Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-07T08:34:51.367Z Has data issue: false hasContentIssue false
  • English
  • Français

Sulfur fertilization increases defense metabolites and nitrogen but decreases plant resistance against a host-specific insect

Published online by Cambridge University Press:  24 October 2017

N.A. Santos ,
N.C. Teixeira ,
J.O.S. Valim ,
E.F.A. Almeida ,
M.G.A. Oliveira  and
W.G. Campos
N.A. Santos
Affiliation:
Department of Biosystems Engineering, Federal University of São João del Rei, São João del Rei, MG, 36301-160, Brazil
N.C. Teixeira
Affiliation:
Department of Biosystems Engineering, Federal University of São João del Rei, São João del Rei, MG, 36301-160, Brazil
J.O.S. Valim
Affiliation:
Department of Biosystems Engineering, Federal University of São João del Rei, São João del Rei, MG, 36301-160, Brazil
E.F.A. Almeida
Affiliation:
Institute of Agricultural Science, Federal University of Minas Gerais, Montes Claros, MG, 39525-000, Brazil
M.G.A. Oliveira
Affiliation:
Department of Biochemistry and Molecular Biology, Federal University of Viçosa, Viçosa, MG 36570-900, Brazil National Institute of Science and Technology in Plant-Pest Interactions, Brazil
W.G. Campos*
Affiliation:
Department of Biosystems Engineering, Federal University of São João del Rei, São João del Rei, MG, 36301-160, Brazil National Institute of Science and Technology in Plant-Pest Interactions, Brazil
*
*Author for correspondence: Tel: +55 (32) 3379-5566 Fax: +55 (32) 3379-5565 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

We tested the sulfur-modulated plant resistance hypothesis using potted cabbage (Brassica oleracea var. capitata) plants that were grown without and with increasing levels of sulfur fertilization. Changes in plant chemical traits were assessed and developmental performance of Plutella xylostella, a highly host-specific leaf-chewing insect, was followed. Leaf sulfur concentration gradually increased with growing addition of sulfur in soil; however, there was a generalized saturation response curve, with a plateau phase, for improvements in total leaf nitrogen, defense glucosinolates and insect performance. Plutella xylostella performed better in sulfur-fertilized cabbage probably because of the higher level of nitrogen, despite of the higher content of glucosinolates, which are toxic for many non-specialized insects. Despite the importance of sulfur in plant nutrition and production, especially for Brassica crops, our results showed that sulfur fertilization could decrease plant resistance against insects with high feeding specialization.

Keywords

plant defensesglucosinolatesplant qualityplant nutritionherbivoryspecialist herbivoresPlutella xylsotellaBrassica oleracea
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 4 , August 2018 , pp. 479 - 486
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aarabi, F., Kusajima, M., Tohge, T., Konishi, T., Gigolashvili, T., Takamune, M., Sasazaki, Y., Watanabe, M., Nakashita, H., Fernie, A.R., Saito, K., Takahashi, H., Hubberten, H.M., Hoefgen, R. & Maruyama-Nakashita, A. (2016) Sulfur deficiency–induced repressor proteins optimize glucosinolate biosynthesis in plants. Sciences Advances 2, e1601087.Google ScholarPubMed
Abdallah, M., Dubousset, L., Meuriot, F., Etienne, P., Avice, J.C. & Ourry, A. (2010) Effect of mineral sulfur availability on nitrogen and Sulfur uptake and remobilization during the vegetative growth of Brassica napus L. Journal of Experimental Botany 61, 2635–2646.CrossRefGoogle ScholarPubMed
Ahmad, A., Khan, I., Anjum, N.A., Abrol, Y.P. & Iqbal, M. (2005) Role of sulphate transporter systems in sulfur efficiency of mustard genotypes. Plant Science 169, 842–846.Google Scholar
