Morphomechanical Innovation Drives Explosive Seed Dispersal

Summary How mechanical and biological processes are coordinated across cells, tissues, and organs to produce complex traits is a key question in biology. Cardamine hirsuta, a relative of Arabidopsis thaliana, uses an explosive mechanism to disperse its seeds. We show that this trait evolved through morphomechanical innovations at different spatial scales. At the organ scale, tension within the fruit wall generates the elastic energy required for explosion. This tension is produced by differential contraction of fruit wall tissues through an active mechanism involving turgor pressure, cell geometry, and wall properties of the epidermis. Explosive release of this tension is controlled at the cellular scale by asymmetric lignin deposition within endocarp b cells—a striking pattern that is strictly associated with explosive pod shatter across the Brassicaceae plant family. By bridging these different scales, we present an integrated mechanism for explosive seed dispersal that links evolutionary novelty with complex trait innovation. Video Abstract

[1]  A. D. Tomos,et al.  Radial Turgor Pressure Profiles in Growing and Mature Zones of Wheat Roots—A Modification of the Pressure Probe , 1989 .

[2]  P. Hallett,et al.  The rheological properties of the seed coat mucilage of Capsella bursa-pastoris L. Medik. (shepherd's purse). , 2013, Biorheology.

[3]  Tetsuro Mimura,et al.  Transcription switches for protoxylem and metaxylem vessel formation. , 2005, Genes & development.

[4]  A. Roeder,et al.  Control of Fruit Patterning in Arabidopsis by INDEHISCENT , 2004, Cell.

[5]  Berend Snel,et al.  SOMBRERO, BEARSKIN1, and BEARSKIN2 Regulate Root Cap Maturation in Arabidopsis[C][W] , 2010, Plant Cell.

[6]  Steven Vogel,et al.  Living in a physical world II. The bio-ballistics of small projectiles , 2005, Journal of Biosciences.

[7]  D. Cosgrove Plant cell wall extensibility: connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. , 2016, Journal of experimental botany.

[8]  Robert D Deegan,et al.  Finessing the fracture energy barrier in ballistic seed dispersal , 2012, Proceedings of the National Academy of Sciences.

[9]  Adrian L. R. Thomas,et al.  Photogrammetric reconstruction of high-resolution surface topographies and deformable wing kinematics of tethered locusts and free-flying hoverflies , 2009, Journal of The Royal Society Interface.

[10]  L. Tait Insectivorous Plants , 1875, Nature.

[11]  Renze Heidstra,et al.  PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development , 2007, Nature.

[12]  J. Schroeder,et al.  Potassium-selective single channels in guard cell protoplasts of Vicia faba , 1984, Nature.

[13]  J Dumais,et al.  The Fern Sporangium: A Unique Catapult , 2012, Science.

[14]  Ballistic seed projection in two herbaceous species. , 2000, American journal of botany.

[15]  T. Beer,et al.  ON THE THEORY OF EXPLOSIVELY DISPERSED SEEDS , 1977 .

[16]  B. Snel,et al.  Arabidopsis PLETHORA Transcription Factors Control Phyllotaxis , 2011, Current Biology.

[17]  K C Hamner,et al.  Circadian Leaf Movements: Persistence in Bean Plants Grown in Continuous High-Intensity Light , 1964, Science.

[18]  P. Koumoutsakos,et al.  MorphoGraphX: A platform for quantifying morphogenesis in 4D , 2015, eLife.

[19]  Yuval Eshed,et al.  SHATTERPROOF MADS-box genes control seed dispersal in Arabidopsis , 2000, Nature.

[20]  Gerhard A. Holzapfel,et al.  Nonlinear Solid Mechanics: A Continuum Approach for Engineering Science , 2000 .

[21]  A. Roeder,et al.  The Role of the REPLUMLESS Homeodomain Protein in Patterning the Arabidopsis Fruit , 2003, Current Biology.

[22]  L. Mahadevan,et al.  How the Venus flytrap snaps , 2005, Nature.

[23]  Miltos Tsiantis,et al.  The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta , 2006, Nature Genetics.

[24]  Cris Kuhlemeier,et al.  Cellular Force Microscopy for in Vivo Measurements of Plant Tissue Mechanics1[W][OA] , 2012, Plant Physiology.

[25]  G. Bassel,et al.  Mechanical constraints imposed by 3D cellular geometry and arrangement modulate growth patterns in the Arabidopsis embryo , 2014, Proceedings of the National Academy of Sciences.

[26]  D. Whitaker,et al.  Botany: A record-breaking pollen catapult , 2005, Nature.

