Morphological Plant Modeling: Unleashing Geometric and Topological Potential within the Plant Sciences

The geometries and topologies of leaves, flowers, roots, shoots, and their arrangements have fascinated plant biologists and mathematicians alike. As such, plant morphology is inherently mathematical in that it describes plant form and architecture with geometrical and topological techniques. Gaining an understanding of how to modify plant morphology, through molecular biology and breeding, aided by a mathematical perspective, is critical to improving agriculture, and the monitoring of ecosystems is vital to modeling a future with fewer natural resources. In this white paper, we begin with an overview in quantifying the form of plants and mathematical models of patterning in plants. We then explore the fundamental challenges that remain unanswered concerning plant morphology, from the barriers preventing the prediction of phenotype from genotype to modeling the movement of leaves in air streams. We end with a discussion concerning the education of plant morphology synthesizing biological and mathematical approaches and ways to facilitate research advances through outreach, cross-disciplinary training, and open science. Unleashing the potential of geometric and topological approaches in the plant sciences promises to transform our understanding of both plants and mathematics.

[1]  Radomír Mech,et al.  Self-organizing tree models for image synthesis , 2009, ACM Trans. Graph..

[2]  Gideon F. Smith,et al.  The price of collecting life , 2003, Nature.

[3]  P. Klinkhamer Plant allometry: The scaling of form and process , 1995 .

[4]  Paul R Zurek,et al.  GiA Roots: software for the high throughput analysis of plant root system architecture , 2012, BMC Plant Biology.

[5]  Abhiram Das,et al.  Overcoming the Law of the Hidden in Cyberinfrastructures. , 2017, Trends in plant science.

[6]  D. Barthélémy,et al.  Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. , 2007, Annals of botany.

[7]  P. Langridge,et al.  Breeding Technologies to Increase Crop Production in a Changing World , 2010, Science.

[8]  Catherine A. Rushworth,et al.  The evolution of quantitative traits in complex environments , 2013, Heredity.

[9]  Przemyslaw Prusinkiewicz,et al.  The Algorithmic Beauty of Plants , 1990, The Virtual Laboratory.

[10]  J. Roden Modeling the light interception and carbon gain of individual fluttering aspen (Populus tremuloides Michx) leaves , 2003, Trees.

[11]  Richard M. Clark,et al.  A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture , 2006, Nature Genetics.

[12]  P. B. Green,et al.  Expression of pattern in plants: combining molecular and calculus-based biophysical paradigms. , 1999, American journal of botany.

[13]  S. Mooney,et al.  Plant roots use a patterning mechanism to position lateral root branches toward available water , 2014, Proceedings of the National Academy of Sciences.

[14]  K. Okada,et al.  Reaction-Diffusion Pattern in Shoot Apical Meristem of Plants , 2011, PloS one.

[15]  Herbert Edelsbrunner,et al.  DynamicRoots: A Software Platform for the Reconstruction and Analysis of Growing Plant Roots , 2015, PloS one.

[16]  Anuj Srivastava,et al.  Landmark-free statistical analysis of the shape of plant leaves. , 2014, Journal of Theoretical Biology.

[17]  A. M. Turing,et al.  The chemical basis of morphogenesis , 1952, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[18]  J. Grace The turbulent boundary layer over a flapping Populus leaf , 1978 .

[19]  M. Drew,et al.  COMPARISON OF THE EFFECTS OF A LOCALISED SUPPLY OF PHOSPHATE, NITRATE, AMMONIUM AND POTASSIUM ON THE GROWTH OF THE SEMINAL ROOT SYSTEM, AND THE SHOOT, IN BARLEY , 1975 .

[20]  S. Vogel Life in Moving Fluids: The Physical Biology of Flow , 1981 .

[21]  Steven Vogel,et al.  Twist-to-Bend Ratios and Cross-Sectional Shapes of Petioles and Stems , 1992 .

[22]  Jacek Majewski,et al.  The study of eQTL variations by RNA-seq: from SNPs to phenotypes. , 2011, Trends in genetics : TIG.

[23]  Jerzy Nakielski,et al.  The tensor-based model for growth and cell divisions of the root apex. I. The significance of principal directions , 2008, Planta.

[24]  J. Dinneny,et al.  Environmental Control of Root System Biology. , 2016, Annual review of plant biology.

[25]  Daniel Huber The ASTM E57 file format for 3D imaging data exchange , 2011, Electronic Imaging.

