Cell Wall Microdomains in the External Glands of Utricularia dichotoma Traps
Abstract
:1. Introduction
2. Results
2.1. Gland General Structure
2.2. The Arabinogalactan Protein (AGPs) Distribution
3. Discussion
3.1. Secondary Cell Wall
3.2. Transfer Cells
4. Materials and Methods
4.1. Plant Material
4.2. Histological and Immunochemical Analysis
4.3. Immunogold Labeling Distribution of AGP
4.4. Scanning Transmission Electron Microscopy
4.5. Scanning Electron Microscopy
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
References
- Müller, K.; Borsch, T.; Legendre, L.; Porembski, S.; Theisen, I.; Barthlott, W. Evolution of carnivory in Lentibulariaceae and the Lamiales. Plant Biol. 2004, 6, 477–490. [Google Scholar] [CrossRef] [PubMed]
- Müller, K.F.; Borsch, T.; Legendre, L.; Porembski, S.; Barthlott, W. Recent progress in understanding the evolution of carnivorous Lentibulariaceae (Lamiales). Plant Biol. 2006, 8, 748–757. [Google Scholar] [CrossRef] [PubMed]
- Fonseca, L.H.M. Combining molecular and geographical data to infer the phylogeny of Lamiales and its dispersal patterns in and out of the tropics. Mol. Phylogenetics Evol. 2021, 164, 107287. [Google Scholar] [CrossRef] [PubMed]
- Lloyd, F.E. The Carnivorous Plants; Chronica Botanica Company: Waltham, MA, USA, 1942. [Google Scholar]
- Heslop-Harrison, Y. Scanning electron microscopy of fresh leaves of Pinguicula. Science 1970, 167, 172–174. [Google Scholar] [CrossRef] [PubMed]
- Heslop-Harrison, Y.; Knox, R.B. A cytochemical study of the leaf-gland enzymes of insectivorous plants of the genus Pinguicula. Planta 1971, 96, 183–211. [Google Scholar] [CrossRef] [PubMed]
- Karlsson, P.S.; Nordell, K.O.; Eirefelt, S.; Svensson, A. Trapping Efficiency of Three Carnivorous Pinguicula Species. Oecologia 1987, 73, 518–521. [Google Scholar] [CrossRef] [PubMed]
- Reut, M.S. Trap structure of the carnivorous plant Genlisea (Lentibulariaceae). Bot. Helv. 1993, 103, 101–111. [Google Scholar]
- Płachno, B.J.; Kozieradzka-Kiszkurno, M.; Świątek, P. Functional Ultrastructure of Genlisea (Lentibulariaceae) Digestive Hairs. Ann. Bot. 2007, 100, 195–203. [Google Scholar] [CrossRef]
- Barthlott, W.; Porembski, S.; Fischer, E.; Gemmel, B. First protozoa-trapping plant found. Nature 1998, 392, 447. [Google Scholar] [CrossRef]
- Płachno, B.J.; Adamus, K.; Faber, J.; Kozłowski, J. Feeding behaviour of carnivorous Genlisea plants in the laboratory. Acta Bot. Gall. 2005, 152, 159–164. [Google Scholar] [CrossRef]
- Juniper, B.E.; Robins, R.J.; Joel, D.M. The Carnivorous Plants; Academic Press Ltd.: London, UK, 1989; pp. 1–353. [Google Scholar]
- Meyers-Rice, B. Are Genlisea traps active? A crude calculation. Carniv. Plant Newsl. 1994, 23, 40–42. [Google Scholar] [CrossRef]
- Adamec, L. Zero water flows in the carnivorous genus Genlisea. Carniv. Plant Newsl. 2002, 32, 46–48. [Google Scholar] [CrossRef]
- Studnička, M. Further problem in Genlisea trap untangled. Carniv. Plant Newsl. 2003, 32, 40–45. [Google Scholar] [CrossRef]
- Fleischmann, A. Monograph of the Genus Genlisea; Redfern Natural History Productions: Poole, UK, 2012. [Google Scholar]
