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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.

Girondé A, Etienne P, Trouverie J, Bouchereau A, Le Cahérec F, Leport L, Orsel M, Niogret MF, Nesi N, Carole D, Soulay F, Masclaux-Daubresse C, Avice JC - BMC Plant Biol. (2015)

Bottom Line: Oilseed rape is the third largest oleaginous crop in the world but requires high levels of N fertilizer of which only 50% is recovered in seeds.Nitrate restriction decreased seed yield and oil quality for both genotypes but Aviso had the best seed N filling.The results confirm the importance of foliar N remobilization after bolting to satisfy seed filling and highlight that an efficient proteolysis is mainly associated with (i) cysteine proteases and proteasome activities and (ii) a fine coordination between proteolysis and export mechanisms.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Oilseed rape is the third largest oleaginous crop in the world but requires high levels of N fertilizer of which only 50% is recovered in seeds. This weak N use efficiency is associated with a low foliar N remobilization, leading to a significant return of N to the soil and a risk of pollution. Contrary to what is observed during senescence in the vegetative stages, N remobilization from stems and leaves is considered efficient during monocarpic senescence. However, the contribution of stems towards N management and the cellular mechanisms involved in foliar remobilization remain largely unknown. To reach this goal, the N fluxes at the whole plant level from bolting to mature seeds and the processes involved in leaf N remobilization and proteolysis were investigated in two contrasting genotypes (Aviso and Oase) cultivated under ample or restricted nitrate supply.

Results: During seed filling in both N conditions, Oase efficiently allocated the N from uptake to seeds while Aviso favoured a better N remobilization from stems and leaves towards seeds. Nitrate restriction decreased seed yield and oil quality for both genotypes but Aviso had the best seed N filling. Under N limitation, Aviso had a better N remobilization from leaves to stems before the onset of seed filling. Afterwards, the higher N remobilization from stems and leaves of Aviso led to a higher final N amount in seeds. This high leaf N remobilization is associated with a better degradation/export of insoluble proteins, oligopeptides, nitrate and/or ammonia. By using an original method based on the determination of Rubisco degradation in the presence of inhibitors of proteases, efficient proteolysis associated with cysteine proteases and proteasome activities was identified as the mechanism of N remobilization.

Conclusion: The results confirm the importance of foliar N remobilization after bolting to satisfy seed filling and highlight that an efficient proteolysis is mainly associated with (i) cysteine proteases and proteasome activities and (ii) a fine coordination between proteolysis and export mechanisms. In addition, the stem may act as transient storage organs in the case of an asynchronism between leaf N remobilization and N demand for seed filling.

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N fluxes in Aviso (A) and Oase (B) in HN conditions between D70 and D99. The plants were supplied with an ample concentration of nitrate (HN, 3.75 mM of nitrate). D70 corresponds to the start of seed filling and D99 to the mature seed stage. Fluxes of N from remobilization or uptake in the different organs are expressed as mg of N remobilized or taken up, respectively. A shaded box means that the organ was not present during these growing stages. For fluxes of N remobilization, the N amount is indicated with a minus sign (−) when N is remobilized from a source organ, or it is indicated with a plus sign (+) when remobilized N is redistributed towards a sink organ. Data are indicated as the mean value ± standard error. Hashes represent significant differences between genotypes (n = 4 plants; p < 0.05).
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Fig3: N fluxes in Aviso (A) and Oase (B) in HN conditions between D70 and D99. The plants were supplied with an ample concentration of nitrate (HN, 3.75 mM of nitrate). D70 corresponds to the start of seed filling and D99 to the mature seed stage. Fluxes of N from remobilization or uptake in the different organs are expressed as mg of N remobilized or taken up, respectively. A shaded box means that the organ was not present during these growing stages. For fluxes of N remobilization, the N amount is indicated with a minus sign (−) when N is remobilized from a source organ, or it is indicated with a plus sign (+) when remobilized N is redistributed towards a sink organ. Data are indicated as the mean value ± standard error. Hashes represent significant differences between genotypes (n = 4 plants; p < 0.05).

Mentions: The 15 N labelling method used in this study gave the opportunity to determine precisely the N fluxes at the whole plant level (remobilization and uptake) between D0-D42, D42-D70 and D70-D99. Due to the fact that genotype and N treatment effects were observed for NRE solely between D70 and D99 in HN plants (Table 2), only the N fluxes between these two growing stages are given in Figure 3 (for other growing stages, N fluxes are given in Additional files 3 and 4). In HN conditions, N remobilization was around 3-fold higher in Aviso (Figure 3A) than Oase (Figure 3B). For both genotypes, the stem was the main source organ: 47% (i.e. 57.32 mg N) and 59% (i.e. 24.70 mg N) of the total N remobilized in Aviso and Oase, respectively. For Aviso, the other source organs were the leaves, pod walls, flowers and roots while for Oase the source organs were leaves and roots. For Oase, the N amount remobilized from leaves was 4.4-fold lower than for Aviso. The N remobilized from source organs was mainly distributed to the seeds with a significantly greater amount in Aviso (119.18 mg N) than Oase (31.66 mg N). Contrary to Aviso, the flowers of Oase are sink organs (7.46 mg N) for remobilized N. There was no significant difference in the amount of N uptake between genotypes (202.8 mg N for Aviso and 217.6 mg N for Oase; Figure 3). However, the allocation of N towards seeds is more important for Oase (135.6 mg N) than for Aviso (87.97 mg N). Despite this higher allocation of N towards seeds in Oase, the total N distributed to Oase seeds was not the same as in Aviso (−40 mg N for Oase compared with Aviso; Figure 3).Figure 3


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.

