Plant Growth and Development - Basic Knowledge and Current Views

One of the most intriguing questions in life science is how living organisms develop and maintain their predominant form and shape via the cascade of the processes of differentiation starting from the single cell. Mathematical modeling of these developmental processes could be a very important tool to properly describe the complex processes of evolution and geometry of mor- phogenesis in time and space. Here, we summarize the most important biological knowledge on plant development, exploring the different layers of investigation in developmental processes such as plant morphology, genetics, plant physiology, molecular biology and epigenetics. As knowledge on the fundamentals of plant embryogenesis, growth and development is constantly improving, we gather here the latest data on genetic, molecular and hormonal regulation of plant development to- gether with the basic background knowledge. Special emphasis is placed on the regulation of cell cycle progression, on the role of the signal molecules phytohormones in plant development and on the details of plant meristems (loci containing plant stem cells) function. We also explore several proposed biological models regarding regulating plant development. The information presented here could be used as a basis for mathematical modeling and computer simulation of developmen- tal processes in plants.

[1]  G. Jürgens,et al.  The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo , 1993 .

[2]  P. Benfey,et al.  Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. , 2000, Development.

[3]  J. Mol,et al.  The No Apical Meristem Gene of Petunia Is Required for Pattern Formation in Embryos and Flowers and Is Expressed at Meristem and Primordia Boundaries , 1996, Cell.

[4]  Kexue Li,et al.  Arabidopsis EIN2 modulates stress response through abscisic acid response pathway , 2007, Plant Molecular Biology.

[5]  S. D. de Vries,et al.  The CUP-SHAPED COTYLEDON3 Gene Is Required for Boundary and Shoot Meristem Formation in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.012203. , 2003, The Plant Cell Online.

[6]  Robert W. Williams,et al.  The CLAVATA1 Gene Encodes a Putative Receptor Kinase That Controls Shoot and Floral Meristem Size in Arabidopsis , 1997, Cell.

[7]  Stephen J. Elledge,et al.  Cell Cycle Checkpoints: Preventing an Identity Crisis , 1996, Science.

[8]  G. Jürgens,et al.  Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, post-embryonic development of Arabidopsis , 2003, Development.

[9]  K. Thimann,et al.  Studies on the Growth Hormone of Plants: III. The Inhibiting Action of the Growth Substance on Bud Development. , 1933, Proceedings of the National Academy of Sciences of the United States of America.

[10]  P. Benfey,et al.  Intercellular movement of the putative transcription factor SHR in root patterning , 2001, Nature.

[11]  M. Aida,et al.  Morphogenesis and Patterning at the Organ Boundaries in the Higher Plant Shoot Apex , 2006, Plant Molecular Biology.

[12]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[13]  R. Moe,et al.  Day and night temperature responses in Arabidopsis: effects on gibberellin and auxin content, cell size, morphology and flowering time. , 2003, Annals of botany.

[14]  S. Hake,et al.  Shoot Meristem Formation in Vegetative Development. , 1997, The Plant cell.

[15]  N. H. Boke.  LEAF AND AREOLE DEVELOPMENT IN CORYPHANTHA , 1952 .

[16]  G. Grafi.  How cells dedifferentiate: a lesson from plants. , 2004, Developmental biology.

[17]  R. Poethig,et al.  Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant , 1993 .

[18]  W. Lukowitz,et al.  Cytokinesis in the Arabidopsis Embryo Involves the Syntaxin-Related KNOLLE Gene Product , 1996, Cell.

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

[20]  R. Simon,et al.  Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. , 1999, Science.

[21]  Luis Herrera-Estrella,et al.  Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System1 , 2002, Plant Physiology.

[22]  M. Lenhard,et al.  Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1 , 2003, Development.

[23]  D. Inzé,et al.  Auxin Transport Promotes Arabidopsis Lateral Root Initiation , 2001, Plant Cell.

[24]  F. Went.  PLANT GROWTH UNDER CONTROLLED CONDITIONS. III. CORRELATION BETWEEN VARIOUS PHYSIOLOGICAL PROCESSES AND GROWTH IN THE TOMATO PLANT , 1944 .

[25]  C. Bell,et al.  Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. , 1991, The Plant cell.

[26]  G. Jürgens,et al.  The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. , 1999, Development.

[27]  Heiko Schoof,et al.  Role of WUSCHEL in Regulating Stem Cell Fate in the Arabidopsis Shoot Meristem , 1998, Cell.

[28]  M. Rao,et al.  Transdifferentiation—fact or artifact , 2003, Journal of cellular biochemistry.

[29]  G. Jürgens,et al.  The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. , 2002, Genes & development.

