Nitrogen uptake and carbon-nitrogen synergistic translocation improve yield and nitrogen use efficiency in the dep1 rice line

doi:10.1016/j.jia.2025.02.050

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Nitrogen uptake and carbon-nitrogen synergistic translocation improve yield and nitrogen use efficiency in the dep1 rice line

Guohui Li^{1, 2, 3}, Yan Zhang^{1, 2, 3}, Jiwei Xu^{1, 2, 3}, Changjin Zhu^{1, 2, 3}, Qiuqian Hu⁴, Ke Xu^{1, 2, 3#}

¹ Jiangsu Key Laboratory of Crop Genetics and Physiology/Jiangsu Key Laboratory of Crop Cultivation and Physiology, Agricultural College, Yangzhou University, Yangzhou 225009, China

² Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, China

³ Research Institute of Rice Industrial Engineering Technology, Yangzhou University, Yangzhou 225009, China

⁴ School of Landscape and Horticulture, Yangzhou Polytechnic College, Yangzhou 225009, China

Highlights

l High carbon metabolism enzyme activity and sugar translocation gene expression explain high NSC translocation in the dep1 rice line.

l Good root characteristics and high nitrogen metabolism enzyme activities and gene expression contribute to high nitrogen uptake in the dep1 rice line.

l Upregulated expression of OsNPF2.4 enhances nitrogen translocation in the dep1 rice line.

Abstract
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摘要

提高水稻产量和氮利用效率是协调粮食生产和环境健康的关键挑战，然而水稻高产与氮高效协同的生理机制尚不明确。本研究以两个近等基因系水稻（DEP1和dep1）为材料，在三个氮水平（0、120和270 kg ha^-1）下进行了为期两年的田间试验，探究其碳氮转运的农艺和生理特征。结果表明，dep1相较于DEP1具有更高的产量、结实率、氮吸收和氮利用效率。灌浆期dep1茎中非结构性碳水化合物（NSCs）和氮向籽粒的转运显著高于DEP1，并且茎中NSCs转运与产量显著正相关，氮转运与氮利用效率也显著正相关。进一步分析发现，dep1的关键碳代谢酶活性（包括茎中α-淀粉酶、β-淀粉酶和蔗糖磷酸合成酶，以及籽粒中蔗糖合成酶、ADP-葡萄糖焦磷酸化酶和淀粉合成酶）显著高于DEP1，且其茎中蔗糖转运相关基因（OsSUT1和OsSWEET13）表达显著上调，这些特征促进了茎中NSCs的高效转运。同时，dep1茎中OsNPF2.4的高表达显著增强了氮的转运。对根系分析表明，dep1具有更优的根系形态特征（根干重、根表面积、根长和体积）和结构特征（中柱直径、皮层厚度和导管截面积），这解释了其较高的氮吸收能力，而且籽粒中OsNADH-GOGAT1和OsGS1.3的高表达促进了铵的同化，进一步增强了dep1的氮吸收效率。增加施氮量减少了碳的转运，但通过调节氮代谢酶活性和基因表达提高了氮的转运。总之，本研究结果强调了氮吸收以及茎中碳氮转运是dep1近等基因系水稻实现产量和氮利用效率协同提高的关键生理特征。

