{"title":"Carnivorous Nepenthes pitcher plants combine common developmental processes to make a complex epidermal trapping surface.","authors":"Oona C Lessware, Judith M Mantell, Ulrike Bauer","doi":"10.1093/aob/mcae147","DOIUrl":null,"url":null,"abstract":"<p><strong>Background and aims: </strong>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.</p><p><strong>Methods: </strong>We used cryo-scanning electron microscopy to investigate the detailed morphogenesis and epidermal patterning of the Nepenthes x hookeriana pitcher rim. In addition, we collected morphometric and qualitative data from developing pitcher traps including those sampled for microscopy.</p><p><strong>Key results: </strong>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.</p><p><strong>Conclusions: </strong>We demonstrate that the complex surface microtopography 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.</p>","PeriodicalId":8023,"journal":{"name":"Annals of botany","volume":" ","pages":""},"PeriodicalIF":3.6000,"publicationDate":"2024-09-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Annals of botany","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/aob/mcae147","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Background and aims: 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.
Methods: We used cryo-scanning electron microscopy to investigate the detailed morphogenesis and epidermal patterning of the Nepenthes x hookeriana pitcher rim. In addition, we collected morphometric and qualitative data from developing pitcher traps including those sampled for microscopy.
Key results: 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.
Conclusions: We demonstrate that the complex surface microtopography 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.
背景和目的:由脊和阶梯组成的分层微地形使食肉莲属投手植物的诱捕器边缘异常湿润,潮湿时对昆虫来说很滑。这种复杂的三维表皮结构隐藏在仍处于闭合状态的发育中的投手芽内。在这里,我们揭示了形成陷阱边缘的表皮模式化事件序列。通过将这一序列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瞄准表面发育的各个阶段:方法:我们利用低温扫描电子显微镜研究了尼泊尔麝香草(Nepenthes x hookeriana)捕虫圈的详细形态发生和表皮图案。此外,我们还收集了发育中的蝮蛇诱捕器(包括显微镜取样的诱捕器)的形态计量和定性数据:我们发现了三个连续的模式化事件。首先,严格定向的细胞分裂产生了径向排列的细胞行,并形成了宏观的脊沟图案。接着,锥形乳头状细胞形成,乳头向捕获器内部伸长,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,扁平的乳头形成尖角弧形台阶。最后,细胞径向拉长,从而形成凸领状的边缘。这种表面发育的一般顺序还显示出从外侧到内侧陷阱边缘的空间进展,在任何给定时间内都会同时出现几个连续的发育阶段:结论:我们的研究表明,尼泊金吸虫诱捕器边缘复杂的表面微形貌是通过以一种新的方式将广泛存在且在进化过程中得到保护的表皮模式化过程按顺序结合起来而形成的。这使得景天科捕虫栅成为研究叶片表皮图案机制的绝佳模型。
期刊介绍:
Annals of Botany is an international plant science journal publishing novel and rigorous research in all areas of plant science. It is published monthly in both electronic and printed forms with at least two extra issues each year that focus on a particular theme in plant biology. The Journal is managed by the Annals of Botany Company, a not-for-profit educational charity established to promote plant science worldwide.
The Journal publishes original research papers, invited and submitted review articles, ''Research in Context'' expanding on original work, ''Botanical Briefings'' as short overviews of important topics, and ''Viewpoints'' giving opinions. All papers in each issue are summarized briefly in Content Snapshots , there are topical news items in the Plant Cuttings section and Book Reviews . A rigorous review process ensures that readers are exposed to genuine and novel advances across a wide spectrum of botanical knowledge. All papers aim to advance knowledge and make a difference to our understanding of plant science.