A Genotypic Comparison Reveals That the Improvement in Nitrogen Remobilization Efficiency in Oilseed Rape Leaves Is Related to Specific Patterns of Senescence-Associated Protease Activities and Phytohormones.

Marine Poret,Renier A L Van Der Hoorn,Alain Bouchereau,Ikuko Hara-Nishimura,Bok-Rye Lee,Balakumaran Chandrasekar,Sylvain Déchaumet,Flavien Macquart,Jean-Christophe Avice,Tae-Hwan Kim

doi:10.3389/fpls.2019.00046

Abstract

Oilseed rape (Brassica napus L.) is an oleoproteaginous crop characterized by low N use efficiency (NUE) that is mainly related to a weak Nitrogen Remobilization Efficiency (NRE) during the sequential leaf senescence of the vegetative stages. Based on the hypothesis that proteolysis efficiency is crucial for the improvement of leafNRE, our objective was to characterize key senescence-associated proteolytic mechanisms of two genotypes (Ténor and Samouraï) previously identified with contrasting NREs. To reach this goal, biochemical changes, protease activities and phytohormone patterns were studied in mature leaves undergoing senescence in two genotypes with contrasting NRE cultivated in a greenhouse under limiting or ample nitrate supply. The genotype with the higher NRE (Ténor) possessed enhanced senescence processes in response to nitrate limitation, and this led to greater degradation of soluble proteins compared to the other genotype (Samouraï). This efficient proteolysis is associated with (i) an increase in serine and cysteine protease (CP) activities and (ii) the appearance of new CP activities (RD21-like, SAG12-like, RD19-like, cathepsin-B, XBCP3-like and aleurain-like proteases) during senescence induced by N limitation. Compared to Samouraï, Ténor has a higher hormonal ratio ([salicylic acid] + [abscisic acid])/([cytokinins]) that promotes senescence, particularly under low N conditions, and this is correlated with the stronger protein degradation and serine/CP activities observed during senescence. Short statement: The improvement in N recycling during leaf senescence in a genotype of Brassica napus L. characterized by a high nitrogen remobilization efficiency is related to a high phytohormonal ratio ([salicylic acid] + [abscisic acid])/([cytokinins]) that promotes leaf senescence and is correlated with an increase or the induction of specific serine and cysteine protease activities.

Highlights

The increase in crop productivity during the last five decades is due to an increase in nitrogen (N) fertilizer inputs (Glass, 2003) in relation to improvements in genetic performance and culture practices
N and 15N contents were followed in a mature leaf (L12, assumed to commence aging and develop as a source tissue during the time course of the experiment) to study senescence progression during the 23 days of the high nitrate (HN) or low nitrogen supply (LN) treatments
Because abscisic acid (ABA), salicylic acid (SA) and cytokinins seem to be strongly involved in the regulation of leaf senescence in B. napus L., we focused our analysis on the content of these phytohormones

Summary

Introduction

The increase in crop productivity during the last five decades is due to an increase in nitrogen (N) fertilizer inputs (Glass, 2003) in relation to improvements in genetic performance and culture practices. Only 50% of the N originating from fertilizers is recovered in the seeds while a significant proportion is returned to the environment (Schjoerring et al, 1995) leading to a negative economic and agro-environmental balance for oilseed rape. A recent screening of NUE, NRE and senescence processes in ten genotypes of oilseed rape defined 4 genotypic profiles with different behaviors during vegetative-stage senescence that were associated with N limitation (Girondé et al, 2015).

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