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Mycol. Res.

92 (2); 129-139 (1989)

129

Prinled in Greal Brilain

THE FOURTH BENEFACTORS' LECTURE

The significance of mycorrhiza

J. 1. HARLEY
The Orchard, Old Marston, Oxford OX3 OPQ

The Fourth Benefactors' Lecture: The significance of mycorrhiza. Mycological Research 92 (2): 129-139 (1989).
This lecture reviews important aspects of the physiology of common kinds of mycorrhiza and considers their relevance to the
ecological importance of these symbioses.
Key words: Mycorrhiza, Mutualism, Nutrition, Ecosystems. Nutrient cycling.

I am extremely honoured to be asked to give the Benefactors'


Lecture on a subject akin to the mineral absorption and
nutrition of fungi. It was inevitable that I should choose the
subject of mycorrhiza which has been an interest of mine for
a long time.
The subject is one in which speculative hypotheses have
been almost inextricably linked with experimentally verified
conclusions, so that one is constantly amazed at the accounts
of it that are published in general mycological works, even in
some of high reputation. Since some knowledge of the
biological significance of mycorrhizal associations is essential
to the interpretation of the ecological behaviour of higher
plants and of fungi, I am going to try to give a general
account. shorn of much detail and without detailed references,
but emphasizing functional aspects of a few of the important
kinds.

TOWARDS A DEFINITION OF
MYCORRHIZA
It is difficult to give a succinct definition of mycorrhiza

because, as we all know, the surface and environs of roots are


inhabitated by populations of micro-organisms, most of which
are, so to speak, commensal rather than symbiotic with the
roots. These rhizosphere and root-surface organisms by their
position and activity alter, by increase, decrease or change of
form, the availability of nutrients to their host and to one
another. Moreover, by competition or antibioisis they may
decrease disease incidence, or, by other means, increase or
cause it.
Amongst these populations certain species of fungi are
present quite consistently on the root surfaces or in the tissues
or cells of the roots of many species of plant, so that dual
organs of consistent morphological and histological paHerns

are formed. These are the mycorrhizas and they conform to a


number of common kinds the world over, and in them the
fungus and the host co-exist in a physiologically, ecologically and reproductively active state for long periods, a state
called mutualistic symbiosis. Just as other micro-organisms of
the root region may affect the supply of nutrients to the roots
or prevent pathogenesis by other organisms, so may also the
mycorrhizal fungi. Table 1 summarizes the characteristics of
the common kinds of mycorrhiza, but of these I shall only
discuss a few in detaiL namely the ectomycorrhizas, the
vesicular-arbuscular mycorrhizas and the ericoid mycorrhizas.

MYCORRHIZA IN THE PLANT KINGDOM


AND AMONGST THE FUNGI
The majority of higher green plants and large numbers of
species of fungi are involved in mycorrhiza formation. We
found (Harley & Harley, 1987) that, in the British flora, 80%
of the species of angiosperms, 100 %of the gymnosperms and
70 % of the pteridophytes were potentially mycorrhizal. That
is, they may develop one or more kind of mycorrhiza in some
circumstances. The figures in Table 2 were abstracted from our
paper by Moore (1987). Although they are of interest in
themselves I felt obliged to add the last column, because crude
numerical statistics give no estimate of constancy or intensity
of fungal colonization. Other compilations of a similar sort
usually stop at families or genera, e.g. Newman & Reddell
(1987), but they express the same point; mycorrhizal
colonization is more common than its absence in higher green
plants.
The fungal species concerned with mycorrhiza belong to all
the larger taxonomic divisions. About eight genera and more
than 100 species of Endogonaceae amongst the Zygomycetes
are mycorrhizal. At least 20 genera comprising several
10-2

The Fourth Benefactors' Lecture

130

Table 1. Characteristics of important kinds of mycorrhizas in their mature state


Kinds of mycorrhiza
Vesiculararbuscular

Character
Fungi
Septate
Aseptate
Hyphae enter cells
Fungal sheath present
Hartig net formed
Hyphal coils in cells
Haustoria
Dichotomous
Not dichotomous
Vesicles in cells or tissues
Achlorophylly
Fungal taxon

Host taxon

)=

+
+

Ectomycorrhiza

Ectendomycorrhiza

Arbutoid
mycorrhiza

Monotropoid Ericoid
mycorrhiza
mycorrhiza

Orchid
mycorrhiza

+
(+)

+
+ or +
+

+
+
+
+

+
+
+

+
+

+
+

+ or -

+
+ or (-)
- or (+)
Phyco

Bryo
Pterido
Gymno
Angio

Basidio
Asco
Phyco
Deutero
Gymno
Angio
(Pterido)

Basidio
Asco?

Gymno
Angio

- or (+)
Basidio

Ericales

+'

+
Basidio

Asco
(Basidio)
Deutero

Basidio

Monotropaceae

Ericales

Orchidaceae

rare. 'All are achlorophyllous when young but may develop chlorophyll later.

hundred species of Ascomycetes mainly Pezizales, but also


Helotiales and Elaphomycetales, form ectomycorrhiza with
gymnospermous and angiospermous trees; at least one species
of Helotiales (Hymenoscyphus) forms mycorrhiza with
Ericaceae. Of the Basidiomycetes, 5000 or more species of
many genera of both Hymenomycetes and Gasteromycetes
are involved in ecto- and ectendomycorrhiza of angiosperms
and gymnosperms. Of the imperfect fungi, many reproductively sterile fungi, which may often be basidiomycetous
or ascomycetous, have been shown to form ectomycorrhiza,
as has Cenococcum geophilum which is very common and
widespread on many hosts; and Oidiodendron griseum has been
reported to form ericoid mycorrhiza (Couture et al., 1983;
Burgeft, 1961).
Non-pathogenic symbiosis, akin to mycorrhiza, is also very
common between bryophytes and fungi, and active research
on the subject is going on in this country and in France. In
addition, the lichens represent fungal associations, of a similar
kind, with algae. Although the fungal species involved with
them are said to comprise 300 genera and perhaps more than
13 000 species, the genera of algae are very few, probably less
than 10.
We are led to conclude that a majority of angiosperms,
gymnosperms and pteridophytes, numerous bryophytes and a
few species of algae associate with at least one quarter of the
known species of fungi in non-pathogenic or mutualistic
symbioses. Amongst these, mycorrhizas, although numerically
fewer than the lichens in respect of the fungi involved, are
very important to both green plants and fungi.

