On the internal architecture of emergent plants

Abstract It remains a puzzling issue why and how the organs in plants living in the same natural environment evolve into a wide variety of geometric architecture. In this work, we explore, through a combination of experimental and numerical methods, the biomechanical morphogenesis of the leaves and stalks of representative emergent plants, which can stand upright and survive in harsh water environments. An interdisciplinary topology optimization method is developed here by integrating both mechanical performance and biological constraint into the bi-directional evolutionary structural optimization technique. The experimental and numerical results reveal that, through natural selection over many million years, these leaves and stalks have been optimized into distinctly different cross-sectional shapes and aerenchyma tissues with intriguing anatomic patterns and improved load-bearing performance. The internal aerenchyma is an optimal compromise between the mechanical performance and functional demands such as air exchange and nutrient transmission. We find that the optimal distribution of the internal material depends on multiple biomechanical factors such as the cross-sectional geometry, hierarchical structures, boundary condition, biological constraint, and material property. This work provides an in-depth understanding of the property–structure–performance–function interrelations of biological materials. The proposed topology optimization method and the presented biophysical insights hold promise for designing highly efficient and advanced structures (e.g., airplane wings and turbine blades) and analyzing other biological materials (e.g., bones, horns, and beaks).

[1]  Yi Min Xie,et al.  Evolutionary Topology Optimization of Continuum Structures: Methods and Applications , 2010 .

[2]  W. Armstrong,et al.  Formation of Aerenchyma and the Processes of Plant Ventilation in Relation to Soil Flooding and Submergence , 1999 .

[3]  D. Evans,et al.  Aerenchyma formation: Tansley review , 2003 .

[4]  Wolfgang Alt,et al.  Generalized Voronoi Tessellation as a Model of Two-dimensional Cell Tissue Dynamics , 2009, Bulletin of mathematical biology.

[5]  M. Bendsøe Optimal shape design as a material distribution problem , 1989 .

[6]  Luquan Ren,et al.  Experimental study and numerical simulation on the structural and mechanical properties of Typha leaves through multimodal microscopy approaches. , 2018, Micron.

[7]  Zi-Long Zhao,et al.  Structures, properties, and functions of the stings of honey bees and paper wasps: a comparative study , 2015, Biology Open.

[8]  Tongming Zhou,et al.  On the study of vortex-induced vibration of a cylinder with helical strakes , 2011 .

[9]  M. Bendsøe,et al.  Topology Optimization: "Theory, Methods, And Applications" , 2011 .

[10]  Ernst Haeckel,et al.  Art Forms in Nature , 2004 .

[11]  O. Sigmund,et al.  Topology optimization approaches , 2013, Structural and Multidisciplinary Optimization.

[12]  Xi-Qiao Feng,et al.  Study of biomechanical, anatomical, and physiological properties of scorpion stingers for developing biomimetic materials. , 2016, Materials science & engineering. C, Materials for biological applications.

[13]  Hong-Keun Choi,et al.  Anatomical patterns of aerenchyma in aquatic and wetland plants , 2008, Journal of Plant Biology.

[14]  Sridhar Komarneni,et al.  Porous Materials: Process technology and applications , 1998 .

[15]  Thomas Geske,et al.  Aerenchyma formation in the rice stem and its promotion by H2O2. , 2011, The New phytologist.

[16]  Marc A. Meyers,et al.  Biological materials: Functional adaptations and bioinspired designs , 2012 .

[17]  D. Weaire,et al.  Soap, cells and statistics – random patterns in two dimensions , 1984 .

[18]  Takaki Yamauchi,et al.  Aerenchyma formation in crop species: A review , 2013 .

[19]  Bo Li,et al.  Activation and synchronization of the oscillatory morphodynamics in multicellular monolayer , 2017, Proceedings of the National Academy of Sciences.

[20]  Xi-Qiao Feng,et al.  Analysis of bending and buckling of pre-twisted beams: A bioinspired study , 2014 .

[21]  Henry C. Lee,et al.  Advances in Fingerprint Technology , 1991 .

[22]  Qi Xia,et al.  Bi-directional Evolutionary Structural Optimization on Advanced Structures and Materials: A Comprehensive Review , 2016, Archives of Computational Methods in Engineering.

[23]  Y. Xie,et al.  Bi-directional evolutionary topology optimization of continuum structures with one or multiple materials , 2009 .