Abstract

Improving rice yield and nitrogen use efficiency (NUE) are crucial challenges for coordinating food production and environmental health. However, little is known about the physiological mechanisms underlying the synergistic effects of high yield and NUE in rice. Using two near-isogenic rice lines (named DEP1 and dep1), a two-year field experiment was conducted to assess agronomic characteristics and the physiological characteristics of carbon and nitrogen translocation under three nitrogen levels. Compared with DEP1, dep1 had higher grain yield, grain filling percentage, nitrogen (N) uptake, and NUE. More non-structural carbohydrates (NSCs) and N in the stems were translocated to grains during grain filling in dep1 than in DEP1. Furthermore, stem NSC translocation was significantly positively correlated with grain yield, while stem N translocation was significantly positively correlated with NUE. Key carbon metabolism enzyme activities (α-amylase, β-amylase and sucrose-phosphate synthase in stems, and sucrose synthase, ADP-glucose pyrophosphorylase and starch synthase in grains) and stem sucrose transporter gene (OsSUT1 and OsSWEET13) expression were higher in dep1 than in DEP1. This contributed to high stem NSC translocation. Higher N translocation in the stems occurred due to the higher expression of OsNPF2.4. Moreover, the higher values of root morphological traits (root dry weight, root surface area, root length and root volume) and structural characteristics (stele diameter, cortical thickness and vessel section area) in dep1 explained its high nitrogen uptake. In addition, higher expression of OsNADH-GOGAT1 and OsGS1.3 promoted the assimilation of ammonium and contributed to higher nitrogen uptake in dep1. The application of N reduced carbon translocation but enhanced N translocation by regulating the corresponding metabolic enzyme activities and gene expression. Overall, these findings highlighted the roles of nitrogen uptake, and carbon and nitrogen translocation from stems as crucial characteristics for synergistically improving yield and NUE in the dep1 rice line.

Keywords: carbon and nitrogen translocation root characteristics enzyme activity gene expression rice (Oryza sativa L.)

Online: 24 February 2025

Fund:

This research was funded by the National Natural Science Foundation of China (32272200, 31901425), the Jiangsu Provincial Key Research and Development Program of China (BE2021361), the Jiangsu Provincial Carbon Peak and Carbon Neutrality Technology Innovation Special Fund Project of China (BE2022425), the Priority Academic Program Development of Jiangsu Higher Education Institutions of China (PAPD), and the Lv Yang Jin Feng Talent Plan of Yangzhou City, China (YZLYJFJH2022YXBS020). We are grateful for the rice seeds provided by Dr. Fei Wang from Huazhong Agricultural University, China.

About author: Guohui Li, Mobile: +86-15623758326, E-mail: lgh@yzu.edu.cn; #Correspondence Ke Xu, Tel: +86-514-87972435, E-mail: xuke@yzu.edu.cn

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Guohui Li, Yan Zhang, Jiwei Xu, Changjin Zhu, Qiuqian Hu, Ke Xu. 2025. Nitrogen uptake and carbon-nitrogen synergistic translocation improve yield and nitrogen use efficiency in the dep1 rice line. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.02.050

Aluko O O, Liu Z, Sun X. 2023. The interplay of carbon and nitrogen distribution: Prospects for improved crop yields. Modern Agriculture, 1, 57-75.

Bowsher A W, Mason C M, Goolsby E W, Donovan L A. 2016. Fine root tradeoffs between nitrogen concentration and xylem vessel traits preclude unified whole‐plant resource strategies in Helianthus. Ecology and Evolution, 6, 1016-1031.

Cai H, Zhou Y, Xiao J, Li X, Zhang Q, Lian X. 2009. Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Reports, 28, 527-537.

Chen L Q, Qu X Q, Hou B H, Sosso D, Osorio S, Fernie A R, Frommer W B. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science, 335, 207-211.

Chen M, Chen G, Di D, Kronzucker H J, Shi W. 2020. Higher nitrogen use efficiency (NUE) in hybrid “super rice” links to improved morphological and physiological traits in seedling roots. Journal of Plant Physiology, 251, 153191.

Cock J H, Yoshida S. 1972. Accumulation of ¹⁴C-labelled carbohydrate before flowering and its subsequent redistribution and respiration in the rice plant. Proceedings of the Crop Science Society of Japan, 41, 226-234.

Deng L, Zhao S, Yang G, Zhu S, Tian J, Wang X. 2021. Soybean GmSUT1 transporter participates in sucrose transport to nodules during rhizobial symbiosis. Plant Growth Regulation, 96, 119-129.

