Table Of ContentB.A.PYEHH · E.B.APUHXOBCKAS!
EMOXMMMfl
H ΦΜ3ΜΟϋΟΓΜΑ
MMMYHMTETA
PACTEHMM
Biochemistry and
Physiology of
Plant Immunity
BY
B.A.RUBIN
and
Ye.V.ARTSIKHOVSKAYA
TRANSLATED FROM THE RUSSIAN BY
HELEN WAREING
TRANSLATION EDITED BY
ELLIS GRIFFITHS
Lecturer in Agricultural Botany
University College of Wales
Aberystwyth
PERGAMON PRESS
OXFORD · LONDON · NEW YORK · PARIS
1963
PERGAMON PRESS LTD.
Headington Hill Hall, Oxford
4 & 5 Fitzroy Square, London W. 1
PERGAMON PRESS INC.
122 East 55th Street, New York 22, N. Y.
GAUTH1ER-VILLARS ED.
55 Quai des Grands-Augustins, Paris 6e
PERGAMON PRESS G.m.b.H.
Kaiserstrasse 75, Frankfurt am Main
Distributed in the Western Hemisphere by
THE MACMILLAN COMPANY NEW YORK
pursuant to a special arrangement with
Pergamon Press Limited
Copyright © 1963
PERGAMON PRESS LTD.
Library of Congress Catalog Card Number 63-10063
This book is translated from
Biokhimiya i Fiziologiya Jmmumteta Rastenii
by B.A.Rubin and Ye. V. Artsikhovskaya,
published by Izdatel'stvo Akademii Nauk SSSR
Moscow 1960
Made in Great Britain
FOREWORD TO THE ENGLISH EDITION
WE are pleased that with the publication of the English edition of
our book the circle of its readers will be considerably extended. While
working on the preparation of this monograph we realized clearly that
many important problems of physiology and biochemistry of plant
immunity were far from being finally solved, and that they required
further efforts on the part of scientists of various specialities
We would be deeply satisfied if our modest work stimulated in
biologists an interest in the problem of immunity and contributed
to experimental development and lively discussion of questions re-
lated to this problem. Only in such conditions could new scientific
facts be obtained, valuable both from the theoretical point of view,
and in relation to their utilization in the practical struggle for the
healthy plant.
B.A.RUBIN
Ye. V. ARTSIKHOVSKAYA
PREFACE
THE problems of plant immunity include a wide range of problems of
primary importance both for theoretical biology and for practical
agriculture. This explains the great attention paid to immunity by
biologists of all specialities. From the biochemical point of view the
special features of metabolism peculiar to host-plant and pathogenic
micro-organisms and of deviations in metabolism which occur during
the interaction of these partners, are of great interest.
The overall results of studies carried out on this problem leave no
doubt that it is the character of these modifications which determines
the degree of resistance or susceptibility of the green plant. From this
point of view it is becoming increasingly clear that immunity is an
adaptive characteristic, the formation of which is connected with the
long co-existence of autotrophic plants and pathogenic micro-
organisms. In other words, immunity is an expression of the character
of reaction peculiar to a higher plant to an intrusion into its life by a
specific heterotrophic organism. From this it also follows that the
development of resistance in green plants, and also of pathogenicity
in micro-organisms has taken place in the process of evolution under
the constant directing and controlling mutual influence of the partners,
and of the conditions of the environment in which their interaction
took place. Only with the acceptance of this point of view it is possible
to understand the causes of the relative and variable level of resistance
of plants, and to understand the importance of nutritional character-
istics of micro-organisms and of many other features distinguishing
the immunity phenomena in the plant world from animal immunity.
The first attempt to bring together all available material on these
questions was undertaken by the authors in 1948. In the intervening
time a great many investigations have been carried out on the bio-
chemistry and physiology of immunity, both in Soviet laboratories
and abroad. Many of them were only rendered possible by the ex-
viii
PREFACE IX
ceptional advances made during this period in the fields of bio-
chemistry and plant physiology.
In our book we have tried to summarize the results of numerous
investigations in the field of biochemistry and physiology of plant
immunity and in related fields. For this purpose we have made full
use of the materials obtained by the Biochemistry Laboratory of
Plant Immunity at the Bakh Biochemical Institute of the Acedemy of
Sciences of the USSR.