[30]  M. McManus,et al.  Hormones, Signals and Target Cells in Plant Development , 2005 .

[31]  M. Rajeevan,et al.  Flower-bud formation in explants of photoperiodic and day-neutral Nicotiana biotypes and its bearing on the regulation of flower formation. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Fletcher,et al.  Shoot and floral meristem maintenance in arabidopsis. , 2002, Annual review of plant biology.

[33]  Marilu A. Hoeppner,et al.  Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. , 1998, Science.

[34]  Masashi Yamada,et al.  Sites and Regulation of Auxin Biosynthesis in Arabidopsis Roots , 2005, The Plant Cell Online.

[35]  Stone,et al.  Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions , 1998, Plant physiology.

[36]  R. D. Meicenheimer.  CHANGES IN EPILOBIUM PHYLLOTAXY INDUCED BY N‐1‐NAPHTHYLPHTHALAMIC ACID AND α‐4‐CHLOROPHENOXYISOBUTYRIC ACID , 1981 .

[37]  P. Prusinkiewicz,et al.  A plausible model of phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Bowman,et al.  Genetic interactions among floral homeotic genes of Arabidopsis. , 1991, Development.

[39]  W. Frommer,et al.  Seed-specific overexpression of a potato sucrose transporter increases sucrose uptake and growth rates of developing pea cotyledons. , 2002, The Plant journal : for cell and molecular biology.

[40]  A. Fleming.  Formation of primordia and phyllotaxy. , 2005, Current opinion in plant biology.

[41]  Patrick Laufs,et al.  MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems , 2004, Development.

[42]  A. Müller,et al.  Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. , 1998, Science.

[43]  E. Meyerowitz,et al.  A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[45]  Javier F. Palatnik,et al.  Control of leaf morphogenesis by microRNAs , 2003, Nature.

[46]  P. León,et al.  Sugar and hormone connections. , 2003, Trends in plant science.

[47]  Didier Reinhardt,et al.  Regulation of phyllotaxis. , 2005, The International journal of developmental biology.

[48]  S. Yoshida,et al.  Control of in vitro organogenesis by cyclin-dependent kinase activities in plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Christophe Godin,et al.  A protocol to analyse cellular dynamics during plant development. , 2005, The Plant journal : for cell and molecular biology.

[50]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[51]  S. Odelberg.  Inducing cellular dedifferentiation: a potential method for enhancing endogenous regeneration in mammals. , 2002, Seminars in cell & developmental biology.

[52]  M. Koornneef,et al.  Somatic embryogenesis in Arabidopsis thaliana is facilitated by mutations in genes repressing meristematic cell divisions. , 1998, Genetics.

[53]  Dirk Inzé,et al.  Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004960. , 2002, The Plant Cell Online.

[54]  K. Feldmann,et al.  Arabidopsis AUX1 Gene: A Permease-Like Regulator of Root Gravitropism , 1996, Science.

[55]  Andrew J. Fleming,et al.  Induction of Leaf Primordia by the Cell Wall Protein Expansin , 1997 .

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

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

[58]  S. Clark,et al.  The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase , 1999, Plant Cell.

[59]  W. Bloom.  CELLULAR DIFFERENTIATION AND TISSUE CULTURE , 1937 .

[60]  V. Volpert,et al.  Modeling of Branching Patterns in Plants , 2008, Bulletin of mathematical biology.

[61]  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.

[62]  E. Nigg,et al.  Cyclin‐dependent protein kinases: Key regulators of the eukaryotic cell cycle , 1995, BioEssays : news and reviews in molecular, cellular and developmental biology.

[63]  K. Jiang,et al.  Auxin metabolism in the root apical meristem. , 2000, Plant physiology.

[64]  A. Fleming,et al.  Manipulation of leaf shape by modulation of cell division. , 2002, Development.

[65]  A. Fleming,et al.  Local expression of expansin induces the entire process of leaf development and modifies leaf shape , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[66]  P. Masson,et al.  The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. , 1999, Development.

[67]  E. Mjolsness,et al.  An auxin-driven polarized transport model for phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[68]  R Swarup,et al.  Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. , 2001, Genes & development.

[69]  G. Jürgens,et al.  Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene , 1993 .

[70]  D. Bartel.  MicroRNAs Genomics, Biogenesis, Mechanism, and Function , 2004, Cell.

[71]  M. Strauss,et al.  The retinoblastoma protein: a master regulator of cell cycle, differentiation and apoptosis. , 1997, European journal of biochemistry.

[72]  R. F. Lyndon.  The shoot apical meristem , 1998 .

[73]  A. Delisle.  THE INFLUENCE OF AUXIN ON SECONDARY BRANCHING IN TWO SPECIES OF ASTER , 1937 .

