Nitrogen Use Efficiency in Rice: Comparison
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Please note this is a comparison between Version 2 by Dean Liu and Version 1 by Sichul Lee.

Rice (

Oryza sativa

L) is a daily staple food crop for more than half of the global population and improving productivity is an important task to meet future demands of the expanding world population. Application of nitrogen (N) fertilization improved rice growth and productivity in the world, but excess use causes environmental and economic issues. One of the main goals of rice breeding is reducing N fertilization while maintaining productivity. Therefore, enhancing rice nitrogen use efficiency (NUE) is essential for the development of sustainable agriculture and has become urgently needed. Many studies have been conducted on the main steps in the use of N including uptake and transport, reduction and assimilation, and translocation and remobilization, and on transcription factors regulating N metabolism. Understanding of these complex processes provides a base for the development of novel strategies to improve NUE for rice productivity under varying N conditions.

  • rice
  • nitrogen use efficiency
  • fertilization
  • productivity

1. Introduction

Rice is one of the major cereal grains to feed half of the world’s population as a key nutritional source [1]. Accordingly, improving the production of rice is indispensable to satisfy the rising demands driven by population growth. The global population is expected to reach 10 billion, which will require a 70–100% increase in global crop production by 2050 [2]. The macronutrient N is an essential element for all living organisms because the synthesis of numerous vital biomolecules such as amino acids, proteins, nucleic acids, chlorophyll, and some plant hormones relies on N availability [3]. Thus, the application of N fertilizer has become a major factor responsible for the increase in crop yield over the past five decades, whereas excess usage of fertilization has caused serious environmental and economic issues [4]. The average nitrogen use efficiency (NUE) in crops is about 40–50% of the applied N, while the rest of the applied N is lost and enters the environments as N pollution [5]. The unutilized N causes water and air pollution affecting health, damage to biodiversity. The production of N fertilizer produced by the Haber–Bosch process requires a high amount of energy and contributes to greenhouse gas and then to climate change [6]. Besides, it represents increasing farmers’ economic costs [7].

Improvement of NUE is one of the main objectives of breeding for rice that efficiently uptakes, assimilates, and remobilizes all available N resources [8]. Rice cultivars with high NUE are not only expected to increase grain yield but also to reduce environmental costs and facilitate low-input sustainable rice cultivation. Consequently, understanding the various processes of N metabolism is critical for increasing NUE.

2. N Assimilation and Reutilization

Assimilation of ammonium and utilization is a complex and tightly regulated process for rice biomass production and grain yield [70][9]. After nitrate is absorbed into roots, it is first reduced to nitrite by nitrate reductase (NR) in the cytoplasm, and then nitrite is further reduced to ammonium by nitrite reductase (NiR) in the plastids [71][10]. OsNR2 encoding a NAD(P)H-dependent nitrate reductase (NR), was isolated as the master gene causing differences in nitrate assimilation and NUE between the indica and japonica rice [71][10]. Variations in indica and japonica OsNR2 alleles result in structurally distinct OsNR2 proteins, with higher NR activity in indica, conferring increased effective tiller number, grain yield, and NUE compared to japonica rice [71][10]. The ammonium from nitrate reduction and ammonium uptake by OsAMTs is assimilated into amino acid via the glutamine synthetase (GS)/glutamine-2-oxoglutarate aminotransferase (GOGAT) cycle (Figure 1 and Table 2) [72][11].

2.1. Glutamine Synthetase

GS catalyzes an ATP-dependent conversion of glutamate (Glu) to glutamine (Gln) using ammonium and plays an essential role in the N metabolism. In rice, there are several homologous genes for the cytosolic GS (OsGS1;1, OsGS1;2, and OsGS1;3) and one chloroplastic gene (OsGS2) [73][12]. OsGS1;1 is expressed in all organs and especially highly expressed in the leaf blade. Its disruption results in severe retardation of growth rate and lower grain productivity [73][12]. OsGS1;1 plays a critical role in maintaining the metabolic balance of rice plants grown under ammonium as an N source [73,74][12][13]. In addition, N assimilation by OsGS1;1 affects plastid development in rice roots [75][14]. The overexpression of OsGS1;1 or OsGS1;2 did not increase the grain yield or total amino acids in seeds [76][15].

OsGS1;2 is mainly expressed in the surface cells of roots that are responsible for the primary assimilation of ammonium [77][16]. Metabolic disorders caused by the lack of GS1;2 lead to a severe reduction of the number of active tiller and grain yield [77,78,79][16][17][18]. OsGS1;3 was exclusively expressed in the spikelet, but its functional role for N assimilation is still unknown [73][12]. OsGS2 isoform is abundant in the leaf and OsGS2 is primarily responsible for re-assimilation of ammonium produced from photorespiration in chloroplasts and assimilation in plastids of ammonium deriving from nitrate reduction [73,80][12][19]. The overexpression of OsGS2 enhanced photoprotection and thereby enhanced tolerance to abiotic stresses [81][20].

