Plant disease fisiology-The infection process

RESPIRATION

Diseased plants invariably show greater respiratory activity ( usually measured as oxygen
consumption ) than healthy plants. In other words, diseased plants “run a respiration” in a
similar way as diseased mammals “run a temperature”. Increased respiratory activity is
characteristic of infected photosynthetic tissue irrespective of whether the plants is infected with
fungal, bacterial or viral pathogens. Fig. 22.5 compares the rate of oxygen consumption in non-
infected barley leaves and those infected with Erysiphe graminis. With most fungal pathogens,
the increase in respiration is obvious within about 48 h after inoculation and reaches a maximum
during the time of sporulation. Allan & Goddard (1938) showed a four to five fold increase in
respiration rate in mildewed wheat leaves. Their result indicated that most of this increase was
localized in the mesophyl l cells of the host (Table 22.2). More recent evidence suggests that the
growing fungus contributes significantly to the observed increased in respiration. However, it
appears that respiration of host tissue in the neighbourhood of the fungal colonies is stimulated
two fold to threefold (Scott, 1972). Further evidence to suggest that much of the increased
respiration is of host origin comes from studies with virus diseases. Viruses being non-cellular
possess no respiratory apparatus of their own. However, virus infections stimulate similar
increases in respiration as do other pathogens.

Days after inoculation

Fig. 22.5. Rate of respiration in uninfected barley leaves and leaves infected with Erysiphe graminis (from
Scott and Smillie, 1966)

TABLE 22.2. Comparison of respiratory rates of normal wheat leaves and those infected with Erysiphe
graminis (from Allen and Goddard,1938)

Tissue Ml O2 consumed/hour/cm2 leaf surface

Non-infected leaf 1.70

Infected leaf 7.92

Infected leaf minus mildew 6.40

Non infected epidermis 0.15

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 Plant disease fisiology-The infection process

Infected epidermis 1.30

Infected epidermis minus mildew 0.14

A number of theories have been put forward to explain why infection cause the host to increase its
respiration rate. No one theory however, has received universal acceptance and the topic is still very
controversial. Some workers have suggest that the increases in respiration is related to “uncoupling”
of electron transfer from oxidative phosphorylation. The main evidence for this suggestion is related
to the effects of 2,4-dinitrophenol (DNP) on healthy and diseased plant tissue. When applied to
healthy tissue, DNP causes an increase in respiration rate. It is been suggested that DNP “uncouples”
electron transfer from oxidative phosphorylation so that ATP is not produced from ADP and
inorganic substrate but electrons are still transferred to oxygen. This leads to an increase in O 2
consumption by the plant. However when DNP is applied to diseased leaf tissue, no increase in
oxygen consumption occurs and it is assumed that electron transfer from oxidative phosphorylation
has already been uncoupled as a result of infection (Fig. 22.6(a) ). Despite the simplicity and
attractiveness of the “uncoupling” hypothesis it is supported by little experimental evidence and
other explanations are equally plausible.

Oxygen consumption is not associated with phosphorylation during the formation of pyruvate from
starch (glycolysis or Embden Meyerhof pathway). An alternative route for the production of
pyruvate is the pentose phosphate pathway (Fig. 22.6(b) ). This pathway is considered to be less
important than glycolysis in healthy plants. Infection however appears to cause an increase in the
activity of the pentose phosphate pathway. This view is supported by such evidence as a decrease in
the C6 / C1 ratio of sugars produced in infected tissue and an increase in enzyme systems associated
with the pentose-phosphate pathway. Increase in respiration rate was associated with a reduction in
photosynthesis, presumably as a result of destruction of chlorophyll and an increase in the NADP + /
NADPH ratio (Scott and Smillie, 1996).

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 Plant disease fisiology-The infection process

Fig.22.6 theories concerning stimulation of respiration in infected plant. (from Dickinson and Lucas, 1977)

Some workers have linked increases in oxygen consumption in infected plants to increases in
activity of enzyme systems such as the polyphenol oxidase and ascorbic acid oxidase systems.
These enzymes appear to be activated in diseased tissue. It has been suggest for example that
orthodiphenols which occur in healthy tissue are converted to orthoquinones in diseased tissue
due to the activity of the polyphenol oxidase systems.