[26]  Michael F. Covington,et al.  A Quantitative Genetic Basis for Leaf Morphology in a Set of Precisely Defined Tomato Introgression Lines[C][W][OPEN] , 2013, Plant Cell.

[27]  Donald R. Kaplan,et al.  The Relationship of Cell and Organism in Vascular PlantsAre cells the building blocks of plant form , 1991 .

[28]  Steven Vogel,et al.  Drag and Flexibility in Sessile Organisms , 1984 .

[29]  When Speed Truly Matters, Openness is the Answer , 2009, Bioethics.

[30]  Mao Li,et al.  Persistent homology and the branching topologies of plants. , 2017, American journal of botany.

[31]  Gaël Varoquaux,et al.  Publishing scientific software matters , 2013, J. Comput. Sci..

[32]  J. Dumais,et al.  Analysis of surface growth in shoot apices. , 2002, The Plant journal : for cell and molecular biology.

[33]  Z. Hejnowicz,et al.  Modeling of meristematic growth of root apices in a natural coordinate system , 1993 .

[34]  Joel E. Cohen,et al.  Mathematics Is Biology's Next Microscope, Only Better; Biology Is Mathematics' Next Physics, Only Better , 2004, PLoS biology.

[35]  Deirdre Ryan,et al.  The Global Plants Initiative Celebrates its Achievements and Plans for the Future , 2013 .

[36]  E Mayr,et al.  Biological Classification: Toward a Synthesis of Opposing Methodologies , 1981, Science.

[37]  Alexander Bucksch,et al.  Revealing the skeleton from imperfect point clouds , 2011 .

[38]  Louis J. Gross Points of View The Interface of Mathematics and Biology , 2004 .

[39]  Jonathan P Lynch,et al.  Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture. , 2015, Plant, cell & environment.

[40]  J. Tyson,et al.  A Bistable Switch Mechanism for Stem Cell Domain Nucleation in the Shoot Apical Meristem , 2016, Front. Plant Sci..

[41]  P. Bayer,et al.  Genome-Wide Association Studies in Plants , 2019, eLS.

[42]  Christopher N Topp,et al.  Quantitative Trait Locus Mapping Reveals Regions of the Maize Genome Controlling Root System Architecture1[OPEN] , 2015, Plant Physiology.

[43]  George Vosselman,et al.  Airborne and terrestrial laser scanning , 2011, Int. J. Digit. Earth.

[44]  A. Thom The exchange of momentum, mass, and heat between an artificial leaf and the airflow in a wind‐tunnel , 1968 .

[45]  R. Borchert,et al.  Bifurcation Ratios and the Adaptive Geometry of Trees , 1981, Botanical Gazette.

[46]  H. Jönsson,et al.  Shifting foundations: the mechanical cell wall and development. , 2016, Current opinion in plant biology.

[47]  S A Etnier,et al.  Reorientation of daffodil(Narcissus: Amaryllidaceae) flowers inwind: drag reduction andtorsional flexibility. , 2000, American journal of botany.

[48]  R. O. Erickson,et al.  Kinematics of plant growth. , 1979, Journal of theoretical biology.

[49]  Robert W. Pearcy,et al.  Effect of leaf flutter on the light environment of poplars , 1993, Oecologia.

[50]  D. Kliebenstein,et al.  Identification of Novel Loci Regulating Interspecific Variation in Root Morphology and Cellular Development in Tomato1[W][OA] , 2013, Plant Physiology.

[51]  Koichi Fujimoto,et al.  A Dynamical Phyllotaxis Model to Determine Floral Organ Number , 2015, PLoS Comput. Biol..

[52]  Takashi Aoyama,et al.  A Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem , 2008, Science.

[53]  J. Lynch,et al.  New roots for agriculture: exploiting the root phenome , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  S. Vogel Convective Cooling at Low Airspeeds and the Shapes of Broad Leaves , 1970 .

[55]  U. Rascher,et al.  Imaging plants dynamics in heterogenic environments. , 2012, Current opinion in biotechnology.

[56]  Patrick Valduriez,et al.  OpenAlea: scientific workflows combining data analysis and simulation , 2015, SSDBM.

[57]  W. Briggs,et al.  Phototropism: Some History, Some Puzzles, and a Look Ahead1 , 2014, Plant Physiology.

[58]  P. Herendeen,et al.  Eocene dry climate and woodland vegetation in tropical Africa reconstructed from fossil leaves from northern Tanzania , 2004 .

[59]  D. Seidel,et al.  Relationship between tree growth and physical dimensions of Fagus sylvatica crowns assessed from terrestrial laser scanning , 2015 .

