Table Of ContentPHYSIOLOGICAL ECOLOGY
A Series of Monographs, Texts, and Treatises
EDITED BY
T. T. KOZLOWSKI
University of Wisconsin
Madison, Wisconsin
T. T. KOZLOWSKI. Growth and Development of Trees, Volumes I and II -
1971
DANIEL HILLEL. Soil and Water: Physical Principles and Processes, 1971
J. LEVITT. Responses of Plants to Environmental Stresses, 1972
V. B. YOUNGNER AND C. M. MCKELL (Eds.). The Biology and Utilization
of Grasses, 1972
T. T. KOZLOWSKI (Ed.). Seed Biology, Volumes I, II, and III - 1972
YOAV WAISEL. Biology of Halophytes, 1972
G. C. MARKS AND T. T. KOZLOWSKI (Eds.). Ectomycorrhizae: Their Ecol
ogy and Physiology, 1973
In Preparation
T. T. KOZLOWSKI (Ed.). Shedding of Plant Parts
Ectomycorrhizae
THEIR ECOLOGY AND PHYSIOLOGY
Edited by
G. C. MARKS
Forests Commission of Victona
Treasury Place
Melbourne, Victoria, Australia
T. T. KOZLOWSKI
Russell Laboratory
University of Wisconsin
Madison, Wisconsin
ACADEMIC PRESS New York and London 1973
A Subsidiary of Harcourt Brace Jovanovich, Publishers
COPYRIGHT © 1973, 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.
Ill Fifth Avenue, New York, New York 10003
United Kingdom Edition published by
ACADEMIC PRESS, INC. (LONDON) LTD.
24/28 Oval Road, London NW1
Library of Congress Cataloging in Publication Data
Marks, G C
Ectomy corrhizae.
(physiological ecology)
Includes bibliographies.
1. Mycorrhiza. I. Kozlowski, Theodore Thomas,
DATE joint author. II. Title.
QK604.M35 581.5'24 72-9332
ISBN 0-12-472850-2
PRINTED IN THE UNITED STATES OF AMERICA
TO A. J. RIKER
List of Contributors
Numbers in parentheses indicate the pages on which the authors' contributions begin.
G. D. BOWEN, Division of Soils, Commonwealth Scientific and Industrial
Research Organization, Glen Osmond, Adelaide, South Australia
(107, 151)
R. C. FOSTER, Forest Products Laboratory, Division of Applied Chemistry,
C.S.I.R.O. South Melbourne, Victoria, Australia (1)
EDWARD HACSKAYLO, U.S.D.A. Forest Service, Forest Physiology Labo
ratory, Beltsville, Maryland (207)
G. C. MARKS, Forests Commission of Victoria, Treasury Place, Melbourne,
Victoria, Australia (1)
DONALD H. MARX, U.S.D.A., Forest Service, Forestry Sciences Laboratory,
Athens, Georgia (351)
F. H. MEYER, Institute for Landscape Management and Nature Con
servation, Herrenharuser, West Germany (79)
PEITSA MIKOLA, Department of Silviculture, University of Helsinki, Fin
land (383)
ANGELO RAMBELLI, Laboratory of Mycology, Institute of Botany, Roma
State University, Rome, Italy (299)
V. SLANKIS, Ministry of Natural Resources, Research Branch, Southern
Research Station, Maple, Ontario (231)
C. THEODOROU, Division of Soils, Commonwealth Scientific and Industrial
Research Organization, Glen Osmond, Adelaide, South Australia
(107)
B. ZAK, Forestry Sciences Laboratory, Pacific Northwest Forest and
Range Experiment Station, U.S.D.A. Forest Services, Corvallis,
Oregon (43)
XI
Preface
This volume summarizes the present state of knowledge and opinion
on the physiological ecology of ectomycorrhizae (which may be defined
as symbiotic associations between nonpathogenic or weakly pathogenic
fungi and living cells of roots). Although the book places considerable
emphasis on forestry aspects of mycorrhizal problems, its wide ranging
subject matter cuts across the boundaries of a number of traditional plant
sciences. Thus, it will be of interest to a wide variety of researchers and
teachers, especially agronomists, biochemists, foresters, horticulturists,
mycologists, plant pathologists, soil scientists, plant ecologists, plant
physiologists, and microbiologists. A short glossary of terms is included
for use by those unfamiliar with mycological terminology.
