Encyclopedia
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 [9][70]. 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 [10][71]. 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 [10][71]. 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 [10][71]. 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) [11][72].
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) [12][73]. 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 [12][73]. OsGS1;1 plays a critical role in maintaining the metabolic balance of rice plants grown under ammonium as an N source [12][13][73,74]. In addition, N assimilation by OsGS1;1 affects plastid development in rice roots [14][75]. The overexpression of OsGS1;1 or OsGS1;2 did not increase the grain yield or total amino acids in seeds [15][76].
OsGS1;2 is mainly expressed in the surface cells of roots that are responsible for the primary assimilation of ammonium [16][77]. Metabolic disorders caused by the lack of GS1;2 lead to a severe reduction of the number of active tiller and grain yield [16][17][18][77,78,79]. OsGS1;3 was exclusively expressed in the spikelet, but its functional role for N assimilation is still unknown [12][73]. 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 [12][19][73,80]. The overexpression of OsGS2 enhanced photoprotection and thereby enhanced tolerance to abiotic stresses [20][81].
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) [21][82]. 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 [22][83]. OsNADH-OsGOAT1 is mainly expressed in the roots after the supply of ammonium [23][84], and OsNADH-OsGOAT1 knockout mutant displays decreased grain yield in paddy field due to the reduced number of active tillers [22][83]. 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 [23][84]. 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 [24][56]. 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 [24][56].
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 [9][70]. OsNADH-GOGAT2 along with OsGS1;1 could be important in the remobilization of N during the senescence stage [23][84]. 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 [25][85]. Mutation of OsFd-GOGAT led to premature leaf senescence and disturbed C/N balance [25][26][85,86].
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][27][28][6,87,88].
Asparagine (Asn) and Gln are the major N forms in phloem sap and play a critical role in dynamic N recycling [29][30][89,90]. 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 [31][91]. In rice, there are two ASN genes, OsASN1 and OsASN2 [32][92]. OsASN1 is mainly expressed in roots in an ammonium-dependent manner, whereas OsASN2 expression is decreased under ammonium supply [32][92]. 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 [33][93]. The mitochondrial NADH-dependent GDH catalyzes the reversible conversion of Glu to 2-OG and ammonia [34][94]. Three OsNADH-GDH genes are differentially expressed in various organs depending on N availability [35][95], 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) [28][88]. The overexpression of OsAAT1 and OsAAT2 resulted in altered N metabolism and increased amino acid content in seeds [28][88].
Table 1.
| Gene Name | Locus Number | Phenotype Observed | References |
|---|---|---|---|
| OsNPF4.1/SP1 | LOC_Os11g12740 | Ko 1: Defective in rice panicle elongation and the short-panicle phenotype | [36][27] |
| OsNPF8.9/OsNRT1.1 | LOC_Os03g13274 | OX 2: Increased biomass under various N supplies | [37][38][28,29] |
| OsNPF7.3/OsPTR6 | LOC_Os04g50950 | OX: Increased growth by N accumulation but decreased NUE 5 under high NH4+ supply | [39][40][30,31] |
| OX: Enhanced NUE in paddy field | [41][32] | ||
| 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 | [42][33] |
| Ko & RNAi: The opposite effects of OX | |||
| OsNPF2.2/OsPTR2 | LOC_Os12g44100 | Ko: Reduction in root-to-shoot nitrate transport and abnormal vasculature development | [43][34] |
| OsNPF2.4 | LOC_Os03g48180 | OX: Enhanced nitrate acquisition and upward transfer to shoot | [44][35] |
| Ko: The opposite effects of OX | |||
| OsNPF6.5/NRT1.1B | LOC_Os10g40600 | NIL 4, OX: Increased grain yield and NUE | [45][36] |
