003, Plant Physiology.

[30]  F. Baluška,et al.  Endocytosis, Actin Cytoskeleton, and Signaling1 , 2004, Plant Physiology.

[31]  Peter W. Barlow,et al.  Root apices as plant command centres: the unique 'brain-like' status of the root apex transition zone , 2004 .

[32]  F. Baluška,et al.  Postmitotic ‘isodiametric’ cell growth in the maize root apex , 1990, Planta.

[33]  Ariel Novoplansky,et al.  Physiologically mediated self/non-self discrimination in roots. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[34]  R. Pierik,et al.  Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant-plant signalling. , 2004, The Plant journal : for cell and molecular biology.

[35]  David A. Morris,et al.  Targeting of auxin carriers to the plasma membrane: effects of monensin on transmembrane auxin transport in Cucurbita pepo L. tissue , 1994, Planta.

[36]  F. Baluška,et al.  The endocytic network in plants. , 2005, Trends in cell biology.

[37]  F. Baluška,et al.  Plant formins come of age: something special about cross-walls. , 2005, The New phytologist.

[38]  Stefano Mancuso,et al.  Noninvasive and continuous recordings of auxin fluxes in intact root apex with a carbon nanotube-modified and self-referencing microelectrode. , 2005, Analytical biochemistry.

[39]  Frantisek Baluska,et al.  Plant synapses: actin-based domains for cell-to-cell communication. , 2005, Trends in plant science.

[40]  F. Baluška,et al.  Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis , 2005, Protoplasma.

[41]  F. Baluška,et al.  What is apical and what is basal in plant root development? , 2005, Trends in plant science.

[42]  F. Baluška,et al.  Importance of the post-mitotic isodiametric growth (PIG) region for growth and development of roots , 1994, Plant and Soil.

[43]  V. Shepherd From semi-conductors to the rhythms of sensitive plants: the research of J.C. Bose. , 2005, Cellular and molecular biology.

[44]  F. Baluška,et al.  Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. , 2006, Developmental cell.

[45]  Richard Karban,et al.  Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. , 2006, Ecology.

[46]  Stefano Mancuso,et al.  Actin Turnover-Mediated Gravity Response in Maize Root Apices , 2006, Plant signaling & behavior.

[47]  František Baluška,et al.  Communication in Plants , 2006 .

[48]  Peter W. Barlow,et al.  Communication in Plants. Neuronal Aspects of Plant Life , 2006 .

[49]  R. Hangarter,et al.  Phototropism: Bending towards Enlightenment , 2006, The Plant Cell Online.

[50]  A. Hahn,et al.  Interacting signal transduction chains in gravity-stimulated maize roots , 2006 .

[51]  Klaus Palme,et al.  Auxin Immunolocalization Implicates Vesicular Neurotransmitter-Like Mode of Polar Auxin Transport in Root Apices , 2006, Plant signaling & behavior.

[52]  K. Palme,et al.  Auxin transport and gravitational research: perspectives , 2006, Protoplasma.

[53]  František Baluška,et al.  Communication in plants : neuronal aspects of plant life , 2006 .

[54]  Stefano Mancuso,et al.  Plant neurobiology: an integrated view of plant signaling. , 2006, Trends in plant science.

[55]  Kris Vissenberg,et al.  The Root Apex of Arabidopsis thaliana Consists of Four Distinct Zones of Growth Activities , 2006, Plant signaling & behavior.

[56]  H. G. Edelmann,et al.  Gravitropic plant growth regulation and ethylene: an unsought cardinal coordinate for a disused model , 2006, Protoplasma.

[57]  Klaus Palme,et al.  Auxin in action: signalling, transport and the control of plant growth and development , 2006, Nature Reviews Molecular Cell Biology.

[58]  František Baluška,et al.  Neurobiological View of Plants and Their Body Plan , 2006 .

[59]  Peter W. Barlow,et al.  Charles Darwin and the Plant Root Apex: Closing a Gap in Living Systems Theory as Applied to Plants , 2006 .

[60]  P. Benfey,et al.  Apical-basal polarity: why plant cells don't stand on their heads. , 2006, Trends in plant science.

[61]  F. Baluška,et al.  Fine Structural Analysis of Brefeldin A-Induced Compartment Formation After High-Pressure Freeze Fixation of Maize Root Epidermis , 2006, Plant signaling & behavior.

[62]  Francisco Calvo Garzón,et al.  The quest for cognition in plant neurobiology. , 2007, Plant signaling & behavior.

[63]  Chris Hawes,et al.  Plant neurobiology: no brain, no gain? , 2007, Trends in plant science.

[64]  H. Xue,et al.  Arabidopsis PLDζ2 Regulates Vesicle Trafficking and Is Required for Auxin Response[W] , 2007, The Plant Cell Online.

[65]  Anthony Trewavas,et al.  Response to Alpi et al.: Plant neurobiology--all metaphors have value. , 2007, Trends in plant science.

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

[67]  G. Jürgens,et al.  Patterning the axis in plants--auxin in control. , 2007, Current opinion in genetics & development.

