Morphomechanical Innovation Drives Explosive Seed Dispersal.
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.
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
Hugo
H
Hofhuis
Mathematical Institute, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK.
Derek
D
Moulton
Mathematical Institute, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK.
Thomas
T
Lessinnes
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
Anne-Lise
AL
Routier-Kierzkowska
Structure and Motion Laboratory, Department of Comparative Biomedical Sciences, Royal Veterinary College, University of London, Hawkshead Lane, Hatfield AL9 7TA, UK.
Richard J
RJ
Bomphrey
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany; Institute of Plant Sciences, University of Bern, Altenbergrain 21, 3013 Bern, Switzerland.
Gabriella
G
Mosca
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
Hagen
H
Reinhardt
Plant Sciences Department, University of Oxford, South Parks Road, Oxford OX1 3RB, UK.
Penny
P
Sarchet
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
Xiangchao
X
Gan
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
Miltos
M
Tsiantis
Mechanical Engineering Department, University College London, Torrington Place, London WC1E 7JE, UK.
Yiannis
Y
Ventikos
Zoology Department, University of Oxford, South Parks Road, Oxford OX1 3PS, UK.
Simon
S
Walker
Mathematical Institute, University of Oxford, Radcliffe Observatory Quarter, Woodstock Road, Oxford OX2 6GG, UK.
Alain
A
Goriely
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany.
Richard
R
Smith
Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829 Köln, Germany. Electronic address: hay@mpipz.mpg.de.
Angela
A
Hay
D017360:Arabidopsis; D005075:Biological Evolution; D001696:Biomechanical Phenomena; D031217:Cardamine / Q000166:cytology* / Q000235:genetics / Q000502:physiology*; D002473:Cell Wall / Q000502:physiology; D005638:Fruit / Q000166:cytology / Q000502:physiology; D008031:Lignin / Q000737:chemistry / Q000378:metabolism; D008954:Models, Biological; D058614:Seed Dispersal
D008031:Lignin