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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

Mechanical and Osmotic Experiments in C. hirsuta and A. thaliana Fruits, Related to Figure 1(A and B) Incision of the C. hirsuta valve shows mechanical tension in situ. Mature fruit before (A) and after a shallow cut is made in the valve outer layers (B). The cut layers immediately gape in the long direction of the fruit, revealing the white, lignified endocarp b cell walls underneath (arrowhead), indicating that the valve was in a state of tension while attached to the fruit.(C and D) The same experiment in A. thaliana shows no tension. Ink was applied to the intact valve (C) to aid visibility of the incision (D, arrowhead), which did not gape.(E–J) Turgor pressure in living cells is required for full valve curvature. Valves of alcohol-dried fruits fall off without explosion and are almost flat (E). Re-hydration in water produces little curvature in alcohol-treated valves (F) or in valves killed by freezing (G), as observed previously upon re-hydration of oven-dried C. parviflora fruits (Hayashi et al., 2010). Valves of living, freshly exploded fruits are curled much more tightly in coils of ∼2 mm diameter (H). Hydration of these same valves in water results in even tighter curling in coils of ∼1 mm diameter (I), while after plasmolysis in 4M salt solution the coils open to ∼5-6 mm diameter (J). Thus, the tight coiling of valves in explosive fruits (H) is an active process requiring living cells that can sustain internal pressure. In contrast to this, the slight residual curvature in dead, hydrated valves (F and G) is passive and could be explained by gradients of cell wall composition within the valve (Hayashi et al., 2010, Vaughn et al., 2011).(K and L) Both inner and outer layers of the valve and turgor pressure are required for curvature. In pure water (K), a valve segment comprising all layers (left) curves, while a segment of excised outer layers (right) remains flat. Please note that these data are presented in Figure 1 of the main text but are also shown here for clarity. In 8 osmoles of salt solution (L), curvature of the same intact valve segment (left) is very reduced, while the same segment of excised outer layers (right) curves slightly in the opposite direction, indicating that the outermost exocarp layer increases in length following plasmolysis.(M) Endocarp layers alone do not curve in water, as shown by separating the outer layers of a valve segment from the endocarp a and b layers (white arrow). The valve segment comprising all layers curves, while each of the separated layers remain flat. Therefore, a bilayer composed of the inner and outer valve layers is necessary and sufficient for curvature, rather than a bilayer composed of the endocarp a and b layers as previously proposed (Hayashi et al., 2010). Scale bars: 1 mm (A-D, K-M), 2 mm (E-J).
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figs1: Mechanical and Osmotic Experiments in C. hirsuta and A. thaliana Fruits, Related to Figure 1(A and B) Incision of the C. hirsuta valve shows mechanical tension in situ. Mature fruit before (A) and after a shallow cut is made in the valve outer layers (B). The cut layers immediately gape in the long direction of the fruit, revealing the white, lignified endocarp b cell walls underneath (arrowhead), indicating that the valve was in a state of tension while attached to the fruit.(C and D) The same experiment in A. thaliana shows no tension. Ink was applied to the intact valve (C) to aid visibility of the incision (D, arrowhead), which did not gape.(E–J) Turgor pressure in living cells is required for full valve curvature. Valves of alcohol-dried fruits fall off without explosion and are almost flat (E). Re-hydration in water produces little curvature in alcohol-treated valves (F) or in valves killed by freezing (G), as observed previously upon re-hydration of oven-dried C. parviflora fruits (Hayashi et al., 2010). Valves of living, freshly exploded fruits are curled much more tightly in coils of ∼2 mm diameter (H). Hydration of these same valves in water results in even tighter curling in coils of ∼1 mm diameter (I), while after plasmolysis in 4M salt solution the coils open to ∼5-6 mm diameter (J). Thus, the tight coiling of valves in explosive fruits (H) is an active process requiring living cells that can sustain internal pressure. In contrast to this, the slight residual curvature in dead, hydrated valves (F and G) is passive and could be explained by gradients of cell wall composition within the valve (Hayashi et al., 2010, Vaughn et al., 2011).(K and L) Both inner and outer layers of the valve and turgor pressure are required for curvature. In pure water (K), a valve segment comprising all layers (left) curves, while a segment of excised outer layers (right) remains flat. Please note that these data are presented in Figure 1 of the main text but are also shown here for clarity. In 8 osmoles of salt solution (L), curvature of the same intact valve segment (left) is very reduced, while the same segment of excised outer layers (right) curves slightly in the opposite direction, indicating that the outermost exocarp layer increases in length following plasmolysis.(M) Endocarp layers alone do not curve in water, as shown by separating the outer layers of a valve segment from the endocarp a and b layers (white arrow). The valve segment comprising all layers curves, while each of the separated layers remain flat. Therefore, a bilayer composed of the inner and outer valve layers is necessary and sufficient for curvature, rather than a bilayer composed of the endocarp a and b layers as previously proposed (Hayashi et al., 2010). Scale bars: 1 mm (A-D, K-M), 2 mm (E-J).

