Mitochondria in Higher Plants. Structure, Function, and Biogenesis PDF
Preview Mitochondria in Higher Plants. Structure, Function, and Biogenesis
AMERICAN SOCIETY OF PLANT PHYSIOLOGISTS MONOGRAPH SERIES Anthony H. C. Huang, Richard N. Trelease, and Thomas S. Moore, Jr. PLANT PEROXISOMES, 1983. Roland Douce MITOCHONDRIA IN HIGHER PLANTS: STRUCTURE, FUNCTION, AND BIOGENESIS, 1985. Mitochondria in Higher Plants Structure, Function, and Biogenesis Roland Douce Centre d'Etudes Nucleates and Universite Scientifique et Medicale Grenoble, France 1985 ACADEMIC PRESS, INC. (Harcourt Brace Jovanovich, Publishers) Orlando San Diego New York London Toronto Montreal Sydney Tokyo COPYRIGHT © 1985, BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS, ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING, OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER. ACADEMIC PRESS, INC. Orlando, Florida 32887 United Kingdom Edition published by ACADEMIC PRESS INC. (LONDON) LTD. 24-28 Oval Road, London NW1 7DX Library of Congress Cataloging in Publication Data Douce, Roland. Mitochondria in higher plants. (American Society of Plant Physiologists monograph series) Bibliography: p. Includes index. 1. Mitochondria. 2. Plant cells and tissues. I. Title. II. Series. QK725.D66 1985 582\087342 84-20398 ISBN 0-12-221280-0 (alk. paper) PRINTED IN THE UNITED STATE OSF AMERICA 85 86 87 88 9 8 7 6 5 4 3 2 1 J am grateful to my teacher and friend Walter D. Bonner for the guidance and training he gave me during the early part of my research career. Foreword From the earliest days of plant science there always have been a few plant physiologists studying respiration, commonly with respect to the activities of fruits, seeds, and roots. It was soon evident that the growth and development of plant tissues required metabolic energy derived from the oxidation ("dissimilation") of reduced carbon, but the chem istry of the process was poorly understood. Even after the essentials of glycolysis and fermentation were uncovered, there remained an exas perating void in the enzymology of the aerobic phase of respiration. Following World War II, however, there was an explosive growth in biological science based in large part on the new techniques of chro matography, radioisotope tracing, and electron microscopy. Among the disclosures was the role of the mitochondrion as the locus of the Krebs cycle and ATP formation in animal cells. Mitochondria (sometimes called "chondriosomes") were long known as cytoplasmic inclusions in plant cells, and were suggested to have an enzymatic role in starch degradation due to an apparent clustering around amyloplasts. By drawing on the techniques used with animal mitochondria, researchers established in the early 1950s that mitochon dria from plants and animals were similar in structure and function, but not entirely. As investigations proceeded, it became evident that in cer tain details there were important differences in cytological relationships, substrate oxidation rates, substrates utilized, electron transport chains, ion transport, etc. Many distinctions were uncovered by plant phys iologists with physiological questions in mind (rarely were plant mito chondria used as material for primary studies of mitochondrial func tion), and failure to meet the rat liver standard was sometimes attributed to damage during isolation. Over the next two decades, however, it became clear that while all mitochondria have a common basic pattern for oxidative phosphorylation and participation in intermediary metabo lism, those from plants have some special adaptations for autotrophic metabolism. Other characteristics of plant mitochondria are shared with lower organisms. In certain cases phenomena are observed which as yet ix χ Foreword have no adequate physiological or biochemical explanation [e.g., exter nal NAD(P)H oxidation and cyanide-resistant respiration]. Enough research has now been done on the special properties of plant mitochondria to justify the effort of bringing the results together in one reference volume. Professor Douce has done this, and done it in the rigorous and scholarly fashion that characterizes the research from his laboratory. The material is logically organized into five chapters begin ning with morphological and cytological observations, and proceeding through membrane and matrix functions to participation in metabolism and biogenesis. Each section presents the unique properties of plant mitochondria within the framework of general mitochondrial structure and function; the student using this book as a text will have little need to supplement it from other sources. It covers the relevant literature very well indeed, and can serve as the standard reference for plant mitochon dria for some years to come. Of special value is the recurring effort to place mitochondrial activities in the larger context of biochemical and physiological functions. Lastly, a challenge appears in this comprehensive summary of what is known about plant mitochondria: dozens of interesting research prob lems present themselves. Perhaps these stimuli will be the most valu able contribution of Professor Douce's book. /. B. Hanson Botany Department University of Illinois Urbana, Illinois