MUTUALISM AND THE CONCEPT OF


BENEFIT
In describing mutualism the great De Bary (1884) defined it as
'parasitism ... in which parasite and host mutually and
permanently further and support one another'. It seems to me
that his definition, which indicates simply a give and take
between symbionts which could be measured, is not as
objectionable as the derived term 'mutual benefit' for the
same relationship. 'Benefit' implies 'doing good' and we as
scientists don't deal in 'good' and 'evil' because we have no
measure of them. The practical objection to this form of
expression, however, arises especially in two contexts. First,
when comparisons are made between mycorrhizal and nonmycorrhizal plants of the same kind and measurements are
made of height, weight, etc. it is often concluded from the
results of such measurements that mycorrhizal colonization
does or does not 'benefit' the host. This form of expression
detracts emphasis or interest from what actually occurs and
has been measured, as well as equating 'benefit' with increase
in height or weight, etc. which is unjustified.
Secondly, many experimenters who aim to produce larger
crops by mycorrhizal infection, transfer in such expressions the
idea of benefit from the farmer or forester over to the plant.
At the same time, most of them do not measure the actual
crop, Le. the grain or timber production, but some increased
feature of the experimental plant which they equate mentally
with the crop and with a 'beneficial' effect of mycorrhiza.
I believe that we can only judge benefit to the host or to

131

J. L. Harley
Table 2. Mycorrhiza in the British flora

Family

Total
species

Mycorrhizal

Species
examined

% of species

(%)

examined

Ranunculaceae
'Cruciferae
'Caryophyllaceae
'Chenopodiaceae

45
98
83
34

56
40
49
44

96
46
30
53

Geraniaceae
Leguminosae
Rosaceae
Onagracae
Umbelliferae
Euphorbiaceae
'Polygonaceae
Salicaceae

20
87
87
21
70
18
41
34

50
47
54
49
56
51
79

90
90
96
100
79
100
38
100

25

84

100

20
16
34
63
8
14
24
160
41
39
15
53
107
173

75
50
47
49
88

100
100
75
90
100
78
92
96
100
63
100
100
31
87

Ericaceae
Primulaceae
Gentianaceae
Boraginaceae
Labiatae
Plantaginaceae
Campanulaceae
Rubiaceae
Compositae
Liliaceae
'Juncaceae
Iridaceae
Orchidaceae
'Cyperaceae
Gramineae

71

64

50
61
71
49
33
92
54
60

Note by J. L. H.

Not constantly present in any species


Species not consistently mycorrhizal
Not consistently present in any
species

Some spp. may be both edo and VA

Many spp. only slightly infeded


Both edo and VA mycorrhiza in
many spp.
Several kinds of mycorrhiza but ericoid
the commonest

VA in most spp.; edo in one


VA in most spp.; edo in one
Usually roots sparsely colonized

Usually roots sparsely colonized

Figures extraded by Moore (1987) from Harley & Harley (1987), relating to some major families.

the fungus by determining the selective advantage to them of


any traits or characters that we measure. That is very, very
difficult to do in any convincing way. Indirectly, we may
observe that the component organisms of a symbiosis are not
found away from their symbiotic companions. This applies to
most of the algae of lichens and to the lichen fungi, to most
of the fungi of mycorrhizas and some of their symbionts. In
such cases we could say that their way of life, their symbiosis,
seems to have given them a selective advantage, i.e. a survival
value. Dare we say 'has benefitted them'?

NUTRITION OF THE SYMBIONTS IN


MYCORRHIZAS
Early assumptions
It was assumed by Frank (1885) that mycorrhizal fungi were
supplied with carbon compounds by their hosts and that their
hyphae, which permeated the soil, especially into the humus,
aided the uptake of nutrients into both symbionts. Nitrogen
uptake was particularly stressed for the reason that the humic

soils of woodlands were deficient in nitrate, although


ammonium and organic nitrogen compounds were present.
These two assumptions have, as we shall see, survived the
test of time and they have been experimentally verified and
much elaborated over the years, in respect of mycorrhiza of
green plants. Much experimental work was at first concentrated on the ectomycorrhiza of forest trees. The importance
of mycorrhizas in the absorption of compounds of nitrogen,
phosphorus and potassium into these symbiotic systems was
verified by numerous experimenters of whom Hatch (1937)
was pre-eminent, but others, especially in the U.S.A. verified
his results. These observers stressed, amongst other features,
the importance of the hyphae in the soil as an extension of the
absorbing surface. Others reinforced this conclusion, but the
first direct demonstration of the importance of the fungal
hyphae in absorption and translocation of material to the host
was by Elias Melin and H. Nilsson, who published between
1950 and 1958 (see Harley, 1969, for references). They grew
pine seedlings in axenic conditions in a closed system in which
isotopically labelled nutrients, phosphate, ammonium, nitrate,
glutamate and cations such as sodium and calcium could be

The Fourth Benefactors' Lecture


fed to the hyphae, where they were absorbed and traced
through the hyphae to the host and to its leaves.
In similar experiments l4C02, fed to the leaves, was traced
to the hyphae as photosynthetic products were translocated
to them.
Over the years from 1920, Elias Melin and his colleagues
(see Melin, 1959; Norkrans, 1950) had isolated ectomycorrhizal fungi and shown that, as a group, they had very limited
powers of using complex carbon polymers, such as cellulose,
lignin and even pectins. Therefore this demonstration of the
translocation of l4C-labelled photosynthate to the fungus
went far to confirm the dependence of the fungi on their hosts
for carbon.
The absorption of substances by mycorrhizas from the soil
has been further studied in detaiL using tracers and other
modem methods enabling low concentrations related to those
expected in the soil to be used. It has been found that the
factors affecting uptake of nutrients are similar to those
affecting the absorbing mechanisms of all plants, viz:
temperature, concentration, availability of carbon substrate,
oxygen supply and metabolic inhibitors (see Harley, 1969).
There will therefore be no need for us to consider this matter
further.

Contact of mycorrhizas with the substrate


Most mycorrhizas possess a considerable hyphal connexion
with the soil as simple branching hyphae or as hyphal strands
which ramify in the substrate. (Those which do not have an
extensive hyphal system, may be smooth or possess short
setae or spines, and will be shortly considered later.) The
extensive hyphae were at first viewed as simple extensions of
the absorbing surface; but Sanders &; Tinker (1973) showed
that this is not the whole story. Following the work of Nye
(see Nye &; Tinker, 1977), it is clear that the concentration of
any poorly mobile nutrient in the soil will fall in the environs
of an absorbing surface, if its rate of absorption exceeds the
rate at which it diffuses or moves towards the surface. II: will
continue to fall till the rate of uptake is equalled by its rate of
replacement at the absorbing surface. In the extreme, a 'zero
sink' or deficiency zone will develop about the absorbing
surface, and then no physiological property of the living
system can increase the rate of uptake, which is entirely
dependent on the rate of movement of the substance through
the soil. The hyphae of mycorrhizal fungi serve to exploit a
wider volume of soil outside the deficiency zone and
translocate absorbed nutrients to the root.
Subsequent work, especially in P. B. Tinker's laboratory,
has served to show that the rates of translocation especially of
phosphate in the hyphae of vesicular-arbuscular mycorrhizal
fungi were great enough to accommodate the rate of inflow
into the root which had been observed. Indeed, the subject of
translocation of inorganic substances and carbohydrates in
mycorrhizal hyphae has been widely investigated, and the
kinds of substances and their rate of translocation have
confirmed that the hyphae are the essential vehicles for
transport of nutrients into and from the mycorrhizal roots (see
Harley &; Smith, 1983, for refs).
Although the hyphae of mycorrhizas serve to cross the