[60]  Francis Hallé,et al.  Opportunistic Tree Architecture , 1978 .

[61]  Peter J. Bradbury,et al.  Genome-wide association study of leaf architecture in the maize nested association mapping population , 2011, Nature Genetics.

[62]  T. Mione,et al.  The evolutionary biology of plants , 1998, Economic Botany.

[63]  Alastair H. Fitter,et al.  AN ARCHITECTURAL APPROACH TO THE COMPARATIVE ECOLOGY OF PLANT ROOT SYSTEMS , 2008 .

[64]  Paul R Zurek,et al.  3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture , 2013, Proceedings of the National Academy of Sciences.

[65]  R. MacCurdy,et al.  Three-Dimensional Root Phenotyping with a Novel Imaging and Software Platform1[C][W][OA] , 2011, Plant Physiology.

[66]  Johannes Auke Postma,et al.  Root Cortical Aerenchyma Enhances the Growth of Maize on Soils with Suboptimal Availability of Nitrogen, Phosphorus, and Potassium1[W][OA] , 2011, Plant Physiology.

[67]  K. Taylor,et al.  Genome-Wide Association , 2007, Diabetes.

[68]  Peter Pfeifer,et al.  A Method for Estimation of Fractal Dimension of Tree Crowns , 1991, Forest Science.

[69]  Ciera C. Martinez,et al.  Left–right leaf asymmetry in decussate and distichous phyllotactic systems , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[70]  B. S. Manjunath,et al.  The iPlant Collaborative: Cyberinfrastructure for Plant Biology , 2011, Front. Plant Sci..

[71]  Brendan Lane,et al.  The use of positional information in the modeling of plants , 2001, SIGGRAPH.

[72]  S. Vogel Drag and Reconfiguration of Broad Leaves in High Winds , 1989 .

[73]  Christophe Godin,et al.  Multiscale Systems Analysis of Root Growth and Development: Modeling Beyond the Network and Cellular Scales , 2012, Plant Cell.

[74]  Evelyne Costes,et al.  Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: QTL mapping , 2008, Tree Genetics & Genomes.

[75]  D. Greenwood,et al.  Fossils and fossil climate: the case for equable continental interiors in the Eocene , 1993 .

[76]  William Stafford Noble A Quick Guide to Organizing Computational Biology Projects , 2009, PLoS Comput. Biol..

[77]  Christian Jauvin,et al.  PypeTree: A Tool for Reconstructing Tree Perennial Tissues from Point Clouds , 2014, Sensors.

[78]  G. Goldstein,et al.  Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity , 1998, Oecologia.

[79]  Jonathan P Lynch,et al.  Reduced Root Cortical Cell File Number Improves Drought Tolerance in Maize1[C][W][OPEN] , 2014, Plant Physiology.

[80]  H. Meinhardt,et al.  A theory of biological pattern formation , 1972, Kybernetik.

[81]  P. Schnable,et al.  Diversity of Maize Shoot Apical Meristem Architecture and Its Relationship to Plant Morphology , 2015, G3: Genes, Genomes, Genetics.

[82]  E. Bayer,et al.  Auxin transport-feedback models of patterning in plants. , 2009, Plant, cell & environment.

[83]  Michael F. Covington,et al.  A Modern Ampelography: A Genetic Basis for Leaf Shape and Venation Patterning in Grape1[C][W][OPEN] , 2013, Plant Physiology.

[84]  M. Kendall Statistical Methods for Research Workers , 1937, Nature.

[85]  Adam Runions,et al.  Modeling Trees with a Space Colonization Algorithm , 2007, NPH.

[86]  Robert D. MacPherson,et al.  Measuring Shape with Topology , 2010, ArXiv.

[87]  Christopher R. Myers,et al.  Universally Sloppy Parameter Sensitivities in Systems Biology Models , 2007, PLoS Comput. Biol..

[88]  J. Casal Photoreceptor signaling networks in plant responses to shade. , 2013, Annual review of plant biology.

[89]  D. Chitwood,et al.  Climate and Developmental Plasticity: Interannual Variability in Grapevine Leaf Morphology1[OPEN] , 2016, Plant Physiology.

[90]  Brett W. Benz,et al.  Foliar trichomes, boundary layers, and gas exchange in 12 species of epiphytic Tillandsia (Bromeliaceae). , 2006, Journal of plant physiology.

[91]  Luoding Zhu,et al.  Reconfiguration and the reduction of vortex-induced vibrations in broad leaves , 2012, Journal of Experimental Biology.