The quinines produced may be toxic to the host cell’s protoplast and induce a necrotic response
in the host. Thus, systems such as those involving polyphenol oxidases give simple explanations
for increased oxygen consumption and perhaps hypersensitive necrosis. There is considerable
evidence to suggest that, in the case of biotrophs, a large number of organic and inorganic
substances accumulate in the infected area relative to healthy tissue. It is likely that disease
lesions act as “metabolic sinks” and that this leads to an increase in respiratory activity. There is
evidence that supports all of the theories discussed above as well as some not discussed in this
chapter. It is not at the moment to relate post infectional physiological changes in the host to
defence mechanisms of plants.

PHOTOSYNTHESIS AND TRANSLOCATION

Pathogens that attack the foliage of plants often cause destruction of photosynthetic tissue.
Outbreaks of diseases such as potato blight often completely defoliate plants. Many foliage
pathogens cause necrotic lesions which may cause a marked reduction in photosynthetic tissue.
It is been shown that infection causes marked reductions in the overall ability of plants to
photosynthesise and leads to a disruption in the translocation of photosynthate.

Severe rust infection on sunflower leaves* (24% leaf area covered with pustules) at the
sporulating stage of development can cause reductions of up to 34% in the uptake of labelled
carbon dioxide. In contrast, some environments moderate levels of infection (9% leaf area
covered with pustules) does not significantly affect uptake of 14CO2 relative to healthy leaves.
These observations suggest that moderate levels of rust infection in plant does not necessarily
affect the rate of 14CO2 uptake whereas high levels of infection result in marked reductions. It
has even been shown that under some conditions infection with bean rust ( Uromyces
appendiculatus) can cause an increase in the utilization of 14Co2 by bean tissue. In general
however, infection results in a reduction in photosynthetic activity either by destroying
photosynthetic tissue or by causing a reduction in the production of photosynthetic tissue.

The rate of translocation of photosynthate from diseased leaves is less than that from healthy
leaves. For example, severe rust infection in sunflower caused 97% of labelled assimilate to be
retained in the leaves where they were produced: only 3% was exported. In uninfected leaves

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 Plant disease fisiology-The infection process

between 30 and 58% assimilate was retained and the remaining 42 to 70% was exported to other
parts of the plant. It would seem that disease lesions caused by several biotrophs (rusts; powdery
mildews etc.) act as, “metabolic sinks” where various elements and compounds tend to
accumulate instead of being distributed to other parts of the plant. It has been shown that when
plants are fed with labelled element the element accumulate preferentially in the vicinity of
disease lesions. Various compounds therefore are not exported to other plant parts as a result of
the pathogen redirecting the host’s metabolism to suit its own requirement. Thus a nutrient stress
is placed on the host and its growth and yield may be affected.

The distribution pattern of assimilate translocated from leaves fed with 14CO2 is modified by rust
infection. During the vegetative stage of growth, the proportion of labelled translocate moving to
leaves was increased and that to roots was decreased by rust infection. This resulted in a
reduction in root development which led to a decrease in the root’s ability to absorb water and
nutrients which in turn affected growth of other plant parts.

TRANSPIRATION

Many pathogen have been shown to cause an increase in the rate of transpiration by plants.
Pathogens which damage the cuticle of plants often cause an increase in culticular (non-
stomatal) transpiration. This may be a major source of water loss and can occur in both light and
darkness. Culticular damage may cause plants to will, particularly during hot, dry weather.

Many pathogens can cause an increase in the rate of stomatal transpiration of plants. Stomatal
openings in the zone surrounding necrotic lesions in potato leaves infected with phytophthora
infestans have been shown to be abnormally wide.

Studies with sunflower plants have shown that rust infection did not significantly affect
transpiration (as measured by a diffusion porometer which measured diffusive movement of air
through stomates and thus gives an indication of the size of stomatal apertures which is related
to transpiration rates) until flecks became visible. After flecking a sharp increase in dark or
circular transpiration (or decrease in diffusive resistance) was observed due presumably to
cuticular damage. Rust infection did not appear to affect light or stomatal transpiration of plants
grown in an adequate moisture regime (Fig. 22.7).

