Cell and Developmental Biology of Arabinogalactan-Proteins Cell and Developmental Biology of Arabinogalactan-Proteins Edited by Eugene A. Nothnagel University of California Riverside, California Antony Bacic and Adrienne E. Clarke University of Melbourne Parkville, Victoria, Australia Springer Science+Business Media, LLC Library of Congress Cataloging-in-Publication Data CeH and developmental biology of arabinogalactan-proteins/edited by Eugene A. Nothnagel, Antony Baeic, and Adrienne E. Clarke. p. cm. "Proceedings of the Twentieth Symposium in Plant Physiology, held lanuary 21-23, 1999, at the University of California, Riverside" - T.p. verso. Includes bibliographical references. ISBN 978-1-4613-6888-5 ISBN 978-1-4615-4207-0 (eBook) DOI 10.1007/978-1-4615-4207-0 1. Arabinogalactan-Congresses. 1. Nothnagel, Eugene A. II. Baeic, A. (Antony) III. Clarke, A. E. (Adrienne Elizabeth) IV. Symposium in Plant Physiology (20th: 1999: University of California, Riverside) QK898.A67 C46 2000 572'.68-dc21 00-058755 Proceedings of the Twentieth Symposium in Plant Physiology, held January 21-23, 1999, at the University of California, Riverside ISBN 978-1-4613-6888-5 © 2000 Springer Science+Business Media New York Originally published by Kluwer Academic / Plenum Publishers, New York in 2000 Softcover reprint of the hardcover 1s t edition 2000 AII rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without writlen permis sion from the Publisher Preface This volume captures a sense of the impact that the study of arabinogalactan-proteins (AGPs) is having in plant physiology. We have moved from a very diffuse set of observations on the distribution of AGPs in plants to a point where we can see some threads of research direction and some critical issues to be resolved. In this context it is interesting to recall that the reviewer of a proposal seeking funding for the meeting held at the University of California at Riverside in January, 1999, noted that "it is difficult to get an idea of where the field is headed other than you can find AGPs wherever you look!" It is true that AGPs are ubiquitous. We are now seeing, however, that different AGPs may have different tissue and cellular locations and that some appear and disappear during development. With this distribution and developmental control of AGPs, it is not unreasonable to consider that they may well have a range of functions. Indeed, some AGPs may be critical to survival, and this could be one reason why many people have observed a very low frequency of plants resulting from antisense experiments using AGP polypeptide backbone genes. In response to the reviewer's comment that it is difficult to get an idea of where the field is headed, one approach is to consider the blockages to further understanding of both the form and function of AGPs and their reciprocal relationships. FORM OF ARABINOGALACTAN-PROTEINS The fact that there are so many closely related but not identical AGPs leads to the questions of "What is an AGP?" and "When does one AGP differ from another?" v VI Preface In this context, both the structure of the polypeptide backbones and the glycosyl constituents need to be understood. Features of the polypeptide backbones needing improved understanding include their domain structure, their diversity, whether they are glycosylphosphatidylinositol-anchored or not, and whether the genes encoding the polypeptide backbones include introns or not. Some of the questions regarding the carbohydrate chains are "How many types of chains?", "Where are the points of glycosylation?", "What parts of the polypeptide backbone are covered or exposed?", "What is the diversity of the carbohydrate sequences?", "What is the overall shape of the molecule?", and "What parts of the polypeptide and the carbohydrate side chains might be accessible for binding to other molecules?" POSSIBLE FUNCTIONS OF ARABINOGALACTAN-PROTEINS Many different functions have been implied from observations of the involvement of AGPs in such diverse physiological effects as programmed cell death, cell division, arrest of growth (reversible), oxidative bursts/wounding, somatic embryogenesis, pollen tube growth, chilling