Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Sulfur limitation increases nitrate and amino acid pools in tropical forages

Fabiana Schmidt A , Fabiano D. De Bona A B and Francisco A. Monteiro A C
+ Author Affiliations
- Author Affiliations

A Soil Science Department, University of São Paulo, Av. Pádua Dias 11, PO Box 9, Piracicaba, SP 13418-900, Brazil.

B National Wheat Research Center, Embrapa Trigo, Rodovia BR 285 294 km, PO Box 451, Passo Fundo, RS 99001-970, Brazil.

C Corresponding author. Email: famontei@usp.br

Crop and Pasture Science 64(1) 51-60 https://doi.org/10.1071/CP12336
Submitted: 29 September 2012  Accepted: 25 March 2013   Published: 22 April 2013

Abstract

Increasing the supply of sulfur (S) to forage plants can change their nitrogen (N) metabolism, causing changes in the N : S ratio that can potentially affect forage production and quality. The present study was focussed on revealing how supply (low, intermediate, high) of S affects amino acid composition and concentrations of total S, total N, sulfate-S, nitrate-N, and soluble protein in the leaves of tropical pasture species.

Greenhouse experiments were conducted in ground quartz (inert solid substrate) culture to examine the effect of S supply in two tropical species: Panicum maximum cv. Tanzania (Guinea grass) and Stylosanthes guianensis cv. Mineirão (stylo). Because legumes have greater S requirement than do grass species, application levels of S varied according to the species. Guinea grass was grown with 0.10, 0.55, 1.00, 1.45, and 1.90 mmol L−1 of S, and stylo with 0.10, 0.70, 1.30, 1.90 and 2.50 mmol L−1 of S. Plants of both species were harvested on two occasions.

Low S availability (0.10 mmol L−1) caused a nutritional imbalance with N in Guinea grass and stylo plants, as shown by a high N : S ratio (>60 : 1), and high concentrations of nitrate-N and free amino acids in plant tissues. Increased S supply regulated the N : S ratio at values close to 20 : 1, which provided N and S concentrations more suitable for protein synthesis and optimum forage production for both forage species. Asparagine was the predominant amino acid present in S-limited Guinea grass, whereas arginine was more abundant in S-limited stylo. This result indicates that a limitation of S increases nitrate-N and free amino acids while decreasing plant growth rates and soluble protein concentrations in these forage species.

Additional keywords: amino acid composition, N : S ratio, nitrate concentration, sulfur fertilisation, tropical forage species.


References

Amir R, Hacham Y (2008) Methionine metabolism in plants. In ‘Sulfur: a missing link between soils, crops, and nutrition’. (Ed. J Jez) pp. 251–279. (American Society of Agronomy, Crop Science Society of America, Soil Science Society of America: Madison, WI)

Azevedo RA, Arruda P, Turner WL, Lea PJ (1997) The biosynthesis and metabolism of the aspartate derived amino acids in higher plants. Phytochemistry 46, 395–419.
The biosynthesis and metabolism of the aspartate derived amino acids in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXms1Snt7g%3D&md5=241abe2f6e3d90efbdcd5374fdfad1bdCAS | 9332022PubMed |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=f2359dae153efeabc331775ee20adeedCAS | 942051PubMed |

Brunold C, Von Ballmoos P, Hesse H, Fell D, Kopriva S (2003) Interactions between sulfur, nitrogen and carbon metabolism. In ‘Sulfur transport and assimilation in plants: regulation, interaction, signaling’. (Eds J-C Davidian, D Grill, LJ De Kok, I Stulen, MJ Hawkesford, E Schnug, H Rennenberg) pp. 45–56. (Backhuys Publishers: Leiden, The Netherlands)

Case AA (1957) Some aspects of nitrate intoxication in livestock. Journal of the American Veterinary Medical Association 130, 323–329.

