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Morphomechanical Innovation Drives Explosive Seed Dispersal

View Article: PubMed Central - PubMed

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus

Turgor-Driven Shrinkage(A–C) Exocarp cells aligned to longitudinal fruit axis. (A) Side view of segmented cells from CLSM stacks of propidium iodine (PI)-stained fruits pre- and post-explosion, in water. (B) Top and side view of PI-stained cells treated with 1 M salt or water prior to imaging, cell outlines in yellow were used for quantitation and crosshairs show principal directions of shrinkage (red) and expansion (white). (C) Side view of cells segmented from CLSM stacks of PI-stained short valve segments treated with 1 M salt or water prior to imaging. Scale bars, 50 μm (A, B), 20 μm (C).(D–F) FEM simulations of cells pressurized from 0 Mpa (left) to 0.7 MPa (right); heatmap shows relative increase (orange) or decrease (blue) in cell length; horizontal yellow line shows initial length. Cell dimensions: 100 × 20 × 20 μm for A. thaliana exocarp cells (D), 50 × 50 × 20 μm for C. hirsuta exocarp cells (E and F). Cell wall material: isotropic (D and E), anisotropic (F). Pressure: 0 MPa (left, D and E), 0.7 MPa (right, D–F).(G) FEM simulations of exocarp cells in immature fruit of cell dimensions 30 × 20 × 14 μm (left) and mature fruit of cell dimensions 50 × 50 × 20 μm (right), micro-indented by a CFM tip. Heatmap shows stress in MPa. Scale bar, 20 μm.(H) Barplot of turgor pressure and cell wall elasticity parameters given by the FEM model for immature (dark gray) and mature (light gray) exocarp cells shown in (G). Young’s modulus in the width (Ewidth) and length (Elength) directions of the cell wall, defined by the fruit’s principal axes.(I) Sensitivity analysis of FEM model. Effect of best-fit parameters and values 15% lower and higher for pressure (dashed lines) and the Young’s modulus ratio (Ewidth:Elength, solid lines) on cell stiffness (N/m) and cell volume (ratio change), shown on the left and right y axes, respectively.See also Table S1 and Movies S3, S4, and S5.
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fig5: Turgor-Driven Shrinkage(A–C) Exocarp cells aligned to longitudinal fruit axis. (A) Side view of segmented cells from CLSM stacks of propidium iodine (PI)-stained fruits pre- and post-explosion, in water. (B) Top and side view of PI-stained cells treated with 1 M salt or water prior to imaging, cell outlines in yellow were used for quantitation and crosshairs show principal directions of shrinkage (red) and expansion (white). (C) Side view of cells segmented from CLSM stacks of PI-stained short valve segments treated with 1 M salt or water prior to imaging. Scale bars, 50 μm (A, B), 20 μm (C).(D–F) FEM simulations of cells pressurized from 0 Mpa (left) to 0.7 MPa (right); heatmap shows relative increase (orange) or decrease (blue) in cell length; horizontal yellow line shows initial length. Cell dimensions: 100 × 20 × 20 μm for A. thaliana exocarp cells (D), 50 × 50 × 20 μm for C. hirsuta exocarp cells (E and F). Cell wall material: isotropic (D and E), anisotropic (F). Pressure: 0 MPa (left, D and E), 0.7 MPa (right, D–F).(G) FEM simulations of exocarp cells in immature fruit of cell dimensions 30 × 20 × 14 μm (left) and mature fruit of cell dimensions 50 × 50 × 20 μm (right), micro-indented by a CFM tip. Heatmap shows stress in MPa. Scale bar, 20 μm.(H) Barplot of turgor pressure and cell wall elasticity parameters given by the FEM model for immature (dark gray) and mature (light gray) exocarp cells shown in (G). Young’s modulus in the width (Ewidth) and length (Elength) directions of the cell wall, defined by the fruit’s principal axes.(I) Sensitivity analysis of FEM model. Effect of best-fit parameters and values 15% lower and higher for pressure (dashed lines) and the Young’s modulus ratio (Ewidth:Elength, solid lines) on cell stiffness (N/m) and cell volume (ratio change), shown on the left and right y axes, respectively.See also Table S1 and Movies S3, S4, and S5.

Mentions: We have identified the role of the endocarp b secondary cell wall in energy release; however, the other critical component for explosive pod shatter is the build-up of elastic energy in the system. To address this mechanism, we investigated the cellular basis for the differential shortening of the fruit valve that generates tension (Figures 1H and 1I). We measured a 20% reduction in cell length in the outermost exocarp layer between the flat valve, attached to the fruit, and the curled, detached valve (Figure 5A; Table S1). To understand the mechanics of this cell shortening, we challenged a previous proposal that shrinkage in the C. hirsuta valve is caused by passive loss of cell turgor pressure via drying (Vaughn et al., 2011). Under the “drying” hypothesis, detached valves would flatten out in pure water where cell turgor pressure is high due to osmosis. Yet, we observed higher curvature in water than in air, which then flattened out upon transfer to salt solution where the cells lost turgor (Figures S1H–S1J). Moreover, explosive shatter can be prevented by drying fruits with alcohol or freezing them (Figures S1E–S1G). These results show that drying is not the cause of exocarp cell shortening in C. hirsuta and suggest that exocarp shortening is an active process, requiring living cells that can sustain turgor pressure.