Girondé A, Etienne P, Trouverie J, Bouchereau A, Le Cahérec F, Leport L, Orsel M, Niogret MF, Nesi N, Carole D, Soulay F, Masclaux-Daubresse C, Avice JC - BMC Plant Biol. (2015)

N fluxes in Aviso (A) and Oase (B) in HN conditions between D70 and D99. The plants were supplied with an ample concentration of nitrate (HN, 3.75 mM of nitrate). D70 corresponds to the start of seed filling and D99 to the mature seed stage. Fluxes of N from remobilization or uptake in the different organs are expressed as mg of N remobilized or taken up, respectively. A shaded box means that the organ was not present during these growing stages. For fluxes of N remobilization, the N amount is indicated with a minus sign (−) when N is remobilized from a source organ, or it is indicated with a plus sign (+) when remobilized N is redistributed towards a sink organ. Data are indicated as the mean value ± standard error. Hashes represent significant differences between genotypes (n = 4 plants; p < 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Fig3: N fluxes in Aviso (A) and Oase (B) in HN conditions between D70 and D99. The plants were supplied with an ample concentration of nitrate (HN, 3.75 mM of nitrate). D70 corresponds to the start of seed filling and D99 to the mature seed stage. Fluxes of N from remobilization or uptake in the different organs are expressed as mg of N remobilized or taken up, respectively. A shaded box means that the organ was not present during these growing stages. For fluxes of N remobilization, the N amount is indicated with a minus sign (−) when N is remobilized from a source organ, or it is indicated with a plus sign (+) when remobilized N is redistributed towards a sink organ. Data are indicated as the mean value ± standard error. Hashes represent significant differences between genotypes (n = 4 plants; p < 0.05).
Mentions: The 15 N labelling method used in this study gave the opportunity to determine precisely the N fluxes at the whole plant level (remobilization and uptake) between D0-D42, D42-D70 and D70-D99. Due to the fact that genotype and N treatment effects were observed for NRE solely between D70 and D99 in HN plants (Table 2), only the N fluxes between these two growing stages are given in Figure 3 (for other growing stages, N fluxes are given in Additional files 3 and 4). In HN conditions, N remobilization was around 3-fold higher in Aviso (Figure 3A) than Oase (Figure 3B). For both genotypes, the stem was the main source organ: 47% (i.e. 57.32 mg N) and 59% (i.e. 24.70 mg N) of the total N remobilized in Aviso and Oase, respectively. For Aviso, the other source organs were the leaves, pod walls, flowers and roots while for Oase the source organs were leaves and roots. For Oase, the N amount remobilized from leaves was 4.4-fold lower than for Aviso. The N remobilized from source organs was mainly distributed to the seeds with a significantly greater amount in Aviso (119.18 mg N) than Oase (31.66 mg N). Contrary to Aviso, the flowers of Oase are sink organs (7.46 mg N) for remobilized N. There was no significant difference in the amount of N uptake between genotypes (202.8 mg N for Aviso and 217.6 mg N for Oase; Figure 3). However, the allocation of N towards seeds is more important for Oase (135.6 mg N) than for Aviso (87.97 mg N). Despite this higher allocation of N towards seeds in Oase, the total N distributed to Oase seeds was not the same as in Aviso (−40 mg N for Oase compared with Aviso; Figure 3).Figure 3

Bottom Line: Oilseed rape is the third largest oleaginous crop in the world but requires high levels of N fertilizer of which only 50% is recovered in seeds.Nitrate restriction decreased seed yield and oil quality for both genotypes but Aviso had the best seed N filling.The results confirm the importance of foliar N remobilization after bolting to satisfy seed filling and highlight that an efficient proteolysis is mainly associated with (i) cysteine proteases and proteasome activities and (ii) a fine coordination between proteolysis and export mechanisms.

View Article: PubMed Central - PubMed

ABSTRACT

Background: Oilseed rape is the third largest oleaginous crop in the world but requires high levels of N fertilizer of which only 50% is recovered in seeds. This weak N use efficiency is associated with a low foliar N remobilization, leading to a significant return of N to the soil and a risk of pollution. Contrary to what is observed during senescence in the vegetative stages, N remobilization from stems and leaves is considered efficient during monocarpic senescence. However, the contribution of stems towards N management and the cellular mechanisms involved in foliar remobilization remain largely unknown. To reach this goal, the N fluxes at the whole plant level from bolting to mature seeds and the processes involved in leaf N remobilization and proteolysis were investigated in two contrasting genotypes (Aviso and Oase) cultivated under ample or restricted nitrate supply.

Results: During seed filling in both N conditions, Oase efficiently allocated the N from uptake to seeds while Aviso favoured a better N remobilization from stems and leaves towards seeds. Nitrate restriction decreased seed yield and oil quality for both genotypes but Aviso had the best seed N filling. Under N limitation, Aviso had a better N remobilization from leaves to stems before the onset of seed filling. Afterwards, the higher N remobilization from stems and leaves of Aviso led to a higher final N amount in seeds. This high leaf N remobilization is associated with a better degradation/export of insoluble proteins, oligopeptides, nitrate and/or ammonia. By using an original method based on the determination of Rubisco degradation in the presence of inhibitors of proteases, efficient proteolysis associated with cysteine proteases and proteasome activities was identified as the mechanism of N remobilization.

Conclusion: The results confirm the importance of foliar N remobilization after bolting to satisfy seed filling and highlight that an efficient proteolysis is mainly associated with (i) cysteine proteases and proteasome activities and (ii) a fine coordination between proteolysis and export mechanisms. In addition, the stem may act as transient storage organs in the case of an asynchronism between leaf N remobilization and N demand for seed filling.

Show MeSH
Related in: MedlinePlus