132

'zero sink' and exploit the soil further and wider, they will
also in time develop similar deficiency zones about themselves.
However, the provision of a new absorbing surface by the
growth of hyphae to contact a new soil zone is much less
expensive in material terms than the growth of a root.
As an example let us assume that the dry weight per unit
volume of roots and hyphae are similar and that the radius of
a hypha is 2 11m and of a root 200 11m. Then the surface areas
per unit volume (or weight) are

for a given length (L). Hence the surface area of the root per
unit volume (or weight) is 0.01 11m 2 and for a hypha 111m 2,
that is they differ by a factor of 100. On these assumptions,
and they are conservative, it takes 100 times as much material
to produce an equal surface area of exploitation by root
growth as by hyphal growth.
These points apply with some force to ions which are
required in quantity but which are relatively immobile in the
soil. Phosphate has a very low mobility and concentration in
the soil solution. Ammonium is ten times more mobile but
required in at least ten times greater quantity. These two ions
are then expected to be especially facilitated in uptake by
mycorrhizal infection. The mobility of potassium is rather
similar to that of ammonium but it is required in smaller
amount. Calcium is usually present in relative excess, and
nitrate, although required in great quantity if it is the main
source of nitrogen, is very mobile and present in good
quantity in eutrophic soil, but is replaced by ammonium in
acid soils with high phenolic content where bacterial action is
low. These latter ions then are not so affected in uptake by
mycorrhizal colonization of the roots as the first three. On the
other hand, trace elements such as copper and zinc have been
found to be more readily absorbed by mycorrhizal plants than
by non-mycorrhizal ones.
The mycorrhizas, usually ectomycorrhizas, with relatively
smooth surfaces (see Dominik 1956; Pachlewski, 1967; and
Harley &; Smith, 1983, for examples) are found in soils which
are unstable, such as the surface litter layers of forest. Here the
voids are large and the solids mobile under the action of soil
fauna, wind and rain. Drainage and movement of solution
over mycorrhizal and root surfaces may be rapid, so here zero
sinks do not readily form and extensive hyphal systems are
not so essential.

Quantity of fungal tissue involved


A few examples will suffice to give some idea of the very
significant amount of fungal tissue involved in mycorrhizal
symbiosis: these are given in Table 3.
From these estimates it is clear that in terms of weight alone
the fungal contribution to mycorrhizal symbioses is large. In
the case of ectomycorrhizas one should bear in mind that we
have to add to the sheath weight the outgoing hyphae and the
fruit bodies, all of which are in the dominant measure
maintained by photosynthetic carbon.

J. L. Harley

133

Table 3. Estimates of quantity of fungus in mycorrhizas


Mycorrhiza

Observation

Author

Ericaceae

42'4% of root volume


Hyphal connexions 2000 em-I

Read & Stribley (1975)

Vesicular-arbuscular

Edomycorrhiza

Hepper (1977)
Tinker (1978)
Bethenfalvay et al. (1982)
Tisdale & Oades (1979)

4-17% d.wt of organ


10% d.wt of organ
11 % d.wt of organ at onset of senescence
1'29-1'36 m of hyphae per em

Fungal sheath
39'10'5% d.wt (Fagus)
37'0 1'9% d.wt (Fagus)
34 % d.wt (Nothofagus)
20-30% d.wt (Pinus)

Carbon nutrition of mycorrhizal fungi


The results of Melin on the movement of photosynthates to
the fungus were confirmed by Nelson and his associates
(Nelson, 1964). They showed that there was a change of
pattern of translocation in mycorrhizal as compared with nonmycorrhizal pine seedlings (Table 4). In 12 h after photosynthesis of 14C02 had begun, 54% of the labelled products had
been translocated to the roots of mycorrhizal as compared
with 5 % to non-mycorrhizal plants. Allowing for the relative
sizes of the root systems, about four times as much was
translocated to the mycorrhizal root system.
Using excised mycorrhizas of Fagus it was possible to feed
the host tissue with [14 Clsucrose and show that it was
translocated to the fungal tissues where it accumulated in
quantities greater than remained in the host. In the fungus it
was converted to the fungal carbohydrates trehalose, mannitol
and glycogen - all substances not readily absorbed or used by
the root tissue. Glucose and fructose, although readily used by
both tissues, were not plentiful in the fungal layer. It was
suggested that the rapid conversion to fungal carbohydrates
constituted what has later been called 'a biochemical valve'.
This pattern of behaviour perceived by Lewis & Harley (1965)
has since been taken as a model which might explain
movement of carbohydrate from host to fungus in many kinds
of mycorrhiza, lichens and in certain pathogens (D. C. Smith
et al., 1969).
It is necessary to point out that the 'biochemical valve' may
well leak. In an experiment, Lewis & Harley (1965) applied an
external concentration of glucose to Fagus mycorrhizas so that
absorption via the sheath was studied (Table 5). From the high
external concentration of 27'8mM glucose, 24% of that
absorbed passed into the host. Stribley & Read (1975) made
a more direct test of leakiness by feeding the hyphae of ericoid
mycorrhiza with [14 C]glucose and showing that it would to a
degree pass into the host plant, and this has been confirmed
to apply to other ectomycorrhizas.
Although movement of carbohydrate from host to fungus
in vesicular-arbuscular mycorrhiza has been observed and
measured, the process seems less active than into ecto- or
ericoid mycorrhiza (Bevege et al., 1975). This may be because
there is less fungal tissue in them. However, specific fungal
carbohydrates do not seem to be so readily formed in them,

Harley & McCready (1952)


Brierley (1953)
Edmonds (unpub!.)
Melin & Nilsson (1958)

Table 4. Translocation in Pinus strobus

Mycorrhizal
Non-mycorrhizal

% in

%in

shoots

roots

46
95

54

% in roots
relative to wt

17.4
4.6

12h translocation in dark after 14C02 in light data of Nelson


(1964).

Table 5. Uptake of [14 Clglucose by Fagus mycorrhizas


Uptake
Sheath
Core
Total

2844
940
3784

Percentage of total
75'2
24'8
100

Concn = 27'8 mM, 20C, 23 h. Sheath and core separated after


uptake, CPM x 10- 1 (Harley & Lewis, 1965).

although recently Arnijee & Stribley (1987) have observed


small quantities of trehalose in some. The view has been
canvassed that either the plentiful lipids of these fungi play the
part of fungal carbohydrates in others, or that, perhaps more
likely, the carbohydrate is rapidly expended in growth and
respiration.
All these mechanisms of absorption of carbohydrates by
the fungi from the host involve phosphorylation for their
initiation, so we must therefore consider phosphate metabolism. However, before passing on to it we must realise that we
have no explanation as to why the roots of the green
symbiont release carbohydrate. Exudation of carbohydrate
occurs from all roots, but it is doubtfully enough to explain
the quantities moving here. The possible magnitude of these
quantities in ecological terms will be considered later.

