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    • Abstract: Sulphur -a general overview and interaction with nitrogen. Arshad Jamal. 1,* , Yong-Sun Moon. 1 , Malik Zainul ... To minimize the gap between the demand and supply of cereals, oilseeds and pulses, intensive efforts are being made to increase ...

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AJCS 4(7):523-529 (2010) ISSN:1835-2707
Review article
Sulphur -a general overview and interaction with nitrogen
Arshad Jamal1,*, Yong-Sun Moon1, Malik Zainul Abdin2
1
Department of Horticulture Science, College of Natural Resources, Yeungnam University, Gyeongsan 712-749,
Republic of Korea
2
Department of Biotechnology, Faculty of Science, Jamia Hamdard, New Delhi-110062, India
*Corresponding author: [email protected]
Abstract
To minimize the gap between the demand and supply of cereals, oilseeds and pulses, intensive efforts are being made to increase their
production. As ever-increasing population and urbanization cannot allow increase in the land area under the cultivation of cereals,
oilseeds and pulses anymore due to the pressure on land, hence, yield per unit area needs to be improved further. To achieve this
objective, agricultural scientists have laid more emphasis on improving production of oilseeds and pulses through proper nutrition of the
crops by evolving high yielding varieties and adopting improved agronomic practices as well as plant protection measures, etc. The most
important constraints to crop growth are those caused by the shortage of plant nutrients. Sulphur (S) requirement of plants has become
increasingly importance in India as well as world agriculture. However, to achieve high yields and rates of S fertilizer should be
recommended on the basis of available soil S and crop requirement.
Keywords: Nitrogen, Sulphur, Fertilizer, Quality, Yield
Introduction
With the improvement of crop productivity through the soil with adequate amounts of S. Now, areas of S deficiency are
adoption of high-yielding varieties and multiple cropping becoming widespread throughout the world due to the use of
systems, fertilizer use has become more and more important to high-analysis low S fertilizers, low S returns with farmyard
increase crops yield and quality. S is an essential plant nutrient manure, high yielding varieties and intensive agriculture,
for crop production. For oil crop producers, S fertilizer is declining use of S containing fungicides and reduced
especially important because oil crops require more S than atmospheric input caused by stricter emission regulation. An
cereal grains. For example, the amount of S required to produce insufficient S supply can affect yield and quality of the crops,
one ton of seed is about 3-4 kg S for cereals (range 1-6); 8 kg S caused by the S requirement for protein and enzyme synthesis
for legume crops (range 5-13); and 12 kg S for oil crops (range as well it is a constituent of the amino acids, methionine and
5-20). In general, oil crops require about the same amount of S cysteine. To overcome the problems associated with S
as, or more than, phosphorus for high yield and product quality. deficiency a number of S-containing fertilizers as well as other
In intensive crop rotations including oil crops, S uptake can be S containing by-products from industrial processes are
very high, especially when the crop residue is removed from the available. The information on impact of S-fertilization and S in
field along with the product. This leads to considerable S general has been reviewed and presented under the following
depletion in soil if the corresponding amount of S is not applied heads: The function of S, Soil organic S, Soil inorganic S, S
through fertilizer. S is increasingly being recognized as the deficiency in soil, Sulphur and nitrogen interaction in soil,
fourth major plant nutrient after nitrogen, phosphorus and Sulphur and nitrogen interaction in plant , Sulphur and nitrogen
potassium. The importance of S in agriculture is being interaction in relation to yield and quality of crop, Sulphur and
increasingly emphasized and its role in crop production is well nitrogen interaction in relation to uptake and assimilation of
recognized (Jamal et al., 2005, 2006a; 2006b; 2006c; 2009; sulphur and nitrogen, N:S ratio in relation to sulphur and
2010; Scherer, 2009). S is best known for its role in the nitrogen interaction.  
formation of amino acids methionine (21% S) and cysteine
(27% S); synthesis of proteins and chlorophyll; oil content of The functions of S
the seeds and nutritive quality of forages (Tandon, 1986; Jamal
et al., 2005, 2006a; 2009). Although S is one of the essential The range of biological compounds that contain sulfur is vast. S
nutrients for plant growth with crop requirement similar to is found in vitamins viz, biotin and thiamine; cofactors S-
phosphorus, this element received little attention for many adenosyl-L-methionine, coenzyme A, molybdenum cofactor
years, because fertilizers and atmospheric inputs supplied the (MoCo), and lipoic acid; the chloroplast lipid sufloquinovosyl
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diacylglycerol; and many secondary compounds (Leustek, (Barber, 1995). Sulphur may precipitate in form of SO42- as
2002, Leustek and Saito, 1999). It also serves important calcium, magnesium or sodium sulphate. In tidal marshlands
structural, regulatory and catalytic functions in the context of large amounts of sulphide metals like pyrite (FeS2) accumulate.