Cowling DW, Bristow AW (1979) Effects of SO2 on sulphur and nitrogen fractions on free amino acids in perennial ryegrass. Journal of the Science of Food and Agriculture 30, 354–360.
Effects of SO2 on sulphur and nitrogen fractions on free amino acids in perennial ryegrass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXitFCisg%3D%3D&md5=6b717f8473ff1d4cb607862eb408bc37CAS |

Crawford N, Kahn ML, Leustek T, Long SR (2000) Nitrogen and sulphur. In ‘Biochemistry and molecular biology of plants’. (Eds BB Buchanan, W Gruissem, RL Jones) pp. 786–849. (American Society of Plant Physiologists: Rockville, MD)

De Bona FD, Fedoseyenko D, Von Wirén N, Monteiro FA (2011) Nitrogen utilization by sulfur-deficient barley plants depends on the nitrogen form. Environmental and Experimental Botany 74, 237–244.
Nitrogen utilization by sulfur-deficient barley plants depends on the nitrogen form.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlChsrnJ&md5=aa578f8309648d5e959140d175d31199CAS |

Dijkshoorn W, Van Wijk SL (1967) The sulphur requirements of plants as evidenced by the sulphur nitrogen ratio in the organic matter: a review of published data. Plant and Soil 26, 129–157.
The sulphur requirements of plants as evidenced by the sulphur nitrogen ratio in the organic matter: a review of published data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2sXnsFarsw%3D%3D&md5=ec732c5122a35aed8a523c349d0f5cdbCAS |

Droux M (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynthesis Research 79, 331–348.
Sulfur assimilation and the role of sulfur in plant metabolism: a survey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsV2qtbc%3D&md5=6ed13fcf3b36a6da40338453241c2e6cCAS | 16328799PubMed |

Dubousset L, Abdallah M, Desfeux AS, Etienne P, Meuriot F, Hawkesford MJ, Gombert J, Ségura R, Bataillé MP, Rezé S, Bonnefoy J, Ameline AF, Ourry A, Le Dily F, Avice JC (2009) Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability. Journal of Experimental Botany 60, 3239–3253.
Remobilization of leaf S compounds and senescence in response to restricted sulphate supply during the vegetative stage of oilseed rape are affected by mineral N availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsValtro%3D&md5=c6abf27989300b2267a49ce5bf0eed5cCAS | 19553370PubMed |

Friedrich JW, Schrader LE (1978) Sulfur deprivation and nitrogen metabolism in maize seedlings. Plant Physiology 61, 900–903.
Sulfur deprivation and nitrogen metabolism in maize seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXltVertrc%3D&md5=84c96937fb34d8876644f5c8a0a75feeCAS | 16660422PubMed |

Haq IU, Carlson RM (1993) Sulphur diagnostic criteria for French prune trees. Journal of Plant Nutrition 16, 911–931.
Sulphur diagnostic criteria for French prune trees.Crossref | GoogleScholarGoogle Scholar |

Hawkesford MJ, De Kok LJ (2006) Managing sulphur metabolism in plants. Plant, Cell & Environment 29, 382–395.
Managing sulphur metabolism in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyltrg%3D&md5=f6d97a3e0454a8f3b455d526f320d638CAS |

Hirai MY, Fujiwara T, Awazuhara M, Kimura T, Noji M, Saito K (2003) Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition. The Plant Journal 33, 651–663.
Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-L-serine as a general regulator of gene expression in response to sulfur nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXislWiuro%3D&md5=094b2b0829eb30cfe869a82629387fe8CAS | 12609039PubMed |

Hoagland D, Arnon DI (1950) The water culture method for growing plants without soil. California Agricultural Experiment Station, Circular No. 347, Berkeley, CA.