[92]  John A. Fozard,et al.  Multiscale models in the biomechanics of plant growth. , 2015, Physiology.

[93]  Christophe Godin,et al.  Functional-structural plant modelling. , 2005, The New phytologist.

[94]  Patrick S. Schnable,et al.  Genetic control of morphometric diversity in the maize shoot apical meristem , 2015, Nature Communications.

[95]  Samuel M. Scheiner,et al.  Phenotypic plasticity : functional and conceptual approaches , 2004 .

[96]  GodinChristophe,et al.  Quantifying the Degree of Self-Nestedness of Trees , 2010 .

[97]  F. Fiorani,et al.  A method to construct dose-response curves for a wide range of environmental factors and plant traits by means of a meta-analysis of phenotypic data. , 2010, Journal of experimental botany.

[98]  E. W. Lindstrom The genetics of maize. , 1930 .

[99]  W Kurth,et al.  Topology, scaling relations and Leonardo's rule in root systems from African tree species. , 2001, Tree physiology.

[100]  Andrew D Higginson,et al.  Heavy use of equations impedes communication among biologists , 2012, Proceedings of the National Academy of Sciences.

[101]  Charles R. Giardina,et al.  Elliptic Fourier features of a closed contour , 1982, Comput. Graph. Image Process..

[102]  Christophe Godin,et al.  A Method for Describing Plant Architecture which Integrates Topology and Geometry , 1999 .

[103]  Alan Boyde,et al.  Quantitative photogrammetric analysis and qualitative stereoscopic analysis of SEM images , 1973 .

[104]  Christopher N Topp,et al.  Revealing plant cryptotypes: defining meaningful phenotypes among infinite traits. , 2015, Current opinion in plant biology.

[105]  P. Wilf When are leaves good thermometers? A new case for Leaf Margin Analysis , 1997, Paleobiology.

[106]  T. DeWitt Expanding the phenotypic plasticity paradigm to broader views of trait space and ecological function. , 2016, Current zoology.

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

[108]  Jonathan Y. Clark,et al.  Automatic Extraction of Leaf Characters from Herbarium Specimens , 2012 .

[109]  M. A. R. Koehl,et al.  Effects of Sea Anemones on the Flow Forces They Encounter , 1977 .

[110]  Nathan D. Miller,et al.  Plasticity of Arabidopsis Root Gravitropism throughout a Multidimensional Condition Space Quantified by Automated Image Analysis1[W][OA] , 2009, Plant Physiology.

[111]  C. Godin,et al.  Structural root architecture of 5-year-old Pinus pinaster measured by 3D digitising and analysed with AMAPmod , 2004, Plant and Soil.

[112]  T. Shiina,et al.  A Scalable Open-Source Pipeline for Large-Scale Root Phenotyping of Arabidopsis[W][OPEN] , 2014, Plant Cell.

[113]  Loïc Pagès,et al.  A Novel Image-Analysis Toolbox Enabling Quantitative Analysis of Root System Architecture1[W][OA] , 2011, Plant Physiology.

[114]  Guillaume Lobet,et al.  GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems , 2015, bioRxiv.

[115]  U. Schurr,et al.  Quantitative 3D Analysis of Plant Roots Growing in Soil Using Magnetic Resonance Imaging1[OPEN] , 2016, Plant Physiology.

[116]  Juha Hyyppä,et al.  Range calibration of airborne profiling radar used in forest inventory , 2016, 2016 IEEE International Geoscience and Remote Sensing Symposium (IGARSS).

[117]  K. Esau Anatomy of seed plants , 1960 .

[118]  J. Molofsky,et al.  The ubiquity of phenotypic plasticity in plants: a synthesis , 2015, Ecology and evolution.

[119]  F. Bookstein,et al.  Morphometric Tools for Landmark Data: Geometry and Biology , 1999 .

[120]  J. Lynch,et al.  Root cortical aerenchyma improves the drought tolerance of maize (Zea mays L.). , 2010, Plant, cell & environment.

[121]  Hans Meinhardt,et al.  Models and Hypotheses , 1976 .

[122]  L. Ku,et al.  The ZmCLA4 gene in the qLA4-1 QTL controls leaf angle in maize (Zea mays L.). , 2014, Journal of experimental botany.

[123]  J. E. Pearson Complex Patterns in a Simple System , 1993, Science.

[124]  J. A. Wolfe Temperature parameters of humid to mesic forests of Eastern Asia and relation to forests of other regions of the Northern Hemisphere and Australasia: analysis of temperature data from more than 400 stations in Eastern Asia , 1979 .

