Advances in agronomy volume 36

ADVANCES IN

AGRONOMY

VOLUME 36


CONTRIBUTORS TO THIS VOLUME
C . AZCON-AGUILAR

J. M. BAREA
P. BEMIS
WILLIAM
E. B. A. BISDOM
JEAN-MARC
BOLLAG
C. M. DONALD

IANB. EDWARDS

KEITHW. T. GOULDING
J. HAMBLIN

KRITONK. HATZIOS
LEMOYNEHOGAN
J. LOLL
MICHAEL
J. NEILRUTGER

K. L. SAHRAWAT

S. S. VIRMANI


ADVANCES IN

AGRONOMY
Prepared in cooperation with the
AMERICAN
SOCIETY OF AGRONOMY

VOLUME 36
Edited by N. C. BRADY
Science and Technology
Agency for International Development
Department of Srate
Washington, D . C .

ADVISORY BOARD
H . J. GORZ.CHAIRMAN

E. J . KAMPRATH T. M. STARLING

J. B. POWELL J . W. BIGGAR
M. A . TABATABAI
M . STELLY.
EX

OFFICIO,

ASA Headquarters

I983

ACADEMIC PRESS, INC.
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This volume is dedicated to
Dr. Arthur Geoffrey Norman,
editor of the first 20 volumes
of Advances in Agronomy.


This Page Intentionally Left Blank


CONTENTS
CONTRIBUTORS
.................................................

xi

PREFACE .......................................................
IN MEMORIAM.................................................

Xlll

...

xv

MYCORRHIZAS AND THEIR SIGNIFICANCE IN NODULATING
NITROGEN-FIXING PLANTS

J . M . Barea and C. Azc6n-Aguilar
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
I1. Mycorrhizas .................................................

1
4
23

111. Mycorrhizas in Legumes ......................................
IV . Mycorrhizas in Nodulating Nitrogen-Fixing Nonlegume Plants . . . . . . .
V. Conclusions and Perspectives ..................................
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

44
45

46

SUBMICROSCOPIC EXAMINATION OF SOILS

E . B . A . Bisdom
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
II. Submicroscopic Techniques ....................................
111. Applications of Electron Microscopy ............................

IV . Applications of Ion Microscopy ................................
V . Applications of Other Forms of Submicroscopy ....................
VI . Conclusions .................................................
References .................................................

55
57

65
88
89
90
91

THE CONVERGENT EVOLUTION OF ANNUAL SEED CROPS IN AGRICULTURE

C. M . Donald and J . Hamblin
I. Introduction .................................................

II. Selection in Domesticated Crops ...............................
I11.
IV .
V.
VI .

Ekotypic Parallelism in Crop Plants ............................
Selection, Evolution, and Crop Yield ...........................
Progress and Prospects in the Development of Annual Seed Crops . . .
A Basic Ideotype for All Annual Seed Crops .....................
References ................................................

vii

97
100
111
112
121
134
139


...

Vlll

CONTENTS
CURRENT STATUS AND FUTURE PROSPECTS FOR BREEDING HYBRID
RICE AND WHEAT

S. S . Virmani and Ian B . Edwards
I . Introduction ................................................
Heterosis in Rice and Wheat ..................................
Advantages of Hybrids over Conventionally Bred Varieties . . . . . . . . .
Cytoplasmic-Genetic Male Sterility Systems in Rice and Wheat . . . . .
Fertility Restoration .........................................
Use of Chemical Pollen Suppressants in Hybrid Production .........
Factors Affecting Cross-Fertilization ............................
Seed Production ............................................
Ix. Quality of Hybrids ..........................................

X . Economic Considerations .....................................
XI . Problems ..................................................
XI1. Conclusion ................................................
References ................................................

