of plants to powdery mildew.
question, why a plant of one species can be attacked by a parasite
and an other plant not, could not be answered until now, for science
has no explanation found yet. At the University of Gießen a
new resistance mechanism was found by Dr. Karl-Heinz Temmen after
several years of investigation of the resistance of plants against
powdery mildew (TEMMEN 1977, TEMMEN et al 1979c).
Powdery mildew is one of the most important obligate prasites in
plant production which attacks leaves, flowers, young stems of mostly
all cultivars and causes death of growing points, distortion of
leaves and the stunting of shoots. Based on susceptible and resistant
plant species, cultivars and clones, the resistance mechanism to
powdery mildew was investigated on leaves of the following cultivars:
black currant (Ribes) apple (Malus), rose(Rosa), cucumber(Cucumis)
and also barley (Hordeum). It was discovered, that the youngest
leaves in the unfolding stage of all dicotyles are always susceptible.
With further development, tolerance to the fungus increases, but
to a different degree in variety and clones of cultivars. On some
plants, leaves 1 to 3, numbered basipetally, are susceptible and
have macroscopically visible fungus colonies, while on other plants
susceptibility extents to leaves 18 – 20. The histological
evaluation of all cultivars , based on safranin-stained sections,
revealed that susceptible leaves had a high percentage of cells
completely filled with cytoplasm, compared to epidermal cells of
resistant leaf stages, which were either partially or completely
vacuolized. When the percentage of these differently stained cells
was determined, a satisfactory correlation between stainability
and susceptibility became apparent. The cell development of epidermal
cells on monocotyledons comparing to dicotyledons is different because
the ontogenetic development of the embryonal epidermal cells in
monocotyledons starts within the stalkknots . The stomata cells,
the auxiliary cells and the short cells develop from the jung epidermal
cells. Each stomata cell with two auxiliary cells is surrounded
by 4 short cells which are in neighbourhood of long cells. After
development of the cells the vacuolization is almost finished exept
in in some stomata and short cells which we call “starter
cells”. Those cells are completely or at least partially filled
with cytoplasm and are essential to initiate fungal development.
To be able to draw their nutrients even from the vacuolized epidermal
cells fingerlike prolongations of the haustoria are being formed.
can it be interpreted?
The natural senescence of cells has long been
known and is a matter for botanical text-books. But the phenomenon
of the difference in susceptibility in correlation to the degree of
vaculozation of epidermal cells of suscetible and resistant cultivars
has been observed for the first time by Dr. Karl-Heinz Temmen.
This means the powdery mildew fungus depends on a sufficient supply
of nutrients in epidermal cells. So the formation of primary haustoria
require epidermal cells rich in cytoplasm. These are called “starter
cells”, which correspond to the auxiliary cells of barley cultivars.
A very early contact of primary haustoria with cytoplsm is necessary
for further fungal development. When secondary mycelium has been formed,
the fungus attempts to establish haustoria also in neighbouring cells,
in order to secure the nutritional basis. Such secondary haustoria
are formed even in completely vacuolized cells, which do not allow
formation of primary haustoria. Such relation has been observed in
all host-parsite-combinations mentioned before. This “lack of
cytoplasm-effect” is strengthened by the fact, that the fungus
can develop on epidermal cells above leaf veins of leaves which do
not permit powdery mildew on interveinal areas. Epidermal cells above
leaf veins are mostly completely filled with cytoplasm, while the
neighbouring cells above interveinal areas are vacuolized.
does this work?
A great number of Ribes cv, Malus cv, Rosa cv , Cumumis cv
and Hordeum cv were tested for their susceptibility. The differences
in susceptibility in all models are linked in the degree of vacuolisation
of epidermal cells. The more pronounced the vacuolization, and the
greater the quantity of the host cytoplasm, the better the fungus
thrives. This can be seen from the fact that powdery mildew generally
thrives better on leaves of well-nourished plants than on leaves of
specially N defiency. For demonstration matter the susceptible cultivar
“Super Star” and the resistent cultivar “Gloria
Dei” were choosen. No macroscopically visible mildew colonies
were detectable on the resistant cv, while the susceptible cv was
heavily infected up to pinnate leaf No. 9, when numbered basipetally
1). Although mildew colonies were macroscopically invisible on
some leaf stages fungal development could be detected by microscopic
examination using the Technicoll technique, which is based on adherence
of fungal structure to the adhesive. On leaf No. 5 of the resistent
cultivar “Gloria Dei” with cells mostly in the stretching
stage the germination, appressoria formation and appearance of secondary
hyphae of the fungus occur within approximately the same time range
as with the succeptable cultivar “Super Star”. However
in opposite to “Super Star” on “Gloria Dei”
only conidiophores are formed but no conidia are produced. A few hours
later hyphae and coniophores shrivel and become dry (Fig.
2). The histological evaluation, based on safranin-stained sections,
revealed that susceptible leaves had a high percentage of epidermal
cells complelely filled with cytoplasm, compard to epidermal cells
of resistant leaf stages, which were either partially or comletely
vacuolized. Top leaflets of the first pinnate leaf of susceptible
cv had more than 50 % non-vacuolized cells, whereas corresponding
leaves of resistant cv had 30 %. In leaves No 3, 5, 7, 9 vacuolization
of epidermal cells steadily progessed; the depletion of cytoplasm
however occured at a faster rate in cells of resistant cv (Fig.
do these differences in cytoplasm content mean?