Deng N, Grassini P, Yang H, Huang J, Cassman K G, Peng S. 2019. Closing yield gaps for rice self-sufficiency in China. Nature Communications, 10, 1725.

Fu J, Huang Z, Wang Z, Yang J, Zhang J. 2011. Pre-anthesis non-structural carbohydrate reserve in the stem enhances the sink strength of inferior spikelets during grain filling of rice. Field Crops Research, 123, 170-182.

Gifford R M, Evans L T. 1981. Photosynthesis, carbon partitioning, and yield. Annual Review of Plant Physiology, 32, 485-509.

Gooding M J, Addisu M, Uppal R K, Snape J W, Jones H E. 2011. Effect of wheat dwarfing genes on nitrogen-use efficiency. The Journal of Agricultural Science, 150, 3-22.

Harberd N P, Belfield E, Yasumura Y. 2009. The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: How an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. The Plant Cell, 21, 1328-1339.

Hu Q, Wang W, Lu Q, Huang J, Peng S, Cui K. 2021. Abnormal anther development leads to lower spikelet fertility in rice (Oryza sativa L.) under high temperature during the panicle initiation stage. BMC Plant Biology, 21, 428.

Huang L, Li X, Zhang Y, Fahad S, Wang F. 2022. dep1 improves rice grain yield and nitrogen use efficiency simultaneously by enhancing nitrogen and dry matter translocation. Journal of Integrative Agriculture, 21, 3185-3198.

Huang X, Qian Q, Liu Z, Sun H, He S, Luo D, Xia G, Chu C, Li J, Fu X. 2009. Natural variation at the DEP1 locus enhances grain yield in rice. Nature Genetics, 41, 494-497.

Huang X, Zhang Y, Wang L, Dong X, Hu W, Jiang M, Chen G, An G, Xiong F, Wu Y. 2021. OsDOF11 affects nitrogen metabolism by sucrose transport signaling in rice (Oryza sativa L.). Frontiers in Plant Science, 12, 703034.

Huang Y, Ji Z, Tao Y, Wei S, Jiao W, Fang Y, Jian P, Shen C, Qin Y, Zhang S, Li S, Liu X, Kang S, Tian Y, Song Q, Harberd N P, Wang S, Li S. 2023. Improving rice nitrogen-use efficiency by modulating a novel monouniquitination machinery for optimal root plasticity response to nitrogen. Nature Plants, 9, 1902-1914.

Inukai Y, Ashikari M, Kitano H, Matsuoka M. 2004. Function of the root system and molecular mechanism of crown root formation in rice. Plant & Cell Physiology, 45, s17.

James D, Borphukan B, Fartyal D, Ram B, Singh J, Manna M, Sheri V, Panditi V, Yadav R, Achary V M M, Reddy M K. 2018. Concurrent overexpression of OsGS1;1 and OsGS2 genes in transgenic rice (Oryza sativa L.): Impact on tolerance to abiotic stresses. Frontiers in Plant Science, 9, 786.

Jiang Z, Wang W, Chu C. 2018. Towards understanding of nitrogen use efficiency in plants. Chinese Bulletin of Life Sciences, 30, 1060-1071.

Ju C, Buresh R J, Wang Z, Zhang H, Liu L, Yang J, Zhang J. 2015. Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. Field Crops Research, 175, 47-55.

Julius B T, Leach K A, Tran T M, Mertz R A, Braun D M. 2017. Sugar transporters in plants: New insights and discoveries. Plant and Cell Physiology, 58, 1442-1460.

Kadam N N, Yin X, Bindraban P S, Struik P C, Jagadish K S V. 2015. Does morphological and anatomical plasticity during the vegetative stage make wheat more tolerant of water deficit stress than rice? Plant Physiology, 167, 1389-1401.

Kichey T, Heumez E, Pocholle D, Pageau K, Vanacker H, Dubois F, Le Gouis J, Hirel B. 2005. Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytologist, 169, 265-278.