11.
I11.
IV .
V.
VI.
VII.
VIII.

146
147
155
157
169
180
183
191
196
198
200
202
206

THERMODYNAMICS AND POTASSIUM EXCHANGE IN SOILS AND CLAY MATERIALS

Keith W . T. Goulding

I. Introduction ................................................
11. The Thermodynamics of Ion-Exchange Equilibria . . . . . . . . . . . . . . . . .
111. Calorimetry in Ion-Exchange Studies ...........................
IV . Thermodynamics Applied to Potassium Exchange in Soils and
Clay Minerals ............................................
V. Exchange Equilibrium and the Kinetics of Potassium Exchange . . . . . .
VI . Summary and Conclusions ....................................
VII. Appendix: List of Symbols ...................................
References ................................................

215
217
228
233
256
258
259
260

HERBICIDE ANTIDOTES: DEVELOPMENT. CHEMISTRY. AND MODE OF ACTION

Kriton K . Hatzios
I . Introduction ................................................
11. Development of Herbicide Antidotes ...........................
III. Chemistry of Herbicide Antidotes ..............................
IV . Field Performance of Herbicide Antidotes .......................
V . Mode of Action of Herbicide Antidotes .........................

265

270
292
296
301


ix

CONTENTS

VI . Degradation of Herbicide Antidotes in Plants . . . . . . . . . . . . . . . . . . . . .
VII . Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

309
310
310

BUFFALO GOURD AND JOJOBA: POTENTIAL NEW CROPS FOR ARID LANDS

LeMoyne Hogan and William P. Bemis
I.
11.
111.
IV .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Buffalo Gourd: Cucurbitu foeridissirnu HBK .....................
Jojoba: Simmondsiu chinensis (Link) Schneider . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

317
319
332
346
347

PROTEIN TRANSFORMATION IN SOIL

Michael J . Loll and Jean-Marc Bollag
I.
I1.
111.
IV .
V.
VI .
VII .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Protein Sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Proteolytic Microorganisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Characteristics of Proteolytic Enzymes in Soils . . . . . . . . . . . . . . . . . . .
Environmental Factors Affecting Proteolysis .....................
Transformation and Binding of Protein in Soil ....................
Ecological and Agronomic Importance of Protein Transformation . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

352
352

354
361
364
370
376
377

APPLICATIONS OF INDUCED AND SPONTANEOUS MUTATION IN
RICE BREEDING AND GENETICS

J . Neil Rutger
I . Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
I1. Breeding Applications of Semidwarf Mutants . . . . . . . . . . . . . . . . . . . .
111. Breeding Applications of Early Maturity Mutants . . . . . . . . . . . . . . . . .
IV . Breeding Applications of Other Types of Mutants . . . . . . . . . . . . . . . . .
V . Genetic Applications of Mutants . . . . . . . . . . . ....................
VI . Future Uses of Mutation in Rice Improvement . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

383
385
396
399
404

408
410


X

CONTENTS

NITROGEN AVAILABILITY INDEXES FOR SUBMERGED RICE SOILS

K . L . Sahrawat
I.
I1.
111.
IV .

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Factors Affecting Mineralization of Organic Nitrogen . . . . . . . . . . . . . .
Biological Indexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Chemical Indexes ...........................................
V . Simple Models of Nitrogen-Supplying Capacity Based on Biological and
Chemical Indexes .........................................
VI . A Values . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VII . Electro-Ultrafiltration ........................................
VIII . Plant Analyses .............................................
IX . Nitrogen-Supplying Capacity and Fertilizer Recommendations . . . . . . .
X . Perspectives ...............................................
References ................................................