proteins, and as a major cellular redox buffer in the form of the After draining these areas, the S compounds are oxidized to
tripeptide glutathione and certain proteins such as thioredoxin, SO42- accompanied by a decrease in pH. If adsorbed SO42- in
glutaredoxin and protein disulfide isomerase. A feature of many soil is not readily available to plants, any treatment causing a
sulfur-containing compounds is that the S moiety is often decrease in retention and a corresponding increase of SO42- in
directly involved in the catalytic or chemical reactiveness of the soil solution should increase SO42-availability to plants (Elkins
compound. A superb example is the way in which cysteine and Ensminger, 1971). Mehlich (1964) found that the release of
residues in proteins sometimes form covalent disulfide bonds. adsorbed SO42- was in relation to the addition of successive
Disulfides can, in turn, be reduced to the thiol form by increments of Ca (OH)2, which is assumed to be the result of
glutathione or redox proteins like thioredoxin (Leustek and increased pH. Therefore, little SO42- adsorption is to be
Saito, 1999; Saito, 2000). For some enzymes, disulfide bond expected in surface soils which are adequately limed (Evans,
formation serves to regulate activity. Many enzymes of carbon 1986) and consequently the joint application of limestone and
dioxide fixation are regulated in this way as a means to gypsum results in an increased availability of SO42- (Serrano et
coordinate their activity with the light reactions of al., 1999). The higher concentration of SO42- in the soil solution
photosynthesis. The regulatory molecule in this case is of the uppermost soil layer (Eriksen, 1996) may also be caused
thioredoxin, which reduces target enzymes using electrons from by the application of S containing fertilizers and other S inputs.
ferredoxin (Leustek and Saito, 1999; Saito, 2000; Scherer, Further, it may be assumed that surface soil material adsorbs
2001; Matsubayashi et al., 2002). less SO42- than does subsoil material, because organic matter
and phosphate accumulations are thought to be major factors,
Soil organic S which block SO42- adsorption sites. Barton et al., (1999) found
that deeper profile layers showed less capacity for SO42- -
Up to 98% of the total soil S may be present as organic S adsorption. Couto et al., (1979) detected that the adsorption of
compounds and is associated with a heterogeneous mixture of SO42- is increased with the depth in the soil profile. According
plant residues, animals and soil microorganisms (Bloem 1998). to their results, this difference between the horizons is assumed
The profile of organic S concentration generally follows the to be caused by the higher organic matter content in the topsoil.
pattern of organic matter concentration in soils with depth Johnson and Todd (1983) found that SO42- - adsorption is
(Probert, 1980). Soil organic S is divided in two main groups: negatively correlated with the soil organic matter content as the
the first group contains S atom in the oxidized state and the adsorption sites of Fe and Al hydroxides can be blocked by
other group contains S atom in the reduced state. According to anionic groups of organic matter. Further, organic anions in
results of Stevenson (1986) between 1 and 3% of the soil soils, which are derived from decomposition of organic
organic S can be accounted for the part of microbiological materials, may affect SO42- -adsorption by occupying adsorption
biomass, while more recent investigations suggest that the soil sites (Martinez et al., 1998) by their preferential adsorption
microbiological biomass S generally accounts for 1.5 -5% of based on the number of oxygen containing functional groups
total soil organic S (Banerjee et al., 1993; Wu et al., 1993). (Inskeep, 1989).
Proteins and amino acids are the major form of S in microbial
cells (Banerjee and Chapman, 1996). Based on dry weight, the S deficiencies in soil
S concentration of most soil microorganisms is ranges between
1 and 10µg/g, the C:S ratio between 57:1 and 85:1 and the N:S S deficiency in crops has only recently become widespread
ratio is about 10:1. However, there is evidence that the C:S ratio (Scherer, 2001). Previously, sufficient S to meet crop
in the biomass is not fixed, but may vary quite rapidly, requirements was obtained from the frequent incidental
depending on the supply of S. When S becomes a limiting additions of S to soils when N and P fertilizers, such as
factor, either because of low S concentrations in the substrate or ammonium sulphate and single superphosphate, were applied.