Kong D, Wang J, Zeng H, Liu M, Miao Y, Wu H, Kardol P. 2016. The nutrient absorption–transportation hypothesis: Optimizing structural traits in absorptive roots. New Phytologist, 213, 1569-1572.

Li G, Cui K, Hu Q, Wang W, Pan J, Zhang G, Shi Y, Nie L, Huang J, Peng S. 2022a. Phloem unloading in developing rice caryopses and its contribution to non-structural carbohydrate translocation from stems and grain yield formation. Plant and Cell Physiology, 63, 1510-1525.

Li G, Hu Q, Shi Y, Cui K, Nie L, Huang J, Peng S. 2018. Low nitrogen application enhances starch-metabolizing enzyme activity and improves accumulation and translocation of non-structural carbohydrates in rice stems. Frontiers in Plant Science, 9, 1128.

Li G, Pan J, Cui K, Yuan M, Hu Q, Wang W, Mohapatra P K, Nie L, Huang J, Peng S. 2017. Limitation of unloading in the developing grains is a possible cause responsible for low stem non-structural carbohydrate translocation and poor grain yield formation in rice through verification of recombinant inbred lines. Frontiers in Plant Science, 8, 1369.

Li G, Zhou C, Yang Z, Zhang C, Dai Q, Huo Z, Xu K. 2022b. Low nitrogen enhances apoplastic phloem loading and improves the translocation of photoassimilates in rice leaves and stems. Plant and Cell Physiology, 63, 991-1007.

Li G H, Zhang Y, Zhou C, Xu J W, Zhu C J, Ni C, Huo Z Y, Dai Q G, Xu K. 2024. Agronomic and physiological characteristics of high yield and nitrogen use efficient varieties of rice: Comparison between two near‐isogenic lines. Food and Energy Security, 13, e539.

Li S, Tian Y, Wu K, Ye Y, Yu J, Zhang J, Liu Q, Hu M, Li H, Tong Y, Harberd N P, Fu X. 2018. Modulating plant growth–metabolism coordination for sustainable agriculture. Nature, 560, 595-600.

Li X, Zhang R, Chen G, Xie J, Xiao Z, Cao F, Ali I, Iqbal A, Wahab A, Huang M, Chen J. 2023. Increasing grain weight and yield stability by increasing pre-heading non-structural carbohydrate reserves per spikelet in short-growth duration rice. The Crop Journal, 11, 1912-1920.

Liu K, Chen Y, Li S, Wang W, Zhang W, Zhang H, Gu J, Yang J, Liu L. 2023. Differing responses of root morphology and physiology to nitrogen application rates and their relationships with grain yield in rice. The Crop Journal, 11, 618-627.

Liu K, Li T, Chen Y, Huang J, Qiu Y, Li S, Wang H, Zhu A, Zhuo X, Yu F, Zhang H, Gu J, Liu L, Yang J. 2020. Effects of root morphology and physiology on the formation and regulation of large panicles in rice. Field Crops Research, 258, 107946.

Liu L, Cui K, Qi X, Wu Y, Huang J, Peng S. 2023. Varietal responses of root characteristics to low nitrogen application explain the differing nitrogen uptake and grain yield in two rice varieties. Frontiers in Plant Science, 14, 1244281.

Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔC_T method. Methods, 25, 402-408.

Lu M Z, Snyder R, Grant J, Tegeder M. 2020. Manipulation of sucrose phloem and embryo loading affects pea leaf metabolism, carbon and nitrogen partitioning to sinks as well as seed storage pools. Plant Journal, 101, 217-236.

Mathan J, Singh A, Ranjan A. 2021. Sucrose transport and metabolism control carbon partitioning between stem and grain in rice. Journal Experimental Botany, 72, 4355-4372.

Mohapatra P, Panigrahi R, Turner N C. 2011. Physiology of spikelet development on the rice panicle. Advances in Agronomy, 110, 333-359.

