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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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Kinetics of dry matter (DM) of Aviso and Oase under ample or low N supply. The plants were supplied with ample (HN, 3.75 mM) or low (LN, 0.375 mM) concentrations of nitrate. Dry matter is expressed in g per plant for Aviso (A,C) and Oase (B,D) at 0 (early bolting), 42 (pod formation), 70 (start of seed filling) and 99 (mature seeds) days after the beginning of bolting (D0). Seeds and pod walls were grouped and called siliques at D42 and they were separated from D70 onwards. Data are indicated as the mean value ± standard error (vertical bars). Different letters (a, b, c) indicate that the total dry matter is significantly different between two dates. Hashes represent significant differences between genotypes in HN or LN conditions and the asterisks represent significant differences between N treatments (n = 4 plants; p < 0.05).
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Fig1: Kinetics of dry matter (DM) of Aviso and Oase under ample or low N supply. The plants were supplied with ample (HN, 3.75 mM) or low (LN, 0.375 mM) concentrations of nitrate. Dry matter is expressed in g per plant for Aviso (A,C) and Oase (B,D) at 0 (early bolting), 42 (pod formation), 70 (start of seed filling) and 99 (mature seeds) days after the beginning of bolting (D0). Seeds and pod walls were grouped and called siliques at D42 and they were separated from D70 onwards. Data are indicated as the mean value ± standard error (vertical bars). Different letters (a, b, c) indicate that the total dry matter is significantly different between two dates. Hashes represent significant differences between genotypes in HN or LN conditions and the asterisks represent significant differences between N treatments (n = 4 plants; p < 0.05).

Mentions: When plants were well supplied with nitrate (HN), the total DM (Figure 1A, B and Additional file 1) was higher for Oase (34 g) compared with Aviso (28 g) during seed filling (D70 to D99), mainly due to differences in the stem DM (12.1 g for Oase vs 8.4 g for Aviso). Under our experimental conditions, the occurrence of the different stages of development was not significantly different between both genotypes or between both N treatments for a given genotype. In low nitrate (LN) conditions, no difference in the total DM was observed between genotypes (Figure 1C, D and Additional file 1). As expected, compared with HN, DM was reduced in leaves from D42, in stems at D70 and in pod walls at D99. In addition, DM declined significantly in siliques at D42 and increased in stems at D70 for Aviso while DM of siliques and stems declined at D70 for Oase. The root DM at D99 was lower in Aviso under LN compared with HN. Under LN supply, a similar decrease in seed production was observed for both genotypes (−41.8% for Aviso, −42.8% for Oase; Figure 1C and D).Figure 1


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)

Kinetics of dry matter (DM) of Aviso and Oase under ample or low N supply. The plants were supplied with ample (HN, 3.75 mM) or low (LN, 0.375 mM) concentrations of nitrate. Dry matter is expressed in g per plant for Aviso (A,C) and Oase (B,D) at 0 (early bolting), 42 (pod formation), 70 (start of seed filling) and 99 (mature seeds) days after the beginning of bolting (D0). Seeds and pod walls were grouped and called siliques at D42 and they were separated from D70 onwards. Data are indicated as the mean value ± standard error (vertical bars). Different letters (a, b, c) indicate that the total dry matter is significantly different between two dates. Hashes represent significant differences between genotypes in HN or LN conditions and the asterisks represent significant differences between N treatments (n = 4 plants; p < 0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4384392&req=5

Fig1: Kinetics of dry matter (DM) of Aviso and Oase under ample or low N supply. The plants were supplied with ample (HN, 3.75 mM) or low (LN, 0.375 mM) concentrations of nitrate. Dry matter is expressed in g per plant for Aviso (A,C) and Oase (B,D) at 0 (early bolting), 42 (pod formation), 70 (start of seed filling) and 99 (mature seeds) days after the beginning of bolting (D0). Seeds and pod walls were grouped and called siliques at D42 and they were separated from D70 onwards. Data are indicated as the mean value ± standard error (vertical bars). Different letters (a, b, c) indicate that the total dry matter is significantly different between two dates. Hashes represent significant differences between genotypes in HN or LN conditions and the asterisks represent significant differences between N treatments (n = 4 plants; p < 0.05).
Mentions: When plants were well supplied with nitrate (HN), the total DM (Figure 1A, B and Additional file 1) was higher for Oase (34 g) compared with Aviso (28 g) during seed filling (D70 to D99), mainly due to differences in the stem DM (12.1 g for Oase vs 8.4 g for Aviso). Under our experimental conditions, the occurrence of the different stages of development was not significantly different between both genotypes or between both N treatments for a given genotype. In low nitrate (LN) conditions, no difference in the total DM was observed between genotypes (Figure 1C, D and Additional file 1). As expected, compared with HN, DM was reduced in leaves from D42, in stems at D70 and in pod walls at D99. In addition, DM declined significantly in siliques at D42 and increased in stems at D70 for Aviso while DM of siliques and stems declined at D70 for Oase. The root DM at D99 was lower in Aviso under LN compared with HN. Under LN supply, a similar decrease in seed production was observed for both genotypes (−41.8% for Aviso, −42.8% for Oase; Figure 1C and D).Figure 1

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