where plant uptake is competing, the C:S ratio of the biomass Industrial pollution as a result of coal combustion also
may reach values between 80 and 100 (Banerjee et al., 1993). contributed substantial amounts of S for plant needs by aerial
The microbiological biomass is relatively labile and thought to deposition. Over the last two decades, however, there has been
be the most active pool for S turnover in soil (Stevenson, 1986). a fundamental shift in the S balance toward deficit in
Generally, the application of organic matter to soil increases the agricultural systems for several reasons. High analysis N and P
microbiological biomass including microbial S. Further fertilizers have gradually replaced traditional ones that contain
microbial S seems to increase with temperature and to decrease S. In addition, yields of agricultural crops have increased
at low soil moisture content (Gupta and Germida, 1989; Ghani markedly, and in some cases more than doubled, during the last
et al., 1990). In incubation studies of Wu et al., (1993), 20% of two decades, resulting in increased removal of nutrients,
the S in barley straw and about 30% of the S from leaves of including S from soils (Scherer, 2001). In intensive crop
oilseed rape incorporated into the soil were converted to rotations including oil crops, S uptake can be very high,
microbial S after 5 days at 250C. especially when the crop residue is removed from the field
along with the product. This leads to considerable S depletion
Soil inorganic S in soil if the corresponding amount of S is not applied through
fertilizer. It is now well established that S deficiency is wide
Inorganic S is usually much less abundant in most of the spread in Indian soils, and in all probability is on the increase. S
agricultural soils than is organically bound S (Bohn et al., deficiency which was noticed many years ago only in localized
1986). Sulphate is the most common form of inorganic S and areas has engulfed much larger area in its fold (Takkar, 1987).
can be divided into SO42- in soil, adsorbed SO42- and mineral S In 1986, ninety districts had been identified to have S-
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deficiency problem of varying degree and intensity (Tandon, 1998; Ahmad et al, 1999; Ahmad and Abdin 2000; Fazli et al.,
1986). In 1991, the number of S-deficient districts increased to 2005; Fazili et al., 2010a; 2010b), sunflower (Hocking et al.,
about 120 (Tandon, 1991). It has been reported that in India 1987) linseed (Verma and Swarankar, 1986) Groundnut (Jamal
more than 41% of soil are deficient in S (Singh, 2001). When a et al., 2006a; 2010) and Soybean (Jamal et al., 2005; 2006b).
soil is deficient in S and the deficiency is not rectified, then full Aulakh et al., (1977) reported the maximum grain yield in
potential of a crop variety can not be realized, regardless of top mustard was obtained with 30 kg S ha-1 supplied as gypsum
husbandry practices (Eppendorfer, 1971). along with 120 kg N ha-1 as urea. Aulakh et al.,(1980), based on
the results of three years of field experiments on mustard,
Sulphur and nitrogen interaction in soil reported that maximum yields of oil were obtained when both
N (75 kg ha-1) and S (60 kg ha-1) rates were high, which
An intensive agriculture with use of improved cultivars and indicate significant S and N interaction. The combined
high analysis fertilization offers conditions of nutrients application of S and N had the largest effect on the
exhaustion resulting in nutrient imbalance in soils. Fazili et al., concentration and uptake of S and N and on protein and oil
(2008) reported that lack of S limits the efficiency of added N, content of grains, and their yield. A field study involving S and
therefore, S addition becomes necessary to achieve maximum N interaction on the yield of turnip rape (Brassica campestris
efficiency of applied nitrogenous fertilizer. Kowalenko and L.) was conducted by Janzen and Bettany (1984), and it was
Lowe (1975) noticed that a high N:S ratio (produced by demonstrated that seed production is very sensitive to S
addition of N) resulted in a decrease in mineralization of S in deficiency. The maximum yield responses of rapeseed to S and
the soil sample during incubation. Janzen and Bettany (1984) N were observed only when the availability of S and N was in
indicated the optimum ratio of available N to available S to be approximate balance. Application of nitrogen alone suppressed
7:1. Ratios below 7 gave the reduced seed yields. A rapeseed the seed yields, whereas S alone produced no seed yield
and mustard crop under field conditions recovered 27-31% of response. McGrath and Zhao (1996) observed an increase of
added S without N, but 37-38% with 60 kg N ha-1 (Sachdev and 42-267% in seed yield of Brassica napus with the application
Deb, 1990). of 40 kg S ha-1 with 180 and 230 kg N ha-1. Seed yield was
found to decrease, when N was applied at the rate of 180-230
Sulphur and nitrogen interaction in plant kg ha-1 without S. In field trials on a soil testing 5.6 ppm
available S, 2.5% increase in mustard oil yield due to S and N
Because of central role of S and N in the synthesis of proteins, application could be attributed to their synergistic effect
the supplies of these nutrients in plants are highly inter-related. (Sachdev and Deb, 1990). Shinde et al., (1980) noted the
Sulphur and nitrogen relationships were established in many significant S and N interaction in winter wheat. The crop did
studies (Zhao et al., 1993; McGrath and Zhao 1996; Ahmad et not respond to S application when N was deficient of optimum,
al., 1998; and Jamal et al., 2005; 2006a; 2010) in terms of dry and S applied with excess N increased straw but not grain yield.
