MOLECULAR BIOLOGY AND BIOTECHNOLOGY OF PLANT ORGANELLES Molecular Biology and Biotechnology of Plant Organelles Chloroplasts and Mitochondria Edited by Henry Daniell Department of Microbiology and Molecular Biology, University of Central Florida, Orlando, Florida, U.S.A. and Christine Chase Horticultural Sciences Department, University of Florida, Gainesville, Florida, U.S..A. A C.I.P. Catalogue record for this book is available from the Library of Congress. ISBN 1-4020-2713-3 (HB) ISBN 1-4020-3166-1 (e-book) Published by Springer, P.O. Box 17, 3300 AADordrecht, The Netherlands. Sold and distributed in North, Central and South America by Springer, 101 Philip Drive, Norwell, MA02061, U.S.A. In all other countries, sold and distributed by Springer, P.O. Box 322, 3300 AHDordrecht, The Netherlands. Printed on acid-free paper All Rights Reserved ©2004 Springer No part of this work 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 written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work. Printed in the Netherlands. CONTENTS Preface vii About the Editors viii Contributors ix Color Plates xi 1. Introduction to the Molecular Biology and Biotechnology of Plant 1 Organelles Henry Daniell and Christine D. Chase SECTION 1: ORGANELLE GENOMES AND PROTEOMICS 2. The Evolutionary Origins of Plant Organelles 15 Michael W. Gray 3. The Somatic Inheritance of Plant Organelles 37 S. Heinhorst, C. L. Chi-Ham, S. W. Adamson and G. C. Cannon 4. The Sexual Inheritance of Plant Organelles 93 Rudolph Hagemann 5. Plastid Genomes 115 R. M. Maier and C. Schmitz-Linneweber 6. Plant Mitochondrial Genomes 151 C. Fauron, J. Allen, S. Clifton and K. Newton 7. Proteomics, Bioinformatics and Genomics Applied to Plant Organelles 179 C. Colas des Francs-Small, B. Szurek and I. Small SECTION 2: ORGANELLE GENE EXPRESSION AND SIGNALING 8. The Transcription of Plant Organelle Genomes 213 Andreas Weihe 9. RNA Editing in Plant Organelles 239 R. Michael Mulligan 10. Plastid and Plant Mitochondrial RNA Processing and RNA Stability 261 A. Marchfelder and S. Binder v 11. Intron Splicing in Plant Organelles 295 Alice Barkan 12. Translational Machinery in Plant Organelles 323 Linda Bonen 13. Regulation of Translation in Chloroplasts 347 William Zerges 14. Targeting Signals and Import Machinery of Plastids and Plant 385 Mitochondria Elzbieta Glaser and Jürgen Soll 15. Proteolysis in Plant Organelles 419 Zach Adam SECTION 3: ORGANELLE BIOTECHNOLOGY 16. Chloroplast Genetic Engineering 443 Henry Daniell, Paul R. Cohill, Shashi Kumar, and Nathalie Dufourmantel 17. Engineering Herbicide Resistance Pathways in Plastids 491 Amit Dhingra and Henry Daniell 18. Metabolic Engineering of Chloroplasts for Abiotic Stress Tolerance 513 Joe H. Cherry and Brent L. Nielsen 19. Metabolic Pathway Engineering For Nutrition Enrichment 527 Niranjan Baisakh and Swapan Datta 20. Plastid Metabolic Pathways for Fatty Acid Metabolism 543 Ikuo Nishida 21. Metabolic Engineering: Plastids as Bioreactors 565 Karen Bohmert, Oliver P. Peoples and Kristi D. Snell 22. Cytoplasmic Male Sterility and Fertility Restoration by Nuclear Genes 593 Christine D. Chase and S. Gabay-Laughnan 23. The Use of Cytoplasmic Male Sterility for Hybrid Seed Production 623 Michael J. Havey 24. Somatic Cell Cybrids and Hybrids in Plant Improvement 635 W. W. Guo, X. D. Cai and J. W. Grosser v i Preface We have taught plant molecular biology and biotechnology at the undergraduate and graduate level for over 20 years. In the past few decades, the field of plant organelle molecular biology and biotechnology has made immense strides. From the green revolution to golden rice, plant organelles have revolutionized agriculture. Given the exponential growth in research, the problem of finding appropriate textbooks for courses in plant biotechnology and molecular biology has become a major challenge. After years of handing out photocopies of various journal articles and reviews scattered through out the print and electronic media, a serendipitous meeting occurred at the 2002 IATPC World Congress held in Orlando, Florida. After my talk and evaluating several posters presented by investigators from my laboratory, Dr. Jacco Flipsen, Publishing Manager of Kluwer Publishers asked me whether I would consider editing a book on Plant Organelles. I accepted this challenge, after months of deliberations, primarily because I was unsuccessful in finding a text book in this area for many years. I signed the contract with Kluwer in March 2003 with a promise to deliver a camera-ready textbook on July 1, 2004. Given the short deadline and the complexity of the task, I quickly realized this task would need a co-editor. Dr. Christine Chase was the first scientist who came to my mind because of her expertise in