Johnson CM, Nishita H (1952) Micro-estimation of sulphur in plant materials, soils and irrigation waters. Analytical Chemistry 24, 736–742.
Micro-estimation of sulphur in plant materials, soils and irrigation waters.Crossref | GoogleScholarGoogle Scholar |

Jones BN, Pääbo S, Stein S (1981) Amino acids analysis and enzymatic sequence determination of peptides by an improved o-phthaldialdehide precolumn labeling procedure. Journal of Liquid Chromatography 4, 565–586.
Amino acids analysis and enzymatic sequence determination of peptides by an improved o-phthaldialdehide precolumn labeling procedure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXktlyht7Y%3D&md5=786b55bf129a53899bf4048743b6771fCAS |

Karmoker JL, Clarkson DT, Saker LR, Rooney JM, Purves JV (1991) Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L.) roots. Planta 185, 269–278.
Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L.) roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXmtVOjsrc%3D&md5=dafaaa790932a202a2c7e0e6c59c536aCAS |

Kaur G, Chandna R, Pandey R, Abrol YP, Iqbal M, Ahmad A (2011) Sulfur starvation and restoration affect nitrate uptake and assimilation in rapeseed. Protoplasma 248, 299–311.
Sulfur starvation and restoration affect nitrate uptake and assimilation in rapeseed.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvFOjt7o%3D&md5=306dbe5f73d31e02a6a572b1462c76d1CAS | 20559852PubMed |

Lavres J, Monteiro FA, Schiavuzzo PF (2008) Sulphur concentration, SPAD value and yield of Marandu grass as related to sulphur supply. Brazilian Journal of Agricultural Sciences 3, 225–231.
Sulphur concentration, SPAD value and yield of Marandu grass as related to sulphur supply.Crossref | GoogleScholarGoogle Scholar |

Lea PJ (1993) Nitrogen metabolism. In ‘Plant biochemistry and molecular biology’. (Eds PJ Lea, RC Leegood) pp. 155–180. (Wiley: London)

Leustek T, Martin MN, Bick JA, Davies JP (2000) Pathways and regulation of sulfur revealed through molecular and genetic studies. Annual Review of Plant Physiology and Plant Molecular Biology 51, 141–165.
Pathways and regulation of sulfur revealed through molecular and genetic studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlsVymtro%3D&md5=4e2b6c8b34376fb1602cc3617bff78b6CAS | 15012189PubMed |

Manfredini D (2008) Calcium and boron for perennial soybean: anatomical and agronomic characteristics and nutrient concentrations. MSc Dissertation. University of São Paulo, Piracicaba, SP, Brazil.

Migge A, Bork C, Hell R, Becker TW (2000) Negative regulation of nitrate reductase gene expression by glutamine and asparagine accumulating in leaves of sulfur-deprived tobacco. Planta 211, 587–595.
Negative regulation of nitrate reductase gene expression by glutamine and asparagine accumulating in leaves of sulfur-deprived tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmt12itro%3D&md5=5963628a6472e21edabafd9f034fc5a8CAS | 11030559PubMed |

Monteiro FA (1986) Sulfur fertilization and nutrient distribution in a Florida spodosol profile under white clover-pensacola bahiagrass. PhD Dissertation. University of Florida, Gainsville, FL, USA.

Monteiro FA, Martins L, Castro JV, Liem TH (1983) Effects of levels of sulphur as gypsum for the growth of forage legumes in the State of São Paulo, Brazil. Journal of Animal Production Science 40, 229–240.

Nelson DW, Sommers LE (1973) Determination of total nitrogen in plant material. Agronomy Journal 65, 109–112.
Determination of total nitrogen in plant material.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXht1eisbs%3D&md5=275baa0e20561f73be78bc99377d3a7fCAS |

Nikiforova VJ, Kopka J, Tolstikov V, Fiehn O, Hopkins L, Hawkesford MJ, Hesse H, Hoefgen R (2005) Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants. Plant Physiology 138, 304–318.
Systems rebalancing of metabolism in response to sulfur deprivation, as revealed by metabolome analysis of Arabidopsis plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks12iu7Y%3D&md5=a039abc94cfe27719430803ffb20ff72CAS | 15834012PubMed |