Ahmad, G., Jan, A., Arif, M., Jan, M.T. & Khattak, R.A. (2007) Influence of nitrogen and sulfur fertilization on quality of canola (Brassica napus L.) under rainfed conditions. Journal of Zhejiang University – Science B. 8, 731–737.CrossRefGoogle ScholarPubMed
Ahuja, I., Rohloff, J. & Bones, A.M. (2010) Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. A review. Agronomy for Sustainable Development 30, 311–348.Google Scholar
Aires, A., Rosa, E. & Carvalho, R. (2006) Effect of nitrogen and sulfur fertilization on glucosinolates in the leaves and roots of broccoli sprouts (Brassica oleracea var. italica). Journal of the Science of Food and Agriculture 86, 1512–1516.CrossRefGoogle Scholar
Andrew, C.S. (1977) The effect of sulphur on the growth, sulphur and nitrogen concentrations, and critical sulphur concentrations of some tropical and temperate pasture legumes. Australian Journal of Agricultural Research 28, 807–820.CrossRefGoogle Scholar
AOAC – Association of Official Analytical Chemists (2000) Official Methods of Analysis. 17th edn. Gaithersburg, Maryland.Google Scholar
Arany, A.M., De Jong, T.J., Kim, H.K., Van Dam, N.M., Choi, Y.H., Verpoorte, R. & van der Meijden, E. (2008) Glucosinolates and other metabolites in the leaves of Arabidopsis thaliana from natural populations and their effects on a generalist and a specialist herbivore. Chemoecology 18, 65–71.CrossRefGoogle Scholar
Badenes-Perez, F.R., Reichelt, M. & Heckel, D.G. (2010) Can sulfur fertilisation improve the effectiveness of trap crops for diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae)? Pest Management Science 66, 832–838.CrossRefGoogle ScholarPubMed
Bohinc, T., Ban, S.G., Ban, D. & Trdan, S. (2012) Glucosinolates on plant protection strategies: a review. Archives of Biological Science Belgrade 63, 821–828.Google Scholar
Brosnan, J.T. & Brosnan, M.E. (2006) The sulfur-containing amino acids: an overview. The Journal of Nutrition 136, 1636–1640.Google Scholar
Campos, W.G., Teixeira, N.C., Valim, J.O.S., Guedes, R.N.C. & Oliveira, M.G.A. (2016) Bottom-up mechanisms generate the same temporal pattern of attack by a specialist and a generalist caterpillar on short-lived plants. Environmental Entomology 45, 550–558.Google Scholar
De Pascale, S., Maggio, A., Pernice, R., Fogliano, V. & Barbieri, G. (2007) Sulfur fertilization may improve the nutritional value of Brassica rapa L. subsp. sylvestris. European Journal of Agronomy 26, 418–424.Google Scholar
Dick, W.A., Kost, D. & Chen, L. (2008) Availability of sulfur to crops from soil and other sources. pp. 59–82 in Jez, J. (Ed.) Sulfur: A Missing Link between Soils, Crops and Nutrition. Madison, American Society of Agronomy.Google Scholar
Droux, M. (2004) Sulfur assimilation and the role of sulfur in plant metabolism: a survey. Photosynthesis Research 79, 331–348.CrossRefGoogle ScholarPubMed
Dubuis, P.H., Marazzi, C., Städler, E. & Mauch, F. (2005) Sulfur deficiency cause a reduction in antimicrobial potential and leads to increased disease susceptibility of oilseed rape. Journal of Phytopathology 153, 27–36.Google Scholar
Falk, K.L., Tokuhisa, J.G. & Gershenzon, J. (2007) The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biology 9, 573–581.CrossRefGoogle ScholarPubMed
Feeny, P. (1976) Plant apparency and chemical defense. pp. 1–40 in Wallace, J.W. & Mansell, R.L. (Eds) Biochemical Interactions between Plants and Insects. New York, Plenum Press.Google Scholar
Friedrich, J.W. & Schrader, L.E. (1978) Sulfur deprivation and nitrogen metabolism in maize seedlings. Plant Physiology 61, 900–903.Google Scholar
