Contribution and Prospect of Erect Panicle Type to japonica Super Rice

Chen Sibo, Tang Liang, Sun Jian, Xu Quan, Xu Zhengjin, Chen Wenfu

Review

Contribution and Prospect of Erect Panicle Type toSuper Rice

Chen Sibo, Tang Liang, Sun Jian, Xu Quan, Xu Zhengjin, Chen Wenfu

()

Over the past 30 years, super rice played an important role in boosting rice yield. The phenotype of erect panicle (EP) architecture controlled by() is the typical characteristic of super rice, and the phenotype has been used in rice breeding for nearly a century. In this review, the molecular genetic basis of EP phenotype, and mechanism of howaffects rice carbon, nitrogen metabolism and grain quality (grain shape and taste quality) were discussed. In addition, we discussed the possible improvement strategies of rice yield and quality. This review provides a quick overview of the whole process for rice quality formation, as well as suggestions and ideas for future research on rice quality improvement.

; nitrogen cycle; carbon cycle; metabolic balance; rice quality; erect panicle; super rice

Rice (L.), as one of the most important human food sources, is a major food staple and source of calorific intake for nearly half of the world’s population. As the population grows and arable land shrinks all over the world, the pressure on food security is becoming increasingly severe (Godfray and Garnett, 2014). The past century has witnessed three major breakthroughs in rice breeding, including the dwarfing breeding (Peng et al, 1999), heterosis breeding (Virmani et al, 1982) and creation of new plant types (super rice) (Chen et al, 2001).

Over the past half century, rice yields have been dramatically improved by the tireless efforts of breeders and the use of high-yielding varieties. In particular, the release of a series of super rice varieties has pushed rice production to a new peak in Northern China (Tang et al, 2017). These significant breakthroughs have made great contributions to international food security (Chen et al, 2017). The erect panicle (EP) architecture is a representative trait of super rice, which significantly increases rice production by decreasing the solar radiation intercepted by panicles, thus increasing the efficiency of solar energy utilization and ameliorating population structure (Xu et al, 1996). In recent years, with advancements in molecular biology, many comprehensive studies have been conducted on the location and function of the() gene, which controls the EP phenotype (Huang et al, 2009; Wang J Y et al, 2009; Zhou et al, 2009). These studies provide a basis for understanding the molecular mechanism of yield increase for EP varieties (Xu et al, 2016).

With the improvement of material living standards, the people’s pursuit of high-quality rice has become increasingly intense. Although the EPvarieties exhibit high-yielding potential undergenetic backgrounds, they tend to have inferior grain qualities, including inferior processing quality, appearance quality, and eating and cooking quality, compared to the curved paniclevarieties (Xu et al, 2004; Xu et al, 2005, 2007a). Does the EP gene have an effect on rice quality while significantly increasing rice yield? If the answer is yes, what should be done to achieve both high yield and good quality?

Molecular genetic basis of EP phenotype

The origin of EP can be traced back to 1902. Researchers from Italy used arice variety, introduced from Japan, which was from a Chinesevariety Chinese Originario, as parents for pure line selection. This had far-reaching significance for the development and application of EP (Ying, 1992). In 1976, China released the first widely promoted commercial EP variety Liaogeng 5, which not only has higher yield potential, but also has better performance in lodging resistance and disease resistance, thereby replacing Japaneserice (e.g. Toyonishiki, Akihikari and Akitakomachi) as the main type ofrice grown in Northern China (Xu et al, 1996).

People have paid close attention to the superiority of the EP type. Soon after the advent of Liaogeng 5, a series of high-yieldingrice varieties with the EP type were bred (Yang, 1987), some of which meet the super rice standards of the Ministry of Agriculture and Rural Affairs of China, including typical representatives Shennong 265 and Qianchonglang 2 (Huang et al, 2009; Sun et al, 2014). The EP varieties dominate northernrice by virtue of their many excellent traits (Chen et al, 2010), and play an increasingly important role in variety advancement and plant type improvement (Xu et al, 2007b).

