title: Pea Border Cell Maturation and Release Involve Complex Cell Wall Structural Dynamics.
abstract: The adhesion of plant cells is vital for support and protection of the plant body and is maintained by a variety of molecular associations between cell wall components. In some specialized cases, though, plant cells are programmed to detach, and root cap-derived border cells are examples of this. Border cells (in some species known as border-like cells) provide an expendable barrier between roots and the environment. Their maturation and release is an important but poorly characterized cell separation event. To gain a deeper insight into the complex cellular dynamics underlying this process, we undertook a systematic, detailed analysis of pea (Pisum sativum) root tip cell walls. Our study included immunocarbohydrate microarray profiling, monosaccharide composition determination, Fourier-transformed infrared microspectroscopy, quantitative reverse transcription-PCR of cell wall biosynthetic genes, analysis of hydrolytic activities, transmission electron microscopy, and immunolocalization of cell wall components. Using this integrated glycobiology approach, we identified multiple novel modes of cell wall structural and compositional rearrangement during root cap growth and the release of border cells. Our findings provide a new level of detail about border cell maturation and enable us to develop a model of the separation process. We propose that loss of adhesion by the dissolution of homogalacturonan in the middle lamellae is augmented by an active biophysical process of cell curvature driven by the polarized distribution of xyloglucan and extensin epitopes.
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.); mravec@plen.ku.dk william.willats@newcastle.ac.uk.|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.); mravec@plen.ku.dk william.willats@newcastle.ac.uk.|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and mravec@plen.ku.dk william.willats@newcastle.ac.uk.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.) mravec@plen.ku.dk william.willats@newcastle.ac.uk.
authors.forename: Jozef
authors.identifier: http://orcid.org/0000-0003-0331-3304
authors.initials: J
authors.lastname: Mravec
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Xiaoyuan
authors.identifier: http://orcid.org/0000-0001-8299-2522
authors.initials: X
authors.lastname: Guo
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Aleksander Riise
authors.identifier: http://orcid.org/0000-0001-7481-8639
authors.initials: AR
authors.lastname: Hansen
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Julia
authors.identifier: http://orcid.org/0000-0001-7402-8768
authors.initials: J
authors.lastname: Schückel
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Stjepan Krešimir
authors.identifier: http://orcid.org/0000-0002-5795-1320
authors.initials: SK
authors.lastname: Kračun
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Maria Dalgaard
authors.identifier: http://orcid.org/0000-0003-4297-6119
authors.initials: MD
authors.lastname: Mikkelsen
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Grégory
authors.identifier: http://orcid.org/0000-0002-5493-754X
authors.initials: G
authors.lastname: Mouille
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Ida Elisabeth
authors.identifier: http://orcid.org/0000-0001-8660-2018
authors.initials: IE
authors.lastname: Johansen
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: Peter
authors.identifier: http://orcid.org/0000-0003-3776-818X
authors.initials: P
authors.lastname: Ulvskov
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.).|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.).|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.).
authors.forename: David S
authors.identifier: http://orcid.org/0000-0001-8800-0061
authors.initials: DS
authors.lastname: Domozych
authors.affiliation: Department of Plant and Environmental Sciences, University of Copenhagen, Frederiksberg 1871, Denmark (J.M., X.G., A.R.H., J.S., S.K.K., M.D.M., I.E.J., P.U.); mravec@plen.ku.dk william.willats@newcastle.ac.uk.|Institut Jean-Pierre Bourgin, Unité Mixte de Recherche 1318 Institut National de la Recherche Agronomique/AgroParisTech, Saclay Plant Sciences, Institut National de la Recherche Agronomique Centre de Versailles, 78026 Versailles cedex, France (G.M.); mravec@plen.ku.dk william.willats@newcastle.ac.uk.|Department of Biology and Skidmore Microscopy Imaging Center, Skidmore College, Saratoga Springs, New York 12866 (D.S.D.); and mravec@plen.ku.dk william.willats@newcastle.ac.uk.|School of Agriculture, Food, and Rural Development, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom (W.G.T.W.) mravec@plen.ku.dk william.willats@newcastle.ac.uk.
authors.forename: William George Tycho
authors.identifier: http://orcid.org/0000-0003-2064-4025
authors.initials: WGT
authors.lastname: Willats
mesh_terms: D053898:Biosynthetic Pathways / Q000235:genetics; D002473:Cell Wall / Q000235:genetics / Q000378:metabolism*; D000939:Epitopes / Q000378:metabolism; D004951:Esterification; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D006031:Glycosylation; D018519:Meristem / Q000166:cytology / Q000378:metabolism / Q000648:ultrastructure; D046228:Microarray Analysis; D008954:Models, Biological; D009005:Monosaccharides / Q000032:analysis; D018532:Pisum sativum / Q000166:cytology* / Q000235:genetics / Q000378:metabolism*; D059828:Plant Cells / Q000378:metabolism* / Q000648:ultrastructure; D011134:Polysaccharides / Q000378:metabolism; D017550:Spectroscopy, Fourier Transform Infrared; D014158:Transcription, Genetic
chemical_list: D000939:Epitopes; D009005:Monosaccharides; D011134:Polysaccharides