Symptomatology of Single Plants
Visual diagnosis of sulfur deficiency in production fields requires adequate expertise and needs to
involve soil or plant analysis (141)
. The literature describes symptoms of sulfur deficiency as being
less specific and more difficult to identify than other nutrient deficiency symptoms (142–145)
symptomatology of sulfur deficiency is very complex and shows some very unique features. In this
section, the basic differences in sulfur deficiency symptoms of species in the Gramineae representative
of monocotyledonous, and species in the Cruciferae and Chenopodiaceae representative of
dicotyledonous crops will be given for individual plants and on a field scale.
When grown side by side and under conditions of sulfur starvation, crops begin to develop
sulfur deficiency symptoms in the order of oilseed rape (canola), followed by potato, sugar beet
(Beta vulgaris L.), beans (Phaseolus vulgaris L.), peas (Pisum sativum L.), cereals, and finally
maize. The total sulfur concentration in tissue corresponding to the first appearance of deficiency
symptoms is highest in oilseed rape (3.5 mg g-1
S), and lowest in the Gramineae (1.2 mg g-1
Potato and sugar beet show symptoms at higher concentrations (2.1 to 1.7 mg g-1
S) than beans or
peas (1 to 1.2 mg g-1
Brassica species, such as oilseed rape, develop the most distinctive expression of symptoms of
any crop deficient in sulfur. The symptoms are very specific and thus are a reliable guide to sulfur
deficiency. There is no difference in the symptomatology of sulfur deficiency in high and low glucosinolate-
containing varieties (103)
. The symptomatology of sulfur deficiency in brassica crops is
characteristic during the whole vegetation period and is described below for specific growth stages
according to the BBCH scale (146)
. Symptoms generally apply to dicotyledonous plants, except
when specific variations are mentioned in the text. Colored guides of sulfur deficiency symptoms
are provided by Bergmann (143)
and Schnug and Haneklaus (53,114,147)
Even before winter, during the early growth of oilseed rape, leaves may start to develop visible
symptoms of sulfur deficiency. As sulfur is fairly immobile within the plant (13)
always show up in the youngest leaves. Though the plants are still small, symptoms can cover
the entire plant. Sulfur fertilization before or at sowing will ensure a sufficient sulfur supply, particularly
on light, sandy soils, and will promote the natural resistance of plants against fungal
Oilseed rape plants suffering from severe sulfur deficiency show a characteristic marbling of the
leaves. Leaves begin to develop chlorosis (149–154)
, which starts from one edge of the leaves and
spreads over intercostal areas; however, the zones along the veins always remain green (103,155)
The reason for the green areas around the veins is most likely the reduced intercellular space in that
part of the leaf tissue, resulting in shorter transport distances and a more effective transport of sulfate.
Sulfur-deficient potato leaves show the same typical color pattern and veining as oilseed rape,
whereas sugar beet, peas, and beans simply begin to develop chlorosis evenly spread over the leaf
without any veining (156,157)
. A comparative evaluation of crop-specific, severe sulfur deficiency
symptoms is given in Figure 7.7.
|FIGURE 7.7 Macroscopic sulfur deficiency symptoms of oil seed rape (Brassica napus L.), cereals, and
sugar beet (Beta vulgaris L.) at stem extension and row closing, respectively (from left to right).
|FIGURE 7.8 Marbling, spoon-like leaf deformations and anthocyanin enrichments of sulfur-deficient
oilseed rape plants (Brassica napus L.) (from left to right).
Chlorosis very rarely turns into necrosis (103,157)
as it does with nitrogen and magnesium
deficiencies, and is an important criterion for differential diagnosis. Even under conditions of
extreme sulfur deficiency, an oilseed rape plant will not wither. The intensity of sulfur deficiency
symptoms of leaves depends on the nitrogen supply of the plants. In general,
a high nitrogen supply promotes the expression of sulfur deficiency symptoms and vice versa (158)
A characteristic secondary symptom of severe sulfur deficiency is a reddish-purple color due to
the enrichment of anthocyanins in the chlorotic parts of brassica leaves (Figure 7.8). Under field
conditions, the formation of anthocyanins starts 4 to 7 days after chlorosis. The phenomenon is initialized
by the enrichment of carbohydrates in the cells after the inhibition of protein metabolism.
Plants detoxify the accumulated carbohydrates as anthocyanates, which result from the reaction
with cell-borne flavonols to avoid physiological disorders (159–165)
. Many other nutrient
deficiencies are also accompanied by formation of anthocyanins, which therefore is a less specific
indicator for sulfur deficiency.
In particular, leaves which are not fully expanded produce spoon-like deformations when struck
by sulfur deficiency (Figure 7.8). The reason for this is a reduced cell growth rate in the chlorotic
areas along the edge of the leaves, while normal cell growth continues in the green areas along the
veins, so that sulfur-deficient leaves appear to be more succulent. The grade of the deformation is
stronger the less expanded the leaf is when the plant is struck by sulfur deficiency. Marbling, deformations,
and anthocyanin accumulation can be detected up to the most recently developed small
leaves inserted in forks of branches (Figure 7.8).
|FIGURE 7.9 White flowering (left) and morphological changes of petals (right) of sulfur-deficient oilseed
rape (Brassica napus L.).
