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129
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.
TOWARDS A DEFINITION OF
MYCORRHIZA
It is difficult to give a succinct definition of mycorrhiza
130
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.
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.
Figures extraded by Moore (1987) from Harley & Harley (1987), relating to some major families.
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.
J. L. Harley
133
Observation
Author
Ericaceae
Vesicular-arbuscular
Edomycorrhiza
Hepper (1977)
Tinker (1978)
Bethenfalvay et al. (1982)
Tisdale & Oades (1979)
Fungal sheath
39'10'5% d.wt (Fagus)
37'0 1'9% d.wt (Fagus)
34 % d.wt (Nothofagus)
20-30% d.wt (Pinus)
Mycorrhizal
Non-mycorrhizal
% in
%in
shoots
roots
46
95
54
% in roots
relative to wt
17.4
4.6
2844
940
3784
Percentage of total
75'2
24'8
100
134
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
136
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.
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