415
417
421
428

INDEX . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

453

435
439
441
442
443
445
447


CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors’ contributions begin

C. AZCON-AGUILAR (l), Unidad de Microbiologia, Estacibn Experimental
del Zaidin, Granuda, Spain
J. M. BAREA (l), Unidad de Microbiologia, Estacibn Experimental del Zaidin,
Granada, Spain
WILLIAM P. BEMIS (3 17), Plant Sciences Department, University of Arizona,
Tucson, Arizona 85721
E. B. A. BISDOM ( 5 3 , Netherlands Soil Survey Institute, 6700 AB Wageningen, The Netherlands
JEAN-MARC BOLLAG (35 1 ) , Department of Agronomy, Pennsylvania State
University, University Park, Pennsylvania I6802
C. M. DONALD (97), Waite Agricultural Research Institute, The University of
Adelaide, Glen Osmond, South Australia 5064
IAN B. EDWARDS (145), Pioneer Hi-Bred Institute, Inc., Glyndon, Minnesota
56547
KEITH W. T. GOULDING (215), Soils and Plant Nutrition Department,
Rothamsted Experimental Station, Harpenden, Herifordshire AL5 2JQ,

United Kingdom
J . HAMBLIN (97), Department of Agriculture, Geraldton District Office,
Marine Terrace, Geraldton, West Australia
KRITON K . HATZIOS (265), Department of Plant Pathology and Physiology,
Virginia Polytechnic Institute and State University, Blacksburg, Virginia
24061
LEMOYNE HOGAN (3 17), Plant Sciences Department, University of Arizona,
Tucson, Arizona 85721
MICHAEL J. LOLL (35 l), Department of Agronomy, Pennsylvania State University, University Park, Pennsylvania 16802
J . NEIL RUTGER (383), U.S. Department of Agriculture, Agricultural Research Service, and Department of Agronomy and Range Science, University
of California, Davis, California 95616
K. L. SAHRAWAT* (4 1 3 , Soil Science Department, ICRISAT, Patancheru
P. O., Andhra Pradesh 502324, India
S. S . VIRMANI ( 1 4 3 , International Rice Research Institute, Manila, Philippines

*Present address: Soil Science Department, University of Wisconsin, Madison, Wisconsin 53706

xi


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PREFACE
Two events occurred in the past year which have special significance for this
review publication. First, the American Society of Agronomy (ASA) celebrated
its 75th anniversary. The first 30 volumes of Advances in Agronomy were prepared under the auspices of this scientific society, and the remaining volumes
have been developed in cooperation with it. This long association has been most
fruitful for the series and has likewise been beneficial to the society. Most of the
articles, particularly in the early years, have been authored by ASA members.

An advisory committee chosen by the society has provided advice and guidance
from the first to the present volume.
The American Society of Agronomy has made great progress during the last
three-quarters of a century and is to be congratulated on its 75 years of service. It
has grown from the handful of dedicated soil and crop scientists, who met in
Chicago in 1907 to form the society, to a membership of more than 12,000 today.
It publishes four major research and education journals whose articles make up a
fair share of those reviewed in Advances in Agronomy. More than 20 major
monographs and 45 special publications have been published by the ASA.
The second event of the past year which has special significance to Advances
in Agronomy is a sad one. Dr. Geoffrey Norman, who was the founding editor
and who continued as editor for the first 20 volumes, passed away on November
14, 1982. Crop and soil scientists throughout the world owe a debt of gratitude to
Dr. Norman: He was not only a world-renowned soil microbiologist in his own
right, but also an intellectual leader who stimulated biological science in general.
We are pleased to publish a brief but meaningful tribute to him in this volume.
The articles in Volume 36 reflect the advice given to me by Dr. Norman when
1 became editor. They each focus on a timely topic of wide interest to agronomists. They are written by scientists and educators from seven countries, illustrating the growing internationality of crop and soil science. And they repregent
balance in subject matter among crops and soils and among basic and applied
research.
Advances in Agronomy continues to play a important role in keeping crop and
soil scientists abreast of major research findings around the world. We are all
challenged to maintain the energy and quality which so characterized Dr. Norman. The 15 scientists who prepared reviews for this volume have set excellent
examples for us to follow.
N. C. BRADY

...