The higher succulence of sulfur-deficient plants (143,166)
was suspected to be caused by enhanced
chloride uptake due to an insufficient sulfate supply (159)
. However, with an increase of chloride concentrations
by 0.4 mg Cl g-1
on account of a decrease of sulfur concentrations by 1 mg g-1
this effect seems to be too small to justify the hypothesis (103)
. More likely, the above-explained
mechanical effects of distortion, together with cell wall thickening, cause the appearance of increased
succulence due to the accumulation of starch and hemicellulose (167)
During flowering of oilseed rape, sulfur deficiency causes one of the most impressive symptoms
of nutrient deficiency: the ‘white blooming’ of oilseed rape (Figure 7.9). The white color presumably
develops from an overload of carbohydrates in the cells of the petals caused by disorders in protein
metabolism, which finally ends up in the formation of colorless leuco-anthocyanins (168)
. As with
anthocyanins in leaves, the symptoms develop most strongly during periods of high photosynthetic
activity. Beside the remarkable modification in color, size, and shape of oilseed rape, the petals
change too (Figure 7.9). The petals of sulfur-deficient oilseed rape flowers are smaller and oval
shaped, compared with the larger and rounder shape of plants without sulfur-deficiency symptoms (169)
. The degree of morphological changes, form, and color, are reinforced by the strength and
duration of severe sulfur deficiency (53)
. The fertility of flowers of sulfur-deficient oilseed rape
plants is not inhibited. However, the ability to attract honeybees may be diminished and can be of
great importance for the yield of nonrestored hybrids, which need pollination by insect vectors (169)
The strongest yield component affected by sulfur deficiency in oilseed rape is the number of
seeds per pod, which is significantly reduced (103)
. As described earlier for leaves, the branches and
pods of S-deficient plants are often red or purple colored due to the accumulation of anthocyanins
(Figure 7.10). Extremely low numbers of seeds per pod, in some cases even seedless ‘rubber pods,’
are characteristic symptoms of extreme sulfur deficiency (Figure 7.10).
Symptomatology of Monocots
The symptoms in gramineous crops such as cereals and corn are less specific than in cruciferous
crops. In early growth stages, plants remain smaller and stunted and show a lighter color than plants
without symptoms (170)
. The general chlorosis is often accompanied by light green stripes along
the veins (Figure 7.11) (170–172)
. Leaves become narrower and shorter than normal (173)
|FIGURE 7.10 Enrichment of anthocyanins during ripening of oilseed rape (Brassica napus L.) (left) and reduction
of number of seeds per pod (right).
|FIGURE 7.11 Macroscopic sulfur deficiency symptoms of winter wheat (Triticum aestivum L.) at stem
There is no morphological deformation to observe, and usually no accumulation of anthocyanins
either. Although the symptoms are very unspecific and are easily mistaken for symptoms of nitrogen
deficiency, their specific pattern in fields provides good evidence for sulfur deficiency. Owing to an
early reduction of fertile flowers per head, sulfur-deficient cereals are characterized by a reduced number
of kernels per head, which alone, however, is not conclusive evidence for sulfur deficiency (174)
Sulfur Deficiency Symptoms on a Field Scale
Some characteristic features in the appearance of fields can provide early evidence of sulfur
deficiency. Sulfur deficiency develops first on the light-textured sections of a field. From above,
these areas appear in an early oilseed rape crop as irregularly shaped plots with a lighter green color
(wash outs). The irregular shape distinguishes the phenomenon from the regular shape of areas
caused by nitrogen deficiency, which usually originates from inaccurate fertilizer application
(Figure 7.12). Owing to frequent soil compaction and limited root growth, sulfur deficiency develops
first along the headlands and tramlines or otherwise compacted areas of a field.
|FIGURE 7.12 Chlorotic patches in a field (left) and resultant effects on mature plants (right), indicating
severe sulfur deficiency symptoms in relation to soil characteristics.
The appearance of sulfur-deficient oilseed rape fields is more obvious at the beginning of blooming;
white flowers of oilseed rape are distinctively smaller and therefore much more of the green
undercover of the crop shines through the canopy of the crop. Another very characteristic indicator of
a sulfur-deficient site is the so-called second flowering of the oilseed rape crop. Even if a sulfurdeficient
crop has finished flowering, it may come back to full bloom if sufficient sulfur is supplied.
The typical situation for this action comes when a wet and rainy spring season up until the end of
blooming is followed suddenly by warm and dry weather. During the wet period precipitation, water,
which has only one-hundredth to one-tenth the sulfur concentrations of the entire soil solution, dilutes
or leaches the sulfate from the rooting area of the plants, so that finally plants are under the condition
of sulfur starvation. With the beginning of warmer weather, evaporation increases and sulfur-rich subsoil
water becomes available to the plants and causes the second flowering of the crop. During maturity,
sulfur deficiency in oilseed rape crops is revealed by a sparse, upright-standing crop.
Similarly, in cereals, sulfur deficiency develops first on light-textured parts of the field, yielding
irregularly shaped ‘wash-out’ areas in images from above. Nitrogen fertilization promotes the
expression of these irregularly distributed deficiency symptoms, such as uneven height and color.
The irregular shape distinguishes these symptoms from areas caused by faulty nitrogen fertilizer
application. In the field, these particular zones can be identified by a green yellowish glow in the
backlight before sunset. Later, vegetation in these areas resembles a crop that is affected by drought.
Owing to an inferior natural resistance, the heads in sulfur-deficient areas
can be infected more severely by fungal disease (e.g., Septoria species), which gives these areas a
darker color as the crop matures.