Phosphate absorption and metabolism


The source of phosphate for mycorrhizas is inorganic
orthophosphate p~esent in the soil solution or readily released
from adsorption. In addition phosphatases capable ofhydrolysing phytates, which constitute a large fraction of the

The Fourth Benefactors' Lecture


phosphate of humic soils, are present on mycorrhizas,
especially ecto- and ericoid mycorrhizas. These enzymes are
many times more active than those on non-mycorrhizal roots
(Barlett & Lewis, 1973; Calleja et al., 1980; Williamson &
Alexander, 1975; Mitchell & Read, 1981). The bulk of these
enzymes is attached to the hyphal surface and their efficacy
depends in great measure on close contact with their substrate,
a point which has led some to query their importance; for if
fixed, their effect on insoluble and therefore immobile
phosphate would be minimal.
Absorption of phosphate results in a rapid conversion to
nucleotide and sugar phosphate, as in many plant materials,
followed by accumulation as inorganic orthophosphate,
organic phosphate and, in the case of mycorrhizal fungi as
polyphosphates (Ling Lee et aI., 1975; Harley & McCready,
1981; Strullu et al., 1982, 1986).
Study of ectomycorrhizas has shown that a large part of
phosphate absorbed from low concentrations, some 80-90 %,
accumulates in the fungus but a continuous 10-20% passes on
into the host. It is inorganic orthophosphate that passes into
the host but it has not passed through the main accumulations
in the fungus, but by a more direct route (Harley &
Loughman, 1963; Harley et al., 1954). The accumulation in the
sheath of Fagus can be utilized, when external phosphate is
unavailable, and translocated to the host by a metabolic
process dependent on oxygen supply and temperature (Harley
& Brierley, 1954, 1955).
The polyphosphates are found in the fungus both as
granules and as soluble polyphosphate (Loughman & Ratcliffe,
1984; Martin et al., 1983), but they were first identified in the
granular form by Strullu & Gourret (1973) and Ashford et al.
(1975). Granules form during phosphate absorption at a rate
roughly parallel to total phosphate absorption (Chilvers &
Harley, 1980), but although 30-40% of phosphate absorbed
from high external concentration of orthophosphate may be
converted to polyphosphates, it seems unlikely that more than
3-7'5 % of total phosphate in Fagus mycorrhizas is in the form
of polyphosphate granules, but in more soluble form.
The importance of the polyphosphates lies in the fact that
the phosphate is linked in them by high energy bonds. This
explains their instability and ready solubilization, as well as
the linear relationship of respiratory rate and phosphate
absorption that is often observed (Harley & McCready,
1981).

Cox et al. (1978, 1980) pointed out that translocation of


polyphosphate in the fungal hyphae might explain the high
rates of the process. They thought granular polyphosphate
might be translocated, but it would appear that soluble
polyphosphate would provide a more credible mechanism.
Equally important is the possibility that polyphosphates
may provide a mechanism for carbohydrate and phosphate
interchange between the symbionts.
In such a system carbohydrates, absorbed as they are
released from the host, would be phosphorylated by the
mediation of polyphosphate. Trehalose, glycogen and mannitol would be formed from the sugar phosphates, and
inorganic orthophosphate released. This mechansim would
provide for a local decrease of the internal concentration of
monosaccharides and an increase in the internal concentration

134

of phosphate in the fungus. In this way conditions would be


set for inward movement of carbohydrate and outward loss of
phosphate by the fungus.

Absorption of nitrogen compounds


It has been found that in eutrophic soils where nitrate is
present, mycorrhizal plants do not absorb nitrogen more
readily than non-mycorrhizal ones. This applies particularly to
vesicular-arbuscular plants which dominate in such places.
However, ammonium and organic nitrogen can also be
utilized by them.
In the habitats of Ericaceae and in temperate broad-leaf and
coniferous forests, nitrate is usually deficient, but ammonium
and organic compounds are present. Some ectomycorrhizas
and ericoid mycorrhizas are unable indeed to reduce and use
nitrate but readily use ammonium and simple organic
compounds. Read and his colleagues (Read & Stribley, 1973;
Stribley & Read, 1974a,b, 1976, 1980) have shown clearly
that ericoid mycorrhizas and ectomycorrhizas can not only
use ammonium and many simple amino acids but also
hydrolyse, and use the products, of insoluble organic nitrogen
compounds of humus. The nitrogen compounds formed in the
fungal tissues were found to be readily translocated in the
hyphae to the host. The mechanism of uptake here results in
the rapid accumulation of glutamine in the fungal hyphae, and
it involves not only the' utilization of organic acids in the
tissue but also the dark fixation of CO 2 , Both the glutamate
dehydrogenase (GDH) and the glutamine synthesase (GS)
pathways have been identified in mycorrhizas (S. E. Smith
et al., 1985; St John et al., 1985; see also France & Reid, 1983),
although it is probable that the GS pathway with lower Km for
ammonium is more important. This would agree with the
results of Harley (1964) and Carrodus (1967) on 14C02
fixation and the labelling of glutamine. It also seems probable
that glutamine is the important compound released into the
host tissues (see Lewis, 1976).
Before leaving consideration of nitrogen metabolism, it is
important to stress two further points. Nitrogen uptake and
accumulation are intimately associated with phosphate
metabolism, and consequently some of the observed effects of
mycorrhiza on growth which have in the past been ascribed
to improved nitrogen availability, may be secondary effects of
phosphate availability. The second point is an extension of
that. Nitrogen fixation by legumes and other plants is
faciliated by mycorrhizal infection, as shown long ago by
Asai (1944), and fully confirmed with isotopic and other
modem methods. This has now been seen as an indirect effect
via phosphate availability, for phosphate is essential to the
bacterial fixation process.

Accumulation of nutrients in the fungus


The hyphae of mycorrhizal fungi, the main absorbing organs
of mycorrhizas, act initially as organs where nutrients
accumulate. This is especially obvious in the case of phosphate
which accumulates particularly as polyphosphates. However,
in the ectomycorrhizas this accumulatory function is especially
pronounced and the sheath acts especially as an organ

J. L. Harley
accumulating nutrients (see Harley & Smith, 1983). It is
noteworthy that in edomycorrhizas, carbohydrates, as we
have seen, also accumulate in the sheath. It is tempting,
therefore, to speculate that this facility for storage is correlated
with the needs of arborescent plants growing in seasonal
climates and having fungal associates producing large fruit
bodies seasonally.