protection, microsporogenesis, growth suppression, and xylem formation. Observations on many of these involvements of AGPs are detailed in this volume, but at present, no one function of a single AGP is understood in detail. In furthering our understanding of both the form and the function of AGPs, it became clear during the meeting that there are several critical issues to be addressed - (i) The specificity of the Yariv reagent. It is important to establish the exact identities of the molecules to which the Yariv reagent binds. Certainly the reagent precipitates AGPs from tissue extracts. It would be valuable, however, to know the key features of both the polysaccharide and the polypeptide components which are required for binding to the Yariv reagent. (ii) Sequence analysis of glycosyl chains. Understanding the precise structure and arrangement of the glycosyl chains is critical to our ultimate understanding of both the form and the function of AGPs. A current roadblock is the lack of routine and facile methods for isolating the glycosyl chains and establishing the monosaccharide com- ponents, linkages, and overall sequence. Commercial availability of glycosidases with defined specificities for the linkages which commonly occur in AGPs would be extremely helpful. The panel of monoclonal antibodies currently available is a useful tool set, although this usefulness is limited by lack of detailed specificity studies for many of these antibodies. Preface VB (iii) Availability of defined oligosaccharide fragments as reagents. The fact that the specificity of the antibodies has been defined in only a few cases reflects the lack of defined oligosaccharides that can be used as reagents. Commercial availability of oligosaccharides of galactose and arabinose in the relevant linkages, for example, would enable rapid progress to be made in applying immunocytochemical techniques to the cellular location and function of different AGPs. (iv) Biosynthesis of AGPs. Understanding how the various chains are formed and at what stage the glycosylation of the polypeptide backbone occurs will give us insight into the groups of AGPs with similar but distinct structural features. (v) The number of AGPs within a particular plant tissue. We do not yet have a sense of the complete range of AGPs in plant tissues. There are salt-extractable, non-salt extractable, membrane-bound, and non- membrane-bound AGPs, but the complete range for any particular tissue or cell type and the differences between the members of this range are still not defined. (vi) Arabidopsis mutants. The range of Arabidopsis mutants available provides an invaluable experimental tool for understanding the relationship between form and function of AGPs. Nonetheless, the precise details of the chemistry of the different AGPs will be required to get an understanding of the mutations in these complex proteoglycans. A related topic discussed during the meeting was the potential commercial use of AGPs. There is evidence supporting the idea that they can be used to induce immunostimulation in animals, and there may be other medicinal uses. Industrial uses rely on their functionality as emulsifiers, for example, in the food and cosmetic industries. There are many opportunities for applying current knowledge of the chemistry of AGPs to these industrial applications, many of which are presently based on empirical observations. All in all, we anticipate that by the time the next meeting is held, we will have created a much broader knowledge base of both the form and the function of AGPs. We can look forward to a further understanding of how the design of these complex and varied proteoglycans is adapted for their seemingly myriad functions. Adrienne E. Clarke University ofMelbourne Acknowledgements As editors of this volume, we wish to thank each of the authors for their scholarly contribution and for their cooperation and patience as this volume was assembled. Prominent acknowledgement and our enormous gratitude go to Nancy Day and Laura Heraty of the Department of Botany and Plant Sciences at Riverside for their editorial assistance and many, many hours of word processing to produce the