- Płachno, B.J.; Kozieradzka-Kiszkurno, M.; Świątek, P.; Darnowski, D.W. Prey attraction in carnivorous Genlisea (Lentibulariaceae). Acta Biol. Cracoviensia Ser. Bot. 2008, 50, 87–94. [Google Scholar]
- Carmesin, C.F.; Fleischmann, A.S.; Klepsch, M.M.; Westermeier, A.S.; Speck, T.; Jansen, S.; Poppinga, S. Structural gradients and anisotropic hydraulic conductivity in the enigmatic eel traps of carnivorous corkscrew plants (Genlisea spp.). Am. J. Bot. 2021, 108, 2356–2370. [Google Scholar] [CrossRef] [PubMed]
- Rutishauser, R. Evolution of unusual morphologies in Lentibulariaceae (bladderworts and allies) and Podostemaceae (river-weeds): A pictorial report at the interface of developmental biology and morphological diversification. Ann. Bot. 2016, 117, 811–832. [Google Scholar] [CrossRef] [PubMed]
- Reut, M.S.; Płachno, B.J. Development, Diversity and Dynamics of Plant Architecture in Utricularia subgenus Polypompholyx—Towards Understanding Evolutionary Processes in the Lentibulariaceae. Bot. Rev. 2023, 89, 201–236. [Google Scholar] [CrossRef]
- Sydenham, P.H.; Findlay, G.P. The rapid movement of the bladder of Utricularia sp. Aust. J. Biol. Sci. 1973, 26, 1115–1126. [Google Scholar] [CrossRef]
- Vincent, O.; Weißkopf, C.; Poppinga, S.; Masselter, T.; Speck, T.; Joyeux, M.; Quilliet, C.; Marmottant, P. Ultra-fast underwater suction traps. Proc. R. Soc. B Biol. Sci. 2011, 278, 2909–2914. [Google Scholar] [CrossRef]
- Vincent, O.; Marmottant, P. Carnivorous Utricularia: The buckling scenario. Plant Signal. Behav. 2011, 6, 1752–1754. [Google Scholar] [CrossRef]
- Poppinga, S.; Daber, L.E.; Westermeier, A.S.; Kruppert, S.; Horstmann, M.; Tollrian, R.; Speck, T. Biomechanical analysis of prey capture in the carnivorous Southern bladderwort (Utricularia australis). Sci. Rep. 2017, 7, 1776. [Google Scholar] [CrossRef] [PubMed]
- Adamec, L. The smallest but fastest: Ecophysiological characteristics of traps of aquatic carnivorous Utricularia. Plant Signal. Behav. 2011, 6, 640–646. [Google Scholar] [CrossRef] [PubMed]
- Taylor, P. The genus Utricularia: A taxonomic monograph. Kew Bull. 1989, 4, 1–724. [Google Scholar]
- Harms, S. Prey selection in three species of the carnivorous aquatic plant Utricularia (bladderwort). Arch. Hydrobiol. 1999, 146, 449–470. [Google Scholar] [CrossRef]
- Jobson, R.W.; Morris, E.C. Feeding ecology of a carnivorous bladderwort (Utricularia uliginosa, Lentibulariaceae). Austral Ecol. 2001, 26, 680–691. [Google Scholar] [CrossRef]
- Gordon, E.; Pacheco, S. Prey composition in the carnivorous plants Utricularia inflata and U. gibba (Lentibulariaceae) from Paria Peninsula, Venezuela. Rev. Biol. Trop. 2007, 55, 795–803. [Google Scholar] [CrossRef] [PubMed]
- Peroutka, M.; Adlassnig, W.; Volgger, M.; Lendl, T.; Url, W.G.; Lichtscheidl, I.K. Utricularia: A vegetarian carnivorous plant? Plant Ecol. 2008, 199, 153–162. [Google Scholar] [CrossRef]
- Alkhalaf, I.A.; Hübener, T.; Porembski, S. Prey spectra of aquatic Utricularia species (Lentibulariaceae) in northeastern Germany: The role of planktonic algae. Flora Morphol. Distrib. Funct. Ecol. 2009, 204, 700–708. [Google Scholar] [CrossRef]