Gallaher, C.M., Gallaher, D.D. & Peterson, S. (2012) Development and validation of a spectrophotometric method for quantification of total glucosinolates in cruciferous vegetables. Journal of Agricultural and Food Chemistry 60, 1358–1362.Google Scholar
Grant, C.A., Mahlib, S.S. & Karamano, R.E. (2012) Sulfur management for rapeseed. Field Crops Research 128, 119–128.CrossRefGoogle Scholar
Gutbrodt, B., Mody, K. & Dorn, S. (2011) Drought changes plant chemistry and causes contrasting responses in lepidopteran herbivores. Oikos 120, 1732–1740.Google Scholar
Halkier, B.A. & Gershenzon, J. (2006) Biology and biochemistry of glucosinolates. Annual Review of Plant Biology 57, 303–333.Google Scholar
Hawkesford, M.J. (2000) Plant responses to sulfur deficiency and the genetic manipulation of sulphate transporters to improve S-utilization efficiency. Journal of Experimental Botany 51, 131–138.CrossRefGoogle ScholarPubMed
Hawkesford, M.J. & De Kok, L.J. (2006) Managing sulphur metabolism in plants. Plant, Cell and Environment 29, 382–395.Google Scholar
Hesse, H., Nikiforova, V., Gakière, B. & Hoefgen, R. (2004) Molecular analysis and control of cysteine biosynthesis: integration of nitrogen and sulphur metabolism. Journal of Experimental Botany 55, 1283–1292.CrossRefGoogle ScholarPubMed
Holst, B. & Williamson, G.A. (2004) Critical review of the bioavailability of glucosinolates and related compounds. Natural Product Reports 21, 425–447.Google Scholar
Hopkins, R.J., Van Dam, N.M. & Van Loon, J.J.A. (2009) Role of glucosinolates in insect–plant relationships and multitrophic interactions. Annual Review of Entomology 54, 57–83.Google Scholar
Howe, R.W. (1953) The rapid determination of the intrinsic rate of increase of an insect population. Annals of Applied Biology 40, 134–151.Google Scholar
Järvan, M., Edesi, L., Adamson, A., Lukme, L. & Akk, A. (2008) The effect of sulfur fertilization on yield, quality of protein and baking properties of winter wheat. Agronomy Research 6, 459–469.Google Scholar
Jezek, J., Haggett, B.G.D., Atkinson, A. & Rawson, D.M. (1999) Determination of glucosinolates using their alkaline degradation and reaction with ferricyanide. Journal of Agricultural and Food Chemistry 47, 4669–4674.Google Scholar
Jordan, H.V. & Ensminger, L.E. (1958) The role of sulfur in soil fertility. Advances in Agronomy 10, 407–434.CrossRefGoogle Scholar
Kim, S.J., Matsuo, T., Watanabe, M. & Watanabe, Y. (2002) Effect of nitrogen and sulfur application on the glucosinolate content in vegetable turnip rape (Brassica rapa L.). Soil Science and Plant Nutrition 48, 43–49.CrossRefGoogle Scholar
Kliebenstein, D.J., Pedersen, D., Barker, B. & Mitchell-Olds, T. (2002) Comparative analysis of quantitative trait lose controlling the glucosinolates, myrosinase and insect resistance in Arabidopsis thaliana. Genetics 161, 325–332.Google Scholar
Kopsell, D.E., Kopsell, D.A., Randle, W.M., Coolong, T.W., Sams, C.E. & Curran-Celentano, J. (2003) Kale carotenoids remain stable while flavor compounds respond to changes in sulfur fertility. Journal of Agricultural and Food Chemistry 51, 5319–5325.Google Scholar
Kos, M., Houshyani, B., Wietsma, R., Kabouw, P., Vet, L.E.M., Van Loon, J.J.A. & Dicke, M. (2012) Effects of glucosinolates on a generalist and specialist leaf-chewing herbivore and an associated parasitoid. Phytochemistry 77, 162–170.CrossRefGoogle Scholar
Larsson, S. (1989) Stressful times for the plant stress–insect performance hypothesis. Oikos 56, 277–283.Google Scholar
Leather, S.R. (1990) Life history traits of insect herbivores in relation to host quality. pp. 175–207 in Bernays, E.A. (Ed.) Insect-Plant Interactions, vol. V. Boca Raton, CRC Press.Google Scholar