[125]  R. Fisher THE USE OF MULTIPLE MEASUREMENTS IN TAXONOMIC PROBLEMS , 1936 .

[126]  J. Dinneny,et al.  The divining root: moisture-driven responses of roots at the micro- and macro-scale. , 2015, Journal of experimental botany.

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

[128]  J. Lynch,et al.  Integration of root phenes for soil resource acquisition , 2013, Front. Plant Sci..

[129]  C. Fournier,et al.  OpenAlea: a visual programming and component-based software platform for plant modelling. , 2008, Functional plant biology : FPB.

[130]  F. Hallé,et al.  Modular Growth in Seed Plants , 1986 .

[131]  Christophe Godin,et al.  Quantifying the Degree of Self-Nestedness of Trees: Application to the Structural Analysis of Plants , 2010, IEEE/ACM Transactions on Computational Biology and Bioinformatics.

[132]  Eckart Zitzler,et al.  A Dynamic Model for Stem Cell Homeostasis and Patterning in Arabidopsis Meristems , 2010, PloS one.

[133]  S. Vogel Leaves in the lowest and highest winds: temperature, force and shape. , 2009, The New phytologist.

[134]  D. Chitwood Imitation, Genetic Lineages, and Time Influenced the Morphological Evolution of the Violin , 2014, PloS one.

[135]  Lianhai Wu,et al.  Modelling root–soil interactions using three–dimensional models of root growth, architecture and function , 2013, Plant and Soil.

[136]  Mathieu Javaux,et al.  Root System Markup Language: Toward a Unified Root Architecture Description Language1[OPEN] , 2015, Plant Physiology.

[137]  C. Juday Weitere experimentelle Untersuchungen über Artveränderung, speziel über das Wesen quantitativer Artuntershiede bei Daphniden , 1910 .

[138]  Daniela Giorgi,et al.  Discrete Laplace-Beltrami operators for shape analysis and segmentation , 2009, Comput. Graph..

[139]  Alexander Bucksch,et al.  Automated Detection of Branch Dimensions in Woody Skeletons of Fruit Tree Canopies , 2011 .

[140]  K. Robertson,et al.  Phenotypic Plasticity of Leaf Shape along a Temperature Gradient in Acer rubrum , 2009, PloS one.

[141]  Bruce E. Shapiro,et al.  Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem , 2005, ISMB.

[142]  J. Clausen,et al.  Regional Differentiation in Plant Species , 1941, The American Naturalist.

[143]  H. de Jong,et al.  Towards multiscale plant models: integrating cellular networks. , 2012, Trends in plant science.

[144]  Sandra D. Mitchell,et al.  The Life of a Leaf , 2013 .

[145]  M. Yano,et al.  Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions , 2013, Nature Genetics.

[146]  Alban Gaignard,et al.  Scientific workflows for computational reproducibility in the life sciences: Status, challenges and opportunities , 2017, Future Gener. Comput. Syst..

[147]  Jun Zhang,et al.  Drag reduction through self-similar bending of a flexible body , 2002, Nature.

[148]  B. Moulia,et al.  The power and control of gravitropic movements in plants: a biomechanical and systems biology view. , 2009, Journal of experimental botany.

[149]  Oscillations of plants' stems and their damping: theory and experimentation. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[150]  W. Silk,et al.  Quantitative Descriptions of Development , 1984 .

[151]  Emeric Bron,et al.  Pectin-Induced Changes in Cell Wall Mechanics Underlie Organ Initiation in Arabidopsis , 2011, Current Biology.

[152]  K. C. Huang,et al.  Cell size and growth regulation in the Arabidopsis thaliana apical stem cell niche , 2016, Proceedings of the National Academy of Sciences.

[153]  Zygmunt Hejnowicz,et al.  Growth tensor of plant organs , 1984 .

[154]  Giuseppe Piccardo,et al.  NON-LINEAR GALLOPING OF SAGGED CABLES IN 1:2 INTERNAL RESONANCE , 1998 .

[155]  J. Dumais,et al.  Universal rule for the symmetric division of plant cells , 2011, Proceedings of the National Academy of Sciences.

[156]  Xianzhong Feng,et al.  Evolution through genetically controlled allometry space. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[157]  J. Hanan,et al.  Rice morphogenesis and plant architecture: measurement, specification and the reconstruction of structural development by 3D architectural modelling. , 2005, Annals of botany.