Mentions: To quantify explosive seed dispersal in C. hirsuta at the plant and organ level, we recorded the shatter of fruit pods using high-speed videography, extrapolated the trajectories of launched seeds, and measured the distribution of seeds dispersed around parent plants. During explosive pod shatter the two valves curl back from the fruit pod, initially peeling the seeds off the inner septum and launching them at speeds in excess of 10 ms−1 (Figures 1A–1C; Movie S1). This process is rapid, taking less than 3 ms, and fires the small seeds upon ballistic trajectories to land within a 2-m radius of the parent plant (Figures 1D and 1E). The exploded valves come to rest in a curled configuration of three or four coils (Figure 1C). We identified key properties of the valve associated with explosive pod shatter by comparing the valves of non-explosive A. thaliana and explosive C. hirsuta fruit. Two striking features differentiated these fruit. First, C. hirsuta valves contain more lignin, localized asymmetrically to cell walls on the inner side of the endocarp b layer (Figures 1F and 1G) (Vaughn et al., 2011). Lignin is a complex phenylpropanoid polymer that adds stiffness to secondary cell walls, suggesting that this inner valve layer is considerably stiffer in the explosive fruit of C. hirsuta. Second, shallow incisions to the outside of the turgid valve caused wounds that gaped instantly in C. hirsuta but not in A. thaliana (Figures S1A–S1D). This observation implies that, in C. hirsuta, the outer tissue layer is under tension while the valve is flat, prior to explosion.


Morphomechanical Innovation Drives Explosive Seed Dispersal
Mechanical and Osmotic Experiments in C. hirsuta and A. thaliana Fruits, Related to Figure 1(A and B) Incision of the C. hirsuta valve shows mechanical tension in situ. Mature fruit before (A) and after a shallow cut is made in the valve outer layers (B). The cut layers immediately gape in the long direction of the fruit, revealing the white, lignified endocarp b cell walls underneath (arrowhead), indicating that the valve was in a state of tension while attached to the fruit.(C and D) The same experiment in A. thaliana shows no tension. Ink was applied to the intact valve (C) to aid visibility of the incision (D, arrowhead), which did not gape.(E–J) Turgor pressure in living cells is required for full valve curvature. Valves of alcohol-dried fruits fall off without explosion and are almost flat (E). Re-hydration in water produces little curvature in alcohol-treated valves (F) or in valves killed by freezing (G), as observed previously upon re-hydration of oven-dried C. parviflora fruits (Hayashi et al., 2010). Valves of living, freshly exploded fruits are curled much more tightly in coils of ∼2 mm diameter (H). Hydration of these same valves in water results in even tighter curling in coils of ∼1 mm diameter (I), while after plasmolysis in 4M salt solution the coils open to ∼5-6 mm diameter (J). Thus, the tight coiling of valves in explosive fruits (H) is an active process requiring living cells that can sustain internal pressure. In contrast to this, the slight residual curvature in dead, hydrated valves (F and G) is passive and could be explained by gradients of cell wall composition within the valve (Hayashi et al., 2010, Vaughn et al., 2011).(K and L) Both inner and outer layers of the valve and turgor pressure are required for curvature. In pure water (K), a valve segment comprising all layers (left) curves, while a segment of excised outer layers (right) remains flat. Please note that these data are presented in Figure 1 of the main text but are also shown here for clarity. In 8 osmoles of salt solution (L), curvature of the same intact valve segment (left) is very reduced, while the same segment of excised outer layers (right) curves slightly in the opposite direction, indicating that the outermost exocarp layer increases in length following plasmolysis.(M) Endocarp layers alone do not curve in water, as shown by separating the outer layers of a valve segment from the endocarp a and b layers (white arrow). The valve segment comprising all layers curves, while each of the separated layers remain flat. Therefore, a bilayer composed of the inner and outer valve layers is necessary and sufficient for curvature, rather than a bilayer composed of the endocarp a and b layers as previously proposed (Hayashi et al., 2010). Scale bars: 1 mm (A-D, K-M), 2 mm (E-J).
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Related In: Results  -  Collection