MYCORRHIZA IN ECOSYSTEMS
Mycorrhizal fungi show a very low specificity to their hosts,
and higher plants are not very selective in the fungi with
which they form mycorrhizas. For example: Hymenoscyphus
ericae ( = Pezizella ericae) forms ericoid mycorrhiza with a wide
range of Ericaceae including species of Erica, Cal/una,
Vaccinium, Rhododendron and many other genera; Cenococcum
geophilum was known as long ago as 1959 to form
ectomycorrhiza with species of 16 genera of forest tree, and
since then it has been widely recorded as mycorrhizal with
many more species of woody plant and with some herbs of
the genera Kobresia, Mycelis and Polygonum. Although these
species of fungi are particularly wide in their mycorrhizal host
range, that of the ectomycorrhizal Pisolithus tinctorius and the
vesicular-arbuscular fungus Glomus fasciculatum is also very
wide indeed. Some further examples given by Harley & Smith
(1983) in their essay on specificity also emphasize this point,
that mycorrhizal fungi and hosts are not generally closely
specific to one another.
This clear conclusion is often criticised or met with definite
disbelief by three classes of biologist for theoretical reasons.
(i) The evolutionists say: there must be a selection for
optimal combinations and this would lead to specificity.
(ii) The pathologists say: since obligate pathogens are highly
specific with gene-for-gene mechanisms, it is much more likely
that non-pathogenic symbionts, which must be closely
adjusted to their hosts, should be highly specific.
(iii) The biochemists say: the close adjustment and interaction
of the mycorrhizal symbionts in all processes of formation and
function must demand high specificity.
All are blinkered by their expertise, especially the
pathologists. For if the fungus plays an efficient part in the
symbiosis and so in the host's activities, any mutation to
resistance by the host will disturb or destroy a condition of
efficiency. Selection will act against such resistance and
towards the acceptance of any such fungus by the host. For
the fungus, any mutation towards specificity will reduce the
available species of root that can be exploited by it in its
habitat and be selected against.
This argument also disposes of the biochemical argument,
for biochemical processes are subject to selection, just as are
all aspects of biological activity, and there will be strong
selection for compatibility.
To the evolutionists the same arguments apply, but one has
to admit that specificity is sometimes found to be closer in
ecological situations than would appear from experiments in
the laboratory. That is, there may be a preference for some
host/fungus combinations in some habitats. Nevertheless,
individual plants may simultaneously form mycorrhizas with

135

several different species of fungi and this may result from


chance meeting or soil diversity (Molina et al., 1978).
Cycling of carbon components

There has not been enough research on the ecological impact


of mycorrhizal formation to formulate clear views or firmly
based hypotheses of its relevance. It is only possible to
speculate in a manner which will stimulate further investigation
of its ecological importance.
It is clear that mycorrhizas facilitate the absorption of
nutrients from the soiL especially those of low mobility which
are needed in quantity by the symbiotic system, or those
present in very low concentrations including some of the trace
metals. It is also clear that mycorrhizas are very common,
probably more common than roots as absorbing organs.
Mycorrhizal plants cannot therefore be viewed as specially
endowed or competing solely with non-mycorrhizal plants.
More generally they compete with mycorrhizal plants of the
same or other species. This must be borne in mind in assessing
the ecological significance of mycorrhiza to the host plant.
Mycorrhizal fungi, on the other hand, have a way of life in
which a constant supply of usable carbohydrate is available to
them from their hosts so that they can compete with nonmycorrhizal micro-organisms for inorganic nutrients, without
competing for carbon compounds, and that is important.
Carbon compounds, readily available to micro-organisms in
soiL are not excessive in quantity, even in highly organic soil
horizons. Except in a few cases, the humic layers are not
accumulations of organic matter which increase continually,
but, in stable ecosystems, the equivalent of the accreted
material in one year is consumed in a year. The soil humus is
simply one of the cycling components with perhaps a
longish half-life.
The active fungi in soil are not present in teeming millions,
they are relatively few and consist of three kinds:
(i) those capable of using complex humic carbon compounds,
being equipped with suitable enzyme systems;
(ii) those which are mycorrhizal or root-surface fungi which
gain all or most carbon from their hosts;
(iii) those usually present as spores but which become
active in the occasional presence of easily available soluble
carbon compounds, e.g. from root exudations, excess products
of group (i), and animal cadavers and faeces.
The activities of these groups, together with those of other
soil organisms, result in the release of CO 2 into the atmosphere.
However, the amount produced greatly exceeds by 50-200%
the amount of carbon made available to the soil by the fall of
leaves, bud scales, flowers, etc. and the decay of roots (see
Harley, 1971, 1973, for references). It is clear that photosynthetic carbon diverted through rhizosphere and mycorrhizal
organisms probably accounts for much of the deficit. On this
point I have given (in the papers quoted) some examples
based on weights of the fruit bodies of mycorrhizal fungi per
hectare, on estimates of CO 2 production by Fagus mycorrhiza,
and on the experimental results of Tranquillini on Pinus
cembra. These estimates showed that more than 10 % of the
carbon photosynthesized by the host was diverted though the
mycorrhizal fungi.

136

The Fourth Benefactors' Lecture


These estimates, rough as they admittedly were, initiated
further detailed work which not only confirmed the sort of
magnitude of the photosynthesized carbon used by the
fungus, but actually suggested that they were under-estimates.
Fogel & Hunt (1979) estimated that of a total annual throughput of 30344 kgjha of carbon in a Pseudotsuga forest, over
50% was ascribable to the carbon consumed by the
mycorrhizal fungi. This estimate seems excessive and it is not
certain that all the sporophores and hyphae recorded by them
were all truly mycorrhizal.
Voght et al. (1982), however, produced figures from two
Abies amabilis forests which agreed closely, showing that of
their net primary production of 24 000 j 25000 kgjha, 14-15 %
was represented by the primary production of the actual
mycorrhizal fungi, and was derived from the host.
All the available evidence therefore suggests that the total
participation of ectomycorrhizal fungi in carbon cycling of
forests is very large. One might not expect that vesiculararbuscular mycorrhizas, which do not produce large fungal
structures such as sheath, fruit bodies and sclerotia, would
play such a prominent part (but proportionate to herbaceous
partners it is likely to be significant). It might be guessed that
ericoid mycorrhiza might be somewhat inbetween the other
two common kinds.

CYCLING OF SOIL-DERIVED NUTRIENTS


The activities of mycorrhizal fungi result in the accumulation
of nutrients in the root region, for they absorb them at a
distance and translocate them to the roots. Mycorrhizas, like
all plant structures, have a life-span; they may grow apically,
producing a new active region whilst their proximal region
ages and senesces, or the whole organ senesces together.
During senescence the hyphae may remain active after the
cells begin to degenerate. This is very obvious in ecto- and
ericoid mycorrhizas (Atkinson, 1976; Bonfante-Fasolo et al.,
1981), and it may be assumed that they absorb the soluble
material and recycle it. Heap & Newman (1980) observed that
in vesicular-arbuscular mycorrhizal plants, phosphate was
translocated out of the roots into the hyphae of plants that
had been decapitated 14 days before.
Material absorbed into the symbiotic systems may therefore
be held and recycled within the system. This may lead to a
deficit of nutrients such as phosphate and nitrogen in the litter
and humus, so retarding its breakdown. Such an effect was
reported in coniferous forest by Gadgil & Gadgil (1975) but
has not been observed by others. However, their result is in
agreement with the contention that ectomycorrhizal trees are
often reported as causing soil degeneration and acidification,
but of course the effect will only develop in soils of initially
low nutrient content. As an example, Singer & Araujo (1979)
have ascribed litter accumulation in the tropical podsols that
they investigated to the dominance of ectomycorrhizal
trees.
Such close cycling of substances is subject to inteference
and disruption by soil fauna. Long ago Buller (1909, 1922)
wrote of slugs and squirrels as mycophagists and many of the
fungal species that he observed as being consumed were
mycorrhizal species. Recent work has much extended these