With the use and promotion of EP varieties, the research on the genetic mechanism controlling EP genes has been identified. When studying the inheritance of rice shattering in rice, it was thought at first that the erect dense panicle is a recessive trait compared to the curved loose panicle, which is controlled by a single nuclear recessive gene (Zhu and Gu, 1979). Subsequently, the ratio of straight panicle to curved panicle in the progeny of pros and cons is basically in line with the theoretical separation ratio of 3:1. Panicle type is a quality trait, controlled by a pair of dominant nuclear genes. Besides, F2progeny has a large variation range, indicating that there are other minor genes that play a role in addition to a pair of additive major nuclear genes (Xu et al, 1995b). Panicle angle is controlled by two major genes with additive-dominance-epistatic effects and also polygenes with additive-dominance-epistatic influences, using major gene-polygene mixed inheritance models and a joint analysis method (Chen et al, 2006). F2and BC1F1populations were constructed from Liaogeng 5 and Fengjin as parents to initially locate the EP gene (Kong et al, 2007), and two adjacent QTLs (and) on chromosome 9 have been found (Yan et al, 2007). The EP gene (named, as) has been identified at the end of the long arm of chromosome 9 by the map-based cloning technology. The 12-bp sequence at the fifth exon (AGATCCTTTTTT) replaces the original 637-bp gene sequence. Other research groups obtained similar results at the same time (Huang et al, 2009; Wang J Y et al, 2009; Zhou et al, 2009). Soon thereafter, a major rice nitrogen use efficiency (NUE) QTL () was cloned from therice variety Qianchonglang 2, which has a strong response to nitrogen fertilization during the vegetative growth period. Subsequent experiments showed thatis a synonym for(Sun et al, 2014).

Effects of dep1 on carbon and nitrogen cycles

Effect of dep1 on photosynthesis

Previous studies have shown that from the perspective of physiological form, theoptimized the populationstructure by controlling the panicle structure, so that the photosynthesis limiting factors such as temperature, light and CO2concentration are improved (Xu H et al, 2016).

By comparing the light intensity in the canopy before and after cutting the panicles, the EP plants are observed less affected by panicle shadows than the curved panicle plants (Xu et al, 1990). Moreover, the EP architecture may improve the circulation of CO2and moisture (Xu et al, 1995a). A population structure analysis based on field investigation showed that the subsequent opening of the plant canopy of EP varieties allows a 10% increase in sunlight penetration compared to that of curved panicle varieties. In addition, the canopy temperature of EP varieties is about 2 oC higher than that of curved panicle varieties at midday (Xu et al, 1996). Rice leaf morphogenesis and its spatial extension posture are important components of ideal plant architecture, which play a significant role in the photosynthetic efficiency (Heath and Gregory, 1938; Donald, 1968).

Sucrose synthesis is mainly accomplished through the Calvin cycle in leaf chloroplasts and a series of biochemical reactions in the cytoplasm (Fernandez et al, 2017). The process includes seven steps from triose-P to sucrose synthesis, and a total of seven enzymes are involved (D’Hulst et al, 2015). As the entry point of CO2into the biosphere, ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) is the rate-limiting step of photosynthesis in rice (Hudson et al, 1992). Phosphoenolpyruvate carboxylase (PEPC) is a tightly controlled enzyme that plays a major role in plant C- metabolism and catalyses the irreversible β-carboxylation of PEPC to form oxaloacetate and Pi (Chollet et al, 1996). At the booting stage, Rubisco and PEPC are suppressed in-overexpression lines when plants were grown under various levels of nitrogen (Zhao et al, 2019). The inhibition of these two enzyme activities means that the ability of the leaves to capture CO2is severely reduced (Jeanneau et al, 2002). At the initial stage of photosynthesis,weakened the enzyme activity of Rubisco and PEPC. In addition,promotes the activity of GS1;1 in leaves (Zhao et al, 2019). It is not clear that it is involved in regulating the activity of fructose-1,6-bisphosphate aldolase (F2BP) and phosphoglucoseisomerase (PGI), but it is certain that the high expression ofinhibits the synthesis and transport of sucrose, which is unfavorable to the carbon cycle pathway (Kusano et al, 2011).

dep1 promotes nitrogen absorption and assimilation

The nitrogen utilization of rice is a complicated physiological and biochemical process that contains multiple processes of absorption, transport, assimilation, remobilization and allocation (Fig. 1). Nitrate (NO3–) and ammonium (NH4+) are the two main inorganic N forms in the soils. Ammonium ions are actively taken up by the roots via ammonium transporters (AMTs) (Xu G H et al, 2012). Rice has 12 AMTs that mediate high-affinity ammonium uptake (Li H et al, 2017). Each member has a specific role in a specific period or is considerable functional redundancy (Li et al, 2012).regulates nitrogen uptake and metabolism by affectingthat is associated with ammonium uptake (Sun et al, 2014). It enhances the ability of the root system to absorb ammonia nitrogen, allowing the plants to accumulate more nitrogen accumulation, and then improves the utilization efficiency of nitrogen (Xu Q et al, 2016). In rice, NRT1.1 (CHL1) is the first nitrate transporter identified in plants (Tsay et al, 1993). NUE QTL() is referred to a nitrate transporter (Hu B et al, 2015). The introduction ofalleles intolines withincreases glutamine synthetase activity, N transfer and grain yield under both low and high N growth conditions (Zhao et al, 2017).