Pan J, Cui K, Wei D, Huang J, Xiang J, Nie L. 2011. Relationships of non-structural carbohydrates accumulation and translocation with yield formation in rice recombinant inbred lines under two nitrogen levels. Physiologia Plantarum, 141, 321-331.

Patrick J W, Botha F C, Birch R G. 2013. Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnology Journal, 11, 142-156.

Peng S, Buresh R J, Huang J, Yang J, Zou Y, Zhong X, Wang G, Zhang F. 2006. Strategies for overcoming low agronomic nitrogen use efficiency in irrigated rice systems in China. Field Crops Research, 96, 37-47.

Pingali P L. 2012. Green revolution: Impacts, limits, and the path ahead. Proceedings of the National Academy of Sciences of the United States of America, 109, 12302-12308.

Rao P S, Mishra B, Gupta S R, Rathore A. 2008. Reproductive stage tolerance to salinity and alkalinity stresses in rice genotypes. Plant Breeding, 127, 256-261.

Scofield G N, Ruuska S A, Aoki N, Lewis D C, Tabe L M, Jenkins C L D. 2009. Starch storage in the stems of wheat plants: Localization and temporal changes. Annals of Botany, 103, 859-868.

Smith M R, Rao I M, Merchant A. 2018. Source-sink relationships in crop plants and their influence on yield development and nutritional quality. Frontiers in Plant Science, 9, 1889.

Spielmeyer W, Ellis M H, Chandler P M. 2002. Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proceedings of the National Academy of Sciences of the United States of America, 99, 9043-9048.

Stein O, Granot D. 2019. An overview of sucrose synthases in plants. Frontiers in Plant Science, 10, 95.

Sun H, Qian Q, Wu K, Luo J, Wang S, Zhang C, Ma Y, Liu Q, Huang X, Yuan Q, Han R, Zhao M, Dong G, Guo L, Zhu X, Gou Z, Wang W, Wu Y, Lin H, Fu X. 2014. Heterotrimeric G proteins regulate nitrogen-use efficiency in rice. Nature Genetics, 46, 652-656.

Tamura W, Hidaka Y, Tabuchi M, Kojima S, Hayakawa T, Sato T, Obara M, Kojima M, Sakakibara H, Yamaya T. 2010. Reverse genetics approach to characterize a function of NADH-glutamate synthase1 in rice plants. Amino Acids, 39, 1003-1012.

Wen R, Zhu M, Yu J, Kou L, Ahmad S, Wei X, Jiao G, Hu S, Sheng Z, Zhao F, Tang S, Shao G, Yu H, Hu P. 2024. Photosynthesis regulates tillering bud elongation and nitrogen-use efficiency via sugar-induced NGR5 in rice. New Phytologist, 243, 1440-1454.

Weng J H, Huang M Y, Yang Z W. 2025. A high yield potential ideotype for irrigated rice: Rice plant types with short culms and long, upright leaves. Field Crops Research, 322, 109696.

Wu W, Dong X, Chen G, Lin Z, Chi W, Tang W, Yu J, Wang S, Jiang X, Liu X, Wu Y, Wang C, Cheng X, Zhang W, Xuan W, Terzaghi W, Ronald P C, Wang H, Wang C, Wan J. 2024. The elite haplotype OsGATA8-H coordinates nitrogen uptake and productive tiller formation in rice. Nature Genetics, 56, 1516-1526.

Xia X, Fan X, Wei J, Feng H, Qu H, Xie D, Miller A J, Xu G. 2015. Rice nitrate transporter OsNPF2.4 functions in low-affinity acquisition and long-distance transport. Journal of Experimental Botany, 66, 317-331.

Xu G, Fan X, Miller A J. 2012. Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology, 63, 153-182.