The ecology of mycorrhizae is a somewhat neglected field of study, yet
it is an area in which research can have its most significant impact on
practical forestry problems. Not only could it assist directly in trans
lating laboratory studies into improving forest yields but research find
ings may also help explain field observations. A vivid example of this
was brought home to one of us (G.C.M.) when he discovered that a
carefully balanced fertilizer mixture greatly reduced field resistance of
Eucalyptus trees sensitive to feeder root rot caused by Phytophthora ein-
namomi despite a very large increase in stand vigor, growth rate, etc.
The information in D. H. Marx's chapter proved very useful when trying
to explain this result.
Investigations into factors controlling genesis of mycorrhizae have
provided a fertile field for controversy over the years. The formation of
mycorrhizae is an important problem with heavy ecological overtones, and
it must be clarified before greater practical use can be made of research
findings. Some of the chapters in this book show that the origin of mycor
rhizae is by no means resolved; it will be left to the student and re
searcher to evaluate the merits of the data presented. Finally, it is hoped
that reviews, interpretations, and concepts proposed by authors of the
xiii
XIV Preface
various chapters will stimulate further work on microecology of forest
tree roots because the information presented tends to highlight the need
for additional research in this field and the lack of agreement on some
fundamental questions.
In planning this book, invitations were extended to a group of leading
modern investigators of the biology of mycorrhizae and their significance.
We express our deep appreciation to each contributor for his scholarly
work, patience, and attention to detail during the production process. The
assistance of Mr. W. J. Davies and Mr. P. E. Marshall in preparation of
the Subject Index is also acknowledged.
G. C. MARKS
T. T. KOZLOWSKI
CHAPTER 7
Structure, Morphogenesis, and
Infrastructure of Ectomycorrhizae
G. C. MARKS1 and R. C. FOSTER2
I. Introduction 2
II. Classification and Structure of Roots Based on External Appearance 2
A. Morphogenesis of Long and Short Roots before Infection . . 3
B. Growth and Branching 3
C. Maturation of Root Tissues 4
III. Process of Infection 5
A. Methods of Infection 5
B. Barriers to Infection 8
C. Factors Affecting Infection 10
IV. Structure of Mycorrhizae 12
A. Peritrophic Associations 13
B. Ectomycorrhizae 13
C. Pseudomycorrhizae 14
D. Ectendomycorrhizae 15
E. Mixed Mycorrhizal Associations 15
F. Senescence in Mycorrhizae 16
V. The Ultrastructure of Ectomycorrhizae 17
A. The Rhizosphere 17
B. The Mantle 21
C. The "Tannin Layer" 23
D. The Hartig Net 29
References 35
1 Senior Forest Pathologist, Forests Commission, Victoria.
2 Senior Research Scientist, Forest Products Laboratory, South Melbourne.
1
2 G. C. Marks and R. C. Foster
I. Introduction
The structure of mycorrhizae has been examined intermittently ever
since the first observations were made by Unger in 1840. Frank (1885)
provided one of the best of the early descriptions of mycorrhizal structure
and he coined the name of this organ. Mycorrhizae have attracted the
attention of foresters, mycologists, tree physiologists, biochemists, and
biophysicists, and considerable information exists on their physiology and
function.
