Autophagy Supports Biomass Production and Nitrogen Use Efficiency at the Vegetative Stage in Rice

Abstract

Much of the nitrogen in leaves is distributed to chloroplasts, mainly in photosynthetic proteins. During leaf senescence, chloroplastic proteins, including Rubisco, are rapidly degraded, and the released nitrogen is remobilized and reused in newly developing tissues. Autophagy facilitates the degradation of intracellular components for nutrient recycling in all eukaryotes, and recent studies have revealed critical roles for autophagy in Rubisco degradation and nitrogen remobilization into seeds in Arabidopsis (Arabidopsis thaliana). Here, we examined the function of autophagy in vegetative growth and nitrogen usage in a cereal plant, rice (Oryza sativa). An autophagy-disrupted rice mutant, Osatg7-1, showed reduced biomass production and nitrogen use efficiency compared with the wild type. While Osatg7-1 showed early visible leaf senescence, the nitrogen concentration remained high in the senescent leaves. 15N pulse chase analysis revealed suppression of nitrogen remobilization during leaf senescence in Osatg7-1. Accordingly, the reduction of nitrogen available for newly developing tissues in Osatg7-1 likely led its reduced leaf area and tillers. The limited leaf growth in Osatg7-1 decreased the photosynthetic capacity of the plant. Much of the nitrogen remaining in senescent leaves of Osatg7-1 was in soluble proteins, and the Rubisco concentration in senescing leaves of Osatg7-1 was about 2.5 times higher than in the wild type. Transmission electron micrographs showed a cytosolic fraction rich with organelles in senescent leaves of Osatg7-1. Our results suggest that autophagy contributes to efficient nitrogen remobilization at the whole-plant level by facilitating protein degradation for nitrogen recycling in senescent leaves.

Identification of Barley (Hordeum vulgare L.) Autophagy Genes and Their Expression Levels during Leaf Senescence, Chronic Nitrogen Limitation and in Response to Dark Exposure

“…We recently showed in Arabidopsis that autophagy is important for nitrogen use efficiency and especially for the remobilization of nitrogen from the rosette leaves to the seeds [18,19]. Similar features were demonstrated in maize [20] and there are several lines of evidence that autophagy also plays a role for nitrogen recycling in rice [21] In addition, Masclaux-Daubresse et al [24] also showed that autophagy is globally important for metabolic and redox homeostasis in the leaves, especially under nitrate limitation. Links between autophagy, redox and stress resistance have been described in Arabidopsis in several reports [39][40][41][42][43] and autophagy also seems involved in plant immunity [44,45].…”

“…Arabidopsis thaliana wild type (Col-0), the atg5 mutant (SAIL_129B07) and the complemented atg5 p35S::HvATG5 mutant (this work) were grown on soil in either a glasshouse or a growth chamber at 60% relative humidity with a 16/8 light/dark cycle at 21 …”

“…Functional analysis of the role of autophagy in plant nitrogen remobilization was started in Arabidopsis [18,19] and has been extended to rice and maize recently [20,21]. The role of autophagy in lipid metabolism in rice has also been reported [22].…”

“…The isolated rice OsATG7 mutant is male sterile. Studies on the role of autophagy in N-resource allocation to the seeds in rice were therefore compromised [21,22]. Recently, Vierstra's group isolated the maize ZmAtg12 mutants and showed that, as in Arabidopsis, maize autophagy mutants could not remobilize nitrogen effectively from their old leaves to their seeds [20].…”

Carbon Assimilation, Biomass Partitioning and Productivity in Grasses

“…), despite removal of the exogenous N supply, new leaves continued to be produced using N remobilized from older organs [46]. Although some loss of N must be expected in senescent biomass, N remobilization is clearly important in determining plant productivity, with a recent paper demonstrating significantly reduced growth in mutant rice plants with reduced capacity for Rubisco degradation, particularly under N limiting conditions [47]. Thus, we can postulate an optimal leaf protein turnover rate which maximises canopy rather than leaf photosynthesis.…”