Li, Q., Eigenbrode, S.D., Stringam, G.R. & Thiagarajah, M.R. (2000) Feeding and growth of Plutella xylostella and Spodoptera eridania on Brassica juncea with varying glucosinolate concentrations and myrosinase activities. Journal of Chemical Ecology 26, 2401–2419.Google Scholar
Mailer, R.J. (1989) Effects of applied sulfur on glucosinolate and oil content in the seeds of rape (Brassica napus L.) and turnip rape (Brassica rapa L.). Australian Journal of Agricultural Research 40, 617–624.CrossRefGoogle Scholar
Malavolta, E. (1980) Elementos de Nutrição Mineral de Plantas. São Paulo, Agronômica Ceres.Google Scholar
Malhi, S.S., Ganb, Y. & Raney, J.P. (2007) Yield, seed quality, and sulfur uptake of Brassica oilseed crops in response to sulfur fertilization. Agronomy Journal 99, 570–577.Google Scholar
Marazzi, C. & Stadler, E. (2004) Influence of plant sulfur nutrition on oviposition and larval performance of the diamondback moth. Entomologia Experimentalis et Applicata 111, 225–332.Google Scholar
Marazzi, C., Patrian, B. & Städler, E. (2004) Secondary metabolites of the leaf surface affected by sulfur fertilization and perceived by the diamondback moth. Chemoecology 14, 81–86.Google Scholar
Martínez-Ballesta, M.C., Moreno, D.A. & Carvajal, M. (2013) The physiological importance of glucosinolates on plant response to abiotic stress in Brassica. International Journal of Molecular Sciences 14, 11607–11625.Google Scholar
Mattson, W.J. (1980) Herbivory in relation to plant nitrogen content. Annual Review of Ecology and Systematics 11, 119–161.Google Scholar
Moreira, L.F., Teixeira, N.C., Santos, N.A., Valim, J.O.S., Maurício, R.M., Guedes, R.N.C., Oliveira, M.G.A. & Campos, W.G. (2016) Diamondback moth performance and preference for leaves of Brassica oleracea of different ages and strata. Journal of Applied Entomology 140, 627–635.Google Scholar
Mylius, S.D. & Diekmann, O. (1995) On evolutionarily stable life histories, optimization and the need to be specific about density dependence. Oikos 74, 218–224.CrossRefGoogle Scholar
Naito, S., Hirai, M.Y., Inaba-Higano, K., Nambara, E., Fujiwara, T., Hayashi, H., Komeda, Y. & Chino, M. (1995) Expression of soybean seed storage protein genes in transgenic plants and their response to sulfur nutritional conditions. Journal of Plant Physiology 145, 614–619.CrossRefGoogle Scholar
Parmar, S., Buchner, P. & Hawkesford, M.J. (2007). Leaf developmental stage affects sulphate depletion and specific sulphate transporter expression during sulfur deprivation in Brassica napus. Plant Biology 9, 647–653.Google Scholar
Rask, L., Andreasson, E., Ekbom, B., Eriksson, S., Pontoppidan, B. & Meijer, J. (2000) Myrosinase: gene family evolution and herbivore defence in Brassicaceae. Plant Molecular Biology 42, 93–113.CrossRefGoogle ScholarPubMed
Ratzka, A., Vogel, H., Kliebenstein, D., Mitchell-Olds, T. & Kroymann, J. (2002) Disarming the mustard oil bomb. Proceedings of the National Academy of Sciences USA 99, 11223–11228.Google Scholar
Rausch, T. & Wachter, A. (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends in Plant Science 10, 503–509.Google Scholar
Rehman, H., Iqbal, Q., Farooq, M., Wahid, A., Afzal, I. & Basra, S.M.A. (2013) Sulphur application improves the growth, seed yield and oil quality of canola. Acta Physiologiae Plantarum 35, 2999–3006.Google Scholar
Rhoades, D.F. & Cates, R.G. (1976) Toward a general theory of plant antiherbivore chemistry. pp. 1681–1213 in Wallace, J. & Mansell, R.L. (Eds) Biochemical Interactions between Plants and Insects. New York, Plenum Press.Google Scholar