Fig. 1. Schematic diagram of rice carbon and nitrogen cycles.

AMT, Ammonium transporter; AS, Asparagine synthetase; Asn, Asparagine; Asp, Aspartate; Gln, Glutamine; Glu, Glutamate; GOGAT, Glutamine- 2-oxoglutarate aminotransferase; GS, Glutamine synthetase; NADH, Nicotinamide adenine dinucleotide; NAR, Partner protein for nitrate transport; NiR, Nitrite reductase; NPF, Nitrate peptide transporter; NR, Nitrate reductase; NRT, Nitrate transporter; PEPC, Phosphoenolpyruvate carboxylase; Rubisco, Ribulose-1,5-bisphosphate carboxylase/oxygenase.

Yellow lines are for amino acid transport, blue lines for ammonium transport, red lines for nitrate transport, green lines for sugar transport, and black lines have no special meaning.

Glutamine synthetase (GS) plays a major role in the condensation of ammonium and glutamate to form the glutamine amino group of the glutamine (Kusano et al, 2011). Glutamate synthase (GOGAT) catalyzes the transamination of glutamine and 2-oxoglutarate to two molecules of glutamate, thus providing glutamate for ammonium assimilation through the GS and for the synthesis of the other amino acids (Bernard and Habash,2009).overexpressed lines have higher expressions ofandgenes, and thus showing higher nitrogen metabolic activity than the wild type under either low or high nitrogen conditions (Zhao et al, 2019). Although researchers have conducted extensive research on the phenotype identification ofin different nitrogen environments and the cooperative expression of genes related to nitrogen utilization, there is still no clear explanation of the molecular mechanism and signal transduction of nitrogen utilization regulation in. Therefore, it is necessary to further study the roles ofand nitrogen utilization genes in genetic networks and pathways in order to make new breakthroughs in future breeding.

In contrast,has a positive effect on the nitrogen cycle. Sincewas defined as a gene with high nitrogen efficiency, more in-depth researches on the effect ofon nitrogen uptake and utilization have been carried out (Sun et al, 2014). In the nitrogen absorption stage,enhances the activity of AMT1 and improves the absorption of ammonium/nitrate forms by rice roots through polymerization with NRT1.1b.promotes the GS1;2 and NADH- GAGOT1 activities to match the high concentration of NH4+in root cells, which enables the upright panicle variety to enrich the higher nitrogen content at the vegetative growth stage. The increase in GS1;1 and AS activities in the mature leaves at the filling stage can accelerate the remobilization of nitrogen in the form of glutamine for long distance transport. This may also be an important reason for the decrease in photosynthesis in leaves due to rapid senescence.provides higher concentrations of Aspartate (Asp), Asparagine (Asn), Glutamate (Glu) and Glutamine (Gln) in grains, which are essential precursor amino acids for protein synthesis and processing, therefore it may be a key factor for increasing the protein content in grains (Wang et al, 2019; Zhao et al, 2019; Lee et al, 2020a, b).

Regulation of dep1 on grain shape

Grain shape is controlled by multiple signaling pathways such as the ubiquitin-proteasome pathway, in addition to phytohormone signaling (cytokinins, brassinosteroids and auxins). Advances in the functional genomics have facilitated the cloning of a series of loci that control grain size (Shomura et al, 2008; Weng et al, 2008; Qi et al, 2012; Hu J et al, 2015; Liu et al, 2015).