[74]  T. Vernoux,et al.  PIN-FORMED 1 regulates cell fate at the periphery of the shoot apical meristem. , 2000, Development.

[75]  Heiko Schoof,et al.  The Stem Cell Population of Arabidopsis Shoot Meristems Is Maintained by a Regulatory Loop between the CLAVATA and WUSCHEL Genes , 2000, Cell.

[76]  David Tosh,et al.  How cells change their phenotype , 2002, Nature Reviews Molecular Cell Biology.

[77]  Guiliang Tang,et al.  siRNA and miRNA: an insight into RISCs. , 2005, Trends in biochemical sciences.

[78]  G. Jürgens,et al.  Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. , 1999, Science.

[79]  H. Rolletschek,et al.  Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds. , 2003, Journal of experimental botany.

[80]  N. Raikhel,et al.  CLV3 Is Localized to the Extracellular Space, Where It Activates the Arabidopsis CLAVATA Stem Cell Signaling Pathway Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002196. , 2002, The Plant Cell Online.

[81]  R. Poethig,et al.  Cell lineage patterns in maize embryogenesis: a clonal analysis , 1986 .

[82]  P. J. Davies,et al.  The Control of Apical Bud Growth and Senescence by Auxin and Gibberellin in Genetic Lines of Peas , 1997, Plant physiology.

[83]  D. Weigel,et al.  A Molecular Link between Stem Cell Regulation and Floral Patterning in Arabidopsis , 2001, Cell.

[84]  S. Hake,et al.  A knotted1-like homeobox gene in Arabidopsis is expressed in the vegetative meristem and dramatically alters leaf morphology when overexpressed in transgenic plants. , 1994, The Plant cell.

[85]  C. Hardtke,et al.  The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development , 1998, The EMBO journal.

[86]  O. Clarenz,et al.  Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. , 2003, Genes & development.

[87]  G. Jürgens,et al.  The GURKE gene is required for normal organization of the apical region in the Arabidopsis embryo. , 1996, The Plant journal : for cell and molecular biology.

[88]  R. L. Taylor.  THE FOLIAR EMBRYOS OF MALAXIS PALUDOSA , 1967 .

[89]  Ari Pekka Mähönen,et al.  Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions , 2008, Nature.

[90]  L. E. Young,et al.  Somatic cell nuclear transfer , 2002, Nature.

[91]  J. A. Yarbrough.  Anatomical and developmental studies of the foliar embryos of Bryophyllum calycinum. , 1932 .

[92]  S. Swarup,et al.  The expression of Brostm, a KNOTTED1-like gene, marks the cell type and timing of in vitro shoot induction in Brassica oleracea , 2001, Plant Molecular Biology.

[93]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[94]  T. Berleth,et al.  Genetic analysis of pattern formation in the Arabidopsis embryo , 2005 .

[95]  Hajime Sakai,et al.  Regulation of Flowering Time and Floral Organ Identity by a MicroRNA and Its APETALA2-Like Target Genes Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016238. , 2003, The Plant Cell Online.

[96]  C. Sherr.  Cancer Cell Cycles , 1996, Science.

[97]  W. Peacock,et al.  Fertilization-independent seed development in Arabidopsis thaliana. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[98]  D. Inzé,et al.  The Role of the Arabidopsis E2FB Transcription Factor in Regulating Auxin-Dependent Cell Divisionw⃞ , 2005, The Plant Cell Online.

[99]  Philippe Mourrain,et al.  Fertile Hypomorphic ARGONAUTE (ago1) Mutants Impaired in Post-Transcriptional Gene Silencing and Virus Resistance , 2002, The Plant Cell Online.

[100]  M. Hobe,et al.  Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. , 2000, Science.

[101]  Detlef Weigel,et al.  Stem cells that make stems , 2002, Nature.

[102]  June I. Medford,et al.  A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis , 1996, Nature.

[103]  Daniel J. Cosgrove,et al.  Loosening of plant cell walls by expansins , 2000, Nature.

[104]  B. Reinhart,et al.  Prediction of Plant MicroRNA Targets , 2002, Cell.

[105]  Julie A. Law,et al.  Establishing, maintaining and modifying DNA methylation patterns in plants and animals , 2010, Nature Reviews Genetics.

[106]  Determination of Arabidopsis floral meristem identity by AGAMOUS. , 1997, The Plant cell.

[107]  E. Meyerowitz,et al.  Patterns of Auxin Transport and Gene Expression during Primordium Development Revealed by Live Imaging of the Arabidopsis Inflorescence Meristem , 2005, Current Biology.

[108]  J. Cock,et al.  A large family of genes that share homology with CLAVATA3. , 2001, Plant physiology.