- Sasago, A.; Sibaoka, T. Water extrusion in the trap bladders of Utricularia vulgaris I. A possible pathway of water across the bladder wall. Bot. Mag. 1985, 98, 55–66. [Google Scholar] [CrossRef]
- Friday, L.E. Rapid turnover of traps in Utricularia vulgaris L. Oecologia 1989, 80, 272–277. [Google Scholar] [CrossRef]
- Adamec, L.; Poppinga, S. Measurement of the critical negative pressure inside traps of aquatic carnivorous Utricularia species. Aquat. Bot. 2016, 133, 10–16. [Google Scholar] [CrossRef]
- Płachno, B.J.; Świątek, P.; Miranda, V.F.O.; Stolarczyk, P. The Structure and Occurrence of a Velum in Utricularia Traps (Lentibulariaceae). Front. Plant Sci. 2019, 10, 302. [Google Scholar] [CrossRef] [PubMed]
- Płachno, B.J.; Adamec, L.; Kamińska, I. Relationship between trap anatomy and function in Australian carnivorous bladderworts (Utricularia) of the subgenus Polypompholyx. Aquat. Bot. 2015, 120, 290–296. [Google Scholar] [CrossRef]
- Vincent, O.; Roditchev, I.; Marmottant, P. Spontaneous firings of carnivorous aquatic Utricularia traps: Temporal patterns and mechanical oscillations. PLoS ONE 2011, 6, e20205. [Google Scholar] [CrossRef] [PubMed]
- Adamec, L. The comparison of mechanically stimulated and spontaneous firings in traps of aquatic carnivorous Utricularia species. Aquat. Bot. 2011, 94, 44–49. [Google Scholar] [CrossRef]
- Adamec, L. Firing and resetting characteristics of carnivorous Utricularia reflexa traps: Physiological or only physical regulation of trap triggering? Phyton 2012, 52, 281–290. [Google Scholar]
- Fineran, B.A. Glandular trichomes in Utricularia: A review of their structure and function. Isr. J. Bot. 1985, 34, 295–330. [Google Scholar]
- Kruck, M. Physiologische und zytologische Studien über die Utricularia blase. Arch. Bot. 1931, 33, 257–309. [Google Scholar]
- Nold, R.H. Die Funktion der Blase von Utricularia vulgaris (Ein Beitrag zur Elektrophysiologie der Drüsenfunktion). Beih. Bot. Cent. 1934, 52, 415–448. [Google Scholar]
- Fineran, B.A.; Lee, M.S.L. Organization of mature external glands on the trap and other organs of the bladderwort Utricularia monanthos. Protoplasma 1980, 103, 17–34. [Google Scholar] [CrossRef]
- Pate, J.S.; Gunning, B.E.S. Transfer cells. Annu. Rev. Plant Physiol. 1972, 23, 173–196. [Google Scholar] [CrossRef]
- Offler, C.E.; McCurdy, D.W.; Patrick, J.W.; Talbot, M.J. Transfer cells: Cells specialized for a special purpose. Annu. Rev. Plant Biol. 2003, 54, 431–454. [Google Scholar] [CrossRef] [PubMed]
- Fineran, B.A. Ontogeny of external glands in the bladderwort Utricularia monanthos. Protoplasma 1980, 105, 9–25. [Google Scholar] [CrossRef]
- Płachno, B.J.; Kapusta, M. The Localization of Cell Wall Components in the Quadrifids of Whole-Mount Immunolabeled Utricularia dichotoma Traps. Int. J. Mol. Sci. 2024, 25, 56. [Google Scholar] [CrossRef]
- Vintéjoux, C. Ultrastructural and cytochemical observations on the digestive glands of Utricularia neglecta L. (Lentibulariaceae): Distribution of protease and acid phosphatase activities. Port. Acta Biol. 1974, 14, 463–474. [Google Scholar]
- Płachno, B.J.; Adamec, L.; Lichtscheidl, I.K.; Peroutka, M.; Adlassnig, W.; Vrba, J. Fluorescence labelling of phosphatase activity in digestive glands of carnivorous plants. Plant Biol. 2006, 8, 813–820. [Google Scholar] [CrossRef] [PubMed]