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 Plant disease fisiology-The infection process

DAYS AFTER INOCULATION

Fig. 22.7. Diffusive resistance of uninfected leaves of sunflower.

However, when palnts were exposed to conditions of moisture stress, rust infection caused a
marked decrease in light diffusive resistance (Table 22.3). One would expect this to be related to
an increase in transpiration.
TABLE 22.3. Effect of rust infection at the sporulation stage of development and leaf water potential on the
diffusive resistance of sunflower leaves (from Siddiqui and Brown, unpublished)

Diffusive Resistensi (sec.cm-1)*

Leaf water potential (bar) Light Darkness

Uninfected Infected Uninfected Infected

3.9a 3.1a 43.6b 3.5a

- 4
3.0a 3.2a 41.2b 3.1a
- 7
37.6b 3.6a 37.9b 3.5a
- 12

* values followed by a different latter differ significantly (P=0.05)

It is likely that the water conserving mechanism (stomatal closure) that operates in healthy
plants fails to operate in diseased plants.

GROWTH AND DEVELOPMENT

Physiological disturbances resulting from infection ultimately lead to modification in the plant’s
growth and differentiation. For example, the effects of rust on growth and yield components of
sunflower are shown in table 22.4.
In addition to causing reductions in growth and loss if yield, some pathogens cause
disturbance to the hormonal balance in plants and abnormal growth and differentiation may
result in the formationof structures such as galls. Whether or not such changes are conducive to
the development of the pathogen depends on its substrate requirements. More details on
histogenic defence mechanisms will be given in the next chapter.
TABLE 22.3. Effect of rust on growth and yield parameters of sunflower.(from Siddiqui and Brown, 1977)

Parameter Uninfected (actual values obtained) Infected by inoculating plants every

10 days (%difference in relation to
uninoculated plants)

Leaves per plant 27 - 8

Leaf dry wt (g) 6 - 13

Plant height (cm) 189 - 13

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 Plant disease fisiology-The infection process

Stem dry wt (g) 16.04 + 62

Root dry (g) 2.86 - 70

Head dry (g) 5.86 - 77

Seeds per head 318 - 63

Dry wt seed/head (g) 13.76 - 81

Dry wt seed per 100 seeds (g) 45.99 - 55

% oil content 53 - 45

Total oil content 7.41 - 85

% fertility 56 - 32

Total plant dry wt (g) 46.4 - 65

Conclusions

The infection process can be divided into three phases; prepenetration, penetration and
postpenetration. If the infection process is blocked at any one of these phases, disease will not
develop. Development of pathogens during the prepenetration phase is influenced by exudates
on or near plant surfaces as well as by other physical, chemical and biological properties of the
plants surface. Pathogens may enter their host through natural openings, by directly penetrating
the, intact surface and through wounds.
The success of development during the postpenetration phase of infection is determined
by: (i) the substrate requirements of the pathogen and; (ii) the reactivity of the host to infection.
Pathogens can be divided into two groups on the basis of their substrate relationships namely,
necrotrophs and biotrophs. Necrotrophs obtain their nutrients from dead host cells which they
kill in advance of invasion. Biotrophs gain nutrients from living host cells. In general,
necrotrophs are less specialized parasites than biotrophs.
Host plants react to invasion by pathogens by producing necrogenic or histogenic
responses. The degree of necrogenic or histogenic response depends on the sensitivity of the
host to the presence of the pathogen. Whether or not a given host’s response confers
susceptibility or resistance to infection depends to a large extent on the substrate requirements of
the pathogen and the pathogen’s sensitivity to the host’s response.
Infected plants show many changes in physiology relative to healthy plants. Moreover
infection of plants by a range of pathogens produces similar changes in respiration, permeability,
accumulation of compounds in diseased tissue and an alteration of processes such as
photosynthesis and transpiration. However, detection and measurement of the effects of
infection on the host’s physiology has contributed little towards an understanding of the
specificity of host-pathogen compatibility.

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