[158]  Ambuj K. Singh,et al.  Bisque: a platform for bioimage analysis and management , 2009, Bioinform..

[159]  P. Diggle,et al.  Charles Darwin and the Origins of Plant Evolutionary Developmental Biology , 2011, Plant Cell.

[160]  D R Kaplan,et al.  The science of plant morphology: definition, history, and role in modern biology. , 2001, American journal of botany.

[161]  T. C. Nesbitt,et al.  fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. , 2000, Science.

[162]  Emmanuel de Langre,et al.  Drag reduction by reconfiguration of a poroelastic system , 2011 .

[163]  Bruno Sudret,et al.  Global sensitivity analysis using polynomial chaos expansions , 2008, Reliab. Eng. Syst. Saf..

[164]  Tobias Wojciechowski,et al.  Digital imaging of root traits (DIRT): a high-throughput computing and collaboration platform for field-based root phenomics , 2015, Plant Methods.

[165]  S. Vogel Drag reduction by leaf aquaplaning in Hexastylis (Aristolochiaceae) and other plant species in floods , 2006, Journal of the North American Benthological Society.

[166]  Jonathan P Lynch,et al.  Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. , 2013, Annals of botany.

[167]  William L. Rooney,et al.  Harnessing Genetic Variation in Leaf Angle to Increase Productivity of Sorghum bicolor , 2015, Genetics.

[168]  Patrick Valduriez,et al.  InfraPhenoGrid: A scientific workflow infrastructure for plant phenomics on the Grid , 2017, Future Gener. Comput. Syst..

[169]  Justin O Borevitz,et al.  Genome-wide association studies in plants: the missing heritability is in the field , 2011, Genome Biology.

[170]  Hans Meinhardt,et al.  Out-of-phase oscillations and traveling waves with unusual properties: the use of three-component systems in biology , 2004 .

[171]  Anne-Gaëlle Rolland-Lagan,et al.  Computational Method for Quantifying Growth Patterns at the Adaxial Leaf Surface in Three Dimensions1[W][OA] , 2012, Plant Physiology.

[172]  Philip Lewis,et al.  Fast Automatic Precision Tree Models from Terrestrial Laser Scanner Data , 2013, Remote. Sens..

[173]  田原 康玄,et al.  生活習慣病とgenome-wide association study , 2015 .

[174]  M. A. R. Koehl,et al.  Mechanical Diversity of Connective Tissue of the Body Wall of Sea Anemones , 1977 .

[175]  Ivo D. Dinov,et al.  A Computational Model of Multidimensional Shape , 2010, International Journal of Computer Vision.

[176]  P. Prusinkiewicz,et al.  Computational models of plant development and form. , 2012, The New phytologist.

[177]  A. Sugden ECOLOGY/EVOLUTION: Phenotypic Plasticity , 2004 .

[178]  Detlef Weigel,et al.  Next-generation genetics in plants , 2008, Nature.

[179]  H. Meinhardt Morphogenesis of lines and nets. , 1976, Differentiation; research in biological diversity.

[180]  G. Schatz Taxonomy and Herbaria in Service of Plant Conservation: Lessons from Madagascar's Endemic Families , 2002 .

[181]  Reaction-diffusion model for phyllotaxis , 1994 .

[182]  Nathan D. Miller,et al.  Computer-vision analysis of seedling responses to light and gravity. , 2007, The Plant journal : for cell and molecular biology.

[183]  J R King,et al.  Multiscale modelling of auxin transport in the plant-root elongation zone , 2011, Journal of Mathematical Biology.

[184]  Christine Granier,et al.  Combined Genetic and Modeling Approaches Reveal That Epidermal Cell Area and Number in Leaves Are Controlled by Leaf and Plant Developmental Processes in Arabidopsis1[W] , 2008, Plant Physiology.

[185]  Anuj Srivastava,et al.  Elastic-string models for representation and analysis of planar shapes , 2004, CVPR 2004.

[186]  Yiannis Ventikos,et al.  Morphomechanical Innovation Drives Explosive Seed Dispersal , 2016, Cell.

[187]  S. Barrett,et al.  Phenotypic plasticity of vegetative and reproductive traits in monoecious and dioecious populations of Sagittaria latifolia (Alismataceae): a clonal aquatic plant , 2004 .

[188]  Evelyne Costes,et al.  Dissecting apple tree architecture into genetic, ontogenetic and environmental effects: mixed linear modelling of repeated spatial and temporal measures. , 2008, The New phytologist.