plant mitochondria, and she readily agreed to work with me on this book. Both of us made a list of the topics and the eminent researchers in chloroplasts and mitochondria. Fortunately almost all invited scientists agreed to contribute a chapter on their topic of expertise. We are extremely thankful to the authors who contributed their knowledge to this book, and their commitment to educate students of future generations. Through meticulous work they ensured that the topics were thoroughly researched, up to date and well presented. We are thankful that they took time from their very busy schedules and submitted chapters in a timely manner. Unfortunately, we lost two of our valued colleagues during the preparation of this book. Professor Rainer Maier died in April 2004 after completing Chapter 5. Professor Lawrence Bogorad died in December 2003 before he could write an overview of this field. He has been Henry Daniell’s mentor and friend for two decades, and will be missed very much. The transformation of the manuscript into a book, in a camera-ready format, involved a myriad of tasks that required the help of many. Jacco Flipsen and Noeline Gibson of Springer Press were patient with our questions regarding style, graphics, and format. Henry Daniell would like to acknowledge the assistance of his lab colleagues Amit Dhingra, Paul Cohill, and Shashi Kumar; Vijay Pattisapu and Suneel Modani were unstinting in their efforts. He is deeply indebted to his wife Shobana for help in editing this book and constant support. Christine Chase would like to thank her first mentor in science, Dr. Rolf Benzinger, for introducing her to the field of genetic transformation. She also thanks her colleagues Drs. Daryl Pring, Susan Gabay-Laughnan, and Ken Cline for countless discussions of organelle biology and genetics over the years and for their insights regarding the content of this volume. We dedicate this book to the memory of Professors Lawrence Bogorad and Rainer Maier. Both of them made major contributions and continue to inspire many scientists to conduct research in chloroplast molecular biology. Henry Daniell Christine Chase vi i About the Editors Henry Daniell was born and educated in India. He moved to the United States as a post-doctoral fellow at the University of Illinois, Urbana-Champaign in 1980. Since then he has served on the faculty of Washington State University, University of Idaho Auburn University and University of Central Florida (as Pegasus Professor & Trustee Chair). He has published over 100 research articles on several areas, including DNA replication in chloroplast and mitochondria, identification of new genes in the mitochondrial genome, promiscuous DNA and their evolutionary significance, maternal inheritance, transgene containment, photosynthesis (Rubisco, electron transport), chlorophyll biosynthesis, chloroplast development, in organello protein synthesis, transcription, RNA processing, RNA stability, translation, protein import, proteolysis and regulation of these processes. He pioneered the chloroplast genetic engineering approach in the 1980s and advanced this concept to confer useful agronomic traits (for biotic & abiotic stress, photoremediation, cytoplasmic male sterility, etc.) and to express vaccine antigens, biopharmaceuticals and biomaterials in transgenic plants. He has extended this technology to major crops, including cotton. Numerous undergraduates, graduates and post-doctoral fellows were trained to use this experimental system. Based on his oldest patents in this field, he is the technical founder of Chlorogen Inc., which is now evaluating chloroplast transgenic crops in the field. He is an editor of the Plant Biotechnology Journal and has received several Distinguished Researcher and Teaching Excellence Awards. Dr. Daniell has served as a consultant to the United Nations in biotechnology and was elected to the National Academy of Sciences, Italy in 2004, a rare honor bestowed on 14 Americans in the past 222 years. Christine Chase was born and raised in rural, upstate New York. She earned a B.S. degree in Science Education from Cornell University in 1973 and a Ph.D. in Biology from the University of Virginia in 1981. During her graduate studies, she was supported by a NIH Traineeship in Genetics awarded through the Biology Department. Her introduction to organelle research began with her postdoctoral training (1981-1984) in the laboratory of Daryl Pring, USDA-ARS, at the University of Florida. She joined the faculty of the University of Florida Institute of Food and Agricultural Sciences in 1985, and she currently holds the rank of Professor in the Horticultural Sciences Department. She was a founding member of the University of Florida Interdepartmental