2.2. Glutamate Synthetase

GOGAT yields two molecules of Glu by transferring the amine group of the amide side chain of Gln to 2-oxoglutarate (2-OG) [82][21]. Subsequently, one Glu molecule serves as a substrate for GS, while the other is used for transport, storage, or further amino acid metabolism. There are two types of GOGAT using either reduced ferredoxin (Fd-GOGAT) or NADH (NADH-GOGAT) as an electron donor. In rice, there are two NADH-type GOGATs and one Fd-GOGAT [83][22]. OsNADH-OsGOAT1 is mainly expressed in the roots after the supply of ammonium [84][23], and OsNADH-OsGOAT1 knockout mutant displays decreased grain yield in paddy field due to the reduced number of active tillers [83][22]. According to similarities in their expression patterns and the phenotypes of their knockout mutants, it was suggested that OsNADH-OsGOAT1 and OsGS1;2 both contribute to the primary assimilation of ammonium in rice roots [84][23]. Enhanced expression of OsNADH-OsGOAT1 was shown to increase N uptake and N remobilization efficiency, but the OsNADH-OsGOAT1 overexpressing plants displayed poor growth benefits and reduced grain yield when grown in paddy field, which revealed some unbalanced use of N [56][24]. Nevertheless, the concomitant overexpression of both OsNADH-OsGOAT1 and OsAMT1;2 conferred enhanced NUE and better grain yield under N limiting growth conditions, which can provide a technical solution for plant performances under nitrate limiting conditions [56][24].

OsNADH-GOGAT2 is expressed mainly in fully expanded leaf blade and sheath. Defects in OsNADH-GOGAT2 caused a remarkable reduction in spikelet number/panicle and grain yield and whole plant biomass [70][9]. OsNADH-GOGAT2 along with OsGS1;1 could be important in the remobilization of N during the senescence stage [84][23]. OsFd-GOGAT is mainly expressed in the chloroplasts of green tissues as well as the mature leaf blade and sheath and plays a major role in photorespiratory ammonium assimilation [85][25]. Mutation of OsFd-GOGAT led to premature leaf senescence and disturbed C/N balance [85,86][25][26].

2.3. Asparagine Synthetase, Glutamate Dehydrogenase, and Aspartate Aminotransferase

In addition to GS/GOGAT, several enzymes including asparagine synthetase (ASN), glutamate dehydrogenase (GDH), and aspartate aminotransferase (AAT) were characterized to play important roles in N metabolism (Figure 1 and Table 1) [6,87,88][6][27][28].

Asparagine (Asn) and Gln are the major N forms in phloem sap and play a critical role in dynamic N recycling [89,90][29][30]. Asparagine synthetase (ASN) can produce asparagine by transferring the amide group from glutamine to aspartate. In Arabidopsis, labeling suggested that asparagine could be synthesized directly using ammonium as an N donor [91][31]. In rice, there are two ASN genes, OsASN1 and OsASN2 [92][32]. OsASN1 is mainly expressed in roots in an ammonium-dependent manner, whereas OsASN2 expression is decreased under ammonium supply [92][32]. Disruption of OsASN1 leads to decreased N uptake and increased sensitivity to N limitation at the seedling stage. It displays reduced grain protein content and productivity, whereas the opposite tendencies are observed in overexpressing lines [93][33]. The mitochondrial NADH-dependent GDH catalyzes the reversible conversion of Glu to 2-OG and ammonia [94][34]. Three OsNADH-GDH genes are differentially expressed in various organs depending on N availability [95][35], but their roles remain unknown. AAT is involved in N and C metabolisms and catalyzes the reversible transamination of aspartate (Asp) to 2-OG, yielding Glu and oxaloacetate (OA) [88][28]. The overexpression of OsAAT1 and OsAAT2 resulted in altered N metabolism and increased amino acid content in seeds [88][28].

Table 1.

 Transporters and enzymes associated with N metabolic steps.