[68]  F. Baluška,et al.  Phospholipase Dζ2 Drives Vesicular Secretion of Auxin for Its Polar Cell-Cell Transport in the Transition Zone of the Root Apex , 2007, Plant signaling & behavior.

[69]  X. Li,et al.  Salt-avoidance tropism in Arabidopsis thaliana , 2008, Plant signaling & behavior.

[70]  Peter W. Barlow,et al.  Reflections on 'plant neurobiology' , 2008, Biosyst..

[71]  Rujin Chen,et al.  Light Plays an Essential Role in Intracellular Distribution of Auxin Efflux Carrier PIN2 in Arabidopsis thaliana , 2008, PloS one.

[72]  Michael Hollmann,et al.  Arabidopsis thaliana glutamate receptor ion channel function demonstrated by ion pore transplantation. , 2008, Journal of molecular biology.

[73]  Klaus Harter,et al.  The root cap determines ethylene-dependent growth and development in maize roots. , 2008, Molecular plant.

[74]  C. Hawes,et al.  BFA effects are tissue and not just plant specific. , 2008, Trends in plant science.

[75]  F. Baluška,et al.  Aluminium toxicity targets PIN2 in Arabidopsis root apices: Effects on PIN2 endocytosis, vesicular recycling, and polar auxin transport , 2008 .

[76]  H. Xue,et al.  Membrane steroid binding protein 1 (MSBP1) stimulates tropism by regulating vesicle trafficking and auxin redistribution. , 2008, Molecular plant.

[77]  J. Friml,et al.  Polar targeting and endocytic recycling in auxin-dependent plant development. , 2008, Annual review of cell and developmental biology.

[78]  Other Tropisms and their Relationship to Gravitropism , 2008 .

[79]  Ulrich Kubitscheck,et al.  The subcellular localization and blue-light-induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. , 2008, Molecular plant.

[80]  L. Meisel,et al.  Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes , 2008, Proceedings of the National Academy of Sciences.

[81]  S. Gilroy Plant tropisms , 2008, Current Biology.

[82]  Holger Meinke,et al.  Plant neurobiology and green plant intelligence: science, metaphors and nonsense , 2008 .

[83]  M. Robertson Ockham's broom: A new series , 2009, Journal of Biology.

[84]  Jan Petrásek,et al.  Auxin transport routes in plant development , 2009, Development.

[85]  J. V. van Loon,et al.  Chemical complexity of volatiles from plants induced by multiple attack. , 2009, Nature chemical biology.

[86]  K. Niklas,et al.  Evolutionary plant physiology: Charles Darwin’s forgotten synthesis , 2009, Naturwissenschaften.

[87]  Viktor Zárský,et al.  Plant intelligence , 2009, Plant signaling & behavior.

[88]  R. Karban,et al.  Self-recognition affects plant communication and defense. , 2009, Ecology letters.

[89]  Angela Hodge,et al.  Root decisions. , 2009, Plant, cell & environment.

[90]  A. Trewavas What is plant behaviour? , 2009, Plant, cell & environment.

[91]  F. Arecchi,et al.  Spatiotemporal dynamics of the electrical network activity in the root apex , 2009, Proceedings of the National Academy of Sciences.

[92]  S. Gilroy,et al.  The exploring root--root growth responses to local environmental conditions. , 2009, Current opinion in plant biology.

[93]  Fred Keijzer,et al.  Cognition in Plants , 2009 .

[94]  G. Arimura,et al.  Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. , 2009, Plant & cell physiology.

[95]  Tom Beeckman,et al.  Arabidopsis lateral root development: an emerging story. , 2009, Trends in plant science.

[96]  Akira Chiba,et al.  Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals , 2009, Proceedings of the National Academy of Sciences.

[97]  U. Kutschera,et al.  From Charles Darwin's botanical country-house studies to modern plant biology. , 2009, Plant biology.

[98]  D. Penny Charles Darwin as a theoretical biologist in the mechanistic tradition , 2009 .

[99]  Y. Wang,et al.  The role of Arabidopsis 5PTase13 in root gravitropism through modulation of vesicle trafficking , 2009, Cell Research.

[100]  František Baluška,et al.  Plants and Animals: Convergent Evolution in Action? , 2009 .

[101]  T. Fujiwara,et al.  The intracellular transport of transporters: membrane trafficking of mineral transporters. , 2009, Current opinion in plant biology.

[102]  Geetanjali Misra,et al.  The Power of Movements , 2009 .

[103]  J. Maloof,et al.  Plant research accelerates along the (bio)informatics superhighway , 2009, EMBO reports.

[104]  Franti ek Vejra ka,et al.  Plant-environment interactions : from sensory plant biology to active plant behavior , 2010 .

[105]  H. Bais,et al.  Root exudates mediate kin recognition in plants , 2010, Communicative & integrative biology.

[106]  Richard Karban,et al.  Explaining evolution of plant communication by airborne signals. , 2010, Trends in ecology & evolution.

[107]  Zdeněk P. Bažant I. Theory , 2022 .

[108]  F. Baluška,et al.  Addendum Vesicular secretion of auxin Evidences and implications , 2022 .