Recent studies have shown that G protein plays an important role in regulating the grain shape of rice (Sun et al, 2014; Sun et al, 2018; Li et al, 2019). DEP1 has a modular arrangement with a conventional plant-specific Gγ subunit protein domain at its N-terminus, followed by two von Willebrand factor type C (VWFC) domains, a tumor necrosis factor receptor (TNFR)/nerve growth factor receptor (NGFR) family cysteine-rich domain, and a VWFC domain at the C-terminus. Its fifth exon is inserted, thereby eliminating the cysteine-rich domain, but not the Gγ domain. The cysteine-rich domain at the C-terminus has an inhibitory effect on the Gγ protein like domain at N-terminus (Botella, 2012; Xu Q et al, 2016). Replacement of theallele eliminates the inhibition of the cysteine-rich domain, thereby resulting in an increase in signaling by the Gβγ dimer. The N-terminal G protein γ-like (GGL) and C-terminal VWFC domains of thehead-to-tail model were obtained from GS3 (Mao et al, 2010). The genetic model indicates that DEP1 and GGC2 positively regulate grain size, while GS3 alone has no effect. However, the competitive interaction of GS3 with RGB1 disrupts the RGB1-DEP1 and RGB1-GGC2 dimers, resulting in short grains (Sun et al, 2018). However, it was also demonstrated that both GS3 and DEP1 play negative roles in the regulation of grain size by promoting the activity of the OsMADS1 transcription factor (Liu et al, 2018). Molecular studies employing CRISPR/Cas9 gene editing technology have verified the function of truncated DEP1 and found that the grains of mutants are significantly lighter than those of wild type plants (Sun et al, 2018; Li et al, 2019).controls grain size mainly through enhancing the endosperm cell proliferation, especially during the early stage of grain development (Zhang et al, 2019).

Effect of dep1 on rice taste quality

dep1 is involved in regulating starch synthesis

In recent years, many researchers have discovered manygenes affecting rice taste quality, which are concentrated in the process of rice starch and protein synthesis (Wang et al, 2005; Han et al, 2012; Peng et al, 2014; Ren et al, 2020). The influence ofon starch synthesis can be reflected by comparing the activities of several key enzymes that control starch synthesis in grains after flowering (Fig. 2-A) (Tang et al, 2009; Keeling and Myers, 2010). The transcript levels of,,andwere significantly lower in the grains ofthan those of, especially at the mid to late stages of grain- filling. Thus, the starch content in grains decreases significantly, but the amylose/amylopectin ratio does not change (Zhang et al, 2019). In addition, we speculated thathas an impact on the distribution of amylopectin length by down-regulating the expression ofand, as well as reducing the production of short chains (Glucose polymerization, DP, ≤ 24) in amylopectin, and thus affecting the starch grain structure, which may also be an important influencing factor in the starch gelatinization process, although the amylose/amylopectin ratio remains unchanged. Furthermore, the grain-filling process is also regulated by several types of small chemical molecules, such as plant hormones, which fluctuate considerably during the grain filling period (Zhang et al, 2016). The levels of these endogenous plant hormones are significantly lower in thethan in thegrains during the mid to late grain filling stage, and the filling time was shortened. Thus, the negative effect ofon the grain filling process occurs largely through changing the biosynthesis of these plant hormones (Zhang et al, 2019).

Effect of dep1 on storage protein

Storage protein is the second major chemical component of rice. It is not only an important index used to evaluate the nutritive quality of rice, but also closely related to the taste quality of rice (Liu et al, 2008). When the protein content is high (> 8%), the rice grain structure is dense and the water absorption speed is slow, resulting that the starch cannot be fully gelatinized and the rice texture is hard (Crofts et al, 2017; Balindong et al, 2018). The effect of protein on rice taste quality is greater than that of amylose (Champagne et al, 2009). Previous studies showed that overexpression ofsignificantly increased the activity of,,andin leaves (Zhao et al, 2019). This means thatmay influence the carbon and nitrogen balance inside the grains in later stage of grouting by regulating the activity of GS.

Yield and quality formation of EP varieties under high nitrogen input conditions

The application of N fertilizer makes a great contribution to crop yields.is considered the major gene controlling panicle type and nitrogen-use efficiency (Sun et al, 2014).

The varieties which can further increase yield with the increase in nitrogen fertilizer input are termed as high- nitrogen-efficiency varieties. These are the ‘super high yield’ varieties pursued by some breeding researchers.is widely used in super rice breeding, such as Shennong 265, a typical variety.expression is positively regulated by nitrogen fertilizer (Palme et al, 2014). Under high nitrogen condition (120 kg/hm2), compared with the non-EP varieties, the EP varieties significantly improves plant type and yield-related traits. Under low nitrogen condition (60 kg/hm2), the yield of the EP varieties is greatly reduced, and even lower than that of the non-EP ones (Tang et al, 2017; Fei et al, 2019b). This means that EPvarieties cannot reach their full production potential given a limited nitrogen supply. The production value of the EP type can only be realized under high nitrogen input condition. Therefore, the nitrogen efficiency ofshould be high yield with high input, which is the ‘high-nitrogen-efficiency’ type. Therefore, the discussion of the quality formation and the possibility of improvement should depend on high levels of nitrogen application, otherwise it will be meaningless.