All comments on the book will be gratefully received by us.
CHAPTER 1
THE EVOLUTION OF PARASITISM
ONE of the main distinguishing characteristics of phytopathogenic
organisms is that they are all heterotrophs, i.e. organisms whose nor-
mal vital activity is only possible when a supply of ready made organic
food substances is present in their environment.
The available data of modern biochemistry and physiology, cos-
mogony and palaeontology leave no doubt that heterotrophy emerged
in the very first stages of the appearance of life on our planet and is a
characteristic possessed by the first representatives of the organic
world. The theory of A. I. Oparin, which has now received universal
recognition, is based precisely on this idea. It is also universally accept-
ed that the whole complex process of the evolution of life on the Earth
is bound with successive changes and further development of the
original, heterotrophic form of nutrition. The result of this develop-
ment is shown by the exceptional heterogeneity of living creatures and
their infinite variety which is based on different methods of nutrition
peculiar to individual representatives.
Parasitic micro-organisms which are the causative agents of various
diseases of higher plants are characterised by a specific type of nutri-
tion. This group of organisms must naturally possess a number of
characteristics, the correct understanding of which is only possible
when the general natural laws of evolution of heterotrophy and the
interrelation between this method of nutrition and autotrophic
nutrition are taken into account. On the basis of Oparin's theory of
the origin of life (Oparin, 1957) we consider that the evolution of
primary heterotrophic organisms, which fed on organic substances
formed abiogenetically (i.e. as a result of purely chemical reactions),
proceeded in different directions. One of these led to the emergence of
autotrophic organisms, the normal existence of which does not de-
pend on the utilization of ready made organic material. As in other
1
2 BIOCHEMISTRY AND PHYSIOLOGY OF PLANT IMMUNITY
cases, the emergence of a new function i.e. autotrophicity, did not
result in a loss by the organisms of the ability to feed on these ready
made organic substances. The ability was retained to a greater or
lesser degree and can be observed under certain conditions in an
overwhelming majority of present day autotrophs. Moreover, the
very concept of autotrophicity must be recognized as being conditional,
insofar as for the development of a number of organisms, capable of
utilizing the carbon from carbon dioxide, it is essential to have present
the ready-made molecules of certain vitamins. The latter are used in the
construction of corresponding enzyme systems. On the other hand,
many organisms, heterotrophic as regards their carbon nutrition,
are able to synthesize enormous quantities of vitamins and other
physiologically active substances required by a number of autotrophs.
It is clear from this example, that in some respects heterotrophy and
autotrophy are not absolute and that it is not always possible to draw
a line between the two.
In the process of evolution, heterotrophy as such has also undergone
complex changes. As has already been pointed out, the primary
forms of living things which evolved at a certain stage of development
of inorganic matter, belonged, by virtue of their type of nutrition, to
heterotrophs. In the course of further evolution, the primary hetero-
trophs must have evolved the capacity for utilizing organic substances,
the products of the vital activities of other heterotrophs, and later
still, the products of the vital activities of autotrophs also. It is most
probable that in the first stages, this capacity was limited to the utiliz-
ation of only the dead remains of other organisms and that only in the
course of the development and perfecting of this ability, did these
organisms become capable of utilizing the contents of living cells and
tissues. In other words, this function had to be converted into an
ability to utilize directly the products of vital activity of other living
organisms. The process of perfecting the methods of nutrition, at the
expense of substances of biological origin, must have reached a
qualitatively new state, after the emergence of autotrophic organisms.
There is every reason to believe that the various pathways of the
evolutionary development of the primary forms of life also included
primary forms of parasitism.
It is generally known that the most powerful factors forming the
properties of living organisms are the properties and characteristics of
those organisms with which they are in constant interaction. There-
THE EVOLUTION OF PARASITISM 3
fore, inextricably bound with the processes of evolution of the charac-
teristics of parasitism, there must have evolved and developed in
nature characteristics of resistance, ensuring for these organisms the
ability to remove or reduce the harmful effects of intrusion. It is not
necessary to prove that only those forms of living things whose tissues
were less accessible to other organisms, than substances formed abio-
genetically or contained in dead tissues, had the ability to survive
and evolve further.