In contrast to the wealth of information that has accumulated on
structure and physiology of mycorrhizae, there is very little published
information on the cytology of these associations. The majority of electron
microscope studies of host/fungus interrelationships have been made on
parasitic associations and have concentrated on fine structure of intra-
cellular haustoria rather than intracellular hyphae. Ehrlich and Ehrlich
(1963), Shaw and Manocha (1965), Manocha and Shaw (1967), and
Van Dyke and Hooker (1969) looked at the Uredinales; McKeen et dl.
(1966) and Bracker (1968) looked at Erisiphales; and Peyton and Bowen
(1963), Berlin and Bowen (1964), and Chou (1970) examined the
Peronosporales. These studies provided useful data with which the
cytology of symbiotic mycorrhizal associations may be compared. Like
lichens, mycorrhizae are truly symbiotic and produce new, consistent
morphological entities in which both organisms benefit from the as
sociation. Only recently, however, have they been examined at the level
of the electron microscope, and *tfee iirfoxE^ätfian *gfea»#d Lgi^es .new in
sight into the interrelationships of the two symbionts.
In this chapter we review information on the structure, cytology, and
morphogenesis of mycorrhizae and describe factors in the environment
that directly affect the latter phenomenon. In this manner a more mean
ingful picture of the organism can be presented. In order to achieve this,
it will be necessary to briefly review the growth and development of
primary tissues of the root and then follow root development once
infection has taken place and a mycorrhiza is established.
II. Classification and Structure of Roots Based on
External Appearance
Mycorrhizae form on unthickened roots of forest trees, and attempts
have been made to classify these uninfected root tips on the basis of their
growth characteristics. Noelle (1910) divided the root systems of conifers
into long and short roots. Aldrich-Blake (1930) added a further category
when he described the very fast-growing "pioneer" roots of Finns laricio
1. Structure, Morphogenesis, and Ultrastructure 3
seedlings. These divisions were based primarily on growth rates of the
roots, their method of branching, and, more recently, on appearance of
the apical meristem (Wilcox, 1968). Although these categories are clearly
defined, an individual root could change from one type to another when
conditions in the environment are altered (Slankis, 1967; Wilcox, 1968).
Separation into these categories is not always possible because they some
times intergrade as in broad-leaved trees (Chilvers and Pryor, 1965;
Harley, 1969; Lyford and Wilson, 1964) and in some gymnosperm species
(How, 1943; Zak, 1969). However, after infection and establishment of
the mycorrhizal habit, the root assumes a different character which is
quite distinctive (Clowes, 1950).
A. MORPHOGENESIS OF LONG AND SHORT ROOTS BEFORE INFECTION
In order to appreciate the events that take place in an infected root
it is essential to compare the differences observed and the changes that
occur in long and short roots prior to infection, since many of the changes
in structure observed in mycorrhizae occur after infection. Separation
of these two stages has not always been made in the literature on
mycorrhizae.
B. GROWTH AND BRANCHING
The long root of conifers shows racemose branching and is capable
of indefinite growth, unlike the dichotomously branched short root which
grows for only a restricted period. The growth rates of the long roots are
considerably greater (Fig. 1) and the duration of growth more prolonged
than that observed in short roots (Hatch, 1937; Aldrich-Blake, 1930).
However, it is worth observing that the growth rate of a long root can
slow down to that of a short root, and the opposite situation often
develops where a short root assumes the growth characteristics of a long
root.
The structure of the apical meristem of an active long root reflects its
increased capacity for growth. The meristem is conical in shape, and of
larger diameter than that of the smaller, more hemispherically shaped
meristem of the short root (Wilcox, 1968). The branches produced on
the root are related to the activity of the apical meristem. In large, fast-
growing long roots, lateral branching is often suppressed (Wilcox, 1968;
Aldrich-Blake, 1930), while small-diameter, subordinate, mother roots
may produce a relatively large number of lateral branches, which emerge
from the cortex and grow vigorously. Wilcox (1968) stated that the
dichotomous type of branching observed in the short roots of Finns
resinosa arose from the precocious growth of the laterals, with growth
being suppressed in the apical meristems.