- Meents, M.J.; Watanabe, Y.; Samuels, A.L. The cell biology of secondary cell wall biosynthesis. Ann. Bot. 2018, 121, 1107–1125. [Google Scholar] [CrossRef]
- Li, Z.; Fernie, A.R.; Persson, S. Transition of primary to secondary cell wall synthesis. Sci. Bull. 2016, 61, 838–846. [Google Scholar] [CrossRef]
- Zhong, R.; Ye, Z.H. Secondary Cell Walls: Biosynthesis, Patterned Deposition and Transcriptional Regulation. Plant Cell Physiol. 2015, 56, 195–214. [Google Scholar] [CrossRef]
- Macquet, A.; Ralet, M.-C.; Kronenberger, J.; Marion-Poll, A.; North, H.M. In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant Cell Physiol. 2007, 48, 984–999. [Google Scholar] [CrossRef]
- Young, R.E.; McFarlane, H.E.; Hahn, M.G.; Western, T.L.; Haughn, G.W.; Samuels, A.L. Analysis of the Golgi apparatus in Arabidopsis seed coat cells during polarized secretion of pectin-rich mucilage. Plant Cell 2008, 20, 1623–1638. [Google Scholar] [CrossRef] [PubMed]
- Griffiths, J.S.; Šola, K.; Kushwaha, R.; Lam, P.; Tateno, M.; Young, R.; Voiniciuc, C.; Dean, G.; Mansfield, S.D.; Debolt, S.; et al. Unidirectional movement of cellulose synthase complexes in Arabidopsis seed coat epidermal cells deposit cellulose involved in mucilage extrusion, adherence, and ray formation. Plant Physiol. 2015, 168, 502–520. [Google Scholar] [CrossRef] [PubMed]
- Haughn, G.W.; Western, T.L. Arabidopsis seed coat mucilage is a specialized cell wall that can be used as a model for genetic analysis of plant cell wall structure and function. Front. Plant Sci. 2012, 3, 64. [Google Scholar] [CrossRef] [PubMed]
- Viudes, S.; Dunand, C.; Burlat, V. Myxospermy Evolution in Brassicaceae: A Highly Complex and Diverse Trait with Arabidopsis as an Uncommon Model. Cells 2021, 10, 2470. [Google Scholar] [CrossRef] [PubMed]
- Harris, P.J. Primary and secondary plant cell walls: A comparative overview. N. Z. J. For. Sci. 2006, 36, 36. [Google Scholar]
- Showalter, A.M. Arabinogalactan-proteins: Structure, expression and function. Cell. Mol. Life Sci. 2001, 58, 1399–1417. [Google Scholar] [CrossRef]
- Showalter, A.M.; Keppler, B.; Lichtenberg, J.; Gu, D.; Welch, L.R. A bioinformatics approach to the identification, classification, and analysis of hydroxyproline-rich glycoproteins. Plant Physiol. 2010, 153, 485–513. [Google Scholar] [CrossRef] [PubMed]
- Lamport, D.T.A.; Várnai, P. Periplasmic arabinogalactan glycoproteins act as a calcium capacitor that regulates plant growth and development. New Phytol. 2013, 197, 58–64. [Google Scholar] [CrossRef] [PubMed]
- Rafińska, K.; Niedojadło, K.; Świdziński, M.; Niedojadło, J.; Bednarska-Kozakiewicz, E. Spatial and Temporal Distribution of Arabinogalactan Proteins during Larix decidua Mill. Male Gametophyte and Ovule Interaction. Int. J. Mol. Sci. 2021, 22, 4298. [Google Scholar] [CrossRef]
- Leszczuk, A.; Kalaitzis, P.; Kulik, J.; Zdunek, A. Review: Structure and modifications of arabinogalactan proteins (AGPs). BMC Plant Biol. 2023, 23, 45. [Google Scholar] [CrossRef]