matter and yield in several crops. Barney and Bush (1985), In wheat crop, the yield increased linearly in the S and N
while working on tobacco plant concluded that there was interaction study (Reneau et al., 1986) with increased N
apparent accumulation of one nutrient when the other nutrient application. It was further suggested that S concentration of
was limited and that accumulated nutrient was used in protein 0.2% and a N/S ratio of 18 in the flag leaf is sufficient for
synthesis when the treatment were reversed. A shortage in the S obtaining higher yields, while Mahler and Maples (1987)
supply to the crops lowers the utilization of the available soil noticed that a minimum S concentration and N:S ratio of wheat
nitrogen, thereby increasing nitrate leaching (Likkineni and tissue for maximum yield were 1050 and 16.5 ppm,
Abrol, 1994). O'Connor and Vartha (1969) observed that large respectively. Hocking et al., (1987) reported a decrease of 30%
dose of gypsum reduced the yield of hay when N status in soil in cysteine and methionine concentration in seeds of S deficient
was unsatisfactory. Likewise, large dose of N created S but N sufficient sunflower plants. Baily (1986) compared
deficiency (Eppendorfer, 1971). It has been established that for alfalfa, rape and barley in their sulphur response and
every 15 parts of N in protein there is 1 part of S which implies requirements. Barley was the most responsive to applied S,
that the N:S ratio is fixed within a narrow range of 15:1. The although it had the lowest concentration of S (0.15 mg S g-1 dry
N:S ratio in the whole plant in general is 20:1 (Cram, 1990). herbage) and highest plant N:S ratio (16) at its highest yield.
Clarkson et al., (1989), while working on barley plants, Dev and Kumar (1982) reported N:S ratio of 15.6, 3.1, 14.8 and
demonstrated that at the whole plant level the apparent 7.1 in grain for maximum response to sulphur in maize,
matching of supply to demand is accompanied by an apparent mustard, groundnut and wheat, respectively. There is a very
linkage of SO42- to NO3- uptake. Sulfur and nitrogen both are narrow range in the N:S ratio that ensures optimum yield and
required for the synthesis of protein, therefore, the ratio of total quality of the crop, and unbalanced fertilizer use adversely
N to total S in plant tissue can reflect the ability of N and S in affects crop production. Sulphur deficiency causes profound
protein synthesis (Brunold and Suter, 1984). Thus, a change in changes in N metabolism with reduced protein synthesis and
the ratio of reduced-N to reduced-S (NR/SR), which is a accumulation of soluble organic and inorganic nitrogenous
reflection of the amount of S amino acids, suggests that protein compounds. Lack of S is accompanied by nitrate accumulation
metabolism has been significantly altered and has important and proteolysis resulting in the formation of NH4+ and organic-
implications for protein quality (Friedrich and Schrader, 1978). N compound such as amide and amino acids (Charliers and
Carpenter, 1956). Amounts of cysteine and methoinine were
Sulphur and nitrogen interaction in relation to yield and lower in S-deficient rice plants and occurrence of asparagine
quality of crops and arginine was thought to indicate abnormal S and N
metabolism (Beaton, 1966). When NO3 was limited in the
A strong interaction of S and N for seed yield was found in nutrient solution or there was a lack of S in the tissue,
rapeseed and mustard (McGrath and Zhao, 1996; Ahmad et al, repression of NR activity resulted. A positive role of sulphate in
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regulating nitrate reductase {an enzyme that perform the rate- kg N ha-1. Randall et al., (1981) observed that S application
limiting step of the nitrate assimilation pathway Beevers and increased the wheat grain S concentration more with low N
Hageman, (1969)}, was reported by Pal et al., (1976), and treatment, but had only small effects on N concentration in
Friedrich and Schrader (1978). Smith (1975) observed the role grain. However, N application increased the grain S
of nitrogen in the regulation of sulphate assimilation at the concentration at high but not at low S and increased grain N
ATP-sulphurylase step. The work of Jamal et al., (2006b) and concentration in all S treatments.
