Lessware Oona C, Mantell Judith M, Bauer Ulrike
School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK.
Wolfson Bioimaging Centre, School of Biomedical Sciences, University of Bristol, University Walk, Bristol BS8 1TD, UK.
Ann Bot. 2025 Mar 13;135(4):643-654. doi: 10.1093/aob/mcae147.
A hierarchical micro-topography of ridges and steps renders the trap rim of carnivorous Nepenthes pitcher plants unusually wettable, and slippery for insects when wet. This complex three-dimensional epidermis structure forms, hidden from plain sight, inside the still-closed developing pitcher bud. Here, we reveal the sequence of epidermal patterning events that shape the trap rim. By linking this sequence to externally visible markers of bud development, we provide a framework for targeting individual stages of surface development in future studies.
We used cryo-scanning electron microscopy to investigate the detailed morphogenesis and epidermal patterning of the Nepenthes × hookeriana pitcher rim. In addition, we collected morphometric and qualitative data from developing pitcher traps including those sampled for microscopy.
We identified three consecutive patterning events. First, strictly oriented cell divisions resulted in radially aligned rows of cells and established a macroscopic ridge-and-groove pattern. Next, conical papillate cells formed, and papillae elongated towards the trap interior, increasingly overlapping adjacent cells and eventually forming continuous microscopic ridges. In between these ridges, the flattened papillae formed acutely angled arched steps. Finally, the cells elongated radially, thereby establishing the convex collar shape of the rim. This general sequence of surface development also showed a spatial progression from the outer to the inner trap rim edge, with several consecutive developmental stages co-occurring at any given time.
We demonstrate that the complex surface micro-topography of the Nepenthes pitcher rim develops by sequentially combining widespread, evolutionarily conserved epidermal patterning processes in a new way. This makes the Nepenthes trap rim an excellent model for studying epidermal patterning mechanisms in leaves.
食肉植物猪笼草捕虫笼边缘具有分层的微观地形，使其异常湿润，且在湿润时对昆虫来说很滑。这种复杂的三维表皮结构在仍闭合的发育中的捕虫笼芽内部形成，肉眼难以察觉。在这里，我们揭示了塑造捕虫笼边缘的表皮图案形成事件的顺序。通过将这个顺序与芽发育的外部可见标记联系起来，我们提供了一个框架，以便在未来的研究中针对表面发育的各个阶段。
我们使用冷冻扫描电子显微镜来研究猪笼草×胡克猪笼草捕虫笼边缘的详细形态发生和表皮图案形成。此外，我们从发育中的捕虫笼收集了形态测量和定性数据，包括用于显微镜观察的样本。
我们确定了三个连续的图案形成事件。首先，严格定向的细胞分裂导致细胞呈放射状排列成行，并建立了宏观的脊沟模式。接下来，形成了圆锥形乳头状细胞，乳头向捕虫笼内部伸长，越来越多地与相邻细胞重叠，最终形成连续的微观脊。在这些脊之间，扁平的乳头形成了锐角拱形台阶。最后，细胞径向伸长，从而形成了边缘的凸领形状。这种表面发育的一般顺序也显示出从捕虫笼边缘外部到内部的空间进展，在任何给定时间都有几个连续的发育阶段同时发生。
我们证明，猪笼草捕虫笼边缘复杂的表面微观地形是通过以一种新的方式依次组合广泛的、进化上保守的表皮图案形成过程而发育的。这使得猪笼草捕虫笼边缘成为研究叶片表皮图案形成机制的一个优秀模型。
