Do nitrogen- and sulphur-remobilization-related parameters measured at the onset of the reproductive stage provide early indicators to adjust N and S fertilization in oilseed rape (Brassica napus L.) grown under N- and/or S-limiting supplies?
Specific combinations of physiological and molecular parameters associated with N and S remobilization measured at the onset of flowering were predictive of final crop performances in oilseed rape.
Oilseed rape (Brassica napus L.) is a high nitrogen (N) and sulphur (S) demanding crop. Nitrogen- and S-remobilization processes allow N and S requirements to reproductive organs to be satisfied when natural uptake is reduced, thus ensuring high yield and seed quality. The quantification of physiological and molecular indicators of early N and S remobilization could be used as management tools to correct N and S fertilization. However, the major limit of this corrective strategy is to ensure the correlation between final performances-related variables and early measured parameters. In our study, four genotypes of winter oilseed rape (OSR) were grown until seed maturity under four nutritional modalities combining high and/or low N and S supplies. Plant final performances, i.e., seed production, N- and S-harvest indexes, seed N and S use efficiencies, and early parameters related to N- or S-remobilization processes, i.e., photosynthetic leaf area, N and S leaf concentrations, leaf soluble protein and leaf sulphate concentrations, and leaf RuBisCO abundance at flowering, were measured. We demonstrated that contrasting final performances existed according to the N and S supplies. An optimal N:S ratio supply could explain the treatment-specific crop performances, thus justifying N and S concurrent managements. Specific combinations of early measured plant parameters could be used to predict final performances irrespective of the nutritional supply and the genotype. This work demonstrates the potential of physiological and molecular indicators measured at flowering to reflect the functioning of N- and S-compound remobilization and to predict yield and quality penalties. However, because the predictive models are N and S independent, instant N and S leaf analyses are required to further adjust the adequate fertilization. This study is a proof of a concept which opens prospects regarding instant diagnostic tools in the context of N and S mineral fertilization management.
KeywordsFertilization Genotype Indicators Nitrogen Oilseed rape Remobilization RuBisCO Sulphur
High nitrogen/high sulphur
Low nitrogen/low sulphur
Large/small subunits of RuBisCO
Nitrogen/sulphur harvest index
The authors thank the BrACySol (Center of biological resources in INRA Rennes, France) for providing the seeds. They are grateful to C. Salon, C. Bernard, K. Palavioux, C. Jeudy, F. Zenk, D. Girondé, and N. El-Miyad for their helpful advice and technical assistance in the 4PMI. They are also very grateful to J. Pichon, M. Bodereau, J. Bonnefoy, and M. Hodel for plant sample preparation and B. Andrieu for his helpful comments on the experimental design and on the manuscript. They also thank PLATIN’, the Plateau d’Isotopie de Normandie ICORE facility for performing the elemental analyses. They eventually thank S. Lavenant-Lemauviel for her helpful advice to perform the correlation and principal component analyses. Genergy and Rapsodyn projects funded by National Research Agency (ANR) and the French program “Investments for the Future”.
- Ahmad A, Abdin MZ (2000) Interactive effect of sulphur and nitrogen on the oil and protein contents and on the fatty acid profiles of oil in the seeds of rapeseed (Brassica campestris L.) and mustard (Brassica juncea L. Czern. and Coss.). J Agron Crop Sci 185:49–54. https://doi.org/10.1046/j.1439-037X.2000.00401.x CrossRefGoogle Scholar
- Brunel-Muguet S, D’Hooghe P, Bataillé M-P et al (2015) Heat stress during seed filling interferes with sulfur restriction on grain composition and seed germination in oilseed rape (Brassica napus L.). Front Plant Sci 6:213. https://doi.org/10.3389/fpls.2015.00213 CrossRefPubMedPubMedCentralGoogle Scholar
- D’Hooghe P, Escamez S, Trouverie J, Avice J-C (2013) Sulphur limitation provokes physiological and leaf proteome changes in oilseed rape that lead to perturbation of sulphur, carbon and oxidative metabolisms. BMC Plant Biol 13:23. https://doi.org/10.1186/1471-2229-13-23 CrossRefPubMedPubMedCentralGoogle Scholar