[109]  G. Jürgens,et al.  Protein Secretion in Plants: from the trans‐Golgi Network to the Outer Space , 2002, Traffic.

[110]  C. Kuhlemeier,et al.  Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs , 2000, Plant Cell.

[111]  T. Vernoux,et al.  Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. , 2002, Development.

[112]  M. Aida,et al.  Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. , 1999, Development.

[113]  R. Reski,et al.  Cyclin D-knockout uncouples developmental progression from sugar availability , 2003, Plant Molecular Biology.

[114]  C. Kidner,et al.  Plant stem cells: divergent pathways and common themes in shoots and roots. , 2003, Current opinion in genetics & development.

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

[116]  A. Whetton,et al.  Homing and mobilization in the stem cell niche. , 1999, Trends in cell biology.

[117]  W. Dewitte,et al.  Competency of Nicotiana tabacum L. stem tissues to dedifferentiate is associated with differential levels of cell cycle gene expression and endogenous cytokinins , 2002, Planta.

[118]  C. Kuhlemeier,et al.  Localized Upregulation of a New Expansin Gene Predicts the Site of Leaf Formation in the Tomato Meristem , 1998, Plant Cell.

[119]  M. Bennett,et al.  Regulation of phyllotaxis by polar auxin transport , 2003, Nature.

[120]  J. Harper,et al.  Coupling of DNA Synthesis and Histone Synthesis in S Phase Independent of Cyclin/cdk2 Activity , 2002, Molecular and Cellular Biology.

[121]  V. Jiménez.  Regulation of in vitro somatic embryogenesis with emphasis on to the role of endogenous hormones , 2001 .

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

[123]  C. Kuhlemeier,et al.  The auxin influx carrier is essential for correct leaf positioning. , 2002, The Plant journal : for cell and molecular biology.

[124]  J. Bonner,et al.  STUDIES ON THE GROWTH HORMONE OF PLANTS : VII. THE FATE OF GROWTH SUBSTANCE IN THE PLANT AND THE NATURE OF THE GROWTH PROCESS. , 1935 .

[125]  P. Benfey,et al.  COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. , 2001, Genes & development.

[126]  W. Gelbart,et al.  The relationship of decapentaplegic and engrailed expression in Drosophila imaginal disks: do these genes mark the anterior-posterior compartment boundary? , 1991, Development.

[127]  E. Glawischnig,et al.  The gene ENHANCER OF PINOID controls cotyledon development in the Arabidopsis embryo , 2005, Development.

[128]  K. Jiang,et al.  Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment , 2003, Development.

[129]  J. Levin,et al.  The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. , 1996, The Plant journal : for cell and molecular biology.

[130]  A. Koltunow.  Apomixis: Embryo Sacs and Embryos Formed without Meiosis or Fertilization in Ovules. , 1993, The Plant cell.

[131]  M. Evans,et al.  Specialized Zones of Development in Roots , 1995, Plant physiology.

[132]  R. Porat,et al.  Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. , 1996, The Plant cell.

[133]  G. Sandberg,et al.  The relative importance of tryptophan-dependent and tryptophan-independent biosynthesis of indole-3-acetic acid in tobacco during vegetative growth , 2000, Planta.

[134]  G. Evan,et al.  Proliferation, cell cycle and apoptosis in cancer , 2001, Nature.

[135]  Suresh Chand,et al.  Interaction of PIN and PGP transport mechanisms in auxin distribution-dependent development , 2008, Development.

[136]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.

[137]  Klaus Palme,et al.  AtPIN2 defines a locus of Arabidopsis for root gravitropism control , 1998, The EMBO journal.

[138]  Isabelle Bohn-Courseau,et al.  Cell proliferation patterns at the shoot apical meristem. , 2005, Current opinion in plant biology.

[139]  Philip N Benfey,et al.  The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling , 2000, Cell.

[140]  A. Nakano,et al.  The Arabidopsis GNOM ARF-GEF Mediates Endosomal Recycling, Auxin Transport, and Auxin-Dependent Plant Growth , 2003, Cell.

[141]  C. Dean,et al.  Embryonic origin of the Arabidopsis primary root and root meristem initials , 1994 .

[142]  Klaus Palme,et al.  AtPIN4 Mediates Sink-Driven Auxin Gradients and Root Patterning in Arabidopsis , 2002, Cell.

[143]  J. Murray,et al.  A family of cyclin D homologs from plants differentially controlled by growth regulators and containing the conserved retinoblastoma protein interaction motif. , 1995, The Plant cell.

[144]  S. Howell.  Molecular Genetics of Plant Development , 1998 .

[145]  S. Hake,et al.  Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot , 1994 .