Xlll

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IN MEMORIAM
ARTHURGEOFFREYNORMAN
1905-1982

A. G. Norman, who was the first editor of Advances in Agronomy, and who
continued in that capacity for a period of 20 years, died November 14, 1982,
after a distinguished career spanning more than half a century. In the Preface to
Volume 1, he wrote, “This volume, Advances in Agronomy, has as its objective
the survey and review of progress in agronomic research and practice. The
editors . . . will be guided in their choice more by what information may be of
use to agronomists than by what constitutes agronomy. The central theme must
be soil-crop relationships, for soils without crops are barren, and field crops
cannot be considered without reference to the soil on which they are produced.”
The broad range of subjects covered by Advances over the years and the status
which it has attained attest to the wisdom of this policy which he initiated. At the
close of his 20 years of editorial service for this publication, he wrote in the
preface to Volume 20, “Those who had a part in what seemed to be an uncertain
venture in 1948 can take some pride in its acceptance . . .” “In the next 20 years
one may confidently expect the accretion of new knowledge about the characteristics of soils and crop plants and of their interactions to proceed at an accelerating rate. These developments will find their way into later volumes and serve the
agronomists of the world in their great task of providing sufficient food for all
men.”
Dr. Norman’s capacity for well-organized expression, both in speaking and
writing, served the American Society of Agronomy well in other editorial
efforts. Shortly after World War I1 he initiated the Monographs Series of the
society and served as editor of the first six volumes. Other service to the society
included a term as President in 1957, a year in which its 50th Anniversary was

commemorated by an outstanding program in meetings at Atlanta, Georgia.
A. G. Norman was born in Birmingham, England in 1905. He received the
B.Sc. degree from the University of Birmingham in 1925 and the Ph.D. in
Biochemistry from the same institution in 1928. This was at a time when biochemistry was just emerging as a separate discipline. Dr. Norman’s training there
kindled a lifelong interest in plant biochemistry. From Birmingham, Norman
went to the Rothamsted Experimental Station, where he began biochemical and
microbiological studies on the decomposition of plant materials with special
emphasis on cell wall substances. He did some of the first quantitative work on
nitrogen transformations in the decomposition of plant materials, which has
xv


xvi

IN MEMORIAM

subsequently had a major impact on crop residue management in practical agriculture. He came to the United States in 1930 as a Rockefeller Fellow at the
University of Wisconsin, where he studied the microbiology of hemicelluloses
and the structure of some fungal polysaccharides. Returning to Rothamsted in
1932, he became head of the Biochemistry Section there in 1933.
In 1937 Dr. Norman moved to Iowa State College at Ames as Professor of
Soils, where he directed a broad-ranging research program dealing with microbial thermogenesis, biochemistry of the major plant constituents and their decomposition processes in soil, fundamental studies on the chemistry of soil
organic matter, and on carbon-nitrogen transformationsduring decomposition of
organic materials. His application of biochemical techniques to studies in soil
microbiology represented a significant departure from the older traditional techniques, which had their roots in medical bacteriology. Dr. Norman pioneered the
application of stable isotope techniques to soil research and was possibly the first
to use both "N- and I3C-labeled plant materials in decomposition studies. As
early as 1943 he published an article indicating the potential of stable tracer
technology in agronomic research. One of his significant early contributions was
the use of "N in greenhouse experiments to measure N2 fixation by legumes.

Field application of this type of methodology is now being made on a worldwide
scale.
During World War I1 Dr. Norman left the Iowa State campus to serve with the
Chemical Corps for 2 years, directing a research program at Camp Detrick,
Maryland. After a brief return to Iowa State, he left late in 1946 to accept a
civilian position with the Chemical Corps dealing with basic studies on plant
growth regulators and inhibitors. In 1952 he went to the University of Michigan
as Professor of Botany and director of a research project in plant nutrition and
root physiology as part of a university program promoting the use of radiation
and radionuclides in the biological sciences. During this period he became much
interested in rhizosphere microorganisms and in metabolic products which, when
excreted, modified root growth and root physiology. Working with a number of
graduate and postdoctoral students, he developed a research program concerned
also with geotropic responses, factors limiting microbial activities in soils, influence of organisms on nutrient uptake, and artificial microbial environments.
Other responsibilities at the University of Michigan included Directorship of the
Botanical Gardens, a facility providing support for instruction and research in
several university departments. In 1964 he was appointed Vice President for
Research at the University of Michigan, in which capacity he continued to serve
until his retirement. During 1963-1964 he was a Staff Advisor to the National
Academy of Sciences, being involved, among other things, with initial organization of U.S. participation in the International Biological Program. From 1965 to
1969 he was Chairman of the Division of Biology in Agriculture of the National
Research Council.


