Pea Border Cell Maturation and Release Involve Complex Cell Wall Structural Dynamics

• Published in: Plant physiology (Bethesda) 2017-06, Vol.174 (2), p.1051-1066
• Main Authors: Mravec, Jozef, Guo, Xiaoyuan, Hansen, Aleksander Riise, Schückel, Julia, Kraćun, Stjepan Krešimir, Mikkelsen, Maria Dalgaard, Mouille, Grégory, Johansen, Ida Elisabeth, Ulvskov, Peter, Domozych, David S., Willats, William George Tycho
• Format: Article
• Language: English
• Subjects: Biosynthetic Pathways - genetics; CELL BIOLOGY; Cell Wall - genetics; Cell Wall - metabolism; Epitopes - metabolism; Esterification; Gene Expression Regulation, Plant; Genes, Plant; Glycosylation; Life Sciences; Meristem - cytology; Meristem - metabolism; Meristem - ultrastructure; Microarray Analysis; Models, Biological; Monosaccharides - analysis; Pisum sativum - cytology; Pisum sativum - genetics; Pisum sativum - metabolism; Plant Cells - metabolism; Plant Cells - ultrastructure; Polysaccharides - metabolism; Spectroscopy, Fourier Transform Infrared; Transcription, Genetic
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.16.00097

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.