Morphomechanical Innovation Drives Explosive Seed Dispersal
Turgor-Driven Shrinkage(A–C) Exocarp cells aligned to longitudinal fruit axis. (A) Side view of segmented cells from CLSM stacks of propidium iodine (PI)-stained fruits pre- and post-explosion, in water. (B) Top and side view of PI-stained cells treated with 1 M salt or water prior to imaging, cell outlines in yellow were used for quantitation and crosshairs show principal directions of shrinkage (red) and expansion (white). (C) Side view of cells segmented from CLSM stacks of PI-stained short valve segments treated with 1 M salt or water prior to imaging. Scale bars, 50 μm (A, B), 20 μm (C).(D–F) FEM simulations of cells pressurized from 0 Mpa (left) to 0.7 MPa (right); heatmap shows relative increase (orange) or decrease (blue) in cell length; horizontal yellow line shows initial length. Cell dimensions: 100 × 20 × 20 μm for A. thaliana exocarp cells (D), 50 × 50 × 20 μm for C. hirsuta exocarp cells (E and F). Cell wall material: isotropic (D and E), anisotropic (F). Pressure: 0 MPa (left, D and E), 0.7 MPa (right, D–F).(G) FEM simulations of exocarp cells in immature fruit of cell dimensions 30 × 20 × 14 μm (left) and mature fruit of cell dimensions 50 × 50 × 20 μm (right), micro-indented by a CFM tip. Heatmap shows stress in MPa. Scale bar, 20 μm.(H) Barplot of turgor pressure and cell wall elasticity parameters given by the FEM model for immature (dark gray) and mature (light gray) exocarp cells shown in (G). Young’s modulus in the width (Ewidth) and length (Elength) directions of the cell wall, defined by the fruit’s principal axes.(I) Sensitivity analysis of FEM model. Effect of best-fit parameters and values 15% lower and higher for pressure (dashed lines) and the Young’s modulus ratio (Ewidth:Elength, solid lines) on cell stiffness (N/m) and cell volume (ratio change), shown on the left and right y axes, respectively.See also Table S1 and Movies S3, S4, and S5.
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fig5: Turgor-Driven Shrinkage(A–C) Exocarp cells aligned to longitudinal fruit axis. (A) Side view of segmented cells from CLSM stacks of propidium iodine (PI)-stained fruits pre- and post-explosion, in water. (B) Top and side view of PI-stained cells treated with 1 M salt or water prior to imaging, cell outlines in yellow were used for quantitation and crosshairs show principal directions of shrinkage (red) and expansion (white). (C) Side view of cells segmented from CLSM stacks of PI-stained short valve segments treated with 1 M salt or water prior to imaging. Scale bars, 50 μm (A, B), 20 μm (C).(D–F) FEM simulations of cells pressurized from 0 Mpa (left) to 0.7 MPa (right); heatmap shows relative increase (orange) or decrease (blue) in cell length; horizontal yellow line shows initial length. Cell dimensions: 100 × 20 × 20 μm for A. thaliana exocarp cells (D), 50 × 50 × 20 μm for C. hirsuta exocarp cells (E and F). Cell wall material: isotropic (D and E), anisotropic (F). Pressure: 0 MPa (left, D and E), 0.7 MPa (right, D–F).(G) FEM simulations of exocarp cells in immature fruit of cell dimensions 30 × 20 × 14 μm (left) and mature fruit of cell dimensions 50 × 50 × 20 μm (right), micro-indented by a CFM tip. Heatmap shows stress in MPa. Scale bar, 20 μm.(H) Barplot of turgor pressure and cell wall elasticity parameters given by the FEM model for immature (dark gray) and mature (light gray) exocarp cells shown in (G). Young’s modulus in the width (Ewidth) and length (Elength) directions of the cell wall, defined by the fruit’s principal axes.(I) Sensitivity analysis of FEM model. Effect of best-fit parameters and values 15% lower and higher for pressure (dashed lines) and the Young’s modulus ratio (Ewidth:Elength, solid lines) on cell stiffness (N/m) and cell volume (ratio change), shown on the left and right y axes, respectively.See also Table S1 and Movies S3, S4, and S5.
Mentions: We have identified the role of the endocarp b secondary cell wall in energy release; however, the other critical component for explosive pod shatter is the build-up of elastic energy in the system. To address this mechanism, we investigated the cellular basis for the differential shortening of the fruit valve that generates tension (Figures 1H and 1I). We measured a 20% reduction in cell length in the outermost exocarp layer between the flat valve, attached to the fruit, and the curled, detached valve (Figure 5A; Table S1). To understand the mechanics of this cell shortening, we challenged a previous proposal that shrinkage in the C. hirsuta valve is caused by passive loss of cell turgor pressure via drying (Vaughn et al., 2011). Under the “drying” hypothesis, detached valves would flatten out in pure water where cell turgor pressure is high due to osmosis. Yet, we observed higher curvature in water than in air, which then flattened out upon transfer to salt solution where the cells lost turgor (Figures S1H–S1J). Moreover, explosive shatter can be prevented by drying fruits with alcohol or freezing them (Figures S1E–S1G). These results show that drying is not the cause of exocarp cell shortening in C. hirsuta and suggest that exocarp shortening is an active process, requiring living cells that can sustain turgor pressure.

View Article: PubMed Central - PubMed

ABSTRACT

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.

No MeSH data available.


Related in: MedlinePlus