IN MEMORIAM

xvii

One of Dr. Norman’s significant contributions to the field of agronomy was
through the students who came under his direction. His clear, well-organized

lectures and his precise and articulate expression had a lasting influence upon his
students. His insistence on clear and concise writing made a valuable contribution to the training of those who took his classes.
A. G. Norman was that rare combination of brilliant research scientist, stimulating and effective teacher, and superbly organized and efficient administrator.
Advances in Agronomy salutes the memory of a man who not only served this
publication well as its editor for 20 years, but who in addition brought great
credit to himself and to his profession.

FRANCES
BROADBENT


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ADVANCES IN AGRONOMY. VOL. 36

MYCORRHIZAS AND THEIR
SIGNIFICANCE IN NODULATING
NITROGEN-FIXING PLANTS
J. M. Barea and C. Azcon-Aguilar
Unidad de Microbiologia, Estaci6n Experimental del Zaidin
Granada, Spain

I. Introduction
............................................
A. Root Microorganisms in the Ecosystem
......................
B. Mycorrhizas and Root Nodules. . . . . . . . . . . . . . . .

............................................

11. Mycorrhizas .
A. General ...................................
B. Physiology of Mycorrhizas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
C. Factors Affecting Mycorrhiza Establishment, Development,
and Function.. . . . . . . . . . . . .
D. Applications of Mycorrhizal P
......................
Horticulture, and Forestry . . .
111. Mycorrhizas' in Legumes . . . . . . . . . . . . . . . . . . . . . . . . . .
A. Introduction ......................................................
B. Occurrence . .
..............
......................
C. Interactions be
cies of Rhizobiu
and Legumes.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
D. Interactions between Added Fertilizers and Myconhizas in
Legume-Rhizobium sp. Systems. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
E. Ecological Significance of Vesicular-Arbuscular Mycorrhizas in Legumes. . ,
F. Practical Field Application of Mycorrhizal Effects on Legume Production
IV. Mycorrhizas in Nodulating Nitrogen-Fixing Nonlegume Plants . . . . . . . . . . . . . . . . ,
A. Occurrence and Distribution ........................................
ical Features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
V.

Conclusions

............................................
......................

1
1
3
4
4
4
10
15
19
23
23
24
25
31
37
41
44
44

44
45
45
46

1. INTRODUCTION
A. ROOT MICROORGANISMS
IN THE

ECOSYSTEM

Microorganisms, which are known to play vital roles in physiological processes in the ecosystem, are invariably present in the root region, the rhi1

Copyright 8 by Academic F'ress, Inc.
All righu of reproduction in any form reserved.
ISBN 0-12600736-3


2

J. M. BAREA AND C. AZC6N-AGUILAR

zosphere, of plants growing in soil. Actually, rhizosphere bacteria (including
actinomycetes) and fungi carry out a range of activities (e.g., the breakdown of
organic matter, nitrogen fixation, secretion of growth substances, increase of the
availability of mineral nutrients, and immobilization of those assimilable) of
great relevance to plant growth; they also cause plant disease or protect the plant
from pathogens. The extent of microbial activity depends, in most cases, on the
supply of organic substrates from the root. Hence, the abundance and activity of
soil microorganisms in general diminish with increasing distance from the root
(Newman, 1979).
From the point of view of their relationships with the plant, microorganisms
can be classified into three groups: (1) saprophytes, usually opportunists but
benefactors in some situations; (2) parasitic syrnbionts or pathogens, potentially
harmful to the plant; and (3) mutualistic symbionts, usually called symbionts in
the literature, which develop activities beneficial to plant growth (for reviews,
see Brown, 1975; Dommergues, 1978; Newman, 1979).
It is widely assumed that one of the most beneficial contributions of soil
microorganisms to plant development is the supply of nutrients essential to plant
growth, particularly those involved in nitrogen (N) and phosphorus (P) cycling.
Among these, the organisms concerned with N fixation and the enhancement of