- Lopes, A.L.; Moreira, D.; Pereira, A.M.; Ferraz, R.; Mendes, S.; Pereira, L.G.; Colombo, L.; Coimbra, S. AGPs as molecular determinants of reproductive development. Ann. Bot. 2023, 131, 827–838. [Google Scholar] [CrossRef]
- Ma, Y.; Johnson, K. Arabinogalactan proteins—Multifunctional glycoproteins of the plant cell wall. Cell Surf. 2023, 9, 100102. [Google Scholar] [CrossRef]
- Basu, D.; Wang, W.; Ma, S.; DeBrosse, T.; Poirier, E.; Emch, K.; Soukup, E.; Tian, L.; Showalter, A.M. Two hydroxyproline galactosyltransferases, GALT5 and GALT2, function in arabinogalactan-protein glycosylation, growth and development in Arabidopsis. PLoS ONE 2015, 10, e0125624. [Google Scholar] [CrossRef] [PubMed]
- Kaur, D.; Moreira, D.; Coimbra, S.; Showalter, A.M. Hydroxyproline-O-Galactosyltransferases Synthesizing Type II Arabinogalactans Are Essential for Male Gametophytic Development in Arabidopsis. Front. Plant Sci. 2022, 13, 935413. [Google Scholar] [CrossRef]
- Lin, S.; Miao, Y.; Huang, H.; Zhang, Y.; Huang, L.; Cao, J. Arabinogalactan Proteins: Focus on the Role in Cellulose Synthesis and Deposition during Plant Cell Wall Biogenesis. Int. J. Mol. Sci. 2022, 23, 6578. [Google Scholar] [CrossRef] [PubMed]
- Fineran, B.A.; Lee, M.S. Organization of quadrifid and bifid hairs in the trap of Utricularia monanthos. Protoplasma 1975, 84, 43–70. [Google Scholar] [CrossRef]
- Płachno, B.J.; Kurczyńska, E.; Świątek, P. Integument cell differentiation in dandelions (Taraxacum, Asteraceae, Lactuceae) with special attention paid to plasmodesmata. Protoplasma 2016, 253, 1365–1372. [Google Scholar] [CrossRef]
- Płachno, B.J.; Świątek, P.; Kozieradzka-Kiszkurno, M.; Szeląg, Z.; Stolarczyk, P. Integument cell gelatinisation-the fate of the integumentary cells in Hieracium and Pilosella (Asteraceae). Protoplasma 2017, 254, 2287–2294. [Google Scholar] [CrossRef]
- Talbot, M.J.; Offler, C.E.; Mccurdy, D.W. Transfer cell wall architecture: A contribution towards understanding localized wall deposition. Protoplasma 2002, 219, 197–209. [Google Scholar] [CrossRef] [PubMed]
- Offler, C.E.; Patrick, J.W. Transfer cells: What regulates the development of their intricate wall labyrinths? New Phytol. 2020, 228, 427–444. [Google Scholar] [CrossRef]
- Jobson, R.W.; Baleeiro, P.C. Radiations of fairy-aprons (Utricularia dichotoma, Lentibulariaceae) in Australia and New Zealand: Molecular evidence and proposal of new subspecies. Aust. Syst. Bot. 2020, 33, 278–310. [Google Scholar] [CrossRef]
- Płachno, B.J.; Świątek, P.; Adamec, L.; Carvalho, S.; Miranda, V.F.O. The Trap Architecture of Utricularia multifida and Utricularia westonii (subg. Polypompholyx). Front. Plant Sci. 2019, 10, 336. [Google Scholar] [CrossRef] [PubMed]
- Fineran, B.A.; Lee, M.S.L. Transfer cells in traps of the carnivorous plant Utricularia monanthos. J. Ultrastruct. Res. 1974, 48, 162–166. [Google Scholar] [CrossRef] [PubMed]
- Broussaud, F.; Vintéjoux, C. Etudes ultrastructurales et cytochimiques des tissues superficiels placs a l’entre des urnes d’Utricularia (Lentibulariace). Bull. Soc. Bot. Fr. Lett. Bot. 1982, 3, 191–201. [Google Scholar]
- Płachno, B.; Jankun, A.; Faber, J. Development of the wall labyrinth in pavement epithelium hairs of some Utricularia species. Acta Biol. Cracoviensia Ser. Bot. 2005, 47, 109–113. [Google Scholar]