observations and it has been shown by observation and


investigation of gut contents, that collembola, nematodes,
ants, wasps, worms and birds as well as slugs and small
mammals, consume mycorrhizal fungi. Maser et al. (1979)
even reported that 79 % of the fragments in the guts of small
mammals in coniferous forests in Oregon were ectomycorrhizal and 10 % were of vesicular-arbuscular mycorrhiza.
Another important problem arises in connexion with close
cycling of nutrients, when we consider non-specificity of
mycorrhizal symbionts in this context. It follows from the
degree of non-specificity observed that plants of more than
one species, of more than one age, of more than one vegetal
layer in an ecosystem, may be interconnected by one or more
mycelia of mycorrhizal fungi. Harley & Smith (1983) called
this 'a social complex of organisms '. Nutrients and carbon
compounds can pass from one to another host plant in such
a system (Hirrell & Gerdemann, 1979; Whittingham & Reid,
1982), and its importance and extent is being further
investigated especially in Dr David Read's laboratory (see for
instance Read et al., 1985; Read, 1987).
You will at once see that this formation of social complexes
of organisms might cause us to revise our views on some
ecological problems, such as root competition and effects of
shading. It would follow that seedling trees or undershrubs
and herbs, to the extent that they shared fungi with the
dominants, might be supplied with carbon by them.
This would imply that root competition, as ordinarily
conceived, would only occur between plants that did not
share common fungi. But if they did share a common fungus
the plant that derived most from the fungus and released least
carbon to it would flourish best. On the latter point, the
experiment of Fitter (1971) with Lolium perenne and Holcus
lanatus, mycorrhizal with the same fungal strain of Glomus,
illustrates the possibility. Both species, grown separately,
absorbed more phosphate and grew better with the fungus
than without. But when grown together with the same fungus
mycelium, Holcus flourished whilst Lolium absorbed a smaller
proportion of the phosphate and did less well.
Grime et al. (1987) have shown how association of diverse
species of plants with a common mycorrhizal fungus might
result in an increase of floristic diversity in an experimental
microcosm, partly due to the translocation of photosynthates
from the dominant species to those subsidiary ones that were
infected, but not to those that were not infected.
It seems a pity that these kinds of effect have not been more
appreciated by plant ecologists, for it is perhaps only the tip
of a very large and important iceberg. Many arborescent
plants, including species of Tilia, Salix, Populus and Prunus and
other rosaceous trees, may be either or both ectomycorrhizal
and vesicular-arbuscular mycorrhizal. The implications of this
in terms of a ' social complex' are great; and yet unconsidered.

CONCLUSION
In conclusion, why are there several common kinds of
mycorrhiza? Why is one not selected for? We can only
conclude that each has unique properties fitting it in some
way for particular conditions and that those species that can
form more than one kind are widely adapted. Vesicular-arbus-

J. L. Harley
cular mycorrhiza is well adapted to eutrophic soil and the
fungi are especially adive in phosphate uptake. The smaller
demand of the fungi for carbon compounds derived from their
hosts leads this kind of mycorrhiza to be seleded against all
others in many habitats and by herbaceous plants, and indeed
it is the most common.
Edomycorrhizas are well-adapted to the absorption of
phosphates and ammonium compounds from soils of high
phenolic content where nitrates are deficient. Their large
fungal sheath tissue and large fungal fruit bodies result in the
carbon demand being high, so that large dominant arborescent
plants can support them best. The facility of the fungal sheath
for storing nutrients and carbohydrates in times of plenty fits
this kind of mycorrhiza to flourish in seasonal climates
alternating cold and warm, or dry and moist; that is to
seasonal growth and demand for nutrients by both symbionts.
Ericoid mycorrhizas are specially fitted for extreme climates
in peaty or humic soils which are acid and high in phenolic
compounds. The fungi absorb phosphate, but particularly
ammonium and soluble and insoluble organic nitrogen
compounds. The fungi proted the host from toxic metals
which are soluble in the very acid soil solutions.
This ledure has been just a quick glimpse of the work on
mycorrhiza - a case, to use a Chinese expression, of 'viewing
the wild flowers from horseback'. I apologize to the many
whose work I have not quoted in detail.

REFERENCES
AMI]EE, F. & STRIBLEY, D. P. (1987). Soluble carbohydrates of
vesicular-arbuscular mycorrhizal fungi. The Mycologist 21,
20-21.
ASAI, T. (1944). Ueber die Mykorrhizenbildung der leguminosen
Pflanzen. japanese journal of Botany 13, 463-485.
ASHFORD, A. E., LING LEE, M. & CHILVERS, G. A. (1975).
Polyphosphate in eucalypt mycorrhizas: a cytochemical demonstration. New Phytologist 74, 447-453.
ATKINSON, M. A. (1975). The fine strudure of Mycorrhizas.
D.Phil. Thesis, Oxford University.
BARTLETT, E. M. & LEWIS, D. H. (1973). Surface phosphatase
adivity of mycorrhizal roots of beech. Soil Biology and Biochemistry
5, 249-257.
BETHENFALVAY, G. J.. BROWN, M. S. & PACOVSKY, R. S.
(1982). Relationships between host and endophyte development
in mycorrhizas of soybeans. New Phytologist 90, 537-543.
BEVEGE, D. I., BOWEN, G. D. & SKINNER, M. F. (1975). Comparative carbohydrate physiology of edo- and endomycorrhizas. In
Endomycorrhizas (ed. F. E. Sanders, B. Mosse & P. B. Tinker),
pp. 149-174. London and New York: Academic Press.
BONFANTE-FASOLO, P., BERTA. G. & GIANINAZZI-PEARSON,
V. (1981). Ultrastrudural aspeds of endomycorrhiza in the
Ericaceae. II. Host/endophyte relationships in Vaccinium myrtillus.
New Phytologist 89, 219-224.
BRlERLEY, J. K. (1953). Absorption of salts by mycorrhizal roots of
Fagus sylvatica. D.Phil. Thesis, Oxford University.
BULLER, A. H. R. (1909). Researches 011 FUl1gi I. London: Longmans
Green & Co.
BULLER, A. H. R. (1922). Researches on Fungi II. London: Longmans
Green & Co.