P uptake by the plant are especially relevant. As it is well known, N and P are
two major elements in plant nutrition that commonly limit plant growth; thus,
they are usually added to soil as industrial fertilizers. However, in addition to the
energy-intensive technology, implied in the synthesis of chemical fertilizers,
most of these compounds are lost when they are added to the soil because they
are not readily used by the plant. Actually, no more than 30% of the N fertilizer
(Postgate and Hill, 1979) and only about 25% of the P fertilizer (Hayman,
1975a) are taken up by the crop in the year of its application. The rest of the N is
lost either in the soil water, causing pollution problems (Bolin and Arrhenius,
1977), or to the atmosphere as a result of denitrification; most of the P fertilizer
added is quickly fixed by some soil components and converted into forms which
are not readily available to plants.
Consequently, N fixation, which cycles N to the biosphere from the atmosphere, is an important factor in biological productivity; it is accepted that more
than 60% of the N input to the plant community through fixation has a biological
origin (Postgate and Hill, 1979; Brill, 1979). The activities of the N-fixing
bacteria either convert N into bacterial proteins (in free-living systems) or make
it directly available to plants as NH, in symbiotic associations which occur in
root nodules.
Many common soil microorganisms can release soluble phosphate from sparingly soluble inorganic and/or organic phosphates known to occur in soil. Several problems inherent with the lack of energy sources in the rhizosphere, micro-


MYCORRHIZAS IN NODULATING N-FIXING PLANTS

3

bial antangonism, difficulties in the translocation of the phosphate ions to the
absorption places at root surface, and other factors make the microbial solubilization of phosphates a minor contribution to the P nutrition of plants (Hayman,
1975a). However, mycorrhizas, mutualistic symbioses between plant roots and
certain soil fungi, play an unquestionable role in P cycling and in the uptake of
phosphate by the plant. Because the known world reserves of P could be depleted

in a few decades (Rhodes, 1980), the contribution of this symbiosis to the
reduction of fertilizer requirements is of increasing interest.
B. MYCORRHUAS
AND ROOT NODULES

All but a few vascular plants are able to form mycorrhizas. Under natural
circumstances, the mycorrhizal condition is the norm for most of the higher
plants. The mycorrhizal fungus has an ecologically protected niche inside the
plant root; the products of photosynthesis arrive here, furnishing abundant energetic substrate for the fungi which by means of their network of hyphae or
mycelial strands extend the mycelium to the surrounding soil, take up nutrients
(mainly phosphate) from the soil solution, and translocate these ions to the host
plant (Tinker, 1975; Hayman, 1978). Mycorrhizas therefore have a worldwide
recognized value for plant survival and nutrient cycling in the ecosystem. They
contribute significantly to plant productivity both in arable and in plantation
crops. Several types of mycorrhizas occur; their characteristics will be described
later.
Three different types of microorganisms (bacteria) are able to induce nodules
on roots of higher plants and to inhabit them by establishing mutualistic symbioses. As a consequence of these associations, the microsymbionts are able to
fix N. The energy requirements for these processes are satisfied by the photosynthate which is directly received by the bacteria at the plant roots (Hardy and
Havelka, 1976). The microorganism exports NH4+ to the plant, avoiding transport and dispersal problems. The bacterial genera and the corresponding host
plants involved are (1) Rhizobium, which nodulates, with one exception, on
legume roots; (2) Frunkiu, actinomycetes that fix N in nodules they form on
nonlegume, often woody, angiosperms; and (3) Nosfoc and Anubuenu,
cyanobacteria (formerly blue-green algae), which form N-fixing nodules on the
roots of plants of the family Cycadaceae (gymnosperms). Legume-Rhizobium
sp. associations are the most important for the incorporation of N into pasture
and agricultural ecosystems, whereas the nodulated angiosperms are similarly
important in forest ecosystems.
Plants bearing N-fixing nodules are usually mycorrhizal when grown in soil.
This fact has great ecological relevance because nodulation and nitrogen fixation

