The BCPH Unit of Molecular Physiology, Department of Chemistry, Biology and Marine Science, University of the Ryukyus, Okinawa, 903-0213, Japan.
BMC Dev Biol. 2020 Mar 31;20(1):6. doi: 10.1186/s12861-020-00211-7.
Eyespot color pattern formation on butterfly wings is sensitive to physical damage and physical distortion as well as physical contact with materials on the surface of wing epithelial tissue at the pupal stage. Contact-mediated eyespot color pattern changes may imply a developmental role of the extracellular matrix in morphogenic signal propagation. Here, we examined eyespot responses to various contact materials, focusing on the hindwing posterior eyespots of the blue pansy butterfly, Junonia orithya.
Contact with various materials, including both nonbiological and biological materials, induced eyespot enlargement, reduction, or no change in eyespot size, and each material was characterized by a unique response profile. For example, silicone glassine paper almost always induced a considerable reduction, while glass plates most frequently induced enlargement, and plastic plates generally produced no change. The biological materials tested here (fibronectin, polylysine, collagen type I, and gelatin) resulted in various responses, but polylysine induced more cases of enlargement, similar to glass plates. The response profile of the materials was not readily predictable from the chemical composition of the materials but was significantly correlated with the water contact angle (water repellency) of the material surface, suggesting that the surface physical chemistry of materials is a determinant of eyespot size. When the proximal side of a prospective eyespot was covered with a size-reducing material (silicone glassine paper) and the distal side and the organizer were covered with a material that rarely induced size reduction (plastic film), the proximal side of the eyespot was reduced in size in comparison with the distal side, suggesting that signal propagation but not organizer activity was inhibited by silicone glassine paper.
These results suggest that physical contact with an appropriate hydrophobic surface is required for morphogenic signals from organizers to propagate normally. The binding of the apical surface of the epithelium with an opposing surface may provide mechanical support for signal propagation. In addition to conventional molecular morphogens, there is a possibility that mechanical distortion of the epithelium that is propagated mechanically serves as a nonmolecular morphogen to induce subsequent molecular changes, in accordance with the distortion hypothesis for butterfly wing color pattern formation.
蝴蝶翅膀上的眼斑颜色图案的形成对物理损伤和物理变形敏感,以及对蛹期翅膀上皮组织表面材料的物理接触敏感。接触介导的眼斑颜色图案变化可能意味着细胞外基质在形态发生信号传播中具有发育作用。在这里,我们研究了各种接触材料对眼斑的反应,重点是蓝菫蝴蝶 Junonia orithya 的后翅后眼斑。
与各种材料接触,包括非生物材料和生物材料,都会引起眼斑扩大、缩小或大小不变,每种材料都有独特的反应特征。例如,硅酮玻璃纸几乎总是导致相当大的缩小,而玻璃板最常引起扩大,而塑料板通常没有变化。这里测试的生物材料(纤连蛋白、多聚赖氨酸、I 型胶原和明胶)导致了各种反应,但多聚赖氨酸诱导了更多的扩大,类似于玻璃板。材料的反应特征不易从材料的化学成分预测,但与材料表面的水接触角(疏水性)显著相关,表明材料表面的物理化学性质是眼斑大小的决定因素。当一个潜在的眼斑的近端被一种缩小尺寸的材料(硅酮玻璃纸)覆盖,而远端和组织者被一种很少引起尺寸缩小的材料(塑料薄膜)覆盖时,与远端相比,眼斑的近端尺寸缩小,这表明信号传播而不是组织者活动被硅酮玻璃纸抑制。
这些结果表明,组织者的形态发生信号正常传播需要与适当的疏水性表面进行物理接触。上皮细胞的顶端表面与对面表面的结合可能为信号传播提供机械支撑。除了传统的分子形态发生素之外,还有一种可能性是,机械传播的上皮细胞的机械扭曲可以作为一种非分子形态发生素,引发随后的分子变化,这与蝴蝶翅膀颜色图案形成的扭曲假说一致。