[189]  L. Xiong,et al.  Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice , 2014, Nature Communications.

[190]  Johann Wolfgang von Goethe,et al.  Versuch die Metamorphose der Pflanzen zu erklären , 1973 .

[191]  J. Nap,et al.  Genetical genomics: the added value from segregation. , 2001, Trends in genetics : TIG.

[192]  Jie Peng,et al.  Resolving Distinct Genetic Regulators of Tomato Leaf Shape within a Heteroblastic and Ontogenetic Context[W][OPEN] , 2014, Plant Cell.

[193]  N. A. Kolchanov,et al.  A model study of the role of proteins CLV1, CLV2, CLV3, and WUS in regulation of the structure of the shoot apical meristem , 2007, Russian Journal of Developmental Biology.

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

[195]  P. Schuepp Studies of forced-convection heat and mass transfer of fluttering realistic leaf models , 1972 .

[196]  S. Wright,et al.  The global spectrum of plant form and function , 2015, Nature.

[197]  Marina Manca,et al.  The decline of , 2000 .

[198]  R. May Uses and Abuses of Mathematics in Biology , 2004, Science.

[199]  J. Doebley The genetics of maize evolution. , 2004, Annual review of genetics.

[200]  C. Waddington,et al.  GENETIC ASSIMILATION OF AN ACQUIRED CHARACTER , 1953 .

[201]  Eric H. Metzler,et al.  Plant Biomechanics : An Engineering Approach to Plant Form and Function , 2017 .

[202]  H. Leitte,et al.  Rules and Self-Organizing Properties of Post-embryonic Plant Organ Cell Division Patterns , 2016, Current Biology.

[203]  O. Hamant,et al.  Regulatory Role of Cell Division Rules on Tissue Growth Heterogeneity , 2012, Front. Plant Sci..

[204]  Alexander Bucksch,et al.  SkelTre - Robust skeleton extraction from imperfect point clouds , 2010, Vis. Comput..

[205]  Jonathan P. Lynch,et al.  Utility of root cortical aerenchyma under water limited conditions in tropical maize (Zea mays L.) , 2015 .

[206]  BY D. F. PARKHURSTt OPTIMAL LEAF SIZE IN RELATION TO ENVIRONMENT * , 2022 .

[207]  D. Chitwood,et al.  Conflict between Intrinsic Leaf Asymmetry and Phyllotaxis in the Resupinate Leaves of Alstroemeria psittacina , 2012, Front. Plant Sci..

[208]  Wojtek Palubicki,et al.  A Computational Study of Tree Architecture , 2013 .

[209]  E. Finnegan,et al.  Plant phenotypic plasticity in a changing climate. , 2010, Trends in plant science.

[210]  Y. Couder,et al.  Developmental Patterning by Mechanical Signals in Arabidopsis , 2009 .

[211]  Utpal Nath,et al.  Divergence in Patterns of Leaf Growth Polarity Is Associated with the Expression Divergence of miR396 , 2015, Plant Cell.

[212]  Herbert Edelsbrunner,et al.  Computational Topology - an Introduction , 2009 .

[213]  P. Prusinkiewicz,et al.  Genetic control of plant development by overriding a geometric division rule. , 2014, Developmental cell.

[214]  Y. Couder,et al.  Phyllotaxis as a Dynamical Self Organizing Process Part II: The Spontaneous Formation of a Periodicity and the Coexistence of Spiral and Whorled Patterns , 1996 .

[215]  Abhiram Das,et al.  Image-Based High-Throughput Field Phenotyping of Crop Roots1[W][OPEN] , 2014, Plant Physiology.

[216]  A. R. Ennos,et al.  Wind as an ecological factor. , 1997, Trends in ecology & evolution.

[217]  Ana I. Caño-Delgado,et al.  The genetic basis of fruit morphology in horticultural crops: lessons from tomato and melon. , 2013, Journal of experimental botany.

[218]  A. D. Bradshaw,et al.  Evolutionary Significance of Phenotypic Plasticity in Plants , 1965 .

[219]  Hu Jianping,et al.  Review of applying X-ray computed tomography for imaging soil-root physical and biological processes , 2015 .

[220]  W. Silk,et al.  Growth and development of sorghum leaves under conditions of NaCl stress , 1993, Planta.

[221]  M. Bennett,et al.  The case for morphogens in plants , 2003, Nature Cell Biology.

[222]  D. Weijers,et al.  Auxin control of embryo patterning. , 2009, Cold Spring Harbor perspectives in biology.