depend on a balanced mineral nutrition of the host plant (in particular, plants


4

J.

M.BAREA AND C. AZC6N-AGUILAR

have high phosphate requirements), and the mycorrhiza can satisfy these demands. Thus, mycorrhizal fungi not only help the plant itself but also aid the
bacterial symbiont to fix N in the nodular tissues. Nodulate and mycorrhizal
plants are therefore adapted to cope with nutrient-deficient situations (Harley,
1973).

The intent of this article is the comprehensive study of the role of mycorrhizas
in the growth and nutrition of N-fixing nodulated plants. As an introduction for a
better understanding of mycorrhizal effects, we will present a brief review of
some general, well-established principles on mycorrhizal types, morphology,
physiology, and function. Current information will be condensed to achieve an
up-to-date presentation of this sllbject and to create a conceptual background for
nonspecialist readers. This will constitute a quantitatively and qualitatively
important part of the article. Then, the interactions between nodular and mycorrhizal endophytes related to the formation and effects of these dual symbioses,
which greatly enhance the development of the common host plant, will be
discussed. This part of the article will be concerned not only with conceptual
principles but also with the rationally stated hypotheses and the current trends in
basic and applied research on this subject. Attention will be given to the ecological significance of plants bearing the two types of symbioses, with emphasis on
the possibilities of harnessing them to increase crop yield.

II. MYCORRHIZAS
A. GENERAL

The previous statements on the concept and function of mycorrhizas, although
concise, may allow us to envisage these widespread associations as the most
metabolically active parts of the absorbing organs of almost all land plants. Both
the autotrophic host plant and the heterotrophic fungal associate derive, in most
cases, physiological and ecological benefits from one another. Furthermore, the
“mycorrhiza-dependent’’ plants cannot develop adequately without their mycorrhizal partner. However, the general term mycorrhiza, broadly considered, is of
little significance. The taxonomic diversity in the fungi and plants involved and
the differences in the morphological, structural, and nutritional features of mycorrhizal associations require a subdivision to reflect the different physiological
relationships that are now recognized.


MYCORRHIZAS IN NODULATING N-FIXING PLANTS

5

I . Mycorrhizal Types and Their Structural
and Nutritional Features
Five types of mycorrhizas can be recognized. These and the main groups of
host plants on whose roots they are formed are recorded in Table I, as summarized from Smith (1980) and Azc6n-Aguilar and Barea (1980). The first type,
ectotrophic mycorrhizas (ECM),is characterized by a lack of intracellular penetration of the fungus into the cortical cells of the root. A network of fungal
mycelia, the Hartig net, is formed by hyphal growth among the host cells. This in
turn establishs a close contact between fungus and root-cell plasmalemma, which
is critical for nutrient exchange in mycorrhizal associations. In most cases the
fungus will develop a mantle or sheath of interwoven hyphae growing around the
feeder roots. The fungal mantle is extended some distance into the surrounding
soil by mycelial strands or rhizomorphs (only rarely by extramatrical hyphae)
(Harley, 1978). The fungi involved are mostly higher basidiomycetes (Boletus,
Suillus, Amanita, Lactarius, Tricholoma, Pisolithus, Scleroderma, Rhizopogon,
etc.), some ascomycetes (Tuber), and zygomycetes (Mam and Krupa, 1978).