As the means of attack became perfected, so also did the means of
defence. The evolution of characteristics ensuring strong aggressive-
ness of parasitic organisms had to be coupled with the perfecting of
protective devices of the autotrophs — resulting in their resistance to
attack.
In this connection it is difficult to accept as correct the views pre-
vailing at the present time which postulate that the ancestors of modern
parasitic organisms could only be those organisms which were charac-
terized by an independent way of life. There is no doubt that the con-
cept of the general line of evolutionary development from hetero-
trophic to autotrophic nutrition does not exclude the possibility that
in individual cases this development could be followed by the loss of
the ability of independent nutrition by certain autotrophic organisms,
e.g. in flower parasites. The pathway of development of heterotrophic
organisms from autotrophs and including the transition to parasitism
from an independent way of life, cannot however be regarded as the
only one; nor does it exclude the genetical connection of parasitic
organisms with heterotrophs, evolved during the first stages of evol-
ution.
The co-existence of different species and types of living things is
inevitably bound with the development in them of characteristics of
mutual adaptability expressed in an infinite diversity of forms. Ac-
cording to the nature of the effect which individual organisms have on
each other, relations between them are divided into two main groups —
symbiotic and antagonistic. These types of contrasting interactions,
have at the same time some common features. In both cases the
characteristic feature is the mutual adaptation of metabolism, reach-
ing in some cases a high degree of perfection. The examples of sym-
biosis and parasitism show particularly clearly the importance of the
interaction of organisms involving various vital characteristics of the
partners. Symbiotic relations, creating favourable conditions for each
4 BIOCHEMISTRY AND PHYSIOLOGY OF PLANT IMMUNITY
of the participating organisms may involve the greater or lesser
specialization of a wide range of processes or functions peculiar to the
partners. The most perfect forms of symbiosis are those where, as a
result of co-existence, a single "organism" is evolved, possessing a
common body and common metabolism. An example of such sym-
biosis is a lichen, an organism consisting of an alga and a fungus which
have completely lost their capacity for independent existence.
Many symbionts are also known which have a stimulating effect on
each other, but are yet capable of independent development. To this
group of symbiotic phenomena for example, belong the associations
of plants with soil micro-organisms — which play an important role in
the nutrition of higher plants (mycorrhiza, rhizobia). Soil organisms
convert phosphates, calcium, iron salts and other mineral compounds
into a soluble form (Stoclasa, 1924). As has been shown by Khu-
dyakov (1955), soil micro-organisms assimilate considerably more
nutrient substances than is required for their own nutrition. This ex-
cess amour t of mineral and organic substances can be passed along a
chain of cells to the roots of plants, over a distance of 300-400 mm.
A considerable number of investigations have been devoted to the
role of mycorrhiza in supplying higher plants with mineral substances,
in particular with phosphorus (see for example, Gerretsen, 1949;
Harley and McCreagy, 1952; Harley and Brierly, 1954). The metabolic
products of the rhizosphere organisms, i.e. vitamins, auxins, antibiotics
etc., are also of great importance in the development of higher plants. In
their turn, the root secretions of plants have a stimulating and selective
action on the associations of soil micro-organisms — e.g. roots secrete
carbon dioxide and various mineral and organic substances. An ex-
tensive review of the literature on this question is given in the report
by Krasil'nikov (1958).
Roots have also been shown to secrete enzymes (Kuprevich, 1949).
Krasil'nikov (1952b) demonstrated that the roots of peas, maize and
wheat secrete amylase and invertase. Phosphatase was also discovered
in root secretions of maize and sunflower (Ratner and Samoilova,
1955) and ß-glucosidase and ß-galactosidase in wheat, cucumbers,
maize, barley, flax and peas (Stenlid, 1957).
Although higher plants are autotrophic, the assimilation of mineral
salts and physiologically active substances with the aid of soil micro-
organisms can stimulate plant development considerably. In some
cases the adaptation of plants to mycotrophic nutrition is so great,
