Effect of mineral sulphur availability on nitrogen and sulphur uptake and remobilization during the vegetative growth of Brassica napus L

Abstract

Because it has a high demand for sulphur (S), oilseed rape is particularly sensitive to S limitation. However, the physiological effects of S limitation remain unclear, especially during the rosette stage. For this reason a study was conducted to determine the effects of mineral S limitation on nitrogen (N) and S uptake and remobilization during vegetative growth of oilseed rape at both the whole-plant and leaf rank level for plants grown during 35 d with 300 microM (34)SO(4)(2-) (control plants; +S) or with 15 microM (34)SO(4)(2-) (S-limited plants; -S). The results highlight that S-limited plants showed no significant differences either in whole-plant and leaf biomass or in N uptake, when compared with control plants. However, total S and (34)S (i.e. deriving from S uptake) contents were greatly reduced for the whole plant and leaf after 35 d, and a greater redistribution of endogenous S from leaves to the benefit of roots was observed. The relative expression of tonoplast and plasmalemma sulphate transporters was also strongly induced in the roots. In conclusion, although S-limited plants had 20 times less mineral S than control plants, their development remained surprisingly unchanged. During S limitation, oilseed rape is able to recycle endogenous S compounds (mostly sulphate) from leaves to roots. However, this physiological adaptation may be effective only over a short time scale (i.e. vegetative growth).

Fig. 1.

(A) Culture conditions and experimental design used to provide two contrasting levels of S nutrition. Six weeks before the start of the experiment (i.e. day 0), the plants were grown on optimal S solution (300 μM SO₄^2–). On day 0 and after subsequent sampling, half the plants were supplied with 300 μM SO₄^2– (control plant; +S) and half with 15 μM SO₄^2– (S-limited plants; –S) with sequential double labelling during the 7 d preceding each harvest. (B) The inset shows a picture of oilseed rape plants growing in aerated hydroponic solution in the greenhouse.

Fig. 2.

Changes of (A) whole plant, whole leaf blade (LB), and root biomass, and (B) LB biomass of leaf ranks 8, 10, and 12 of oilseed rape for control plants (+S; filled symbols) and S-limited plants (–S; open symbols) during the 35 d of treatment. Vertical bars indicate ±SE (n=4) when larger than the symbol. Different letters indicate that mean values are significantly different at a given date between treatments (P <0.05).

Fig. 3.

Changes of (A) whole-plant N and ¹⁵N (i.e. deriving from uptake) and (B) whole-plant S and ³⁴S (i.e. deriving from uptake) of oilseed rape for control plants (+S; filled symbols) and S-limited plants (–S; open symbols) during the 35 d of treatments. Vertical bars indicate ±SE (n=4) when larger than the symbol. Different letters indicate that mean values are significantly different at a given date between treatments (P <0.05).

Fig. 4.

Partitioning (in %) of total S taken up (³⁴S) and total remobilized S (³²S, present on day 0) in leaves, petioles, stem, and roots of oilseed rape for control plants (+S; A) and S-limited plants (–S; B) between day 0 and day 35. Values are given as the mean ±SE (n=4). The thickness of the arrows represents the relative importance (in % of the total S taken up or the total mobilized S) of each flux for accumulated total S taken up or total remobilized S (for details, see Materials and methods).

Fig. 5.

Evolution of (A) total S, (B) accumulated ³⁴S taken up, and (C) accumulated remobilized ³²S contents in leaf blade (LB) of leaf ranks 8, 10, 12 and roots of oilseed rape for control plants (+S; filled symbols) and S-limited plants (–S; open symbols) during 35 d of treatments. Vertical bars indicate ±SE (n=4) when larger than the symbol. Different letters indicate that mean values are significantly different at a given date between treatments (P <0.05).

Fig. 6.

Changes in (A) N/S ratio, (B) N organic/S organic ratio, and (C) S-SO₄^2– content in leaf blade (LB) of leaf ranks 8, 10, 12 and roots of oilseed rape for control plants (+S; filled symbols) and S-limited plants (–S; open symbols) during 35 d of treatments. Organic N (or S) is represented by the difference between total N (or S) and nitrate (or sulphate). Vertical bars indicate ±SE (n=4) when larger than the symbol. Different letters indicate that mean values are significantly different at a given date between treatments (P <0.05).

Fig. 7.

Relative expression of root plasmalemma (A) BnSultr1.1 and (B) BnSultr1.2, and tonoplast (C) Bnsultr4.1 and (D) BnSultr4.2 sulphate transporters in oilseed rape for control plants (+S; dark bars) and S-limited plants (–S; open bars) during 35 d of treatment. Relative expression for each gene is the average ±SE (n=4) of Q-PCR analysis and is expressed relative to the day 0 initial control expression level for that gene. Different letters indicate that mean values are significantly different at a given date between treatments (P <0.05).