- D’Hooghe P, Dubousset L, Gallardo K et al (2014) Evidence for proteomic and metabolic adaptations associated with alterations of seed yield and quality in sulfur-limited Brassica napus L. Mol Cell Proteomics 13:1165–1183. https://doi.org/10.1074/mcp.M113.034215 CrossRefPubMedPubMedCentralGoogle Scholar
- Dubousset L, Abdallah M, Desfeux AS et al (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. J Exp Bot 60:3239–3253. https://doi.org/10.1093/jxb/erp172 CrossRefPubMedPubMedCentralGoogle Scholar
- FAO (2016) http://www.fao.org/faostat/fr/#data/QC
- Gilbert SM, Clarkson DT, Cambridge M et al (1997) SO4 2− deprivation has an early effect on the content of ribulose-1,5-bisphosphatecarboxylase/oxygenase and photosynthesis in young leaves of wheat. Plant Physiol 115:1231–1239. https://doi.org/10.1104/pp.115.3.1231 CrossRefPubMedPubMedCentralGoogle Scholar
- Girondé A, Dubousset L, Trouverie J et al (2014) The impact of sulfate restriction on seed yield and quality of winter oilseed rape depends on the ability to remobilize sulfate from vegetative tissues to reproductive organs. Front Plant Sci 5:695. https://doi.org/10.3389/fpls.2014.00695 CrossRefPubMedPubMedCentralGoogle Scholar
- Girondé A, Etienne P, Trouverie J et al (2015a) The contrasting N management of two oilseed rape genotypes reveals the mechanisms of proteolysis associated with leaf N remobilization and the respective contributions of leaves and stems to N storage and remobilization during seed filling. BMC Plant Biol 15:59. https://doi.org/10.1186/s12870-015-0437-1 CrossRefPubMedPubMedCentralGoogle Scholar
- Girondé A, Poret M, Etienne P et al (2015b) A profiling approach of the natural variability of foliar N remobilization at the rosette stage gives clues to understand the limiting processes involved in the low N use efficiency of winter oilseed rape. J Exp Bot 66:2461–2473. https://doi.org/10.1093/jxb/erv031 CrossRefGoogle Scholar
- Girondé A, Poret M, Etienne P et al (2015c) A comparative study of proteolytic mechanisms during leaf senescence of four genotypes of winter oilseed rape highlighted relevant physiological and molecular traits for NRE improvement. Plants 5:1. https://doi.org/10.3390/plants5010001 CrossRefPubMedPubMedCentralGoogle Scholar
- Koeslin-Findeklee F, Horst W (2016) Contribution of nitrogen uptake and retranslocation during reproductive growth to the nitrogen efficiency of winter oilseed-rape cultivars (Brassica napus L.) differing in leaf senescence. Agronomy 6:1. https://doi.org/10.3390/agronomy6010001 CrossRefGoogle Scholar
- Koeslin-Findeklee F, Becker MA, van der Graaff E et al (2015) Differences between winter oilseed rape (Brassica napus L.) cultivars in nitrogen starvation-induced leaf senescence are governed by leaf-inherent rather than root-derived signals. J Exp Bot 66:3669–3681. https://doi.org/10.1093/jxb/erv170 CrossRefPubMedPubMedCentralGoogle Scholar
- Kowalczyk-Jusko A, Koscik B (2002) Possible use of the chlorophyll meter (SPAD—502) for evaluating nitrogen nutrition of the virginia tobacco. Electron J Polish Agric Univ Agronomy 5(1). http://www.ejpau.media.pl/volume5/issue1/agronomy/art-05.html
- Lancashire PD, Bleiholder H, Van Den Boom T et al (1991) A uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 119:561–601. https://doi.org/10.1111/j.1744-7348.1991.tb04895.x CrossRefGoogle Scholar
- Poret M, Chandrasekar B, van der Hoorn R et al (2017) Proteomic investigations of proteases involved in cotyledon senescence: a model to explore the genotypic variability of proteolysis machinery associated with nitrogen remobilization efficiency during the leaf senescence of oilseed rape. Proteomes 5:29. https://doi.org/10.3390/proteomes5040029 CrossRefPubMedPubMedCentralGoogle Scholar
- R Development Core Team (2019) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
- Sexton PJ, Batchelor WD, Shibles R (1997) Sulfur availability, Rubisco content, and photosynthetic rate of soybean. Crop Sci 37:1801. https://doi.org/10.2135/cropsci1997.0011183X003700060023x CrossRefGoogle Scholar
- Xu HL, Lopez J, Rachii F et al (1996) Effect of sulphate on photosynthesis in greenhouse–grown tomato plants. Physiol Plant 96:722–726. https://doi.org/10.1111/j.1399-3054.1996.tb00248.x CrossRefGoogle Scholar