camera-ready copy of this volume. We also thank MaryAnn McCarra, our editor at Kluwer Academic/Plenum Publishers. th As organizers of the 20 Symposium in Plant Physiology at the University of California, Riverside, upon which this volume is based, we prominently acknowledge Symposium Coordinators Cindi McKernan and Susana Aparicio, whose expertise and tireless attention to every detail in Riverside were greatly appreciated by both the organizers and the attendees at the symposium. We similarly thank Joanne Noble for her coordination and assistance in Melbourne. Our thanks also go to many other members of the Department of Botany and Plant Sciences including Cherie Cooksey, Ann Montejano, and Susan Miller, who handled finances, accounting, and many other essential functions; Van Stout and Lee Gross, who supplied the display boards for the poster session; and Rick Miranda, Watt Pattanagul, Kristen Lennon, Jean-Claude Mollet, David Puthoff, Donna Dubay, and Ricardo Cesped, who provided ground transportation and other assistance. We are sincerely grateful to the following governmental agencies, industrial corporations, and University of California programs and administrators for their financial contributions to the support of the sympoSIum: IX x Acknowledgements United States Department of Agriculture (Award 98-35304-6921 from the Plant Growth and Development Program) National Science Foundation (Award 9808309 from the Integrative Plant Biology Program) Pioneer Hi-Bred International, Inc. Bestfoods Baking Company GLYKO, Inc. Dionex Corporation Biosupplies Australia Pty. Ltd. University of California BioSTAR Project Michael Clegg, Dean, College of Natural and Agricultural Sciences, UCR Elizabeth Lord, Chair, Department ofBotany and Plant Sciences, UCR Neither the symposium nor this volume would have been possible without the financial support of these sponsors. A. E. Clarke E. A. Nothnagel A. Bacic University ofMelbourne University ofCalifornia, Riverside University ofMelbourne Contents Abbreviations xvii SECTION 1: STRUCTURE AND BIOSYNTHESIS OF ARABINOGALACTAN-PROTEINS 1. A Brief History of Arabinogalactan-Proteins 1 B. A. Stone and K. Valenta 2. Structural Classes of Arabinogalactan-Proteins 11 A. Bacic, G. Currie, P. Gilson, S.-L. Mau, D. Oxley, C. Schultz, J. Sommer-Knudsen, and A. E. Clarke 3. Molecular Analysis of Genes Encoding Arabinogalactan-Proteins 25 C. Reuzeau, L. Snogerup, and P. Kjellbom 4. The C-Terminal PAC Domain of a Secreted Arabinogalactan-Protein from Carrot Defines a Family of Basic Proline-Rich Proteins .43 T. C. Baldwin, A. J. van Hengel, and K. Roberts 5. Structure and Biosynthesis ofL-Fucosylated Arabinogalactan-Proteins in Cruciferous Plants 51 Y. Hashimoto Xl XII Contents SECTION 2: LOCALIZATION AND ACTION OF ARABINOGALACTAN- PROTEINS AT THE SUBCELLULAR AND CELLULAR LEVELS 6. Characterization and Localization of a Novel Tomato Arabinogalactan-Protein (LeAGP-l) and the Involvement of Arabinogalactan-Proteins in Programmed Cell Death 61 A. M. Showalter, M. Gao, M. J. KieIiszewski, and D. T. A. Lamport 7. Cell Cycle Arrest by Perturbation of Arabinogalactan-Proteins with Yariv Phenylglycoside 71 J. A. Eyvazzadeh and E. A. Nothnagel 8. A Major Antimicrobial Hybrid Chitin-Binding Protein from French Bean with Features Common to Arabinogalactan-Proteins and Hydroxyproline- Rich Glycoproteins 83 G. P. BolweIl, J. B. Trethowan, and P. Wojtaszek SECTION 3: ARABINOGALACTAN-PROTEINS IN SOMATIC EMBRYOGENESIS 9. Arabinogalactan-Proteins and Cell Development in Roots and Somatic Embryos 95 C. G. Steele-King, W. G. T. Willats, and J. P. Knox 10. Effect of Arabinogalactan-Proteins and Chitinases on Somatic Embryogenesis 109 M. Kreuger, A. van Hengel, and S. de Vries SECTION 4: ARABINOGALACTAN-PROTEINS IN REPRODUCTIVE DEVELOPMENT 11. Arabinogalactan-Proteins in Reproductive Tissues of Flowering Plants 121 A. E. Clarke, G. Currie, P. Gilson, S.-L. Mau, D. Oxley, C. J. Schultz, J. Sommer-Knudsen, and A. Bacic 12. Transcriptional, Post-Transcriptional and Post-Translational Regulation of a Nicotiana Stylar Transmitting Tissue-Specific Arabinogalactan- Protein 133 A. Y. Cheung, X.-Y. Zhan, E. Wong, H. Wang, and H.-M. Wu