Gene Name Locus Number Phenotype Observed References
OsNPF4.1/SP1 LOC_Os11g12740 Ko 1: Defective in rice panicle elongation and the short-panicle phenotype [27][36]
OsNPF8.9/OsNRT1.1 LOC_Os03g13274 OX 2: Increased biomass under various N supplies [28,29][37][38]
OsNPF7.3/OsPTR6 LOC_Os04g50950 OX: Increased growth by N accumulation but decreased NUE 5 under high NH4+ supply [30,31][39][40]
OX: Enhanced NUE in paddy field [32][41]
RNAi 3: Decreased amino acids accumulation and plant growth
OsNPF8.20/OsPTR9 LOC_Os06g49250 OX: Enhanced N uptake, promotion of lateral root formation, and increased grain yield [33][42]
Ko & RNAi: The opposite effects of OX
OsNPF2.2/OsPTR2 LOC_Os12g44100 Ko: Reduction in root-to-shoot nitrate transport and abnormal vasculature development [34][43]
OsNPF2.4 LOC_Os03g48180 OX: Enhanced nitrate acquisition and upward transfer to shoot [35][44]
Ko: The opposite effects of OX
OsNPF6.5/NRT1.1B LOC_Os10g40600 NIL 4, OX: Increased grain yield and NUE [36][45]
OsNPF7.2 LOC_Os02g47090 Ko & RNAi: Retarded growth under high nitrate supply [37][46]
OsNPF8.1/OsPTR7 LOC_Os01g04950 Ko: Less accumulation of dimethyarsinate in rice grain [38][47]
OsNPF7.7 LOC_Os10g42870 OX: Improved N influx in root, grain yield, and NUtE [26][48]
OsNRT1.1A/OsNPF6.3 LOC_Os08g05910 OX: Early maturation and improved N utilization and grain yield [20][49]
Ko: Reduced N utilization and late flowering
OsNPF6.1 LOC_Os01g01360 NIL: Enhancement of N uptake, NUE, and grain yield under low N supply [39][50]
OsNRT2.3a LOC_Os01g50820 RNAi: Defect in long-distance nitrate transport from root to shoot [23][51]
OsNRT2.3b LOC_Os01g50820 OX: Improved growth and NUE [43][52]
OsNRT2.1 LOC_Os02g02170 OX: Fast growth under nitrate supply, but no increase in nitrate uptake [44][53]
OX by OsNAR2.1 promoter: Increased grain yield and NUE
OX: Increased grain yield and grain Mn under alternating wet and dry condition [45][54]
OX: Enhanced the nitrate-dependent root elongation [46][55]
OsCLC1 LOC_Os01g65500 OX: Enhanced salt tolerance and grain yield [24,49][56][57]
Ko: The opposite effects of OX
OsAMT1;1 LOC_Os04g43070 Ko: Decreased N uptake and the growth of roots and shoots [52][58]
OX: Improved NUE and grain yield [53][59]
OX: Decreased biomass at early stages of growth [54][60]
OsAMT1;2 LOC_Os02g40730 Ac: Increased tolerance to N limitation at the seedling stage, but decreased grain yield [56][24]
OsAMT1;3 LOC_Os02g40710 OX: Decreased growth with poor N uptake ability with a higher leaf C/N ratio [57][61]
OsDUR3 LOC_Os10g42960 Ko: Decreased grain filling and grain yield [15][62]
OsAAP6 LOC_Os01g65670 NIL, OX: Increased grain protein content [62][63]
OsAAP3 LOC_Os06g36180 OX: Decrease in tiller number and grain yield [63][64]
Ko: Increased grain yield due to increased bud outgrowth and numbers of tillers
OsAAP5 LOC_Os01g65660 OX: Less tiller number and grain yield [17][65]
RNAi: Increase in tiller number and grain yield
OsAAP1 LOC_Os07g04180 OX: Increased, growth, tillering, and grain yield, higher concentrations of amino acids [64][66]
Ko: Inhibition of axillary bud outgrowth and reduced tiller number

Ko & RNAi: The opposite effects of OX
OsAAP4 LOC_Os12g09300 OX: Increased rice tillering and grain yield [65][67]
OsLHT1 LOC_ Os08g03350 Ko: Reduced amino acids uptake and allocation, growth inhibition, and low yield [66,67,68][68][69][70]
OsNR2 LOC_Os02g53130 NIL: Increased effective tiller number, grain yield, and NUE [71][10]
OsGS1;1 LOC_Os02g50240 Ko: Reduction in growth rate and grain yield [73][12]
Ko: Overaccumulation of free ammonium in the leaf sheath and roots [74][13]
Ko: Abnormal sugar and organic N accumulation [75][14]
OX: Decreases in grain yield and total amino acids in seeds [76][15]
OsGS1;2 LOC_Os03g12290 OX: Reduction in grain yield and total amino acids in seeds [76][15]
Ko: Reduction in active tiller number and grain yield [77,78,79][16][17][18]
OsGS2 LOC_Os04g56400 OX: Enhancement of photorespiration and tolerance to salt stress [81][20]
OsNADH-GOGAT1 LOC_Os01g48960 Ko: Inhibition of the root elongation by NH4+, reduction in tiller number and grain yield [83][22]
Ac: Increased N uptake and remobilization, but a reduction in grain productivity [56][24]
OsNADH-GOGAT2 LOC_Os05g48200 Ko: Reduction in Productivity Via Decrease of Spikelet Number [70][9]
OsFd-GOGAT LOC_Os07g46460 Ko: Premature leaf senescence and reduced grain yield with higher GPC [85][25]
Ko: Accumulation of an excessive amount of amino acids with disturbed C/N balance [86][26]
OsASN1 LOC_Os03g18130 Ko: Reduction in free asparagine content in roots and xylem sap [92][32]
Ko: Decreased N uptake and grain yield [93][33]
OX: Enhanced tolerance and grain yield under N limitation
OsAAT1 LOC_Os02g55420 OX: Increased amino acid content in seeds [88][28]
OsAAT2 LOC_Os01g55540

1 Knockout mutants by T-DNA or Tos17 insertion. 2 Overexpressing transgenic lines driven by maize Ubiquitin or CAMV 35S promoter. 3 Knockdown lines by RNA interference. 4 Japonica cultivars harboring indica allele. 5 Nitrogen Use efficiency.

(References would be added automatically after the entry is online)

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