The degree of vacuolization or depletion of cytoplasm has an influence
on fungal development In the cells packed with cytoplasm the fungus
penetrated and formed haustoria 24 hrs p.i., however papillae were
rarely observed. In cells almost completely vacuolized, the fungus
had formed only penetration pegs 24 hrs p.i., which had become surrounded
by papillae. After prolonged incubation, the number of normal haustoria
had increased in vacuolized cells 144 hrs p.i., penetration of papillae,
however, was not observed.
It appears, that the formation of primary haustoria require epidermal
cells rich in cytoplasm (starter cells), which would correspondent
to the auxiliary cells of Hordeum cv considered essential for the
primary infection by HIRATA and TOGASHI (1957). A low transport of
nutrients in the “starter cells” take place during the
development of bodies of primary haustoria and a high rate of transfer
of substances coincides with the time when bodies have attained full
size (MOUNT and ELLINGBOE 1969).That would explain the question why
a very early contact of the primary haustorium with cytoplasm is necessary
for further fungal attempts to establish haustoria also in neighbouring
cells, in order to secure the nutritional basis. Apparently one haustorium
is not sufficient to allow conidia production (HIRATA; 1967, 1971).
Such secundary haustoria are quite readily formed even in completely
vacuolized cells, which previously did not allow formation of primary
haustoria. Such a relation has been observed in all four host-parasite-combinations
mentioned before. A “starter cell”, rich in cytoplasm,
appears to be a prerequisite for initial fungal development. Once
a primary infection has been established, the fungus can make use
of more or less vacuolized neighbouring cells by secundary haustoria.
Therefore resistant leaves have less epidermal cells with high cytoplasm
content, necessary for the establishment of the primary infection.
Chances to encounter a “starter cell” are thus considerably
reduced. With leaf development the number of “starter cells”
decreases further, thus making the leaves even more inhospitable for
the fungus. Fungal development is not completely suppressed, but retarded
and reduced to such an extent that it appears to nullify its epidemiological
importance. Likewise, there is little or no damage on the attacked
leaves. This condition is considered the basis for horizontal reistance
of plants to powdery mildew.
is the meaning of the frequently observed papillae?
These structures are formed in response to invading pathogens in cells
of susceptible and resistant host plants (HEATH 1974), as well as
in cells of non-host plants (RIDE and PEARCE 1979). At the present
state of knowledge papillae seem to constitute impregnable mechanical
barriers against further fungal penetration. This interpretation is
consistent with the results of most histological investigations, but
a question remains unanswered: why, e.g., can primary infection not
develop haustoria in vacuolized cells but only papillae, whereas secundary
infections can do so readily? Even though these questions cannot be
answered at the moment it seems that vacuolized cells cannot deliver
nutrients for the development of a primary haustorium so that the
hostcell is able to repair the damage during penetration by forming
is the meaning of horzontal and vertical resistance?
There are 3 host-parasite-interactions to be differentiated:
- vertical - or race specific resistance is predestinated not
for haustoria formation but only for papillae (Fig.
4a). This means, that either a fungal race with sufficient
virulence does not exist or it is a question of a non-host-interaction.
For example the rose cv “Super Star”, first introduced
in Great Britain, was resistant to powdery mildew for about 10
years, when it suddenly became susceptible. This example is not
an argument against the postulated horizontal resistance. According
to the percentage of epidermal cells rich in cytoplasm this cv
has to be considered susceptible. Due to absence of a fungal race
with sufficient virulence, this cv was resistant during the early
years of cultivation. Thus it constitutes an example for vertical
resistance which must not be confused with the horizontal resistance
exhibited by “Gloria Dei”.
- Horizontal resistance is predestinated by primary haustoria
in cells rich in cytoplasm (starter cells), formation of papillae
during primary infection in cells poor of cytoplasm, forming of
secundary haustoria in all kind of epidermal cells, absence of
sporulation because of few cells rich in cytoplasm. (Fig.
- Susceptibility occurs on those leaves of which cells are rich
in cytoplasm. Primary haustoria find sufficient cells with high
cytoplasm content. Papillae are rare and sporulation ist normal
because of enough cells rich in cytoplasm (Fig.
Investigation on Ribes cv against powdery mildew (Dissertation)
K.-H., GRUPPE, W. and SCHLÖSSER, E. (1979c)
Investigations on the resistance of plants to powdery mildew.
III. The basis for
horizontal reistance of Ribes spp.
in Plant Disease (1980) How Plants Defend Themselves, p.164 Academic
New York- London, Toronto, Sydney, San Francisco, 1980
K. & TOGASHI, K., 1957
in R.M. SPENCER (ed.): the Powdery Mildews, p. 268
Academic Press, London-New York-San Francisco, 1978
S.M. & ELLINGBOE, A.H.
Phytopahtology, 1969, 59, 235
HIRATA, K., 1967, 1971
in R.M. SPENCER (ed.). The Powdery Mildews, p. 204
Physiol. Plant Path., 1974, 4 , 303-414
RIDE, J.P. & PEARCE. R.B.
Physiol. Pl. Path. 1979,15, 79-92