[223]  Christophe Eloy,et al.  Leonardo's rule, self-similarity, and wind-induced stresses in trees. , 2011, Physical review letters.

[224]  Nathan D. Miller,et al.  Image analysis is driving a renaissance in growth measurement. , 2013, Current opinion in plant biology.

[225]  Andrei G. Jablokow,et al.  Carbon cost of root systems: an architectural approach , 1994, Plant and Soil.

[226]  Daniel Koenig,et al.  Natural Variation in Leaf Morphology Results from Mutation of a Novel KNOX Gene , 2008, Current Biology.

[227]  A. Atlan,et al.  Phenotypic Plasticity in Reproductive Traits of the Perennial Shrub Ulex europaeus in Response to Shading: A Multi-Year Monitoring of Cultivated Clones , 2015, PloS one.

[228]  H. Meinhardt,et al.  Applications of a theory of biological pattern formation based on lateral inhibition. , 1974, Journal of cell science.

[229]  J. A. Wolfe A method of obtaining climatic parameters from leaf assemblages , 1993 .

[230]  Greg Turk,et al.  The Fiber Walk: A Model of Tip-Driven Growth with Lateral Expansion , 2013, PloS one.

[231]  P. Benfey,et al.  From Genotype to Phenotype: Systems Biology Meets Natural Variation , 2008, Science.

[232]  Przemyslaw Prusinkiewicz,et al.  Self-Similarity in Plants: Integrating Mathematical and Biological Perspectives , 2004 .

[233]  Shengping Zhang,et al.  Computer vision cracks the leaf code , 2016, Proceedings of the National Academy of Sciences.

[234]  E. W. Sinnott,et al.  A BOTANICAL INDEX OF CRETACEOUS AND TERTIARY CLIMATES. , 1915, Science.

[235]  P. Prusinkiewicz,et al.  Constraints of space in plant development. , 2009, Journal of experimental botany.

[236]  W. Zhang,et al.  Quantitative trait loci mapping of leaf angle and leaf orientation value in maize (Zea mays L.) , 2010, Theoretical and Applied Genetics.

[237]  J. Lynch,et al.  Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply , 2005, Theoretical and Applied Genetics.

[238]  F. Hallé,et al.  Architecture and Growth of Tropical Trees Exemplified by the Euphorbiaceae , 1971 .

[239]  J. Keulemans,et al.  Study of tree architecture of apple (Malus  ×  domestica Borkh.) by QTL analysis of growth traits , 2007, Molecular Breeding.

[240]  Volko Green plants : electrochemical interfaces , 2000 .

[241]  G. Smith,et al.  Nobel Lecture: The invention and early history of the CCD , 2010 .

[242]  Jonathan P Lynch,et al.  Large Root Cortical Cell Size Improves Drought Tolerance in Maize1[C][W][OPEN] , 2014, Plant Physiology.

[243]  J. Bangham,et al.  Growth dynamics underlying petal shape and asymmetry , 2003, Nature.

[244]  Alexander Bucksch,et al.  A practical introduction to skeletons for the plant sciences1 , 2014, Applications in plant sciences.

[245]  Richard H. Grant,et al.  The scaling of flow in vegetative structures , 1983 .

[246]  Cris Kuhlemeier,et al.  Leaf Asymmetry as a Developmental Constraint Imposed by Auxin-Dependent Phyllotactic Patterning[OA] , 2012, Plant Cell.

[247]  D. Kendall SHAPE MANIFOLDS, PROCRUSTEAN METRICS, AND COMPLEX PROJECTIVE SPACES , 1984 .

[248]  Alexander Bucksch,et al.  Automated detection of branch dimensions in woody skeletons of leafless fruit tree canopies , 2009 .

[249]  Y. Couder,et al.  PHYLLOTAXIS AS A DYNAMICAL SELF ORGANIZING PROCESS. PART I: THE SPIRAL MODES RESULTING FROM TIME-PERIODIC ITERATIONS , 1996 .

[250]  I. Paran,et al.  Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper. , 2007, Journal of experimental botany.

[251]  R. E. Sharp,et al.  Growth of the Maize Primary Root at Low Water Potentials : III. Role of Increased Proline Deposition in Osmotic Adjustment. , 1991, Plant physiology.

[252]  M. Vastaranta,et al.  Combining Lidar and Synthetic Aperture Radar Data to Estimate Forest Biomass: Status and Prospects , 2015 .

[253]  Reinhard Klein,et al.  Hybrid tree reconstruction from inhomogeneous point clouds , 2014, The Visual Computer.