Rosa, E. & Heaney, R. (1996) Seasonal variation in protein, mineral and glucosinolate composition of Portuguese cabbages and kale. Animal Feed Science and Technology 57, 111–127.Google Scholar
Sarfraz, M., Dosdall, L.M. & Keddie, B.A. (2006) Diamondback moth–host plant interactions: implications for pest management. Crop Protection 25, 625–639.Google Scholar
Scherer, H.W. (2001) Sulfur in crop production. European Journal of Agronomy 14, 81–111.Google Scholar
Scriber, J. M. & Slansky, F. (1981) The nutritional ecology of immature insects. Annual Review of Entomology 26, 183–211.Google Scholar
Soufbaf, M., Fathipour, Y., Zalucki, M.P. & Hui, C. (2012) Importance of primary metabolites in canola in mediating interactions between a specialist leaf-feeding insect and its specialist solitary endoparasitoid. Arthropod–Plant Interactions 6, 241–250.Google Scholar
Spencer, D., Rerie, W.G., Randall, P.J. & Higgins, T.J.V. (1990) The regulation of pea seed storage protein genes by sulfur stress. Australian Journal of Plant Physiology 17, 355–363.Google Scholar
Spencer, K. (1975) Sulfur requirements of plants. pp. 98–116 in McLachlan, K.D. (Ed.) Sulfur in Australasian Agriculture. Sydney, Sydney Univ. Press.Google Scholar
Staley, J.T., Stewart-Jones, A., Poppy, T.W., Leather, S.R. & Wright, D.J. (2009) Fertilizer affects the behaviour and performance of Plutella xylostella on brassicas. Agricultural and Forest Entomology 11, 275–282.Google Scholar
Stam, J.M., Kroes, A., Li, Y., Gols, R., van Loon, J.J.A., Poelman, E.H. & Dicke, M. (2014) Plant interactions with multiple insect herbivores: from community to genes. Annual Review of Plant Biology 65, 689–713.Google Scholar
Tabatabai, M.A. (1984) Importance of sulfur in crop production. Biochemistry 1, 45–62.Google Scholar
Tabatabai, M.A. & Bremner, J.M. (1970) An alkaline oxidation method for determination of total sulfur in soils. Soil Science Society American Proceeding 34, 62–65.Google Scholar
Tedesco, M.J., Gianello, C., Bissani, C.A., Bohnen, H. & Volkweiss, S.J. (1995) Análise de solo, plantas e outros materiais. Boletim técnico de solos 5. Universidade Federal do Rio Grande do Sul, Porto Alegre.Google Scholar
Valim, J.O.S., Teixeira, N.C., Santos, N.A., Oliveira, M.G.A. & Campos, W.G. (2016) Drought-induced acclimatization of a fast-growing plant decreases insect performance in leaf-chewing and sap-sucking guilds. Arthropod–Plant Interactions 10, 351–363.Google Scholar
Winde, I. & Wittstock, U. (2011) Insect herbivore counter adaptations to the plant glucosinolate–myrosinase system. Phytochemistry 72, 1566–1575.Google Scholar
Wittstock, U., Kliebenstein, D.J., Lambrix, V.M., Reichelt, M. & Gershenzon, J. (2003) Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. pp. 101–125 in Romeo, J.T. (Ed.) Integrative Phytochemistry: from Ethnobotany to Molecular Ecology. Amsterdam, Elsevier.Google Scholar
Yusuf, S.W. & Collins, G.G. (1998) Effect of soil sulfur levels on feeding preference of Brevicoryne brassicae on Brussels sprouts. Journal of Chemical Ecology 24, 417–424.Google Scholar
Zalucki, M.P., Shabbir, A., Silva, R., Adamson, D., Shu-Sheng, L. & Furlong, M.J. (2012) Estimating the economic cost of one of the world's major insect pests, Plutella xylostella (Lepidoptera: Plutellidae): just how long is a piece of string? Journal of Economic Entomology 105, 1115–1129.Google Scholar
Zhao, F.J., Hawkesford, M.J. & Mcgrath, S.P. (1999 a) Sulfur assimilation and effects on yield and quality of wheat. Journal of Cereal Science 30, 1–17.Google Scholar
Zhao, F.J., Wood, A.P. & McGrath, S.P. (1999 b) Effects of sulfur nutrition on growth and nitrogen fixation of pea (Pisum sativum L.). Plant and Soil 212, 207–217.Google Scholar