Biomechanical proposal as a cause of incomplete seed and pericarp development of the sunflower (Helianthus annuus L.) fruits

Abstract

Absence or underdevelopment of sunflower fruits come usually from failure in fertilization, stresses as well as physiological and morphological defects in the ovary. Thigmomorphogenesis has never been included as a possible cause. We have previously shown that a 2-3 day fertilization shift can occur between neighboring florets in the sunflower capitulum. It is proposed here that those ovaries with advanced fertilization can generate a significant radial and axial compressive stress on ovaries with delayed fertilization. This mechanical stimulus could be strong enough to trigger a thigmo response that affects further ovary development. In vivo tests were performed, isolating ovaries by removing the adjacent flowers and rubbing them several times using a micromanipulator applying a force of 1 to 3 N. Total peroxidases in treated and untreated ovaries, isolated and not isolated were measured 24 h after treatments. Ovary development was studied in control and isolated flowers, both rubbed and not rubbed. Also a mechanical a model was made to simulate the mechanical behavior of an ovary surrounded by advanced growing neighboring ovaries. A meshed 3-D model of a young ovary was constructed and a computer simulation was performed using finite element analysis. Shear stresses generated by the friction of neighboring ovaries in contact with the model, fertilized three days later, were then estimated. After rubbing, isolated ovaries in planta showed a thigmo response that resulted in empty or incompletely developed fruits. Total peroxidase levels (ΔAbs470 min-1.g fresh weight-1) rose from 22 in control ovaries to 72 in rubbed ones. The number of ovaries that did not develop any seed from these incompletely developed fruits rose from 16.2 to 20.0% in the control non-isolated flowers to 61.1 to 86.7% in the rubbed ovaries, but dropped to 6.7 to 7.3% in the non-rubbed but isolated ovaries. From the simulation it was found that the area of contact with the receptacle was prone to show a higher magnitude of stress after deformation induced by shear forces generated by neighboring ovaries. Thigmomorphogenesis can also explain the failures observed at early stages of the sunflower ovary development. The ovary tissue sensitivity at this stage could contribute to the rapid response of the mechanically generated stimulus between neighbouring ovaries.