Graduate Program in Plant Molecular and Cellular Biology, and she served as Co-Director (1993-1995) and Director (1995-1997) of that program. Dr. Chase teaches in graduate-level Advanced Genetics and Plant Molecular Biology courses. Her research exploits the unique biology and genetics of S cytoplasmic male sterility in maize to study plant mitochondrial biogenesis and function. This research platform presents an array of interesting biological questions that can be addressed through a variety of experimental approaches, and numerous undergraduate and graduate students have been introduced to research via this experimental system. vi ii CONTRIBUTORS ADAM, Z. - Institute of Plant Sciences, The Hebrew University of Jerusalem, Israel ADAMSON, S. W. - Department of Chemistry and Biochemistry, University of Southern Mississippi, Mississippi, Hattiesburg, USA ALLEN, J. - Biological Sciences, University of Missouri, Columbia, Missouri, USA BAISAKH, N. - Plant Breeding, Genetics, and Biochemistry Division, International Rice Research Institute, Manila, Philippines BARKAN, A. - Institute of Molecular Biology, University of Oregon, Eugene, Oregon, USA BINDER, S. - Allgemeine Botanik, Universitäät Ulm, Germany BOHMERT, K. - Metabolix, Inc., Cambridge, Massachusetts, USA BONEN, L. - Biology Department, University of Ottawa, Canada CAI, X. D. - National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China CANNON, G. C. - Department of Chemistry and Biochemistry, University of Southern Mississippi, Hattiesburg, Mississippi, USA CHASE, C. - Horticultural Sciences Department, University of Florida, Gainesville, Florida, USA CHERRY, J. H. - Auburn University, Auburn, Alabama, USA CHI-HAM, C. L. - Department of Chemistry and Biochemistry, University of Southern Mississippi, Hattiesburg, USA CLIFTON, S. - Genome Sequencing Center, Washington University, St. Louis, Missouri, USA COHILL, P. R. - Department of Microbiology and Molecular Biology, University of Central Florida, Orlando, Florida, USA COLAS DES FRANCS-SMALL, C. - Institut de Biotechnologie des Plants, Université Paris- Sud, Orsay, France DANIELL, H. - Department of Microbiology and Molecular Biology, University of Central Florida, Orlando, Florida, USA DATTA, S. - Plant Breeding, Genetics, and Biochemistry Division, International Rice Research Institute, Manila, Philippines DHINGRA, A. - Department of Microbiology and Molecular Biology, University of Central Florida, Orlando, Florida, USA DUFOURMANTEL, N. - CEA Cadarache, DSV, DEVM, CNRS-CEA, Aix-Marseille II, Saint-Paul-lez-Durance, France ix FAURON, C. - Eccles Institute of Genetics, University of Utah, Salt Lake City, Utah, USA GABAY-LAUGHNAN, S. - Department of Plant Biology, University of Illinois, Urbana- Champaign, Illinois, USA GLASER, E. - Department of Biochemistry and Biophysics, Stockholm University, Sweden GRAY, M. W. - Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Canada GROSSER, J. W. - Citrus Research and Education Center, University of Florida, Lake Alfred, Florida, USA GUO, W. W. - National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China HAGEMANN, R. - Institut für Genetik, Martin-Luther-Universität, Halle/S, Germany HAVEY, M. J. - USDA, ARS Vegetable Crops Unit, Department of Horticulture, University of Wisconsin, Madison, Wisconsin, USA HEINHORST, S. - Department of Chemistry and Biochemistry, University of Southern Mississippi, Hattiesburg, Mississippi, USA KUMAR, S. - Department of Microbiology and Molecular Biology, University of Central Florida, Orlando, Florida, USA MAIER, R. M. - Cell Biology, Philipps University, Marburg, Germany MARCHFELDER, A. - Molekulare Botanik, Universitat Ulm, Germany MULLIGAN, R. M. - Department of Developmental and Cell Biology, University of California, Irvine, California, USA NEWTON, K. - Biological Sciences, University of Missouri, Columbia, Missouri, USA NIELSEN, B. L. - Department of Microbiology and Molecular Biology, Brigham Young University, Provo, Utah, USA NISHIDA, I. - Graduate School of Sciences, University of Tokyo, Japan PEOPLES, O. P. - Metabolix, Inc., Cambridge, Massachusetts, USA SCHMITZ-LINNEWEBER, C. - Institute of Molecular Biology, University of Oregon, Eugene, Oregon, USA SOLL, J. - Department für Biologie I, Botanik, Ludwig-Maximilians-Universität, München, Germany SMALL, I. - Unite de Recherche en Genomique Vegetale, Cremieux, France SNELL, K. D. - Metabolix, Inc., Cambridge, Massachusetts, USA SZUREK, B. - Unité de Recherche en Génomique Végétale, Cremieux, France WEIHE, A. - Institut füür Biologie, Humboldt-Universitäät, Berlin, Germany ZERGES, W. - Biology Department, Concordia University, Montreal, Canada x Plate 1: Comparison of various plant mitochondrial genomes. See Chapter 6, Figure 3. xi