137
BURGEFF, H. (1961). Mikrobiologie des Hochmoores. Stuttgart. Gustav
Fischer verlag.
CALLEJA. M., MOUSAIN, D., LECOUVREUR, B. & D'AUZAC J.
(1980). Influence de la carence phosphatee sur les adivMs
phosphatases acidides de trois champignons mycorrhiziens:
Hebeloma edurum Metrod, Suillus granulatus (L. & Fr.) O. Kuntze et
Pisolithus tinctorius (Pers.) Coker & Couch. Physiologie Wgetale 18,
489-504.
CARRODUS, B. B. (1967). Absorption of nitrogen by mycorrhizal
roots of beech 2. Ammonium and nitrate as sources of nitrogen.
New Phyt%gist 66, 1-4.
CHILVERS, G. A. & HARLEY, J. L. (1980). Visualization of phosphate
accumulation in beech mycorrhizas. New Phytologist 84, 319-326.
COUTURE, M., FORTIN, J. A. & DALPE, Y. (1983). Oidiodendron
griseum Robak, an endophyte of ericoid mycorrhizas in Vaccinium
spp. New Phytologist 95, 375-380.
COX, G. c., MORAN, K. J., SANDERS, F. E., NOCKOLDS, C. &
TINKER, P. B. (1980). Translocation and transfer of nutrients in
vesicular-arbuscular mycorrhizas. III. Polyphosphate granules and
phosphorus translocation. New Phytologist 84, 649-659.
COX, G. c.. SANDERS, F. E., TINKER, P. B. & WILD, J, A. (1975).
Ultrastrudural evidence relating to host-endophyte transfer in a
vesicular-arbuscular mycorrhiza. In Endomycorrhizas (ed. F. E.
Sanders, B. Mosse & P. B. Tinker), pp. 297-312. London and New
York: Academic Press.
De BARY, A. (1884). Comparative Morphology and Biology of the
Fungi, Mycetoza and Bacteria. Translated by H. E. F. Garnsey,
revised I. B. Balfour 1887. Oxford: Clarendon Press.
DOMINIK, T. (1956). Vorschlag einer neuer Klassifikation der
ekrotrophen Mycorrhizen auf morphologisch-anatomischen Merkmalen begrundet. Roczniki Nauk Lesnych (Frace) 14, 223-245. [In
Polish with German summary].
FITTER, A. H. (1977). Influence of mycorrhizal infedion on
competition for phosphorus and potassium by two grasses. New
Phytologist 79, 119-125.
FOGEL, R. & HUNT, C. (1979). Fungal and arboreal biomass in a
western Oregon Douglas fir ecosystem; distribution patterns and
turnover. Canadian journal of Forest Research 9, 245-256.
FRANCE, R. C. & REID, C. P. (1983). Interadion of nitrogen and
carbon in the physiology of edomycorrhizae. Canadian journal of
Botany 61, 964-984.
FRANK, A. B. (1885). Ueber die auf Wurzelsymbiose beruhende
Ernahrung gewisser Baume durch unterirdische Pilze. Bericht der
deutschen botanischen Gesellschaft 3, 128-145.
GADGIL, R. L. & GADGIL, P. D. (1975). Suppression of litter
decomposition by mycorrhizal roots of Pinus radiata. New Zealand
journal of Forest Science 5, 35-41.
GRIME, J. P., MACKEY, J. M. L., HILLIER, S. H. & READ, D. J.
(1987). Floristic diversity in a model system using experimental
microcosms. Nature, London 328, 420-422.
HARLEY. J. L. (1964). Incorporation of carbon dioxide into excised
beech mycorrhizas in the presence and absence of ammonium.
New Phytologist 63, 203-208.
HARLEY, J. L. (1969). The Biology of Mycorrhiza, 2nd edn. London:
Leonard Hill.
HARLEY, J. L. (1971). Fungi in ecosystems. journal of Ecology 59,
653-668.
HARLEY, J. L. (1973). Symbiosis in the ecosystem. journal of the
National Science Council of Sri Lanka 1, 31-48.
HARLEY, J. L. & BRIERLEY, J. K. (1954). Uptake of phosphate by
excised mycorrhizal roots of the beech. VI. Active transport of
phosphorus from the fungal sheath into the host tissue. New
Phytologist 53. 240-252.
HARLEY, J. L. & BRIERLEY, J. K. (1955). Uptake of phosphate by

The Fourth Benefactors' Lecture


excised mycorrhizal roots of the beech. VII. Active transport of
32p from fungus to host during uptake of phosphate from solution.
New Phyt%gist 54, 296-30l.
HARLEY, J. L., BRIERLEY, J. K. & McCREADY, C. C. (1954). The
uptake of phosphate by excised mycorrhizal roots of the beech. V.
The examination of possible sources of misinterpretation of the
quantities of phosphorus passing into the host. New Phytologist 53,
92-98.
HARLEY, J. L. & HARLEY, E. L. (1987). A check-list of mycorrhiza
in the British Flora. New Phyt%gist (supplement) 105, 1-102.
HARLEY, J. L. & LOUGHMAN, B. C. (1963). The uptake of
phosphate by excised mycorrhizal roots of the beech. IX. The
nature of phosphate compounds passing to the host. New
Phytologist 62, 350-359.
HARLEY, J. L. & McCREADY, C. C. (1952a). Uptake of phosphate
by excised mycorrhizal roots of the beech. II. Distribution of
phosphorus between host and fungus. New Phyt%gist 51,
56-64.
HARLEY, J. L. & McCREADY, C. C. (1952 b). Uptake of phosphate
by excised mycorrhizal roots of the beech. III. The effect of the
fungal sheath on the availability of phosphate to the core. New
Phytologist 51, 342-348.
HARLEY, J. L. & McCREADY, C. C. (1981a). The relation between
phosphate absorption and oxygen uptake in excised beech
mycorrhizas. New Phytologist 88, 675-68l.
HARLEY, J. L. & McCREADY, C. C. (1981 b). Phosphate accumulation in Fagus mycorrhizas. New Phyt%gist 89, 75-80.
HARLEY, J. L. & SMITH, S. E. (1983). Mycorrhizal Symbiosis. London
and New York: Academic Press.
HATCH, A. B. (1937). The physical basis of mycotrophy in the
genus Pinus. B/ack Rock Forest Bulletin 6, 1-168.
HEAP, A. J. & NEWMAN, E. I. (1980). The influence of vesicular-arbuscular mycorrhiza on phosphorus transfer between plants.
New Phyt%gist 85, 173-179.
HEPPER, C. M. (1977). A colorimetric method for estimating
vesicular-arbuscular mycorrhizal infection in roots. Soil Bi%gy and
Biochemistry 9, 15-18.
HIRRELL, M. C. & GERDEMANN, J. W. (1979). Enhanced carbon
transfer between onions infected with a vesicular-arbuscular
mycorrhizal fungus. New Phytologist 83, 731-738.
LEWIS, D. H. (1976). Interchange of metabolites in biotrophic
symbioses between angiosperms and fungi. In Perspectives in
Experimental Biology 2, Botany (ed. N. Sunderland), pp. 208-219.
Oxford: Pergamon Press.
LEWIS, D. H. & HARLEY, J. L. (1965). Carbohydrate physiology of
mycorrhizal roots of beech. New Phytologist 64, 224-269.
LING LEE M, CHILVERS, G. A. & ASHFORD, A. E. (1975).
Polyphosphate granules in three different kinds of tree mycorrhiza.
New Phytologist 75, 551-554.
LOUGHMAN, B. C. & RATCLIFFE, R. G. (1984). Nuclear magnetic
resonance and the study of plants. Advances in Plant Nutrition 1,
241-283.
MARTIN, F., CANET, D., ROLLIN, D., MARCHAL, J. P. &
LARNER, F. (1983). Phosphorus 31 nuclear magnetic resonance
study of polyphosphate metabolism in mycorrhizal fungi. Plant
and Soil 71, 469-476.
MASER, c.. TRAPPE, J. M & NUSSBAUM, R. A. (1978). Fungal/
small mammal interrelationships with emphasis on Oregon
coniferous forests. Ecology 59, 799-809.
MELIN, E, & NILSSON, H. (1958). Translocation of nutrient
elements through mycorrhizal mycelium to pine seedlings.
Botaniska Notiser 111, 251-256.
MELIN, E. (1959). Mycorrhiza. In Encyclopaedia of Plant Physiology XI
(ed. W. Ruhland), pp. 605-638.