Extensive in-depth research has been conducted on the gene function of(Huang et al, 2009; Sun et al,2014). The influence ofon yield can be described more systematically in the form of source, sink and flux (Fig. 3-A). First of all, the interaction effect betweenandprovides rice with an ideal plant type and optimizes the population structure, givingrice stronger photosynthetic potential and more favorable photosynthetic conditions, including temperature, light, water and gas exchange conditions (Lu et al, 2013; Xu et al, 2014; Fei et al, 2019b). In addition, the interaction effects positively promote the transport capacity of AMT and NRT to different forms of nitrogen in soil, and GS-GOGAT, which is highly expressed in roots and leaves, promotes nitrogen assimilation (Sun et al, 2014; Hu B et al, 2015; Zhao et al, 2017). As an important yield component, the number of grains per panicle is closely related to panicle traits, especially the number of branches and stems. Although the panicle length is shorter, the upright-panicle-type cultivars have more branches and higher grain density. In particular, the number of secondary branches and the number of grains on secondary branches are significantly increased, so that they have higher grain number per panicle and greater yield potential.inrice, as a gene controlling the grain number per panicle, encodes cytokinin oxidase/dehydrogenase, and regulates meristematic tissue activity, spikelet number per branch and grain number by influencing cytokinin level (Ashikari et al, 2005). A NIL-line has the same number of primary branches as the control line but develops a higher number of secondary branches (Ashikari et al, 2005). The restorer line 9311 with bothandalleles, shows significant yield increases (Liu et al, 2012), and the directed aggregation of the dominant allele may help to further promote the yield increases. Compared with curved-panicle varieties, upright- panicle varieties have thicker stem, which not only provides mechanical strength and prevents lodging, but also provides developed vascular tissue for the smooth transport of compounds. The size and number of vascular bundles are influenced by both genes and environments (Lei et al, 2014; Liu and Li, 2016). Fei et al (2019) found thatreduces the level of endogenous ABA by inhibiting the expression of ABA synthesis gene, thus promoting the development of vascular tissue; in addition,inhibits cell division during the vegetative growth period and thus reducing the plant height, which also provides favorable conditions for the horizontal growth of stem (Du et al, 2020).

Fig. 2. Processing of starch and protein biosynthesis in rice endosperm and regulatory role played by.

A,down-regulates the expression of,andgenes, thereby affecting the starch component and content.

B, Activity of GS1;1 increases the content of amino acid/amide in endosperm cells and provides more substrates for protein synthesis and thus increases the content of grain protein. However, the influence of amino acid/amide content on protein composition is not clear.

C, Non-targeted metabolite profiling reveals the decrease of aspartate family and glutamate family content in the leaf blade ofknockout lines in the metabolite levels. The content of carbohydrate metabolites increases significantly.promotes the expression of, indicating that it can achieve the opposite metabolite content by increasing the activity of GS1;1.

ADPG, ADP-glucose; Asn, Asparagine; Asp, Aspartate; BG, Branch glucan; CA, Chain amino acid; CCV, Clathrin coated vesicle; DP, Degree of glucose polymerization; DPE, Disproportionating enzyme; DV, Dense vesicle; F6P, Fructose-6-phosphate; Fru, Fructose; G3P, Glucose-3-phosphate; G6P, Glucose-6-phosphate; GBSS, Granule bound starch synthase; Gln, Glutamine; Glu, Glucose; GPA, Glutelin precursor accumulation; Ile, Isoleucine; ISA, Isoamylase; LG, Linear glucan; Lys, Lysine; Met, Methionine; MVB, Multivesicular body; PAC, Precursor-accumulating vesicle; PB, Protein body; PDIL, Protein disulphide isomerase-like; Pho1, Phosphorylase1; Pro, Proline; PSV, Protein storage vacuole; SBE, Starch branching enzyme; SS, Starch synthase; Thr, Threonine; VPE, Vacuolar processing enzyme.

Fig. 3. Effects ofon rice yield and quality formation.

A, Contribution ofto yield improvement under the background of high nitrogen input was expounded from the perspectives of morphology and physiology.

B,changes the composition and content of starch and protein in the original endosperm cells by regulating the expression of key genes in the carbon and nitrogen metabolism pathway. At the same time, the changes of endogenous hormone levels also have a negative effect on the filling duration. These factors may be the key to the influence ofon rice quality traits.

Full lines represent the reported conclusion, dotted lines represent the inferred conclusion, arrowheads represent promotion, and vertical lines represent suppression.