Xu Z, He P, Yin X, Struik P C, Ding W, Liu K, Huang Q. 2022. Simultaneously improving yield and nitrogen use efficiency in a double rice cropping system in China. European Journal of Agronomy, 137, 126513.

Xue G, McIntyre C L, Jenkins C L D, Glassop D, van Herwaarden A F, Shorter R. 2008. Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiology, 146, 441-454.

Yamamoto Y, Yoshida T, Enomoto T, Yoshikawa G. 1991. Characteristics for the efficiency of spikelet production and the ripening in high-yielding japonica-indica hybrid and semidwarf indica rice varieties. Japanese Journal of Crop Science, 60, 365-372.

Yamaya T, Obara M, Nakajima H, Sasaki S, Hayakawa T, Sato T. 2002. Genetic manipulation and quantitative-trait loci mapping for nitrogen recycling in rice. Journal of Experimental Biology, 53, 917-925.

Yang G, Xiang H, Fu Y, Zhou C, Wang X, Yuan S, Yu X, Peng S. 2024. Optimal nitrogen management increases nitrogen use efficiency of direct-seeded double-season rice using ultrashort-duration cultivars. Field Crops Research, 316, 109495.

Yang J, Peng S, Gu S, Visperas R M, Zhu Q. 2001a. Changes in activities of three enzymes associated with starch synthesis in rice grains during grain filling. Acta Agronomica. Sinica, 27, 157-164. (in Chinese)

Yang J, Zhang J. 2010. Grain-filling problem in 'super' rice. Journal of Experimental Botany, 61, 1-5.

Yang J, Zhang J, Liu L, Wang Z, Zhu Q. 2002. Carbon remobilization and grain filling in japonica/indica hybrid rice subjected to postanthesis water deficits. Agronomy Journal, 94, 102-109.

Yang J, Zhang J, Wang Z, Zhu Q. 2001b. Activities of starch hydrolytic enzymes and sucrose-phosphate synthase in the stems of rice subjected to water stress during grain filling. Journal of Experimental Botany, 52, 2169-2179.

Yoshida S, Forno D A, Cock J H, Gomez K A. 1976. Laboratory Manual for Physiological Studies of Rice. International Rice Research Institute Press, Manila. pp. 46-49.

You L, Ros G H, Chen Y, Shao Q, Young M D, Zhang F, de Vries W. 2023. Global mean nitrogen recovery efficiency in croplands can be enhanced by optimal nutrient, crop and soil management practices. Nature Communications, 14, 5747.

Yu X, Keitel C, Zhang Y, Wangeci A N, Dijkstra F A. 2022. Global meta-analysis of nitrogen fertilizer use efficiency in rice, wheat and maize. Agriculture, Ecosystems & Environment, 338, 108089.

Zang Y, Yao Y, Xu Z, Wang B, Mao Y, Wang W, Zhang W, Zhang H, Liu L, Wang Z, Liang G, Yang J, Zhou Y, Gu J. 2022. The relationships among “STAY-GREEN” trait, post-anthesis assimilate remobilization, and grain yield in rice (Oryza sativa L.). International Journal of Molecular Sciences, 23, 13668.

Zhang H, Li H, Yuan L, Wang Z, Yang J, Zhang J. 2012. Post-anthesis alternate wetting and moderate soil drying enhances activities of key enzymes in sucrose-to-starch conversion in inferior spikelets of rice. Journal of Experimental Botany, 63, 215-227.

Zhao Y, Zhao P, Luo J, Tian L, Tian Z, Ndayambaje J. 2019. Effects of different types of nano-carbon biological fertilizers on the growth and quality of crops. Nanoscience and Nanotechnology Letters, 11, 11.

Zhu K, Yan J, Shen Y, Zhang W, Xu Y, Wang Z, Yang J. 2022. Deciphering the morpho–physiological traits for high yield potential in nitrogen efficient varieties (NEVs): A japonica rice case study. Journal of Integrative Agriculture, 21, 947-963.

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