138
MITCHELL, D. T. & READ, D. J. (1981). Utilization of inorganic and
organic phosphates by the mycorrhizal endophytes of Vaccinillm
microcarpon and Rhododendron ponticum. Transactions of the British
Mycological Society 76, 255-260.
MOLINA, R. J., TRAPPE, J. M & STRICKLER, G. S. (1978).
Mycorrhizal fungi associated with Festuca in western United States
and Canada. Canadian Journal of Botany 56, 1691-1695.
MOORE, P. D. (1987). The distribution of mycorrhiza throughout
the British Flora. Nature, London 327, 100.
NELSON, C. D. (1964). The production and translocation of
photosynthate C 14 in conifers. In Formation of Wood in Forest Trees
(ed. M. H. Zimmerman), pp. 235-257. New York: Maria Moors
Cabot Foundation.
NEWMAN, E. I. & REDDELL, P. (1987). The distribution of
mycorrhizas among the families of vascular plants. New Phytologist
106, 745-75l.
NORKRANS, B. (1950). Studies in the growth and cellulolytic
enzymes of Tricholoma. Symbolae botanicae Upsalienses 11, 1126.
NYE, P. H. & TINKER, P. B. (1977). Solute Movement in the Soil/
Root System. Oxford: Blackwell Scientific Publications.
PACHLEWSKL R. (1967). Investigations of Pure Culture of Mycorrhizae
of Pine. Translated Dzieciolowski, R. Warsaw Forest Research
Institute, pp. 192.
READ, D. J. (1987). Development and function of mycorrhizal
hyphae in the soil. In Mycorrhizae in the Next Decade (ed. D. M
Sylvia, L. L. Hung & J. H. Graham). Institute of Food and
Agricultural Sciences, University of Florida, Gainesville, Florida,
U.S.A.
READ, D. J., FRANCIS, R. & FINLAY, R. D. (1985): Mycorrhizal
mycelia and nutrient cycling in plant communities. In Ecological
Interactions in Soil (ed. A. H. Fitter). Oxford: Blackwell Scientific
Publications.
READ, D. J. & STRlBLEY, D. P. (1973). Effect of mycorrhizal
infection on nitrogen and phosphorus nutrition of ericaceous
plants. Nature, London 244, 81-82.
READ, D. J. & STRIBLEY, D. P. (1975). Some mycological aspects of
the biology of mycorrhiza in the Ericaceae. In Endomycorrhizas (ed.
F. E. Sanders, B. Mosse & P. B. Tinker), pp. 105-117. London and
New York: Academic Press.
ST JOHN, B. J" SMITH, S. E., NICHOLAS, D. J. D. & SMITH, F. A.
(1985). Enzymes of ammonium assimilation in the mycorrhizal
fungus Pezizella ericae Read. New Phytologist 100, 579-584.
SANDERS, F. E. & TINKER, P. B. (1973B. Phosphate flow into
mycorrhizal roots. Pesticide Science 4, 385-395.
SINGER, R. & ARAUJO I. de J. da S. (1979). Litter decomposition
and ectomycorrhiza in Amazonian forests. Acta Amawnica 9,
25-4l.
SMITH, D. c.. MUSCATINE, L. & LEWIS, D. H. (1969). Carbohydrate
movement from autotrophs to heterotrophs in parasitic and
mutualistic symbiosis. Biological Review 44, 17-19.
SMITH, S. E., ST JOHN, B. J" SMITH, F. A. & NICHOLAS, D. J. D.
(1985). Activity of glutamine and synthetase and glutamate
dehydrogenase in Trifolium subterraneum and Allium cepa: effects
of mycorrhizal infection and phosphate nutrition. New Phyt%gist
99, 211-227.
STRIBLEY, D. P. & READ, D. J. (1974a), The biology of mycorrhiza
in the Ericaceae. III. Movement of carbon-14 from host to fungus.
New Phytologist 73, 731-741.
STRIBLEY, D. P. & READ, D. J. (1974 b). The biology of mycorrhiza
in the Ericaceae. IV. The effect of mycorrhizal infection on uptake
of 1N from labelled soil by Vaccinium macrocarpum Ait. New
Phytologist 73, 1149-1155.
STRlBLEY, D. P. & READ, D. J. (1975). Some nutritional aspects of

J. L. Harley
the biology of ericaceous plants. In Endomycorrhiws (ed. F. E.
Sanders, B. Mosse & P. B. Tinker), pp. 193-207. London and New
York: Academic Press.
STRIBLEY, D. P. & READ, D.]. (1976). The biology of mycorrhiza
in the Ericaceae. VI. The effects of mycorrhizal infection and
concentration of ammonium nitrogen on growth of Cranberry
(Vaccinium macrocarpum Ait.) in sand culture. New Phyfologisf 77,
63-72.
STRIBLEY, D. P. & READ, D.]. (1980). The biology of mycorrhiza
in the Ericaceae. VIII. The relationship between mycorrhizal
infection and the capacity to utilize complex organic nitrogen
sources. New Phyfologisf 86, 365-371.
STRULLU, D. G. & GOURRET, j. P. (1973). Etudes des mycorrhizes
ectotrophes Pinus brutia Ten. en microscopie eJectronique 11
balayage et 11 transmission. Comptes rendus hebdomadaires des
Sciances de l'Acadimie des Sciences, Paris 277, 1757-1760.
STRULLU, D. G., HARLEY, ]. L., GOURRET, ]. P. & GARREC, ]. P.
(1982). Ultrastructure and microanalysis of polyphosphate granules

139
of ectomycorrhiza of Fagus sylvatica. New Phytologist 92, 417423.
STRULLU, D. G., GRELLIER, B., GARREC, j. P., McCREADY, C. C.
& HARLEY, ]. L. (1986). The effects of monovalent and divalent
cations on phosphate absorption by beech mycorrhizas. New
Phytologist 103, 403-416.
TINKER, P. B. (1978). Effects of vesicular-arbuscular mycorrhizas on
plant nutrition and plant growth. Physiologie Vigitale 16,743-751.
TISDALE, ]. M. & OADES, j. M. (1979). Stabilization of soil
aggregates by the root system of rye grass. Australian Journal of
Soil Research 17, 429-444.
WHITTINGHAM, ]. & READ, D. J. (1982). Vesicular-arbuscular
mycorrhizas in natural vegetational systems. III. Nutrient transfer
between plants with mycorrhizal interconnections. New Phytologist
90, 277-284.
WILLIAMSON, B. & ALEXANDER, I. (1975). Acid phosphatases
localized in the sheath of beech mycorrhizas. Soil Biology and
Biochemistry 7, 195-198.

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