The second group, vesicular-arbuscular mycorrhizas (VAM), is by far the
most widespread type of mycorrhiza. The nomenclature refers to the formation
of vesicles and arbuscules, typical morphological structures that will be considered later. As with ericoid, arbutoid, and orchidaceous mycorrhizas, the VA
fungus penetrates into the cortical host cells, but the invading mycelium usually
lives only a short time intracellularly (Smith, 1980); lysis of intracellular struc-

Table I
Mycorrhizal Types and the Main Groups of Host Plants Involved
Nomenclature
Traditional

Actual

Ectotrophic

Ectotrophic or
sheathing

Endotrophic

Vesicular-arbuscular

Ericoid
Arbutoid
Orchidaceous

Typical host plants
Pinaceae, Fagaceae, Betulaceae,*Eucalyptus,
Rosaceae,a Leguminosae" (woody),
Cupressaceae

Four-fifths of all land plants including agronomically important crops such as woody and
herbaceous legumes" (pasture, forage, and
grain) and Gramineae
Calluna, Vaccinium, Erica, Epacris
Arbutus, Monotropa
Orchidaceae

"Groups of plants also bearing nitrogen-fixing root nodules.


6

J. M. BAREA AND

c. AZCON-AGUILAR

tures (the arbuscules in VAM) then occurs, but the host cell survives and can be
colonized again by the fungus. Vesicular-arbuscular fungi do not form sheaths
around the root, but a network of extramatrical hyphae usually develops. This
grows into the soil and can extend the mycelium several centimeters beyond the
root surface. The total hyphal length can reach more than 1 m of hyphae per
centimeter of infected root (see Smith, 1980; Hayman, 1982). These VA fungi
are members of the family Endogonaceae that are placed in the genera Glomus,
Sclerocystis, Gigaspora, and Acaulospora (Gerdemann and Trappe, 1974). Because they cannot be successfully subcultured axenically, they must be considered ecologically obligate symbionts (i.e., they do not complete their life cycle
unless they can colonize a suitable host plant) (Lewis, 1973).
An ascomycete (Pezizella ericae) has proved to be a fungal partner of the third
type of mycorrhiza, namely, the ericoid, which occurs on roots of some autotrophic shrubs in the families Ericaceae, Epacridaceae, and Empetraceae (Read
and Stribley, 1975; Read, 1983). Intracellular coils and extramatrical hyphae are
typical structures of these mycorrhizas.
The structure of arbutoid mycorrhizas, the fourth type, is characterized by the

formation of a sheath but not a Hartig net, and they also form intracellular
haustoria. Their nutritional features are not yet fully understood.
Confined to the family Orchidaceae, the fifth group of mycorrhizas shows
unique characteristics; they infect protocorms and rhizomes, but rarely the terrestrial roots. Their hosts are temporarily or permanently achlorophyllic, and the
mycorrhizal fungi (Rhizoctonia spp. and Armillaria melea), which are pathogens
for nonorchidaceous hosts, aid the heterotrophic orchid in assimilation of carbohydrates, probably from a simultaneous association with another true autotrophic
host plant (Mosse, 1978).
The major types of mycorrhizas and the groups of plants on which they occur
having been described, the discussion may now be limited to ECM and VAM,
the only mycorrhizal types formed on plant families also bearing N-fixing root
nodules (Table I). Emphasis will be placed on VA mycorrhizas because these are
the commonest type occurring on nodulated plants and also because these mycorrhizas, as deduced from their near omnipresence, play an integral role in most
crop-production systems.
2 . Occurrence and Distribution
Mycorrhizas, mainly VAM, can be found in most plant species growing in
most plant habitats under tropical, temperate, and even arctic conditions (Hayman, 1982). To understand the worldwide distribution and ecological implications of this symbiosis, it is interesting to go back 400 million years and consider
the role played by a fairly similar mutualistic association-the “ancestral mycorrhiza”-in the evolution of terrestrial plants (Pirozynski and Malloch, 1975). As