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figs1: Mechanical and Osmotic Experiments in C. hirsuta and A. thaliana Fruits, Related to Figure 1(A and B) Incision of the C. hirsuta valve shows mechanical tension in situ. Mature fruit before (A) and after a shallow cut is made in the valve outer layers (B). The cut layers immediately gape in the long direction of the fruit, revealing the white, lignified endocarp b cell walls underneath (arrowhead), indicating that the valve was in a state of tension while attached to the fruit.(C and D) The same experiment in A. thaliana shows no tension. Ink was applied to the intact valve (C) to aid visibility of the incision (D, arrowhead), which did not gape.(E–J) Turgor pressure in living cells is required for full valve curvature. Valves of alcohol-dried fruits fall off without explosion and are almost flat (E). Re-hydration in water produces little curvature in alcohol-treated valves (F) or in valves killed by freezing (G), as observed previously upon re-hydration of oven-dried C. parviflora fruits (Hayashi et al., 2010). Valves of living, freshly exploded fruits are curled much more tightly in coils of ∼2 mm diameter (H). Hydration of these same valves in water results in even tighter curling in coils of ∼1 mm diameter (I), while after plasmolysis in 4M salt solution the coils open to ∼5-6 mm diameter (J). Thus, the tight coiling of valves in explosive fruits (H) is an active process requiring living cells that can sustain internal pressure. In contrast to this, the slight residual curvature in dead, hydrated valves (F and G) is passive and could be explained by gradients of cell wall composition within the valve (Hayashi et al., 2010, Vaughn et al., 2011).(K and L) Both inner and outer layers of the valve and turgor pressure are required for curvature. In pure water (K), a valve segment comprising all layers (left) curves, while a segment of excised outer layers (right) remains flat. Please note that these data are presented in Figure 1 of the main text but are also shown here for clarity. In 8 osmoles of salt solution (L), curvature of the same intact valve segment (left) is very reduced, while the same segment of excised outer layers (right) curves slightly in the opposite direction, indicating that the outermost exocarp layer increases in length following plasmolysis.(M) Endocarp layers alone do not curve in water, as shown by separating the outer layers of a valve segment from the endocarp a and b layers (white arrow). The valve segment comprising all layers curves, while each of the separated layers remain flat. Therefore, a bilayer composed of the inner and outer valve layers is necessary and sufficient for curvature, rather than a bilayer composed of the endocarp a and b layers as previously proposed (Hayashi et al., 2010). Scale bars: 1 mm (A-D, K-M), 2 mm (E-J).
Mentions: To quantify explosive seed dispersal in C. hirsuta at the plant and organ level, we recorded the shatter of fruit pods using high-speed videography, extrapolated the trajectories of launched seeds, and measured the distribution of seeds dispersed around parent plants. During explosive pod shatter the two valves curl back from the fruit pod, initially peeling the seeds off the inner septum and launching them at speeds in excess of 10 ms−1 (Figures 1A–1C; Movie S1). This process is rapid, taking less than 3 ms, and fires the small seeds upon ballistic trajectories to land within a 2-m radius of the parent plant (Figures 1D and 1E). The exploded valves come to rest in a curled configuration of three or four coils (Figure 1C). We identified key properties of the valve associated with explosive pod shatter by comparing the valves of non-explosive A. thaliana and explosive C. hirsuta fruit. Two striking features differentiated these fruit. First, C. hirsuta valves contain more lignin, localized asymmetrically to cell walls on the inner side of the endocarp b layer (Figures 1F and 1G) (Vaughn et al., 2011). Lignin is a complex phenylpropanoid polymer that adds stiffness to secondary cell walls, suggesting that this inner valve layer is considerably stiffer in the explosive fruit of C. hirsuta. Second, shallow incisions to the outside of the turgid valve caused wounds that gaped instantly in C. hirsuta but not in A. thaliana (Figures S1A–S1D). This observation implies that, in C. hirsuta, the outer tissue layer is under tension while the valve is flat, prior to explosion.

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