Carnivorous Nepenthes pitcher plants combine common developmental processes to make a complex epidermal trapping surface.
Autor: | Lessware OC; School of Biological Sciences, University of Bristol, 24 Tyndall Avenue, BS8 1TQ, Bristol, UK., Mantell JM; Wolfson Bioimaging Centre, School of Biomedical Sciences, University of Bristol, University Walk, BS8 1TD, Bristol, UK., Bauer U; Department of Biosciences, University of Exeter, Geoffrey Pope Building, Stocker Road, EX4 4QD, Exeter, UK. |
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Jazyk: | angličtina |
Zdroj: | Annals of botany [Ann Bot] 2024 Sep 06. Date of Electronic Publication: 2024 Sep 06. |
DOI: | 10.1093/aob/mcae147 |
Abstrakt: | 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. (© The Author(s) 2024. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.) |
Databáze: | MEDLINE |
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