Dynamics of Exogenous Nitrogen Partitioning and Nitrogen Remobilization from Vegetative Organs in Pea Revealed by 15N in Vivo Labeling throughout Seed Filling

Abstract

The fluxes of (1) exogenous nitrogen (N) assimilation and (2) remobilization of endogenous N from vegetative plant compartments were measured by 15 N labeling during the seed-filling period in pea (Pisum sativum L. cv Caméor), to better understand the mechanism of N remobilization. While the majority (86%) of exogenous N was allocated to the vegetative organs before the beginning of seed filling, this fraction decreased to 45% at the onset of seed filling, the remainder being directed to seeds. Nitrogen remobilization from vegetative parts contributed to 71% of the total N in mature seeds borne on the first two nodes (first stratum). The contribution of remobilized N to total seed N varied, with the highest proportion at the beginning of filling; it was independent of the developmental stage of each stratum of seeds, suggesting that remobilized N forms a unique pool, managed at the whole-plant level and supplied to all filling seeds whatever their position on the plant. Once seed filling starts, N is remobilized from all vegetative organs: 30% of the total N accumulated in seeds was remobilized from leaves, 20% from pod walls, 11% from roots, and 10% from stems. The rate of N remobilization was maximal when seeds of all the different strata were filling, consistent with regulation according to the N demand of seeds. At later stages of seed filling, the rate of remobilization decreases and may become controlled by the amount of residual N in vegetative tissues.Pea (Pisum sativum) is an important agricultural crop grown primarily for its high seed protein content. However, the protein yield of the pea crop remains too low and variable between cropping area and years (http://apps.fao/faostat/, http://www.prolea.com/ unip/) to sustain the needs in plant protein of European countries. To extend the pea crop in Europe and to increase use of pea seed in the feed industry, breeders have to develop varieties with better harvest and nitrogen (N) indices. Toward this aim, a better understanding of the processes involved in the elaboration of seed protein content is needed. The final protein yield of seeds depends both upon the genotype and on environmental factors during seed filling (Lhuillier-Soundélé et al., 1999a). Nitrogen accumulation by seeds during filling depends upon the external N supply: soil mineral N assimilation and/or symbiotic fixation of atmospheric N 2 . However, exogenous N cannot generally sustain the high N demand of filling seeds, so endogenous N previously accumulated in vegetative parts is largely remobilized to fulfill this demand (Sinclair and de Wit, 1976;Salon et al., 2001). Seed N concentration is correlated to N availability within plants, and the extent of the contribution of N remobilization to seed N yield varies among legumes: 70% in field-grown pea (Atta et al., 2004), 80% to 90% in soybean (Glycine max; Warembourg and Fernandez, 1985;Grandgirard, 2002), 43% to 94% in rain-fed grown lentil (Lens culinaris; Kurdali et al., 1997), 84% in bean plants (Phaseolus vulgaris;Westermann et al., 1...

Legumes are different: Leaf nitrogen, photosynthesis, and water use efficiency

“…There is also abundant evidence that remobilization of nitrogen from foliage and other plant tissues may account for 70-90% of seed nitrogen in annual agricultural legumes (28). Prolific flowering and generation of seedpods and seeds are features of many N 2 FP (Fig.…”

Comprehensive Dissection of Spatiotemporal Metabolic Shifts in Primary, Secondary, and Lipid Metabolism during Developmental Senescence in Arabidopsis

“…Nutrient remobilization from leaves to seeds during plant senescence is important for establishing seed yield and quality in crops and, therefore, has been studied extensively (Schiltz et al, 2005;Howarth et al, 2008;Munier-Jolain et al, 2008;Slewinski, 2012). Leafseed balance has also commonly been thought to be an important factor in monocarpic plants for the regulation of leaf senescence, given that sink size and the metabolism in sinks affect the reallocation of nutrients from the senescing leaves, even though this control does not seem to occur in all monocarpic plants, including Arabidopsis (Killingbeck, 1996;Noodén and Penney, 2001;van Doorn, 2004).…”

Plant N Fluxes and Modulation by Nitrogen, Heat and Water Stresses: A Review Based on Comparison of Legumes and Non Legume Plants

“…During the reproductive stage, N compounds provided via the recycling and remobilization associated to leaf senescence are largely requisitioned for optimum flowering and grain filling (Brouquisse et al, 2001;Gallais et al, 2006;Guiboileau et al, 2010;Malagoli et al, 2005;Masclaux-Daubresse et al, 2008). Indeed, at this stage, N assimilation usually decreases, mostly due to abiotic stress and as such, leaves are solicited for supplying amino acids to the reproductive organs, between 50 to 80% of their N needs, for legumes , Schiltz et al, 2005, oilseed rape (Malagoli et al, 2005), wheat (Kichey et al, 2007), maize or rice (Tabuchi et al, 2007). Mobilised amino acids are issued from a) proteolysis of chloroplastic proteins (70 to 80% of total leaf -Liu et al, 2008 -mostly consisting of Rubisco, Mae et al, 1993), b) exo/endopeptidases attack of cytosolic proteins via sequestration within double membrane vesicles called autophagosomes (Ishida et al, 2008;Wada et al, 2009) pathway and senescence-associated vesicle (SAV that contains cysteine protease SAG12; Otegui et al, 2005) trafficking , c) removal of short lived proteins through the ubiquitin-26S proteasome for regular cell maintenance.…”

“…The photosynthetic activity is then progressively reduced by N remobilisation. During N mobilisation from senescent leaves to filling seeds in pea (Schiltz et al, 2005), a proteomic approach has also reported the induction of chloroplastic proteases such as ATP-dependent Clp protease and ATP-dependent Zn-activated protease (FtsH) which were concomitant with the decline of leaf proteins. During leaf senescence, proteolysis of chloroplast proteins would release glutamate that serves as a substrate of the glutamate dehydrogenase (GDH, Purnell & Botella, 1997).…”

“…Further investigations may improve the understanding of the effect of high temperature on N assimilate partitioning and their physiological basis. Seed N accumulation comes from daily N accumulation by the plant and from N remobilised from vegetative parts in both legumes and non-legumes plants (in wheat: Jeuffroy et al, 2000;in pea : Pate, 1985;Schiltz et al, 2005). The rate of seed N accumulation is mostly determined by plant N availability from these two sources (in pea: LhuillierSoundélé et al, 1999b;in soybean: Hayati et al, 1996;in wheat : Jenner et al, 1991), consequently any effect of temperature on plant N available for seeds should also affect the rate of seed N accumulation.…”