Cyto-architecture of Byblis Glands and Leaf Cells Based on Freeze-substitution and Conventional TEM

Overview

Journal Ann Bot

Publisher Oxford University Press

Specialty Biology

Date 2024 Sep 27

PMID 39331380

Authors

Bartosz J Plachno

Sue Lancelle

Piotr Swiatek

Peter K Hepler

Marieluise Weidinger

Irene Lichtscheidl

Affiliations

Soon will be listed here.

Abstract

Background And Aims: Byblis liniflora (Byblidaceae) is a carnivorous plant that has developed sticky flypaper traps with two types of glandular trichomes producing digestive enzymes and sticky mucilage. This study aimed to analyse the ultrastructure of these glandular leaf trichomes based on rapid freeze-fixation and conventional chemical fixation in the attempt to understand their functional contribution to the carnivorous performance of the plants.

Methods: The Byblis cells were studied in transmission electron microscopy, scanning electron microscopy and scanning transmission electron microscopy using cryo-techniques for fixation and substitution in addition to conventional chemical fixation.

Key Results: We show in detail the architecture of both the digestive glands and the mucilage glands with their relevant sets of organelles. Both mitochondria and plastids have a conspicuous plasticity, with branches and constrictions, and they associate to form clusters. The glandular cells appear to be transfer cells with cell wall ingrowths. Digestive glands occur in different states of development. Their cuticle forms discontinuities that are unique among glands of carnivorous plants. They look like cuticular holes - the cuticle separates from the cell wall in only one spot and then ruptures. Cuticular discontinuities thus differ from the cuticular gaps and cuticular pores so far described in carnivorous plants. We therefore propose for them the term 'cuticular holes'.

Conclusions: Application of cryo-techniques made it possible to show the true structure of the cell wall and the relationship between cell wall ingrowths and organelles, as well as the morphology and structure of organelles and their associations.

Citing Articles

Direct Nuclear Delivery of Proteins on Living Plant via Partial Enzymatic Cell Wall Digestion.

Gu Q, Ming N, Aizezi Y, Wei X, Yuan Y, Esquivel B Curr Issues Mol Biol. 2024; 46(12):14487-14496.

PMID: 39727998 PMC: 11674260. DOI: 10.3390/cimb46120870.

References

Ojeda F, Carrera C, Paniw M, Garcia-Moreno L, Barbero G, Palma M . Volatile and Semi-Volatile Organic Compounds May Help Reduce Pollinator-Prey Overlap in the Carnivorous Plant Drosophyllum lusitanicum (Drosophyllaceae). J Chem Ecol. 2021; 47(1):73-86. DOI: 10.1007/s10886-020-01235-w. View

Karahara I, Kang B . High-pressure freezing and low-temperature processing of plant tissue samples for electron microscopy. Methods Mol Biol. 2013; 1080:147-57. DOI: 10.1007/978-1-62703-643-6_12. View

Fisher D . Structure of functional soybean sieve elements. Plant Physiol. 1975; 56(5):555-69. PMC: 541872. DOI: 10.1104/pp.56.5.555. View

Boulogne C, Gillet C, Hughes L, LE Bars R, Canette A, Hawes C . Functional organisation of the endomembrane network in the digestive gland of the Venus flytrap: revisiting an old story with a new microscopy toolbox. J Microsc. 2020; 280(2):86-103. DOI: 10.1111/jmi.12957. View

Volgger M, Lang I, Ovecka M, Lichtscheidl I . Plasmolysis and cell wall deposition in wheat root hairs under osmotic stress. Protoplasma. 2009; 243(1-4):51-62. DOI: 10.1007/s00709-009-0055-6. View

Kuo J . Processing plant tissues for ultrastructural study. Methods Mol Biol. 2007; 369:35-45. DOI: 10.1007/978-1-59745-294-6_3. View

Plachno B, Kurczynska E, Swiatek P . Integument cell differentiation in dandelions (Taraxacum, Asteraceae, Lactuceae) with special attention paid to plasmodesmata. Protoplasma. 2015; 253(5):1365-72. PMC: 5009155. DOI: 10.1007/s00709-015-0894-2. View

Heslop-Harrison Y . Enzyme release in carnivorous plants. Front Biol. 1975; 43(4):525-78. View

Foissner I . Microfilaments and microtubules control the shape, motility, and subcellular distribution of cortical mitochondria in characean internodal cells. Protoplasma. 2004; 224(3-4):145-57. DOI: 10.1007/s00709-004-0075-1. View

10.

Li Y, Chen A, Leu W . Sessile Trichomes Play Major Roles in Prey Digestion and Absorption, While Stalked Trichomes Function in Prey Predation in . Int J Mol Sci. 2023; 24(6). PMC: 10048915. DOI: 10.3390/ijms24065305. View

11.

Heslop-Harrison Y, Knox R . A cytochemical study of the leaf-gland enzymes of insectivorous plants of the genus Pinguicula. Planta. 2014; 96(3):183-211. DOI: 10.1007/BF00387439. View

12.

Paiva E . How do secretory products cross the plant cell wall to be released? A new hypothesis involving cyclic mechanical actions of the protoplast. Ann Bot. 2016; 117(4):533-40. PMC: 4817504. DOI: 10.1093/aob/mcw012. View

13.

Kreuzwieser J, Scheerer U, Kruse J, Burzlaff T, Honsel A, Alfarraj S . The Venus flytrap attracts insects by the release of volatile organic compounds. J Exp Bot. 2014; 65(2):755-66. PMC: 3904726. DOI: 10.1093/jxb/ert455. View

14.

Huebinger J, Han H, Grabenbauer M . Reversible Cryopreservation of Living Cells Using an Electron Microscopy Cryo-Fixation Method. PLoS One. 2016; 11(10):e0164270. PMC: 5053471. DOI: 10.1371/journal.pone.0164270. View

15.

Poppinga S, Knorr N, Ruppert S, Speck T . Chemonastic Stalked Glands in the Carnivorous Rainbow Plant LINDL. (Byblidaceae, Lamiales). Int J Mol Sci. 2022; 23(19). PMC: 9569831. DOI: 10.3390/ijms231911514. View

16.

Kiss J, Giddings Jr T, Staehelin L, Sack F . Comparison of the ultrastructure of conventionally fixed and high pressure frozen/freeze substituted root tips of Nicotiana and Arabidopsis. Protoplasma. 1990; 157:64-74. DOI: 10.1007/BF01322639. View

17.

Anderson B . Adaptations to foliar absorption of faeces: a pathway in plant carnivory. Ann Bot. 2005; 95(5):757-61. PMC: 4246731. DOI: 10.1093/aob/mci082. View

18.

Plachno B, Swiatek P, Miranda V, Stolarczyk P . The Structure and Occurrence of a Velum in Traps (). Front Plant Sci. 2019; 10:302. PMC: 6454230. DOI: 10.3389/fpls.2019.00302. View

19.

Galloway A, Knox P, Krause K . Sticky mucilages and exudates of plants: putative microenvironmental design elements with biotechnological value. New Phytol. 2019; 225(4):1461-1469. DOI: 10.1111/nph.16144. View

20.

Studer D, Graber W, Al-Amoudi A, Eggli P . A new approach for cryofixation by high-pressure freezing. J Microsc. 2001; 203(Pt 3):285-94. DOI: 10.1046/j.1365-2818.2001.00919.x. View