[24]  Huajian Gao,et al.  Biomechanical tactics of chiral growth in emergent aquatic macrophytes , 2015, Scientific Reports.

[25]  Yi Min Xie,et al.  Evolutionary Structural Optimization , 1997 .

[26]  D'arcy W. Thompson On growth and form i , 1943 .

[27]  Xi-Qiao Feng,et al.  Collective dynamics of cancer cells confined in a confluent monolayer of normal cells. , 2017, Journal of biomechanics.

[28]  P. Stevens Patterns in Nature , 1974 .

[29]  Luquan Ren,et al.  The Structure and Flexural Properties of Typha Leaves , 2017, Applied bionics and biomechanics.

[30]  Y. Xie,et al.  Convergent and mesh-independent solutions for the bi-directional evolutionary structural optimization method , 2007 .

[31]  C. Mattheck Trees: The Mechanical Design , 1991 .

[32]  N. Pugno,et al.  Mechanical properties of a hollow-cylindrical-joint honeycomb , 2014 .

[33]  Hui Li,et al.  Spatial modeling of bone microarchitecture , 2012, Electronic Imaging.

[34]  J. Skinner,et al.  On the origin, evolution and phylogeny of giraffes Giraffa camelopardalis , 2003 .

[35]  Andrew I. Cooper,et al.  Function-led design of new porous materials , 2015, Science.

[36]  G. Allaire,et al.  A level-set method for shape optimization , 2002 .

[37]  Yasuaki Seki,et al.  Biological materials: Structure and mechanical properties , 2008 .

[38]  Wei Xu,et al.  Topological design and additive manufacturing of porous metals for bone scaffolds and orthopaedic implants: A review. , 2016, Biomaterials.

[39]  Y. Xie,et al.  A simple evolutionary procedure for structural optimization , 1993 .

[40]  G. Allaire,et al.  Structural optimization using sensitivity analysis and a level-set method , 2004 .

[41]  Xi-Qiao Feng,et al.  Static and dynamic mechanical properties of cattle horns , 2011 .

[42]  F. O. Bower,et al.  Comparative Anatomy of the Vegetative Organs of the Phanerogams and Ferns , 2009, Nature.

[43]  N. Perrimon,et al.  The emergence of geometric order in proliferating metazoan epithelia , 2006, Nature.

[44]  James K. Guest,et al.  Imposing maximum length scale in topology optimization , 2009 .

[45]  M. Zhou,et al.  The COC algorithm, Part II: Topological, geometrical and generalized shape optimization , 1991 .

[46]  J. Petersson,et al.  Numerical instabilities in topology optimization: A survey on procedures dealing with checkerboards, mesh-dependencies and local minima , 1998 .

[47]  Xi-Lu Ni,et al.  Programmed cell death during aerenchyma formation in Typha angustifolia leaves , 2014 .

[48]  Yanlan Mao,et al.  Fundamental physical cellular constraints drive self‐organization of tissues , 2016, The EMBO journal.

[49]  F. T. Lewis,et al.  A comparison between the mosaic of polygons in a film of artificial emulsion and the pattern of simple epithelium in surface view (cucumber epidermis and human amnion) , 1931 .

[50]  Xi-Qiao Feng,et al.  Chirality-dependent flutter of Typha blades in wind , 2016, Scientific Reports.

[51]  Xi-Qiao Feng,et al.  Synergistic Effects of Chiral Morphology and Reconfiguration in Cattail Leaves , 2015 .

[52]  Ole Sigmund,et al.  Giga-voxel computational morphogenesis for structural design , 2017, Nature.

[53]  T. E. Bruns,et al.  Topology optimization of non-linear elastic structures and compliant mechanisms , 2001 .

[54]  Njuki W. Mureithi,et al.  Bending and torsional reconfiguration of chiral rods under wind and gravity , 2017 .

[55]  A. Love A treatise on the mathematical theory of elasticity , 1892 .

[56]  Jianxiang Wang,et al.  Hierarchical, multilayered cell walls reinforced by recycled silk cocoons enhance the structural integrity of honeybee combs , 2010, Proceedings of the National Academy of Sciences.

[57]  B. Bourdin Filters in topology optimization , 2001 .

[58]  F. T. Lewis,et al.  The correlation between cell division and the shapes and sizes of prismatic cells in the epidermis of cucumis , 1928 .

[59]  Ole Sigmund,et al.  Topology optimization by distribution of isotropic material , 2004 .