Nikiforova VJ, Bielecka M, Gakière B, Krueger S, Rinder J, Kempa S, Morcuende R, Scheible W-R, Hesse H, Hoefgen R (2006) Effect of sulfur availability on the integrity of amino acid biosynthesis in plants. Amino Acids 30, 173–183.
Effect of sulfur availability on the integrity of amino acid biosynthesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1OksbY%3D&md5=6ea4273ed890f95a240bf7dd4ce07c9dCAS | 16552493PubMed |

Osweiler GD, Carson TL, Buck WB, Van Gelder GA (1985) ‘Clinical and diagnostic veterinary toxicology.’ (Kendall/Hunt Publishing Company: Dubuque, IA)

Prosser IM, Schneider A, Hawkesford MJ, Clarkson DT (1997) Changes in nutrient composition, metabolite concentrations and enzyme activities in spinach in the early stages of S-deprivation. In ‘Sulphur metabolism in higher plants’. (Eds WJ Cram, LJ De Kok, I Stulen, H Rennenberg) pp. 339–341. (Backhuys Publishers: Leiden, The Netherlands)

Prosser IA, Purves JV, Saker LR, Clarkson DT (2001) Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate. Journal of Experimental Botany 52, 113–121.
Rapid disruption of nitrogen metabolism and nitrate transport in spinach plants deprived of sulphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhvVOit7w%3D&md5=990a4a404525693cac1d04358649a74dCAS |

Saito K (2004) Sulfur assimilatory metabolism. The long and smelling road. Plant Physiology 136, 2443–2450.
Sulfur assimilatory metabolism. The long and smelling road.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOrtbo%3D&md5=c1073ad33d4f3f3a496124f8ecbdc3c2CAS | 15375200PubMed |

SAS Institute (SAS) (2004) ‘Statistical analysis system for Windows: Version 9.1.2.’ (SAS Institute: Cary, NC)

Sinclair A (1974) An autoanalyzer method for determination of extractable sulphate in plant material. Plant and Soil 40, 693–697.
An autoanalyzer method for determination of extractable sulphate in plant material.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXlvV2qtbk%3D&md5=e38b3e495409a0a687d12f4d6b1bee2dCAS |

Tabatabai MA (1982) Sulfur. In ‘Methods of soil analysis. Part 2’. (Eds AL Page, RH Miller, DR Keeney) pp. 501–538 (American Society of Agronomy: Madison, WI)

Tallec T, Diquelóu S, Fauveau C, Bataillé MP, Ourry A (2008) Effects of nitrogen and sulfur gradients on plant competition, N and S use efficiences and species abundance in a grassland plant mixture. Plant and Soil 313, 267–282.
Effects of nitrogen and sulfur gradients on plant competition, N and S use efficiences and species abundance in a grassland plant mixture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlyjsLfK&md5=3bdca38e4dfd59ef13462f254729c5b3CAS |

Tedesco MJ, Gianello C (1979) Set modulated glass steam distillation of ammonia by the Kjeldahl method. Brazilian Journal of Soil Science 3, 61–63.

Tedesco MJ, Gianello C, Bissani CA, Bohnen H, Volkweiss SJ (1995) ‘Soil, plant and other materials analysis’. (Departamento de Solos/UFRGS: Porto Alegre, BR)

Thomas SG, Bilsborrow PE, Hocking TJ, Bennett J (2000) Effect of sulphur deficiency on the grown and metabolism of sugar beet (Beta vulgaris cv Druid). Journal of the Science of Food and Agriculture 80, 2057–2062.
Effect of sulphur deficiency on the grown and metabolism of sugar beet (Beta vulgaris cv Druid).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslGmtr4%3D&md5=79f5c16c8d5c3085826dc9e35ec21445CAS |

Wright MJ, Davison KL (1964) Nitrate accumulation in crops and nitrate poisoning in animals. Advances in Agronomy 16, 197–247.
Nitrate accumulation in crops and nitrate poisoning in animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF2MXisFaltg%3D%3D&md5=98c03ad293f4412a45ad68291d715ac6CAS |