[27]  N. Harris,et al.  ‘Pod shatter’ in Arabidopsis thalianaBrassica napus and B. juncea , 1996 .

[28]  R. P. Randall,et al.  A Global Compendium of Weeds , 2002 .

[29]  H. Kudoh,et al.  Ecological distribution and phenology of an invasive species, Cardamine hirsuta L., and its native counterpart, Cardamine flexuosa With., in central Japan , 2003 .

[30]  Marcus Roper,et al.  Dispersal of fungal spores on a cooperatively generated wind , 2010, Proceedings of the National Academy of Sciences.

[31]  J. Uhrig,et al.  MIDGET Unravels Functions of the Arabidopsis Topoisomerase VI Complex in DNA Endoreduplication, Chromatin Condensation, and Transcriptional Silencing[W] , 2007, The Plant Cell Online.

[32]  Anne-Lise Routier-Kierzkowska,et al.  Measuring the mechanical properties of plant cells by combining micro-indentation with osmotic treatments , 2015, Journal of experimental botany.

[33]  F. Vuolo,et al.  Leaf Shape Evolution Through Duplication, Regulatory Diversification, and Loss of a Homeobox Gene , 2014, Science.

[34]  Bertrand Tondu,et al.  Modelling of the McKibben artificial muscle: A review , 2012 .

[35]  L Wang,et al.  Modelling the mechanical properties of single suspension-cultured tomato cells. , 2004, Annals of botany.

[36]  Martin Bringmann,et al.  Impaired Cellulose Synthase Guidance Leads to Stem Torsion and Twists Phyllotactic Patterns in Arabidopsis , 2013, Current Biology.

[37]  A. Bowling,et al.  The mechanism for explosive seed dispersal in Cardamine hirsuta (Brassicaceae). , 2011, American journal of botany.

[38]  Vipin T. Sreedharan,et al.  Multiple reference genomes and transcriptomes for Arabidopsis thaliana , 2011, Nature.

[39]  J. Dinneny,et al.  Drawing lines and borders: how the dehiscent fruit of Arabidopsis is patterned , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[40]  F. Netter,et al.  Supplemental References , 2002, We Came Naked and Barefoot.

[41]  Jacob N. Barney,et al.  The biology of invasive alien plants in Canada. 5. Polygonum cuspidatum Sieb. & Zucc. [=Fallopia japonica (Houtt.) Ronse Decr.]. , 2006 .

[42]  Marika Hayashi,et al.  The mechanics of explosive seed dispersal in orange jewelweed (Impatiens capensis) , 2009, Journal of experimental botany.

[43]  K. Shinozaki,et al.  NAC Transcription Factors, NST1 and NST3, Are Key Regulators of the Formation of Secondary Walls in Woody Tissues of Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[44]  L. Mahadevan,et al.  Physical Limits and Design Principles for Plant and Fungal Movements , 2005, Science.

[45]  R. Mott,et al.  Cardamine hirsuta: a versatile genetic system for comparative studies. , 2014, The Plant journal : for cell and molecular biology.

[46]  Josef Kittler,et al.  Applications of Graph Transformations with Industrial Relevance , 2011, Lecture Notes in Computer Science.

[47]  Miltos Tsiantis,et al.  A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta , 2008, Nature Genetics.

[48]  D. Ehrhardt,et al.  Visualization of Cellulose Synthase Demonstrates Functional Association with Microtubules , 2006, Science.

[49]  Anthony Maxwell,et al.  BIN4, a Novel Component of the Plant DNA Topoisomerase VI Complex, Is Required for Endoreduplication in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[50]  Keekyoung Kim,et al.  Multiscale stress-strain characterization of onion outer epidermal tissue in wet and dry states. , 2015, American journal of botany.

[51]  K. Ueda,et al.  Visualization of microtubules in living cells of transgenicArabidopsis thaliana , 1999, Protoplasma.

[52]  D. Ellerby,et al.  The seed dispersal catapult of Cardamine parviflora (Brassicaceae) is efficient but unreliable. , 2010, American journal of botany.

[53]  Haimin Yao,et al.  Journal of the Mechanics and Physics of Solids , 2014 .

[54]  M. D. Swaine,et al.  EXPLOSIVE SEED DISPERSAL IN HURA CREPITANS L. (EUPHORBIACEAE) , 1977 .

[55]  Karen Jones,et al.  The biology of invasive alien plants in Canada. 9. Impatiens glandulifera Royle. , 2008 .

[56]  M. Pfaffl,et al.  A new mathematical model for relative quantification in real-time RT-PCR. , 2001, Nucleic acids research.

[57]  J. Dunlop,et al.  Micromechanis of cell walls , 2011 .