- Heslop-Harrison, Y.; Heslop-Harrison, J. The Digestive Glands of Pinguicula: Structure and Cytochemistry. Ann. Bot. 1981, 47, 293–319. [Google Scholar] [CrossRef]
- Vassilyev, A.E.; Muravnik, L.E. The Ultrastructure of the Digestive Glands in Pinguicula vulgaris L. (Lentibulariaceae) Relative to their Function. I. The Changes During Maturation. Ann. Bot. 1988, 62, 329–341. [Google Scholar] [CrossRef]
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Feldo, M.; Świątek, P. Do arabinogalactan proteins occur in the transfer cells of Utricularia dichotoma? IJMS 2024, submitted.
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Wójciak, M.; Świątek, P. Immunocytochemical analysis of bifid trichomes in Aldrovanda vesiculosa L. Traps. Int. J. Mol. Sci. 2023, 24, 3358. [Google Scholar] [CrossRef]
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Świątek, P.; Strzemski, M.; Miranda, V.F.O. Immunocytochemical Analysis of the Wall Ingrowths in the Digestive Gland Transfer Cells in Aldrovanda vesiculosa L. (Droseraceae). Cells 2022, 11, 2218. [Google Scholar] [CrossRef]
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Świątek, P. Arabinogalactan proteins in the digestive glands of Dionaea muscipula J. Ellis Traps. Cells 2022, 11, 586. [Google Scholar] [CrossRef] [PubMed]
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Świątek, P. Stellate trichomes in Dionaea muscipula Ellis (Venus Flytrap) Traps, Structure and Functions. Int. J. Mol. Sci. 2023, 24, 553. [Google Scholar] [CrossRef] [PubMed]
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Świątek, P.; Lichtscheidl, I. Differences in the Occurrence of Cell Wall Components between Distinct Cell Types in Glands of Drosophyllum lusitanicum. Int. J. Mol. Sci. 2023, 24, 15045. [Google Scholar] [CrossRef] [PubMed]
- Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Świątek, P. Do Cuticular Gaps Make It Possible to Study the Composition of the Cell Walls in the Glands of Drosophyllum lusitanicum? Int. J. Mol. Sci. 2024, 25, 1320. [Google Scholar] [CrossRef] [PubMed]
- Samaj, J.; Samajova, O.; Baluska, E.; Lichtscheidl, I.; Knox, J.P.; Volkmann, D. Immunolocalization of LM2 arabinogalactan protein epitope associated with endomembranes of plant cells. Protoplasma 2000, 212, 186–196. [Google Scholar] [CrossRef]
- Vaughn, K.C.; Talbot, M.J.; Offler, C.E.; McCurdy, D.W. Wall ingrowths in epidermal transfer cells of Vicia faba cotyledons are modified primary walls marked by localized accumulations of arabinogalactan proteins. Plant Cell Physiol. 2007, 48, 159–168. [Google Scholar] [CrossRef] [PubMed]
- Dahiya, P.; Brewin, N.J. Immunogold localization of callose and other cell wall components in pea nodule transfer cells. Protoplasma 2000, 214, 210–218. [Google Scholar] [CrossRef]
- Ligrone, R.; Vaughn, K.C.; Rascio, N. A cytochemical and immunocytochemical analysis of the wall labyrinth apparatus in leaf transfer cells in Elodea canadensis. Ann. Bot. 2011, 107, 717–722. [Google Scholar] [CrossRef]
- Henry, J.S.; Lopez, R.A.; Renzaglia, K.S. Differential localization of cell wall polymers across generations in the placenta of Marchantia polymorpha. J. Plant Res. 2020, 133, 911–924. [Google Scholar] [CrossRef]
