Growth and tension in explosive fruit

Abstract

Exploding seed pods of the common weed Cardamine hirsuta have the remarkable ability to launch seeds far from the plant. The energy for this explosion comes from tension that builds up in the fruit valves. Above a critical threshold, the fruit fractures along its dehiscence zone and the two valves coil explosively, ejecting the seeds. Tension is commonly generated as seed pods dry, causing fruit tissues to deform. However, this does not happen in C. hirsuta. Instead, tension is produced by active contraction of growing exocarp cells in the outer layer of the fruit valves. Exactly how growth leads to contraction in these cells is unknown. Here we show that microtubule dynamics in the exocarp cell cortex control the specific orientation of cellulose microfibrils in the cell wall, and the consequent cellular growth pattern, which together drive contraction. We used mechanical modeling and simulations to show how tension emerges through the general process of plant cell growth, due to the highly anisotropic orientation of load-bearing cellulose microfibrils and their effect on cell shape. By explicitly defining the cell wall as multi-layered in our model, we discovered that a cross-lamellate pattern of cellulose microfibrils further enhances the developing tension in growing cells. Therefore, the interplay of cell wall properties with turgor-driven growth enables the fruit exocarp layer to develop sufficient tension to explode.