Regarding the effect ofon the formation of quality traits, researchers have conducted extensive research but there is no clear conclusion. We use a simplified model to speculate on its possible impact (Fig. 3-B). Under the background of high nitrogen input,can enrich the high nitrogen content in the plants at the vegetative stage. When the filling stage begins, nitrogen is remobilized by GS1;1 to accumulate in grains. Previous studies have shown thatcan significantly improve GS1;1 activity and protein contentin grains (Fei et al, 2019b; Wang et al, 2019). Therefore, the ability to delay senescence of plants is weakened, and the filling time is shortened. In production practice, grain fertilizer can be applied to high- nitrogen and high-efficiency varieties to ensure the ability to prolong grain filling of the plant (Feng et al, 2000). However, nitrogen input at the later stage will cause a significant negative impact on rice quality (Xu et al, 2018). In addition, changes in the starch content and components in grains are also important factors affecting quality. Research on the texture properties of the parent line and recombination inbred lines in the four areas revealed thatmight affect rice eating quality through regulating the amylopectin chain length distribution (Xu et al, 2019). CRISPR-rice has a higher hardness score but lower stickiness and taste scores than WT-(Fei et al, 2019a). Therefore, how to improve quality while ensuring yield will be a key issue to solve in the future.

Perspectives

In the past three decades, panicle erectness, as an important characteristic of high yieldingvarieties, has drawn increasing attention from rice breeders. A great number of EPvarieties have been successfully developed and released for production and rapidly become the dominant rice varieties in Northern China. Although EP varieties have made great breakthroughs in yield, their eating quality is usually inferior tovarieties with drooping panicles. Therefore, it is a challenge for rice breeders to elucidate the molecular mechanism of howaffects eating quality and to genetically improve the eating quality and yield potential ofvarieties.

Rice quality formation is a very complex physiologicalprocess, which depends on the rice carbon and nitrogencycles. During the rice filling period, tens of thousands of genes participate in the regulation of this process, so the influence of other genotypes should be excluded in the evaluation of the influence of. Genetically modified material can eliminate the differences caused by other genetic backgrounds. Due to the advantages of a short acquisition period and strong targeting, transgenic materials can be used as good materials for basic research on the function of.

How to realize quality improvement under the background of the high yield of EP varieties has been a research hot spot in recent years. It is feasible to improve the rice yield and grain quality of EPcultivars by replacing favorable alleles simultaneously (Yang et al, 2020). This strategy could also be applied in the improvement of commoncultivars. Moreover, based on previous studies, the activity regulation offoris the main factor affecting the carbon and nitrogen accumulation imbalance in grains during the filling period. Therefore, the follow- up research can also be used as an entry point to reduce the negative influence ofon eating quality. There are several suggestions with regard to the study of EP varieties: (i) developing a set of rice eating quality evaluation systems with objectivity, versatility and operability, (ii) building suitable populations to avoid interference due to genetic effects, (iii) further study the adjustment mechanism ofonduring the filling period, (iv) finding the molecular mechanism ofon the enzyme activity of photosynthetic system, and (v) finding the molecular mechanism ofon the regulation of source hormonelevel during grain filling. Therefore, a complete system should be established in the near future to systematically clarify the influence mechanism ofon carbon and nitrogen metabolism during the rice quality formation period by means of the combination of transcriptions, metabonomics and proteomics. This will be a great help in achieving rice quality improvement while pursuing high yields.

Under the background of current green agriculture methods, the application of nitrogen fertilizer has become more precise and economical. Under these conditions, whether the use ofgenes has limitations, this seems to be a critical issue. However, affected by the current epidemic and the complex international situation, the new economic pattern dominated by domestic circulation has become a new direction for future development. Therefore, an in-depth analysis of the function ofin the process of N redistribution and the reduction of its negative effects will be the key to improving the quality of EP varieties. Consequently, researchers focusing on the use and improvement ofunder the combined influence of multiple factors should pay equal attention to high yield and high quality and reduce production costs under the premise of safe production. It is believed that in the future, more EP varieties will provide greater contribution to China’s food security.

ACKNOWLEDGEMENTs

This study was supported by the National Key Research and Development Program of China (Grant No. 2016YFD0300504), and Liaoning Revitalization Talent Program of China (Grant No. XLYC1807233).

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6 December 2020;

14 May 2021

TANG Liang (tangliang@syau.edu.cn)

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http://dx.doi.org/10.1016/j.rsci.2021.07.004

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