Leaf mineral nutrient remobilization during leaf senescence and modulation by nutrient deficiency

Abstract

Higher plants have to cope with fluctuating mineral resource availability. However, strategies such as stimulation of root growth, increased transporter activities, and nutrient storage and remobilization have been mostly studied for only a few macronutrients. Leaves of cultivated crops (Zea mays, Brassica napus, Pisum sativum, Triticum aestivum, Hordeum vulgare) and tree species (Quercus robur, Populus nigra, Alnus glutinosa) grown under field conditions were harvested regularly during their life span and analyzed to evaluate the net mobilization of 13 nutrients during leaf senescence. While N was remobilized in all plant species with different efficiencies ranging from 40% (maize) to 90% (wheat), other macronutrients (K-P-S-Mg) were mobilized in most species. Ca and Mn, usually considered as having low phloem mobility were remobilized from leaves in wheat and barley. Leaf content of Cu-Mo-Ni-B-Fe-Zn decreased in some species, as a result of remobilization. Overall, wheat, barley and oak appeared to be the most efficient at remobilization while poplar and maize were the least efficient. Further experiments were performed with rapeseed plants subjected to individual nutrient deficiencies. Compared to field conditions, remobilization from leaves was similar (N-S-Cu) or increased by nutrient deficiency (K-P-Mg) while nutrient deficiency had no effect on Mo-Zn-B-Ca-Mn, which seemed to be non-mobile during leaf senescence under field conditions. However, Ca and Mn were largely mobilized from roots (-97 and -86% of their initial root contents, respectively) to shoots. Differences in remobilization between species and between nutrients are then discussed in relation to a range of putative mechanisms.

Keywords: Brassica napus; crop species; ionomic; nutrient deficiencies; remobilization; senescence; trees.

Figure 1

Changes in whole leaf-blade biomass (A,B) and chlorophyll content (C,D) during the leaf life span (days after leaf emergence) of Q. robur (A,C) and Z. mays (B,D). Dashed lines in (C) and (D) indicate the beginning of chlorophyll degradation and hence senescence initiation. Vertical bars indicate ± S.E. for n = 3 when larger than the symbol. Total leaf life span (days), growth cessation (as % of total leaf life span) and senescence initiation (as % of total leaf life span) are then provided for the eight ligneous and annual crop species. The relative leaf life span (% of maximum) is given on the bottom of each graph.

Figure 2

Changes in nitrogen and potassium (A,B), sulfur and phosphorus (C,D) and calcium and manganese (E,F) contents in leaves during their leaf life span in Q. robur (A,C,E) and Z. mays (B,D,F). Vertical bars indicate ± S.E. for n = 3 when larger than the symbol. The apparent nutrient remobilization (ANR) is given with its confidence interval (p = 0.05). Dashed lines indicate the beginning of chlorophyll degradation and hence senescence initiation. The relative leaf life span (% of maximum) is given on the bottom of each graph.

Figure 3

Apparent nutrient remobilization (ANR) of macronutrients (A,B): N, K, P, S, Ca, Mg, and micronutrients (C,D): Zn, Fe, Mn, B, Ni, Cu, and Mo, expressed as % of maximum nutrient content during leaf senescence in three tree species; Q. robur, P. nigra, A. glutinosa and five crop species: Z. mays, T. aestivum, H. vulgare, P. sativum and B. napus. Species grown on the same soil are represented by a solid line and species like A. glutinosa and P. sativum harvested on another soil are represented by a dashed line. The ANR was calculated from Equation (3) given in material and methods. Each value is the mean for n = 9. For reasons of clarity, confidence intervals are not indicated (see Supplemental Data SD3–10).

Figure 4

Dry weight of young petioles, young leaves, mature petioles, mature leaves, and roots of Brassica napus L. at t = 0 and after 30 days of culture in control plants and in N, P, S, K, Mg, Ca, Zn, Mo, Cu, Ni, Fe, B, or Mn deficient plants. The number of days required to reach a significant growth reduction is given for each deficiency on the top of each column. Significant differences in total plant dry weight between deficient and control plant are indicated by ^*, ^**, or ^***, for P < 0.05, P < 0.01, or P < 0.001, respectively. Vertical bars indicate S.E. for n = 4.

Figure 5

Sulfur (A), calcium (B), copper (C), and zinc (D) contents per plant in hydroponically grown Brassica napus subjected to S, Ca, Cu, and Zn deficiency, respectively. For each nutrient, uptake by control plants (unlimited supply of nutrients) is given as the mean ± S.E. for n = 4. Black and white boxes indicate nutrient content for each organ, before and after nutrient deficiency, respectively, and are given as the mean ± S.E. for n = 4. Apparent nutrient remobilization (negative value) from an organ was calculated from Equation (4) given in Material and Methods and allocation (positive value) as well as allocation of nutrient taken up by roots are given as the mean ± S.E. for n = 16. Level of significance are indicated by ^*, ^**, or ^***, for P < 0.05, P < 0.01, or P < 0.001, between nutrient deficient plants and t = 0 control plants. Question marks indicate flows that cannot be calculated. NS: No significant uptake.

Figure 6

Apparent nutrient remobilization (ANR), expressed as % of maximum nutrient content in leaves of B. napus grown under field condition (calculated from Equation (3) given in material and methods, n = 12 or 15 depending on the nutrient) or in mature leaves of hydroponically grown plants [calculated from Equation (4) given in Material and Methods, n = 16] subjected to individual nutrient deficiency. Vertical bars indicate ± S.E.