- Henry, J.S.; Renzaglia, K.S. The placenta of Physcomitrium patens: Transfer cell wall polymers compared across the three bryophyte groups. Diversity 2021, 13, 378. [Google Scholar] [CrossRef]
- Henry, J.S.; Ligrone, R.; Vaughn, K.C.; Lopez, R.A.; Renzaglia, K.S. Cell wall polymers in the Phaeoceros placenta reflect developmental and functional differences across generations. Bryophyt. Divers. Evol. 2021, 43, 265–283. [Google Scholar] [CrossRef] [PubMed]
- McCurdy, D.W.; Patrick, J.W.; Offler, C.E. Wall ingrowth formation in transfer cells: Novel examples of localized wall deposition in plant cells. Curr. Opin. Plant Biol. 2008, 11, 653–661. [Google Scholar] [CrossRef]
- Paul Knox, PhD, University of Leeds. Available online: https://www.kerafast.com/cat/799/paul-knox-phd (accessed on 13 November 2023).
- Knox, J.P.; Day, S.; Roberts, K. A set of cell surface glycoproteins forms an early marker of cell position, but not cell type, in the root apical meristem of Daucus carota L. Development 1989, 106, 47–56. [Google Scholar] [CrossRef]
- Knox, J.P.; Linstead, P.J.; Cooper, J.P.C.; Roberts, K. Developmentally regulated epitopes of cell surface arabinogalactan proteins and their relation to root tissue pattern formation. Plant J. 1991, 1, 317–326. [Google Scholar] [CrossRef] [PubMed]
- Pennell, R.I.; Knox, P.J.; Scofield, G.N.; Selvendran, R.R.; Roberts, K. A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J. Cell Biol. 1989, 108, 1967–1977. [Google Scholar] [CrossRef] [PubMed]
- Pennell, R.I.; Janniche, L.; Kjellbom, P.; Scofield, G.N.; Peart, J.M.; Roberts, K. Developmental regulation of a plasma membrane arabinogalactan protein epitope in oilseed rape flowers. Plant Cell 1991, 3, 1317–1326. [Google Scholar] [CrossRef]
- Płachno, B.J.; Świątek, P.; Jobson, R.W.; Małota, K.; Brutkowski, W. Serial block face SEM visualization of unusual plant nuclear tubular extensions in a carnivorous plant (Utricularia, Lentibulariaceae). Ann. Bot. 2017, 120, 673–680. [Google Scholar] [CrossRef]
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Płachno, B.J.; Kapusta, M.; Stolarczyk, P.; Feldo, M.; Świątek, P. Cell Wall Microdomains in the External Glands of Utricularia dichotoma Traps. Int. J. Mol. Sci. 2024, 25, 6089. https://doi.org/10.3390/ijms25116089
Płachno BJ, Kapusta M, Stolarczyk P, Feldo M, Świątek P. Cell Wall Microdomains in the External Glands of Utricularia dichotoma Traps. International Journal of Molecular Sciences. 2024; 25(11):6089. https://doi.org/10.3390/ijms25116089
Chicago/Turabian StylePłachno, Bartosz J., Małgorzata Kapusta, Piotr Stolarczyk, Marcin Feldo, and Piotr Świątek. 2024. "Cell Wall Microdomains in the External Glands of Utricularia dichotoma Traps" International Journal of Molecular Sciences 25, no. 11: 6089. https://doi.org/10.3390/ijms25116089
APA StylePłachno, B. J., Kapusta, M., Stolarczyk, P., Feldo, M., & Świątek, P. (2024). Cell Wall Microdomains in the External Glands of Utricularia dichotoma Traps. International Journal of Molecular Sciences, 25(11), 6089. https://doi.org/10.3390/ijms25116089