Ahmad et al., (2007) showed that sulphur availability has a role
in regulating nitrate reductase, in addition to its role in N:S ratio in relation to sulphur and nitrogen interaction
regulating ATP-sulphurylase. Moreover, nitrogen availability
has a role in regulating ATP-sulphurylase as well as in A number of studies on S requirement of the crop in relation to
regulating nitrate reductase. The synthesis of cysteine as a N have been reported (Jamal et al., 2005; 2006a, 2006b, 2009,
result of the incorporation of sulphide moiety into O- 2010). There is a significant positive S x N interaction in
acetylserine appears to be the meeting point between N-and S- relation to the oil content and yield. Adequate N: S ratio has
metabolism. Naturally occurring thiol compounds viz., cysteine been found to be 7.5:1 in grains, above which deficiency of S
and glutathione were shown to influence nitrate reductase can be observed (Aulakh et al., 1980). There is a strong
activity in wheat and Brassica (Lakkineni and Abrol, 1992; relationship between S and N content in plants. The ratio of
Ahmad et al., 1999). It has also been reported (Lopez-Jurado total N to total S and protein S determine the degree of
and Hunnway, 1985; Jamal et al., 2010) that S is specifically availability of deficiency of S in protein. The N and S ratio is
involved in nitrogen fixation in legumes and S additions often preferred over concentration as a diagnostic criterion for S
significantly increased N2 fixation, nodule weight plant-1, deficiency (Stewart and Whitefield, 1965). The total S content
nodule weight per unit weight of root and N2-fixation per unit in plant tissues varies among plant species. In greenhouse trails
weight nodule. Friedrich et al., (1977) also observed severe with subterranean clover, N: S ratio was shown to be less
reduction in nitrate reductase activity (NRA) in S-deprived variable with plant age and N supply than total S and total
maize seedlings. sulphate (Freney et al., 1977). Experiments with rapeseed
showed that the N:S ratio of rapeseed tops sampled at the
Sulphur and nitrogen interaction in relation to uptake and rosette stage was very sensitive and changes due to change in
assimilation of sulphur and nitrogen sites, year and seed varieties and these changes were sometimes
greater than differences between S deficient and S sufficient
Nitrogen increased utilization of fertilizer-S in plants (Dhankar rapeseed (Maynard et al., 1983). Dev and Saggar (1974)
et al., 1995). Eppendorfer (1971) observed that large doses of N observed that S application lowered total N: total S ratios in
created a deficiency of S. Application of S in the absence of N soybean. It was also shown that at the S levels where
decreased the N concentration in mustard plants, but when N consistency in total N and total S ratios was obtained, one part
was added, the effect was synergistic (Dev and Kumar, 1982). of S was required for every 14 and 16 parts of N in protein
However, N content in Chinese cabbage was found to increase formation in different varieties of soybean. Dev et al., (1981)
marginally with sulphur application (Hazra, 1988). Kastori and reported that application of 20 kg S ha-1 lowered N: S ratio in
Jocic (1995) reported high positive correlation between S and N mustard seeds from a range of 14:1-16:1 to 11:1- 12:1 and it
content on wheat. Application of S in the absence of N was further reduced to 10:1, when S was applied at 40 kg ha-1.
decreased nitrogen concentration in mustard plants, but when N Aulakh et al., (1977) found N: S ratio of 15.5:1 in plant tissue
was added, the effect was synergistic (Dev and Kumar, 1982). of mustard to be critical, above which the inadequacy of S may
Similar results were reported for amide S and N in sunflower by cause drastic reduction in grain yield.
Sharma and Dev (1980). Fazli et al., (2008) found that uptake
of N was considerably reduced under S deficiency in E. sataiva. Conclusion
Aulakh et al., (1977, 1980) noticed the positive and significant
interaction between applied S and N in plant tissues of brown Sulphur is an important nutrient for plant growth and
sarson. The concentration of S and N in brown sarson was the development. Sulphur interactions with nitrogen nutrients are
highest with combined application of 75 kg N ha-1 and 60 kg S directly related to the alteration of physiological and
ha-1. Janzen and Bettany (1984) reported that application of S biochemical responses of crops, and thus required to be studied
and N increased their respective uptake by rapeseed. However, in depth. This would help to understand nutritional behaviour of
the effect of N rate on S uptake varied with S application rate. sulphur in relation to nitrogen nutrients and provide guidelines
Sulphur application had no appreciable effect on N uptake at for inventing balanced fertilizer recommendations in order to
low N application rates but significantly enhanced dry matter optimise yield and quality of crops.
produced. Singh et al., (1980) reported S and N interaction non-
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