| OsNPF7.2 | LOC_Os02g47090 | Ko & RNAi: Retarded growth under high nitrate supply | [46][37] |
| OsNPF8.1/OsPTR7 | LOC_Os01g04950 | Ko: Less accumulation of dimethyarsinate in rice grain | [47][38] |
| OsNPF7.7 | LOC_Os10g42870 | OX: Improved N influx in root, grain yield, and NUtE | [48][26] |
| OsNRT1.1A/OsNPF6.3 | LOC_Os08g05910 | OX: Early maturation and improved N utilization and grain yield | [49][20] |
| Ko: Reduced N utilization and late flowering | |||
| OsNPF6.1 | LOC_Os01g01360 | NIL: Enhancement of N uptake, NUE, and grain yield under low N supply | [50][39] |
| OsNRT2.3a | LOC_Os01g50820 | RNAi: Defect in long-distance nitrate transport from root to shoot | [51][23] |
| OsNRT2.3b | LOC_Os01g50820 | OX: Improved growth and NUE | [52][43] |
| OsNRT2.1 | LOC_Os02g02170 | OX: Fast growth under nitrate supply, but no increase in nitrate uptake | [53][44] |
| OX by OsNAR2.1 promoter: Increased grain yield and NUE | |||
| OX: Increased grain yield and grain Mn under alternating wet and dry condition | [54][45] | ||
| OX: Enhanced the nitrate-dependent root elongation | [55][46] | ||
| OsCLC1 | LOC_Os01g65500 | OX: Enhanced salt tolerance and grain yield | [56][57][24,49] |
| Ko: The opposite effects of OX | |||
| OsAMT1;1 | LOC_Os04g43070 | Ko: Decreased N uptake and the growth of roots and shoots | [58][52] |
| OX: Improved NUE and grain yield | [59][53] | ||
| OX: Decreased biomass at early stages of growth | [60][54] | ||
| OsAMT1;2 | LOC_Os02g40730 | Ac: Increased tolerance to N limitation at the seedling stage, but decreased grain yield | [24][56] |
| OsAMT1;3 | LOC_Os02g40710 | OX: Decreased growth with poor N uptake ability with a higher leaf C/N ratio | [61][57] |
| OsDUR3 | LOC_Os10g42960 | Ko: Decreased grain filling and grain yield | [62][15] |
| OsAAP6 | LOC_Os01g65670 | NIL, OX: Increased grain protein content | [63][62] |
| OsAAP3 | LOC_Os06g36180 | OX: Decrease in tiller number and grain yield | [64][63] |
| Ko: Increased grain yield due to increased bud outgrowth and numbers of tillers | |||
| OsAAP5 | LOC_Os01g65660 | OX: Less tiller number and grain yield | [65][17] |
| RNAi: Increase in tiller number and grain yield | |||
| OsAAP1 | LOC_Os07g04180 | OX: Increased, growth, tillering, and grain yield, higher concentrations of amino acids | [66][64] |
| 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 | [67][65] |
| OsLHT1 | LOC_ Os08g03350 | Ko: Reduced amino acids uptake and allocation, growth inhibition, and low yield | [68][69][70][66,67,68] |
| OsNR2 | LOC_Os02g53130 | NIL: Increased effective tiller number, grain yield, and NUE | [10][71] |
| OsGS1;1 | LOC_Os02g50240 | Ko: Reduction in growth rate and grain yield | [12][73] |
| Ko: Overaccumulation of free ammonium in the leaf sheath and roots | [13][74] | ||
| Ko: Abnormal sugar and organic N accumulation | [14][75] | ||
| OX: Decreases in grain yield and total amino acids in seeds | [15][76] | ||
| OsGS1;2 | LOC_Os03g12290 | OX: Reduction in grain yield and total amino acids in seeds | [15][76] |
| Ko: Reduction in active tiller number and grain yield | [16][17][18][77,78,79] | ||
| OsGS2 | LOC_Os04g56400 | OX: Enhancement of photorespiration and tolerance to salt stress | [20][81] |
| OsNADH-GOGAT1 | LOC_Os01g48960 | Ko: Inhibition of the root elongation by NH4+, reduction in tiller number and grain yield | [22][83] |
| Ac: Increased N uptake and remobilization, but a reduction in grain productivity | [24][56] | ||
| OsNADH-GOGAT2 | LOC_Os05g48200 | Ko: Reduction in Productivity Via Decrease of Spikelet Number | [9][70] |
| OsFd-GOGAT | LOC_Os07g46460 | Ko: Premature leaf senescence and reduced grain yield with higher GPC | [25][85] |
| Ko: Accumulation of an excessive amount of amino acids with disturbed C/N balance | [26][86] | ||
| OsASN1 | LOC_Os03g18130 | Ko: Reduction in free asparagine content in roots and xylem sap | [32][92] |
| Ko: Decreased N uptake and grain yield | [33][93] | ||
| OX: Enhanced tolerance and grain yield under N limitation | |||
| OsAAT1 | LOC_Os02g55420 | OX: Increased amino acid content in seeds | [28][88] |
| 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)