Preface Plants are capable of utilizing light energy for the photosynthetic re duction of the atmospheric carbon dioxide plus water into carbohydrates and oxygen. This is a complex process that is performed in chloroplasts of land plants and the corresponding brown, red, and green plastids of the aquatic algae, including the phytoplankton of the sea. It is this process that perhaps more than anything else distinguishes plants from animals. The total amount of organic compounds formed each year by plants has been estimated at more than 100 billion tons. A biochemical operation of this magnitude would quickly deplete the earth's atmo sphere of its carbon dioxide if there were no compensating process. This compensating process known as respiration (i.e., the complex oxidation of carbohydrate to carbon dioxide and water, molecular oxygen serving as the ultimate electron acceptor) occurs not only in animal cells but also in plant cells. Oxygen uptake and carbon dioxide output are the external manifestations of this process. In plants, as in other organisms, respira tion takes place in mitochondria, where the energy freed in oxidation of cellular organic substrates is converted into the phosphate bond energy of adenosine triphosphate. Flemming (1882) and Altmann (1890) discovered mitochondria in ani mal cells. The evidence that mitochondria also occur in plant cells (in tapetum cells of the anthers of Nymphae) first dates from the beginning of this century (Meves, 1904), and the mitochondria of a cell were collec tively designated by the term chondriome (Guillermond et al., 1933). In the three decades since the pioneering work of Millerd et al. (1951), the experimental literature on the dynamics of plant mitochondrial reactions has been growing enormously in both volume and complexity. Al though work on the activities of higher plant mitochondria has lagged behind that conducted on the animal counterpart, particularly mam malian mitochondria (largely because of technical difficulties in handling the plant material), it is becoming more and more obvious that the basic enzymology of the biological oxidations and phosphorylations of higher plant mitochondria is remarkably similar to that found in animal sys tems. It is also obvious, however, that in addition to this highly conser- xi xii Preface vative basic system, developed at an early stage of evolution, the mito chondria of higher plants possess several additional features that are absent in animal systems. The aim of this book, then, is to collect and interpret the rapidly growing experimental information on plant mitochondria, not only the basic enzymology of ATP synthesis coupled to electron transport that appears to constitute the major activity of the mitochondria but also many other aspects that make plant mitochondria rather more diverse than their animal counterparts. Finally, we have tried to emphasize the important problem of mitochondria functioning under the wide variety of metabolic conditions encountered in the cytoplasm of plant cells. This book is intended not only for research workers and students interested in the enzymology of plant mitochondria respiration but also for graduate and undergraduate students in the field of plant biochemis try, cell physiology, and molecular biology. We also hope that this book may be useful as a starting point for those students wishing to pursue special studies in this field. Roland Douce Acknowledgments The author is greatly indebted to Dr. Michel Neuburger for criticism and advice. He is also grateful to Dr. David Day, who read the entire manuscript carefully and provided numerous helpful suggestions. Er rors of fact and interpretation that remain are, of course, my own responsibility. I owe major debts to Dr. Richard Bligny, who did some illustrations with artistic skill. Mme. Frangoise Bucharles has given valuable as sistance by typing innumerable drafts. As for the technical assistance, I particularly thank Agnes Jourdain. Finally I am indebted to Jacques Joyard, Etienne Journet, and research worker friends who gave me the idea that the book should be written. xiii 1 General Organization of Plant Mitochondria I. MITOCHONDRIA IN THE INTACT CELL The technique of electron microscopy which has provided the most information on plant mitochondrial structure is thin sectioning. Spec imens are fixed, dehydrated, and then embedded in epoxy resins or polyester resins. Reagents widely used as fixatives include glutaralde- hyde, osmium tetroxide, and potassium permanganate. Frequently, combinations of these reagents either sequentially or together are em ployed. Staining is carried out during fixation with osmium tetroxide or potassium permanganate or subsequently by treating the fixed spec imen with a solution of heavy-metal salt (uranyl acetate, lead citrate). Osmium tetroxide, which is a strong oxidant, can cross-link and stabilize molecules such as proteins and polar lipids. A primary fixation with glutaraldehyde that reacts with amino groups of polypeptide chains assures a rapid stabilization of proteins. Under these conditions, the subcellular structures containing proteins and nucleoproteins are well l
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